Growth Performance, Serum Biochemical Profile, Oxidative Status,...

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Research Article Growth Performance, Serum Biochemical Profile, Oxidative Status, and Fertility Traits in Male Japanese Quail Fed on Ginger (Zingiber officinale, Roscoe) Essential Oil Tchoffo Herve , 1 Kana Jean Raphaël , 2 Ngoula Ferdinand, 1 Folack Tiwa Laurine Vitrice, 2 Adoum Gaye, 1 Moussa Mahamat Outman, 1 and Ngouozeu Moyo Willy Marvel 2 1 Animal Physiology and Health Research Unit, Faculty of Agronomy and Agricultural Sciences, University of Dschang, P.O. Box 188, Dschang, Cameroon 2 Animal Nutrition and Production Research Unit, Faculty of Agronomy and Agricultural Sciences, University of Dschang, P.O. Box 188, Dschang, Cameroon Correspondence should be addressed to Tchoffo Herve; tchoff[email protected] Received 12 January 2018; Revised 8 February 2018; Accepted 14 February 2018; Published 28 June 2018 Academic Editor: Maria Laura Bacci Copyright © 2018 Tchoffo Herve et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. is study was designed to evaluate the effect of ginger (Zingiber officinale, Rosc.) essential oil on growth performance, serum biochemical profile, oxidative stress, and histological structure of testes and fertility traits in Japanese quail (Coturnix coturnix japonica). 96 three-week-old male Japanese quail weighing between 120 and 130 g were randomly assigned to 4 dietary treatment groups in a completely randomized design. Each group was divided into 4 replicates of 6 quails. Quails in control group received orally 100 l/kg bw of distilled water, while the three test groups received, respectively, by gastric intubation 50, 100, and 150 l/kg bw of ginger essential oil. At 12 weeks old, twelve birds per treatment were randomly selected and fasted for 24 hours, weighed, and slaughtered to assess organ and biochemical parameters. At the same period, 4 mature male quails per treatment were chosen at ran- dom and individually housed in cages, each with four untreated females for fertility and hatchability traits. e main results revealed that growth characteristics were not markedly ( > 0.05) affected by essential oil whatever the dose. e leſt testis weight increased significantly ( < 0.05) with 100 and 150 l/kg bw of essential oil compared to the control. e serum content in total cholesterol and triglycerides, the liver weight, the serum content in transaminases, and malondialdehyde decreased in treated quails. e serum content in total protein and globulin and the antioxidant enzymes activities increased in treated birds compared to the control. e histological changes in the testis were less visible in treated Japanese quails. At the doses of 100 and 150 l/kg bw, this essential oil induced a significant increase ( < 0.05) in fertility rate compared to the control. Under the conditions of this study, the ginger rhizomes essential oil can be used in poultry to reduce the lipid peroxidation in reproductive tissues and improve the fertility traits. 1. Introduction e lack of the intestinal reservoir containing microorgan- isms that can inhibit the growth of pathogenic microorgan- isms and degrading toxins before their intestinal absorption in birds [1] led to the massive use of antibiotics in the poultry industry to improve growth performances, as well as reducing morbidity and mortality. Since 2006, the European Union and the authorities of many countries in the world banded the use of antibiotics as feed additives in livestock because of speculated risk in generating antibiotic resistance in pathogenic microbiota [2]. As a result, studies on natural products such as essential oils produced by aromatic plants, due to their diverse biological activities, have recently gained a great attention [3–5]. Among those aromatic plants, Z. offic- inale is used worldwide as spice and medicinal plant. e Z. officinale phytoconstituents essentially made up by flavonoid, phenolic acid, and terpenoid possesses many important pharmacological activities such as cardioprotective, anti- inflammatory, antimicrobial, antioxidant, antiproliferative, Hindawi Veterinary Medicine International Volume 2018, Article ID 7682060, 8 pages https://doi.org/10.1155/2018/7682060

Transcript of Growth Performance, Serum Biochemical Profile, Oxidative Status,...

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Research ArticleGrowth Performance Serum Biochemical ProfileOxidative Status and Fertility Traits in Male Japanese Quail Fedon Ginger (Zingiber officinale Roscoe) Essential Oil

Tchoffo Herve 1 Kana Jean Raphaeumll 2

Ngoula Ferdinand1 Folack Tiwa Laurine Vitrice2 AdoumGaye1

Moussa Mahamat Outman1 and NgouozeuMoyoWilly Marvel2

1Animal Physiology and Health Research Unit Faculty of Agronomy and Agricultural Sciences University of DschangPO Box 188 Dschang Cameroon2Animal Nutrition and Production Research Unit Faculty of Agronomy and Agricultural Sciences University of DschangPO Box 188 Dschang Cameroon

Correspondence should be addressed to Tchoffo Herve tchoffohervyahoofr

Received 12 January 2018 Revised 8 February 2018 Accepted 14 February 2018 Published 28 June 2018

Academic Editor Maria Laura Bacci

Copyright copy 2018 Tchoffo Herve et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

This study was designed to evaluate the effect of ginger (Zingiber officinale Rosc) essential oil on growth performance serumbiochemical profile oxidative stress and histological structure of testes and fertility traits in Japanese quail (Coturnix coturnixjaponica) 96 three-week-old male Japanese quail weighing between 120 and 130 g were randomly assigned to 4 dietary treatmentgroups in a completely randomized design Each group was divided into 4 replicates of 6 quails Quails in control group receivedorally 100120583lkg bw of distilled water while the three test groups received respectively by gastric intubation 50 100 and 150 120583lkgbw of ginger essential oil At 12 weeks old twelve birds per treatment were randomly selected and fasted for 24 hours weighed andslaughtered to assess organ and biochemical parameters At the same period 4maturemale quails per treatment were chosen at ran-dom and individually housed in cages eachwith four untreated females for fertility and hatchability traitsThemain results revealedthat growth characteristics were not markedly (119875 gt 005) affected by essential oil whatever the doseThe left testis weight increasedsignificantly (119875 lt 005) with 100 and 150 120583lkg bw of essential oil compared to the control The serum content in total cholesteroland triglycerides the liver weight the serum content in transaminases andmalondialdehyde decreased in treated quailsThe serumcontent in total protein and globulin and the antioxidant enzymes activities increased in treated birds compared to the controlThehistological changes in the testis were less visible in treated Japanese quails At the doses of 100 and 150 120583lkg bw this essential oilinduced a significant increase (119875 lt 005) in fertility rate compared to the control Under the conditions of this study the gingerrhizomes essential oil can be used in poultry to reduce the lipid peroxidation in reproductive tissues and improve the fertility traits

1 Introduction

The lack of the intestinal reservoir containing microorgan-isms that can inhibit the growth of pathogenic microorgan-isms and degrading toxins before their intestinal absorptionin birds [1] led to the massive use of antibiotics in thepoultry industry to improve growth performances as well asreducing morbidity and mortality Since 2006 the EuropeanUnion and the authorities of many countries in the worldbanded the use of antibiotics as feed additives in livestock

because of speculated risk in generating antibiotic resistancein pathogenic microbiota [2] As a result studies on naturalproducts such as essential oils produced by aromatic plantsdue to their diverse biological activities have recently gaineda great attention [3ndash5] Among those aromatic plants Z offic-inale is used worldwide as spice and medicinal plant The Zofficinale phytoconstituents essentially made up by flavonoidphenolic acid and terpenoid possesses many importantpharmacological activities such as cardioprotective anti-inflammatory antimicrobial antioxidant antiproliferative

HindawiVeterinary Medicine InternationalVolume 2018 Article ID 7682060 8 pageshttpsdoiorg10115520187682060

2 Veterinary Medicine International

Table 1 Phytochemical constituents of ginger essential oil

Constituents (+) present (minus) absentAlkaloids +Triterpenoid +Steroid minus

Flavonoid +Phenol +

immunomodulatory neuroprotective and hepatoprotectiveproperties [6] which can be used in animal farm to boostgrowth reduce oxidative stress and histological alteration invital organs and subsequently improve fertility In poultryproducing the maximum number of fertile eggs and viablechicks is a major concern The health of testes plays a centralrole in sperm fertilizing capability which is positively corre-lated to hatchability rate Testicularweight is highly correlatedto the physiological reproductive status in poultry breeders[7] A direct relationship has been established betweensperm production and testes weight in boiler breeders [8]Ferrouk et al [9] reported that testicular size is the primaryendpoint for spermatogenesis since seminiferous tubules andgerminal elements take about 98 of the total testismassThebeneficial effects of ginger powder in poultry growth perfor-mances egg production and quality carcass traits and bloodbiochemistry parameters can be attributed to the phenolicsand flavonoids compounds present [5 10] However up tonow few studies have been designed to assess the efficiencyof these actives compounds on poultry reproduction

The objective of this study was to find out the effectsof graded levels of ginger roots essential oil on growth andreproductive performances in male Japanese quail

2 Materials and Methods

21 Study Area This study was carried out at the poultryunit in the Teaching and Research Farm of the Universityof Dschang Cameroon This farm is located at 5∘261015840 northand 10∘261015840 EST and at an altitude of 1420m above sea levelAnnual temperature varies between 10∘C and 25∘C Rainfallranges from 1500 to 2000mm per annum over a 9-monthrainy season (March to November)

22 Origin of Essential Oil Fresh ginger rhizomes wereharvested from Santchou (LN 5∘1610158405510158401015840 LE 9∘5810158402710158401015840) in theMenoua division West Region of Cameroon Oil extractionwas done by hydrodistillation in PYTORICA LaboratoryBonapriso Douala Cameroon as described by Wang andWeller [11]

23 Phytochemical Screening of Essential Oil The phyto-chemical screening of essential oil (Table 1) was done asdescribed by Banso and Ngbede [12] and Ngbede et al [13]

24 Animals and Experimental Design Ninety-six 3-week-old male Japanese quail (Coturnix coturnix japonica) weigh-ing between 120 and 130 g produced from a parent stockin the Teaching and Research Farm of the University of

Table 2 Composition of the experimental diet

Ingredients Amount (kg100 kg)Maize 60Wheat bran 45Soybean meal 22Fishmeal 45Oeister shell 2Bone meal 2Premix 5lowast 5Total 100Calculated chemical compositionCrude protein () 2015Metabolizable energy (KcalKg) 290680Calcium () 203Phosphorus () 127Lysine () 044Methionine () 014Sodium () 022lowastPremix 5 mixture of vitamins A B complex D K and E

Dschang were used for testing Each quail was identified bya ring bearing his number in one of its paws

At the beginning of the experiment quails were weighedand randomly assigned to 4 dietary treatment groups in acompletely randomized design Each group was divided into4 subgroups of 6 quails Quails in control group receivedorally 100 120583lkg bw of distilled water while birds in theother three test groups during the same period respectivelyreceived by gastric intubation 50 100 and 150120583lkg bodyweight of essential oil At 12 weeks old twelve birds pertreatment were randomly selected and slaughtered for organscharacteristics assessment and blood samples were collectedfor biochemical analysis At the same period 4 male quailsper treatmentwith hypertrophy of cloacal glandwere selectedand individually housed in the same cage with four untreatedfemales and reared under the same conditions for fertilityhatchability traits and chick weight assessment During theexperimental period feed (Table 2) and water were offeredad libitum to quail in adapted equipment

This study was carried out in strict accordance withrecommendations of institutional guidelines for the care anduse of laboratory animals Quails were humanly handledwith respect to the ethical standards laid down in the 1964Declaration of Helsinki and its later amendments

25 Growth Characteristics Feed intake and life body weightfor individual quail were recorded weekly body weight gainwas obtained by the difference in life body weight of twoconsecutive weeks according to the procedures of McDonaldet al [14] Feed conversion ratio was obtained by dividingweekly feed intake by weekly body weight gain

26 Blood Sampling and Organ Weights At the end of theexperiment 12 quails per treatment were randomly selectedand fasted for 24 hours weighed and slaughtered as des-cribed by Jourdain [15] Blood samples were collected from

Veterinary Medicine International 3

the jugular vein in nonheparinized tubes the serum isolatedwas stored at minus20∘C for biochemical analysis

Testes and liver of slaughtered quails were carefullyremoved rid of adipose tissue blotted dry and weighedseparately using a scale of 160 g capacity and 10minus3 g precisionThe relative organ weight was calculated as follows

Relative organ weight ()

=Organ weight (mg)Live body weight (g)

times 100(1)

The left testis was homogenized in a known volume of cold09 NaCl followed by a centrifugation (3000 rpm 30min)and the resultant supernatants were subsequently stored atminus20∘C for antioxidant status assessment

27 Biochemical Analysis Serum content in proteins wasdetermined by Biuret method [16] Alanine aminotransferase(ALT) and aspartate aminotransferase (AST) contents wereevaluated by the enzymatic analysis method using commer-cial kits CHRONOLAB Ref 101-0255 and CHRONOLABRef 101-0256 respectively Total cholesterol and triglycerideswere determined by colorimetric methods using commercialkits CHRONOLAB Ref 101-0576 and CHRONOLAB Ref101-0241 respectively Total globulins were calculated asdescribed by Abdel-Fattah et al [17]

28 Oxidative Stress Characteristics The malondialdehydeconcentration was evaluated by the thiobarbituric acidmethod [18] Superoxide dismutase (SOD) catalase (CAT)and reduced glutathione (GSH) activities were evaluatedas described by Misra and Fridovich [19] Sinha [20] andEllman and Fiches [21] respectively

29Histology Histological screening of testeswas carried outas described by Wolfang [22] for organ or tissues Brieflythe right testis was fixed by immersion in Bouin solutionfor 1 week and then washed dehydrated in ascending gradealcohol bath clarified in xylene immersion and embeddedin paraffin Sections of 5120583m were stained with hematoxylin-eosin for histological observations under a light microscope(400x)

210 Fertility and Hatchability Traits A total of 56 eggs pergroup were collected during 8 days weighted individuallyand incubated After artificial incubation for 19 days allunhatched eggs were cracked and classified as infertile orembryonic mortalityThe fertility rate was then calculated bydividing the number of fertile eggs over the total number ofeggs incubated The individual chickrsquos weight was obtainedby dividing the total chickrsquos weight over the number of chickshatch per group

211 Statistical Analysis The statistical analysis was carriedout using the SPSS 200 software Results were expressed asmean plusmn standard deviation Differences between groups wereassessed using one-way ANOVA followed by Duncan posthoc test with the significance level set at 005 119875 value wasdone using the Studentrsquos 119905-test A 119875 value of less than 005 was

considered as significantThe normality of data was tested bythe Shapiro-Wilk Test and the relationships between differentparameters were highlighted by the correlation coefficient ofBravais-Pearson

3 Results

31 Growth Characteristics As shown in Table 3 feed intakelive body weight body weight gain and feed conversion ratio(FCR) were not significantly affected (119875 gt 005) by the dosesof essential oil used However the values of these growthcharacteristics tend to decrease in treated quails compared tothe quails in control group

32 Organs Weight The relative weight of the left testisincreased significantly (119875 lt 005) in quails treatedwith essen-tial oil at 100 and 150120583lkg bw compared to quails in thecontrol group and quails fed on the smallest dose of essentialoil (50 120583lkg bw) The relative weight of the right testis intreated quails was comparable (119875 gt 005) to that of the quailsin the control group although this weight tended to increasein birds treated with 100 and 150 120583lkg of bw (Table 3)

The relative weight of the liver recorded in quails treatedwith oil whatever the dose was comparable (119875 gt 005) to thatof the quails in the control group However this weight tendsto decrease with 100 and 150 120583lkg bw compared to the weightof liver recorded in the control group and quails fed on thesmallest dose of the essential oil (50120583lkg of bw) (Table 3)

33 Serum Biochemical Parameters The ginger essential oilwhatever the dose induced a significant increase (119875 lt 005)in protein and globulin serum contents compared to thecontrol However the serum contents in protein and globulinrecorded with 100 and 150 120583lkg bwwere comparable and sig-nificantly higher (119875 lt 005) relative to the quantity recordedin quails treated with the lowest dose of this essential oil(50 120583lkg bw) (Table 4) The alanine aminotransferase (ALT)activity decreased significantly (119875 lt 005) in quails treatedwith essential oil whatever the dose compared to the controlgroup Although statistically comparable the activity of ALTtends to decrease in quails treated with 150 120583lkg bw ascompared to 50 and 100120583lkg bw The oral administration ofginger essential oil induced a decrease in aspartate amino-transferase (AST) activity relative to the control Howeverthis decreasewas significant onlywith 150120583lkg bw comparedto other essential oil dosesThe serum content in total choles-terol decreased significantly (119875 lt 005) and linearly withthe increasing doses of the essential oil relative to the con-trol Essential oil significantly (119875 lt 005) decreases triglyc-eride content compared to the control (Table 4)

34 Antioxidant Status The malondialdehyde (MDA) levelin the treated quails decreased significantly (119875 lt 005) andlinearly with the increasing doses of the essential oil com-pared to the control group The oral administration of theessential oil induced an increase in superoxide dismutase(SOD) activity relative to the control However this increasewas significant only with 150120583lkg bw compared to all otherdoses (Table 4) The glutathione (GSH) activities in quails

4 Veterinary Medicine International

ICSPZ

N

N

IC0

ST

IC

IC

150100

50

L

LL

ST

ST

SPZ

Figure 1 Histological structure of Japanese quail testes as affected by ginger roots essential oil (400x) 0 (control) 50 100 and 150 doses ofginger roots essential oil (120583lkg body weight) SPZ spermatozoa ST seminiferous tubules IC interstitial cells L lumen and N necrosis

Table 3 Effects of graded level of ginger roots essential oil on growth characteristics and relative organ weightsof male Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Growth characteristicsFeed intake (g) 907 plusmn 4354 91013 plusmn 4819 85763 plusmn 4783 88915 plusmn 3775 017Live body weight (g) 20927 plusmn1502 20745 plusmn 2490 20427 plusmn 1527 20225 plusmn 1772 080Body weight gain (g) 22529 plusmn 4675 22786 plusmn 3798 21943 plusmn 4659 23314 plusmn 4547 095FCR 598 plusmn 207 579 plusmn 179 511 plusmn 069 463 plusmn 089 039Organ weights (g100 g bw)Liver 155 plusmn 033 157 plusmn 029 146 plusmn 039 147 plusmn 036 085Pair of testes 201 plusmn 048a 208 plusmn 016a 263 plusmn 021b 254 plusmn 032b 001Right testis 100 plusmn 024 104 plusmn 016 118 plusmn 023 114 plusmn 022 056Left testis 101 plusmn 026a 105 plusmn 017a 146 plusmn 007b 141 plusmn 033b 001abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails FCR = feed conversion ratio

treated with essential oil at 100 and 150120583lkg bw werecomparable and significantly (119875 lt 005) higher than activitiesrecorded in control group and the group of quails treatedwith50 120583lkg bw The catalase (CAT) activities were comparablewith 100 and 150120583lkg bw but significantly higher (119875 lt 005)than CAT activity recorded in the control group (Table 4)

35 Histological Structure of the Testes The testes of thequails in the control group showed slight alterations of theseminiferous tubules with necrosis The oral administrationof the essential oil whatever the dose improved the histo-logical structure of the testes compared to the control Thehistological changes observed in the testes of the treatedquails whatever the dose were almost identical (Figure 1)

36 Fertility and Hatchability Traits The fertility rate ofquails treated with the essential oil except the lowest dose(50 120583lkg bw) significantly increased (119875 lt 005) compared tothe control group However the fertility rate of quails treatedwith 100 120583lkg bw is comparable to the fertility of quailstreated with the highest dose of essential oil (150 120583lkg bw)The relative weight of the testes is positively and significantlycorrelated to the fertility rate (120588 = +099 119875 lt 001) the sameobservation was made between GSH and the fertility rate (120588= +095 119875 lt 005) (Table 5)

The oral administration of ginger rhizome essential oil atthe entire used dose tends to increase the hatching rate offertile eggs and the total hatch rate compared to the control(Table 6) However the highest fertile egg hatched and total

Veterinary Medicine International 5

Table 4 Effects of graded levels of ginger essential oil on serum biochemical and testes oxidative stress characteristics

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Serum metabolitesSerum proteins (gdl) 206 plusmn 004a 238 plusmn 019b 266 plusmn 019c 270 plusmn 035c 000Globulins (gdl) 016 plusmn 005a 031 plusmn 006b 049 plusmn 007c 048 plusmn 016c 000AST (UL) 16800 plusmn 2024b 14624 plusmn 1511ab 16324 plusmn 1129ab 13749 plusmn 1688a 000ALT (UL) 5750 plusmn 1049b 4285 plusmn 346a 4000 plusmn 1014a 3343 plusmn 607a 000Total cholesterol (mgdl) 12727 plusmn 798d 11809 plusmn 541c 11006 plusmn 583b 10027 plusmn 198a 000Triglycerides (mgdl) 7346 plusmn 1039b 5718 plusmn 443a 5691 plusmn 649a 5607 plusmn 616a 000Testes oxidative stress (gram of tissue)MDA 9779 plusmn 960c 8220 plusmn 993b 5249 plusmn 839a 5057 plusmn 1783a 000SOD 292 plusmn 048a 347 plusmn 033a 344 plusmn 055a 408 plusmn 023b 000GSH 18373 plusmn 3515a 20147 plusmn 1774a 26507 plusmn 4825b 27402 plusmn 5416b 000CAT 282 plusmn 031a 336 plusmn 073ab 378 plusmn 063b 360 plusmn 089b 004abcdOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails MDA = malondialdehyde GSH = reducedglutathione CAT = catalase SOD = superoxide dismutase AST = aspartate aminotransferase ALT = alanine aminotransferase values are presented as meansplusmn standard deviation

Table 5 Correlations between testes weight GSH sperm motilitytotal hatch and fertility rate

Parameters Pair of testesrelative weight Fertility rate Total hatch rate

Fertility rate 099lowastlowast - 065Sperm motility 099lowast 099lowastlowast -GSH 098lowast 095lowast -lowastThe correlation is significant at the 005 level lowastlowastThe correlation is signifi-cant at the 001 level

hatch rates were recorded in quails treated with 100 120583lkgbw A positive and nonsignificant correlation was recordedbetween the fertility rate and the total hatch rate (120588 = +065119875 gt 005) (Table 5)

The embryonic mortality rate was not significantlyaffected (119875 gt 005) by the doses of the essential oil usedHow-ever it tends to decrease with essential oil whatever the dosecompared to the controlThe lowest embryonicmortality ratewas recorded in quails treated with 100 120583lkg bw The gingeressential oil whatever the dose induced a nonsignificant(119875 gt 005) increase in chickrsquos weight compared to the con-trol However the highest chick weight was recorded with100 120583lkg bw of the essential oil (Table 6)

4 Discussion

The present study revealed that feed intake live body weightand body weight gain were not significantly affected by theginger essential oil treatments over the 12-week period Thisobservation agreed with the findings of Dieumou et al [23]who recorded no significant differences in feed intake bodyweight gain and feed conversion ratio with 10 20 and40mgkg bw of ginger essential oil for seven consecutiveweeks in broilers The findings of Fakhim et al [5] alsorevealed no improvement in body weight gain of chickens fed

on ginger supplements compared to the control group Feedconversion ratio decreased nonsignificantly and linearly withthe increasing doses of essential oil compared to the controlThis effect could be explained by the various properties ofphenolic and flavonoid compounds of the ginger essential oilin the digestive system of the animal These bioactive com-pounds possess antimicrobial and antioxidant properties thatallow them to reduce the free radical and pathogenic micro-bersquos attacks and a better use of the nutrients in the digestivetract

The present study revealed that the oral administrationof essential oil whatever the dose increased significantly theserum content in total protein and globulin compared tothe control This result is consistent with the findings ofZhang et al [24] with 5 gkg of ginger rhizomes powder inbroiler feed The present results contradicted the findings ofmany other studies which recorded a significant decrease inserum protein and globulin levels in chickens fed on diet sup-plemented with ginger rhizomes powder [25 26] The differ-ences between these studies could be the result of differencein the doses used the shape of the plant (powder essentialoil etc) the route of administration and the experimentalconditions The increase in total protein and globulin maybe due to phenolic components including gingerol shogaolsgingerdiol gingerdione and some related phenolic ketonederivatives of ginger essential oil [4] which have powerfulantioxidant and immunostimulatory properties that allowthem to improve immune responses

Serum content in aspartate aminotransferase (AST) andalanine aminotransferase (ALT) significantly decreased inquails fed on ginger rhizomes essential whatever the dosecompared to the control birds These results are consistentwith the findings of Malekizadeh et al [27] who reporteda significant decrease in serum AST and ALT levels inHyline leghorns (W-36) fed on diet supplemented with3 ginger rhizome powder for 9 weeks The decrease in

6 Veterinary Medicine International

Table 6 Effects of graded levels of ginger essential oil on fertility rate and hatchability traits in Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Fertility () 8189 plusmn 491a 8214 plusmn 311a 9071 plusmn 490b 8854 plusmn 202b 001Hatchability of fertile eggs () 6500 plusmn 1401 7893 plusmn 653 8429 plusmn 1119 7250 plusmn 1509 018Total hatchability () 6071 plusmn 2143 7143 plusmn 1016 7857 plusmn 2736 6714 plusmn 1447 063Embryonic mortality () 1008 plusmn 223 948 plusmn 372 946 plusmn 119 966 plusmn 059 099Chickrsquos weight (g) 808 plusmn 104 817 plusmn 107 842 plusmn 122 833 plusmn 076 040abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails

the transaminases levels suggested that the doses of oiladministered were not toxic and regulated the liver activityof the quails According to Zounongo [28] an increase inserum transaminase levels indicates hepatic cytolysis In factthe weight of the liver in the present study tends to decreasein treated quails at the doses of 100 and 150 120583lkg bw

The malondialdehyde (MDA) as an indicator of lipidperoxidation and oxidative stress significantly decreased in alltreatments groups compared to the control The activities ofthe antioxidant enzymes (superoxide dismutase catalase andreduced glutathione) increased with the oral administrationof this essential oil in quails Antioxidant activity is one of themain defense systems of the body against the harmful effectsof reactive oxygen species in animals The antioxidant actionof ginger has been attributed to the protective actions ofginger bioactive substances against free radical attack [29 30]This antioxidant action of ginger essential oil subsequentlyreduced the lipid peroxidation responsible for apoptosis inspermatogenic cells Indeed the testicular histology in quailstreated with ginger rhizomes essential oil revealed structuralimprovements compared to the control birds that showedmild necrosis In accordance with this result Zancan etal [31] revealed that ginger has protective effects againstcisplatin-induced testicular damage and oxidative stress inanimals Shanoon [32] mentioned that the ginger rhizomesbioactive molecules improve testicular structure by increas-ing the thickness of the seminiferous tubules and the germcell membrane and consequently increase testicular weightviability and motility of the spermatozoa

All the above-mentioned properties contribute to thefertility of the quail treated with different doses of the gingerroots essential oil resulting in an increase in the fertility rateThe present results are consistent with the findings of Ezzatet al [33] in Cobb 500 parent broiler treated with gingerrhizome powder at the doses of 25 and 5 gkg of feed for14 weeks This elevating effect can be attributed to the gin-ger essential oil active compounds (alkaloids and terpenes)which improve the characteristics of the spermatozoa andconsequently make them more active in the female genitaltract According to Froman et al [34] a higher proportionof highly motile spermatozoa enter the sperm storage tubulesof female birds resulting in a high proportion of fertile eggsThe ginger rhizomes essential oil whatever the dose increasedthe hatching rate of fertile eggsThis effect could be related tosperm characteristics (membrane and DNA integrity viabil-ity andmobility) enhanced by the phenolic compounds of theessential oil Indeed the sperm cell membrane is particularly

rich in polyunsaturated fatty acid which predisposes themto lipid peroxidation by reactive oxygen species which isassociated withmale infertility [35] Large amounts of radicaloxygen species have been shown to interferewith the integrityof sperm DNA and thereby influence embryo development[36] The supplementation of the male bird diet with gingerrhizomes essential oil rich in antioxidant property couldreduce the impairment in sperm membrane and DNA Inaccordance with the present result Hoe et al [37] mentionedthat the ginger essential oil protects the DNA from oxidationby hydrogen peroxide and from the harmful effects of thereactive oxygen species This ginger essential oil activityconsequently increases the fertility and hatching rate andreduces the mortality rate The present results revealed apositive correlation between the fertility and the hatching rateof fertile eggs suggesting an improvement in this parameterwith the increasing rate of the fertility

5 Conclusion

The present results revealed that ginger rhizome essentialoil can be used in quails to reduce the lipid peroxidationin reproductive cells and promote fertility without adverseeffects on growth performances

Data Availability

Thedata sets used during the current study are available fromthe corresponding author on reasonable request

Conflicts of Interest

The authors certify that no conflicts of interest exist

References

[1] ldquoAssessment of the risks associated with the presence of myco-toxins in human and animal food chainsrdquoMaisons-Alfort 2009Federation Senegalaise des Societes drsquoAssurances (FSSA)

[2] F Alleman I Gabriel VDufourcq F Perrin and J-FGabarrouldquoEssential oils in poultry feeding 1 Growth performances andregulation aspectsrdquo Productions Animales vol 26 no 1 pp 3ndash12 2013

[3] C Wenk ldquoWhy all the discussion about herbs Biotechnolgyin the feed industryrdquo in Proceedings of the Alltechrsquos 16th AnnualSympsium Alltech Technical Puplications pp 79ndash96 Notting-ham Universty Press Nicholasville 2000

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

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Page 2: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

2 Veterinary Medicine International

Table 1 Phytochemical constituents of ginger essential oil

Constituents (+) present (minus) absentAlkaloids +Triterpenoid +Steroid minus

Flavonoid +Phenol +

immunomodulatory neuroprotective and hepatoprotectiveproperties [6] which can be used in animal farm to boostgrowth reduce oxidative stress and histological alteration invital organs and subsequently improve fertility In poultryproducing the maximum number of fertile eggs and viablechicks is a major concern The health of testes plays a centralrole in sperm fertilizing capability which is positively corre-lated to hatchability rate Testicularweight is highly correlatedto the physiological reproductive status in poultry breeders[7] A direct relationship has been established betweensperm production and testes weight in boiler breeders [8]Ferrouk et al [9] reported that testicular size is the primaryendpoint for spermatogenesis since seminiferous tubules andgerminal elements take about 98 of the total testismassThebeneficial effects of ginger powder in poultry growth perfor-mances egg production and quality carcass traits and bloodbiochemistry parameters can be attributed to the phenolicsand flavonoids compounds present [5 10] However up tonow few studies have been designed to assess the efficiencyof these actives compounds on poultry reproduction

The objective of this study was to find out the effectsof graded levels of ginger roots essential oil on growth andreproductive performances in male Japanese quail

2 Materials and Methods

21 Study Area This study was carried out at the poultryunit in the Teaching and Research Farm of the Universityof Dschang Cameroon This farm is located at 5∘261015840 northand 10∘261015840 EST and at an altitude of 1420m above sea levelAnnual temperature varies between 10∘C and 25∘C Rainfallranges from 1500 to 2000mm per annum over a 9-monthrainy season (March to November)

22 Origin of Essential Oil Fresh ginger rhizomes wereharvested from Santchou (LN 5∘1610158405510158401015840 LE 9∘5810158402710158401015840) in theMenoua division West Region of Cameroon Oil extractionwas done by hydrodistillation in PYTORICA LaboratoryBonapriso Douala Cameroon as described by Wang andWeller [11]

23 Phytochemical Screening of Essential Oil The phyto-chemical screening of essential oil (Table 1) was done asdescribed by Banso and Ngbede [12] and Ngbede et al [13]

24 Animals and Experimental Design Ninety-six 3-week-old male Japanese quail (Coturnix coturnix japonica) weigh-ing between 120 and 130 g produced from a parent stockin the Teaching and Research Farm of the University of

Table 2 Composition of the experimental diet

Ingredients Amount (kg100 kg)Maize 60Wheat bran 45Soybean meal 22Fishmeal 45Oeister shell 2Bone meal 2Premix 5lowast 5Total 100Calculated chemical compositionCrude protein () 2015Metabolizable energy (KcalKg) 290680Calcium () 203Phosphorus () 127Lysine () 044Methionine () 014Sodium () 022lowastPremix 5 mixture of vitamins A B complex D K and E

Dschang were used for testing Each quail was identified bya ring bearing his number in one of its paws

At the beginning of the experiment quails were weighedand randomly assigned to 4 dietary treatment groups in acompletely randomized design Each group was divided into4 subgroups of 6 quails Quails in control group receivedorally 100 120583lkg bw of distilled water while birds in theother three test groups during the same period respectivelyreceived by gastric intubation 50 100 and 150120583lkg bodyweight of essential oil At 12 weeks old twelve birds pertreatment were randomly selected and slaughtered for organscharacteristics assessment and blood samples were collectedfor biochemical analysis At the same period 4 male quailsper treatmentwith hypertrophy of cloacal glandwere selectedand individually housed in the same cage with four untreatedfemales and reared under the same conditions for fertilityhatchability traits and chick weight assessment During theexperimental period feed (Table 2) and water were offeredad libitum to quail in adapted equipment

This study was carried out in strict accordance withrecommendations of institutional guidelines for the care anduse of laboratory animals Quails were humanly handledwith respect to the ethical standards laid down in the 1964Declaration of Helsinki and its later amendments

25 Growth Characteristics Feed intake and life body weightfor individual quail were recorded weekly body weight gainwas obtained by the difference in life body weight of twoconsecutive weeks according to the procedures of McDonaldet al [14] Feed conversion ratio was obtained by dividingweekly feed intake by weekly body weight gain

26 Blood Sampling and Organ Weights At the end of theexperiment 12 quails per treatment were randomly selectedand fasted for 24 hours weighed and slaughtered as des-cribed by Jourdain [15] Blood samples were collected from

Veterinary Medicine International 3

the jugular vein in nonheparinized tubes the serum isolatedwas stored at minus20∘C for biochemical analysis

Testes and liver of slaughtered quails were carefullyremoved rid of adipose tissue blotted dry and weighedseparately using a scale of 160 g capacity and 10minus3 g precisionThe relative organ weight was calculated as follows

Relative organ weight ()

=Organ weight (mg)Live body weight (g)

times 100(1)

The left testis was homogenized in a known volume of cold09 NaCl followed by a centrifugation (3000 rpm 30min)and the resultant supernatants were subsequently stored atminus20∘C for antioxidant status assessment

27 Biochemical Analysis Serum content in proteins wasdetermined by Biuret method [16] Alanine aminotransferase(ALT) and aspartate aminotransferase (AST) contents wereevaluated by the enzymatic analysis method using commer-cial kits CHRONOLAB Ref 101-0255 and CHRONOLABRef 101-0256 respectively Total cholesterol and triglycerideswere determined by colorimetric methods using commercialkits CHRONOLAB Ref 101-0576 and CHRONOLAB Ref101-0241 respectively Total globulins were calculated asdescribed by Abdel-Fattah et al [17]

28 Oxidative Stress Characteristics The malondialdehydeconcentration was evaluated by the thiobarbituric acidmethod [18] Superoxide dismutase (SOD) catalase (CAT)and reduced glutathione (GSH) activities were evaluatedas described by Misra and Fridovich [19] Sinha [20] andEllman and Fiches [21] respectively

29Histology Histological screening of testeswas carried outas described by Wolfang [22] for organ or tissues Brieflythe right testis was fixed by immersion in Bouin solutionfor 1 week and then washed dehydrated in ascending gradealcohol bath clarified in xylene immersion and embeddedin paraffin Sections of 5120583m were stained with hematoxylin-eosin for histological observations under a light microscope(400x)

210 Fertility and Hatchability Traits A total of 56 eggs pergroup were collected during 8 days weighted individuallyand incubated After artificial incubation for 19 days allunhatched eggs were cracked and classified as infertile orembryonic mortalityThe fertility rate was then calculated bydividing the number of fertile eggs over the total number ofeggs incubated The individual chickrsquos weight was obtainedby dividing the total chickrsquos weight over the number of chickshatch per group

211 Statistical Analysis The statistical analysis was carriedout using the SPSS 200 software Results were expressed asmean plusmn standard deviation Differences between groups wereassessed using one-way ANOVA followed by Duncan posthoc test with the significance level set at 005 119875 value wasdone using the Studentrsquos 119905-test A 119875 value of less than 005 was

considered as significantThe normality of data was tested bythe Shapiro-Wilk Test and the relationships between differentparameters were highlighted by the correlation coefficient ofBravais-Pearson

3 Results

31 Growth Characteristics As shown in Table 3 feed intakelive body weight body weight gain and feed conversion ratio(FCR) were not significantly affected (119875 gt 005) by the dosesof essential oil used However the values of these growthcharacteristics tend to decrease in treated quails compared tothe quails in control group

32 Organs Weight The relative weight of the left testisincreased significantly (119875 lt 005) in quails treatedwith essen-tial oil at 100 and 150120583lkg bw compared to quails in thecontrol group and quails fed on the smallest dose of essentialoil (50 120583lkg bw) The relative weight of the right testis intreated quails was comparable (119875 gt 005) to that of the quailsin the control group although this weight tended to increasein birds treated with 100 and 150 120583lkg of bw (Table 3)

The relative weight of the liver recorded in quails treatedwith oil whatever the dose was comparable (119875 gt 005) to thatof the quails in the control group However this weight tendsto decrease with 100 and 150 120583lkg bw compared to the weightof liver recorded in the control group and quails fed on thesmallest dose of the essential oil (50120583lkg of bw) (Table 3)

33 Serum Biochemical Parameters The ginger essential oilwhatever the dose induced a significant increase (119875 lt 005)in protein and globulin serum contents compared to thecontrol However the serum contents in protein and globulinrecorded with 100 and 150 120583lkg bwwere comparable and sig-nificantly higher (119875 lt 005) relative to the quantity recordedin quails treated with the lowest dose of this essential oil(50 120583lkg bw) (Table 4) The alanine aminotransferase (ALT)activity decreased significantly (119875 lt 005) in quails treatedwith essential oil whatever the dose compared to the controlgroup Although statistically comparable the activity of ALTtends to decrease in quails treated with 150 120583lkg bw ascompared to 50 and 100120583lkg bw The oral administration ofginger essential oil induced a decrease in aspartate amino-transferase (AST) activity relative to the control Howeverthis decreasewas significant onlywith 150120583lkg bw comparedto other essential oil dosesThe serum content in total choles-terol decreased significantly (119875 lt 005) and linearly withthe increasing doses of the essential oil relative to the con-trol Essential oil significantly (119875 lt 005) decreases triglyc-eride content compared to the control (Table 4)

34 Antioxidant Status The malondialdehyde (MDA) levelin the treated quails decreased significantly (119875 lt 005) andlinearly with the increasing doses of the essential oil com-pared to the control group The oral administration of theessential oil induced an increase in superoxide dismutase(SOD) activity relative to the control However this increasewas significant only with 150120583lkg bw compared to all otherdoses (Table 4) The glutathione (GSH) activities in quails

4 Veterinary Medicine International

ICSPZ

N

N

IC0

ST

IC

IC

150100

50

L

LL

ST

ST

SPZ

Figure 1 Histological structure of Japanese quail testes as affected by ginger roots essential oil (400x) 0 (control) 50 100 and 150 doses ofginger roots essential oil (120583lkg body weight) SPZ spermatozoa ST seminiferous tubules IC interstitial cells L lumen and N necrosis

Table 3 Effects of graded level of ginger roots essential oil on growth characteristics and relative organ weightsof male Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Growth characteristicsFeed intake (g) 907 plusmn 4354 91013 plusmn 4819 85763 plusmn 4783 88915 plusmn 3775 017Live body weight (g) 20927 plusmn1502 20745 plusmn 2490 20427 plusmn 1527 20225 plusmn 1772 080Body weight gain (g) 22529 plusmn 4675 22786 plusmn 3798 21943 plusmn 4659 23314 plusmn 4547 095FCR 598 plusmn 207 579 plusmn 179 511 plusmn 069 463 plusmn 089 039Organ weights (g100 g bw)Liver 155 plusmn 033 157 plusmn 029 146 plusmn 039 147 plusmn 036 085Pair of testes 201 plusmn 048a 208 plusmn 016a 263 plusmn 021b 254 plusmn 032b 001Right testis 100 plusmn 024 104 plusmn 016 118 plusmn 023 114 plusmn 022 056Left testis 101 plusmn 026a 105 plusmn 017a 146 plusmn 007b 141 plusmn 033b 001abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails FCR = feed conversion ratio

treated with essential oil at 100 and 150120583lkg bw werecomparable and significantly (119875 lt 005) higher than activitiesrecorded in control group and the group of quails treatedwith50 120583lkg bw The catalase (CAT) activities were comparablewith 100 and 150120583lkg bw but significantly higher (119875 lt 005)than CAT activity recorded in the control group (Table 4)

35 Histological Structure of the Testes The testes of thequails in the control group showed slight alterations of theseminiferous tubules with necrosis The oral administrationof the essential oil whatever the dose improved the histo-logical structure of the testes compared to the control Thehistological changes observed in the testes of the treatedquails whatever the dose were almost identical (Figure 1)

36 Fertility and Hatchability Traits The fertility rate ofquails treated with the essential oil except the lowest dose(50 120583lkg bw) significantly increased (119875 lt 005) compared tothe control group However the fertility rate of quails treatedwith 100 120583lkg bw is comparable to the fertility of quailstreated with the highest dose of essential oil (150 120583lkg bw)The relative weight of the testes is positively and significantlycorrelated to the fertility rate (120588 = +099 119875 lt 001) the sameobservation was made between GSH and the fertility rate (120588= +095 119875 lt 005) (Table 5)

The oral administration of ginger rhizome essential oil atthe entire used dose tends to increase the hatching rate offertile eggs and the total hatch rate compared to the control(Table 6) However the highest fertile egg hatched and total

Veterinary Medicine International 5

Table 4 Effects of graded levels of ginger essential oil on serum biochemical and testes oxidative stress characteristics

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Serum metabolitesSerum proteins (gdl) 206 plusmn 004a 238 plusmn 019b 266 plusmn 019c 270 plusmn 035c 000Globulins (gdl) 016 plusmn 005a 031 plusmn 006b 049 plusmn 007c 048 plusmn 016c 000AST (UL) 16800 plusmn 2024b 14624 plusmn 1511ab 16324 plusmn 1129ab 13749 plusmn 1688a 000ALT (UL) 5750 plusmn 1049b 4285 plusmn 346a 4000 plusmn 1014a 3343 plusmn 607a 000Total cholesterol (mgdl) 12727 plusmn 798d 11809 plusmn 541c 11006 plusmn 583b 10027 plusmn 198a 000Triglycerides (mgdl) 7346 plusmn 1039b 5718 plusmn 443a 5691 plusmn 649a 5607 plusmn 616a 000Testes oxidative stress (gram of tissue)MDA 9779 plusmn 960c 8220 plusmn 993b 5249 plusmn 839a 5057 plusmn 1783a 000SOD 292 plusmn 048a 347 plusmn 033a 344 plusmn 055a 408 plusmn 023b 000GSH 18373 plusmn 3515a 20147 plusmn 1774a 26507 plusmn 4825b 27402 plusmn 5416b 000CAT 282 plusmn 031a 336 plusmn 073ab 378 plusmn 063b 360 plusmn 089b 004abcdOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails MDA = malondialdehyde GSH = reducedglutathione CAT = catalase SOD = superoxide dismutase AST = aspartate aminotransferase ALT = alanine aminotransferase values are presented as meansplusmn standard deviation

Table 5 Correlations between testes weight GSH sperm motilitytotal hatch and fertility rate

Parameters Pair of testesrelative weight Fertility rate Total hatch rate

Fertility rate 099lowastlowast - 065Sperm motility 099lowast 099lowastlowast -GSH 098lowast 095lowast -lowastThe correlation is significant at the 005 level lowastlowastThe correlation is signifi-cant at the 001 level

hatch rates were recorded in quails treated with 100 120583lkgbw A positive and nonsignificant correlation was recordedbetween the fertility rate and the total hatch rate (120588 = +065119875 gt 005) (Table 5)

The embryonic mortality rate was not significantlyaffected (119875 gt 005) by the doses of the essential oil usedHow-ever it tends to decrease with essential oil whatever the dosecompared to the controlThe lowest embryonicmortality ratewas recorded in quails treated with 100 120583lkg bw The gingeressential oil whatever the dose induced a nonsignificant(119875 gt 005) increase in chickrsquos weight compared to the con-trol However the highest chick weight was recorded with100 120583lkg bw of the essential oil (Table 6)

4 Discussion

The present study revealed that feed intake live body weightand body weight gain were not significantly affected by theginger essential oil treatments over the 12-week period Thisobservation agreed with the findings of Dieumou et al [23]who recorded no significant differences in feed intake bodyweight gain and feed conversion ratio with 10 20 and40mgkg bw of ginger essential oil for seven consecutiveweeks in broilers The findings of Fakhim et al [5] alsorevealed no improvement in body weight gain of chickens fed

on ginger supplements compared to the control group Feedconversion ratio decreased nonsignificantly and linearly withthe increasing doses of essential oil compared to the controlThis effect could be explained by the various properties ofphenolic and flavonoid compounds of the ginger essential oilin the digestive system of the animal These bioactive com-pounds possess antimicrobial and antioxidant properties thatallow them to reduce the free radical and pathogenic micro-bersquos attacks and a better use of the nutrients in the digestivetract

The present study revealed that the oral administrationof essential oil whatever the dose increased significantly theserum content in total protein and globulin compared tothe control This result is consistent with the findings ofZhang et al [24] with 5 gkg of ginger rhizomes powder inbroiler feed The present results contradicted the findings ofmany other studies which recorded a significant decrease inserum protein and globulin levels in chickens fed on diet sup-plemented with ginger rhizomes powder [25 26] The differ-ences between these studies could be the result of differencein the doses used the shape of the plant (powder essentialoil etc) the route of administration and the experimentalconditions The increase in total protein and globulin maybe due to phenolic components including gingerol shogaolsgingerdiol gingerdione and some related phenolic ketonederivatives of ginger essential oil [4] which have powerfulantioxidant and immunostimulatory properties that allowthem to improve immune responses

Serum content in aspartate aminotransferase (AST) andalanine aminotransferase (ALT) significantly decreased inquails fed on ginger rhizomes essential whatever the dosecompared to the control birds These results are consistentwith the findings of Malekizadeh et al [27] who reporteda significant decrease in serum AST and ALT levels inHyline leghorns (W-36) fed on diet supplemented with3 ginger rhizome powder for 9 weeks The decrease in

6 Veterinary Medicine International

Table 6 Effects of graded levels of ginger essential oil on fertility rate and hatchability traits in Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Fertility () 8189 plusmn 491a 8214 plusmn 311a 9071 plusmn 490b 8854 plusmn 202b 001Hatchability of fertile eggs () 6500 plusmn 1401 7893 plusmn 653 8429 plusmn 1119 7250 plusmn 1509 018Total hatchability () 6071 plusmn 2143 7143 plusmn 1016 7857 plusmn 2736 6714 plusmn 1447 063Embryonic mortality () 1008 plusmn 223 948 plusmn 372 946 plusmn 119 966 plusmn 059 099Chickrsquos weight (g) 808 plusmn 104 817 plusmn 107 842 plusmn 122 833 plusmn 076 040abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails

the transaminases levels suggested that the doses of oiladministered were not toxic and regulated the liver activityof the quails According to Zounongo [28] an increase inserum transaminase levels indicates hepatic cytolysis In factthe weight of the liver in the present study tends to decreasein treated quails at the doses of 100 and 150 120583lkg bw

The malondialdehyde (MDA) as an indicator of lipidperoxidation and oxidative stress significantly decreased in alltreatments groups compared to the control The activities ofthe antioxidant enzymes (superoxide dismutase catalase andreduced glutathione) increased with the oral administrationof this essential oil in quails Antioxidant activity is one of themain defense systems of the body against the harmful effectsof reactive oxygen species in animals The antioxidant actionof ginger has been attributed to the protective actions ofginger bioactive substances against free radical attack [29 30]This antioxidant action of ginger essential oil subsequentlyreduced the lipid peroxidation responsible for apoptosis inspermatogenic cells Indeed the testicular histology in quailstreated with ginger rhizomes essential oil revealed structuralimprovements compared to the control birds that showedmild necrosis In accordance with this result Zancan etal [31] revealed that ginger has protective effects againstcisplatin-induced testicular damage and oxidative stress inanimals Shanoon [32] mentioned that the ginger rhizomesbioactive molecules improve testicular structure by increas-ing the thickness of the seminiferous tubules and the germcell membrane and consequently increase testicular weightviability and motility of the spermatozoa

All the above-mentioned properties contribute to thefertility of the quail treated with different doses of the gingerroots essential oil resulting in an increase in the fertility rateThe present results are consistent with the findings of Ezzatet al [33] in Cobb 500 parent broiler treated with gingerrhizome powder at the doses of 25 and 5 gkg of feed for14 weeks This elevating effect can be attributed to the gin-ger essential oil active compounds (alkaloids and terpenes)which improve the characteristics of the spermatozoa andconsequently make them more active in the female genitaltract According to Froman et al [34] a higher proportionof highly motile spermatozoa enter the sperm storage tubulesof female birds resulting in a high proportion of fertile eggsThe ginger rhizomes essential oil whatever the dose increasedthe hatching rate of fertile eggsThis effect could be related tosperm characteristics (membrane and DNA integrity viabil-ity andmobility) enhanced by the phenolic compounds of theessential oil Indeed the sperm cell membrane is particularly

rich in polyunsaturated fatty acid which predisposes themto lipid peroxidation by reactive oxygen species which isassociated withmale infertility [35] Large amounts of radicaloxygen species have been shown to interferewith the integrityof sperm DNA and thereby influence embryo development[36] The supplementation of the male bird diet with gingerrhizomes essential oil rich in antioxidant property couldreduce the impairment in sperm membrane and DNA Inaccordance with the present result Hoe et al [37] mentionedthat the ginger essential oil protects the DNA from oxidationby hydrogen peroxide and from the harmful effects of thereactive oxygen species This ginger essential oil activityconsequently increases the fertility and hatching rate andreduces the mortality rate The present results revealed apositive correlation between the fertility and the hatching rateof fertile eggs suggesting an improvement in this parameterwith the increasing rate of the fertility

5 Conclusion

The present results revealed that ginger rhizome essentialoil can be used in quails to reduce the lipid peroxidationin reproductive cells and promote fertility without adverseeffects on growth performances

Data Availability

Thedata sets used during the current study are available fromthe corresponding author on reasonable request

Conflicts of Interest

The authors certify that no conflicts of interest exist

References

[1] ldquoAssessment of the risks associated with the presence of myco-toxins in human and animal food chainsrdquoMaisons-Alfort 2009Federation Senegalaise des Societes drsquoAssurances (FSSA)

[2] F Alleman I Gabriel VDufourcq F Perrin and J-FGabarrouldquoEssential oils in poultry feeding 1 Growth performances andregulation aspectsrdquo Productions Animales vol 26 no 1 pp 3ndash12 2013

[3] C Wenk ldquoWhy all the discussion about herbs Biotechnolgyin the feed industryrdquo in Proceedings of the Alltechrsquos 16th AnnualSympsium Alltech Technical Puplications pp 79ndash96 Notting-ham Universty Press Nicholasville 2000

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

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Submit your manuscripts atwwwhindawicom

Page 3: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

Veterinary Medicine International 3

the jugular vein in nonheparinized tubes the serum isolatedwas stored at minus20∘C for biochemical analysis

Testes and liver of slaughtered quails were carefullyremoved rid of adipose tissue blotted dry and weighedseparately using a scale of 160 g capacity and 10minus3 g precisionThe relative organ weight was calculated as follows

Relative organ weight ()

=Organ weight (mg)Live body weight (g)

times 100(1)

The left testis was homogenized in a known volume of cold09 NaCl followed by a centrifugation (3000 rpm 30min)and the resultant supernatants were subsequently stored atminus20∘C for antioxidant status assessment

27 Biochemical Analysis Serum content in proteins wasdetermined by Biuret method [16] Alanine aminotransferase(ALT) and aspartate aminotransferase (AST) contents wereevaluated by the enzymatic analysis method using commer-cial kits CHRONOLAB Ref 101-0255 and CHRONOLABRef 101-0256 respectively Total cholesterol and triglycerideswere determined by colorimetric methods using commercialkits CHRONOLAB Ref 101-0576 and CHRONOLAB Ref101-0241 respectively Total globulins were calculated asdescribed by Abdel-Fattah et al [17]

28 Oxidative Stress Characteristics The malondialdehydeconcentration was evaluated by the thiobarbituric acidmethod [18] Superoxide dismutase (SOD) catalase (CAT)and reduced glutathione (GSH) activities were evaluatedas described by Misra and Fridovich [19] Sinha [20] andEllman and Fiches [21] respectively

29Histology Histological screening of testeswas carried outas described by Wolfang [22] for organ or tissues Brieflythe right testis was fixed by immersion in Bouin solutionfor 1 week and then washed dehydrated in ascending gradealcohol bath clarified in xylene immersion and embeddedin paraffin Sections of 5120583m were stained with hematoxylin-eosin for histological observations under a light microscope(400x)

210 Fertility and Hatchability Traits A total of 56 eggs pergroup were collected during 8 days weighted individuallyand incubated After artificial incubation for 19 days allunhatched eggs were cracked and classified as infertile orembryonic mortalityThe fertility rate was then calculated bydividing the number of fertile eggs over the total number ofeggs incubated The individual chickrsquos weight was obtainedby dividing the total chickrsquos weight over the number of chickshatch per group

211 Statistical Analysis The statistical analysis was carriedout using the SPSS 200 software Results were expressed asmean plusmn standard deviation Differences between groups wereassessed using one-way ANOVA followed by Duncan posthoc test with the significance level set at 005 119875 value wasdone using the Studentrsquos 119905-test A 119875 value of less than 005 was

considered as significantThe normality of data was tested bythe Shapiro-Wilk Test and the relationships between differentparameters were highlighted by the correlation coefficient ofBravais-Pearson

3 Results

31 Growth Characteristics As shown in Table 3 feed intakelive body weight body weight gain and feed conversion ratio(FCR) were not significantly affected (119875 gt 005) by the dosesof essential oil used However the values of these growthcharacteristics tend to decrease in treated quails compared tothe quails in control group

32 Organs Weight The relative weight of the left testisincreased significantly (119875 lt 005) in quails treatedwith essen-tial oil at 100 and 150120583lkg bw compared to quails in thecontrol group and quails fed on the smallest dose of essentialoil (50 120583lkg bw) The relative weight of the right testis intreated quails was comparable (119875 gt 005) to that of the quailsin the control group although this weight tended to increasein birds treated with 100 and 150 120583lkg of bw (Table 3)

The relative weight of the liver recorded in quails treatedwith oil whatever the dose was comparable (119875 gt 005) to thatof the quails in the control group However this weight tendsto decrease with 100 and 150 120583lkg bw compared to the weightof liver recorded in the control group and quails fed on thesmallest dose of the essential oil (50120583lkg of bw) (Table 3)

33 Serum Biochemical Parameters The ginger essential oilwhatever the dose induced a significant increase (119875 lt 005)in protein and globulin serum contents compared to thecontrol However the serum contents in protein and globulinrecorded with 100 and 150 120583lkg bwwere comparable and sig-nificantly higher (119875 lt 005) relative to the quantity recordedin quails treated with the lowest dose of this essential oil(50 120583lkg bw) (Table 4) The alanine aminotransferase (ALT)activity decreased significantly (119875 lt 005) in quails treatedwith essential oil whatever the dose compared to the controlgroup Although statistically comparable the activity of ALTtends to decrease in quails treated with 150 120583lkg bw ascompared to 50 and 100120583lkg bw The oral administration ofginger essential oil induced a decrease in aspartate amino-transferase (AST) activity relative to the control Howeverthis decreasewas significant onlywith 150120583lkg bw comparedto other essential oil dosesThe serum content in total choles-terol decreased significantly (119875 lt 005) and linearly withthe increasing doses of the essential oil relative to the con-trol Essential oil significantly (119875 lt 005) decreases triglyc-eride content compared to the control (Table 4)

34 Antioxidant Status The malondialdehyde (MDA) levelin the treated quails decreased significantly (119875 lt 005) andlinearly with the increasing doses of the essential oil com-pared to the control group The oral administration of theessential oil induced an increase in superoxide dismutase(SOD) activity relative to the control However this increasewas significant only with 150120583lkg bw compared to all otherdoses (Table 4) The glutathione (GSH) activities in quails

4 Veterinary Medicine International

ICSPZ

N

N

IC0

ST

IC

IC

150100

50

L

LL

ST

ST

SPZ

Figure 1 Histological structure of Japanese quail testes as affected by ginger roots essential oil (400x) 0 (control) 50 100 and 150 doses ofginger roots essential oil (120583lkg body weight) SPZ spermatozoa ST seminiferous tubules IC interstitial cells L lumen and N necrosis

Table 3 Effects of graded level of ginger roots essential oil on growth characteristics and relative organ weightsof male Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Growth characteristicsFeed intake (g) 907 plusmn 4354 91013 plusmn 4819 85763 plusmn 4783 88915 plusmn 3775 017Live body weight (g) 20927 plusmn1502 20745 plusmn 2490 20427 plusmn 1527 20225 plusmn 1772 080Body weight gain (g) 22529 plusmn 4675 22786 plusmn 3798 21943 plusmn 4659 23314 plusmn 4547 095FCR 598 plusmn 207 579 plusmn 179 511 plusmn 069 463 plusmn 089 039Organ weights (g100 g bw)Liver 155 plusmn 033 157 plusmn 029 146 plusmn 039 147 plusmn 036 085Pair of testes 201 plusmn 048a 208 plusmn 016a 263 plusmn 021b 254 plusmn 032b 001Right testis 100 plusmn 024 104 plusmn 016 118 plusmn 023 114 plusmn 022 056Left testis 101 plusmn 026a 105 plusmn 017a 146 plusmn 007b 141 plusmn 033b 001abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails FCR = feed conversion ratio

treated with essential oil at 100 and 150120583lkg bw werecomparable and significantly (119875 lt 005) higher than activitiesrecorded in control group and the group of quails treatedwith50 120583lkg bw The catalase (CAT) activities were comparablewith 100 and 150120583lkg bw but significantly higher (119875 lt 005)than CAT activity recorded in the control group (Table 4)

35 Histological Structure of the Testes The testes of thequails in the control group showed slight alterations of theseminiferous tubules with necrosis The oral administrationof the essential oil whatever the dose improved the histo-logical structure of the testes compared to the control Thehistological changes observed in the testes of the treatedquails whatever the dose were almost identical (Figure 1)

36 Fertility and Hatchability Traits The fertility rate ofquails treated with the essential oil except the lowest dose(50 120583lkg bw) significantly increased (119875 lt 005) compared tothe control group However the fertility rate of quails treatedwith 100 120583lkg bw is comparable to the fertility of quailstreated with the highest dose of essential oil (150 120583lkg bw)The relative weight of the testes is positively and significantlycorrelated to the fertility rate (120588 = +099 119875 lt 001) the sameobservation was made between GSH and the fertility rate (120588= +095 119875 lt 005) (Table 5)

The oral administration of ginger rhizome essential oil atthe entire used dose tends to increase the hatching rate offertile eggs and the total hatch rate compared to the control(Table 6) However the highest fertile egg hatched and total

Veterinary Medicine International 5

Table 4 Effects of graded levels of ginger essential oil on serum biochemical and testes oxidative stress characteristics

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Serum metabolitesSerum proteins (gdl) 206 plusmn 004a 238 plusmn 019b 266 plusmn 019c 270 plusmn 035c 000Globulins (gdl) 016 plusmn 005a 031 plusmn 006b 049 plusmn 007c 048 plusmn 016c 000AST (UL) 16800 plusmn 2024b 14624 plusmn 1511ab 16324 plusmn 1129ab 13749 plusmn 1688a 000ALT (UL) 5750 plusmn 1049b 4285 plusmn 346a 4000 plusmn 1014a 3343 plusmn 607a 000Total cholesterol (mgdl) 12727 plusmn 798d 11809 plusmn 541c 11006 plusmn 583b 10027 plusmn 198a 000Triglycerides (mgdl) 7346 plusmn 1039b 5718 plusmn 443a 5691 plusmn 649a 5607 plusmn 616a 000Testes oxidative stress (gram of tissue)MDA 9779 plusmn 960c 8220 plusmn 993b 5249 plusmn 839a 5057 plusmn 1783a 000SOD 292 plusmn 048a 347 plusmn 033a 344 plusmn 055a 408 plusmn 023b 000GSH 18373 plusmn 3515a 20147 plusmn 1774a 26507 plusmn 4825b 27402 plusmn 5416b 000CAT 282 plusmn 031a 336 plusmn 073ab 378 plusmn 063b 360 plusmn 089b 004abcdOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails MDA = malondialdehyde GSH = reducedglutathione CAT = catalase SOD = superoxide dismutase AST = aspartate aminotransferase ALT = alanine aminotransferase values are presented as meansplusmn standard deviation

Table 5 Correlations between testes weight GSH sperm motilitytotal hatch and fertility rate

Parameters Pair of testesrelative weight Fertility rate Total hatch rate

Fertility rate 099lowastlowast - 065Sperm motility 099lowast 099lowastlowast -GSH 098lowast 095lowast -lowastThe correlation is significant at the 005 level lowastlowastThe correlation is signifi-cant at the 001 level

hatch rates were recorded in quails treated with 100 120583lkgbw A positive and nonsignificant correlation was recordedbetween the fertility rate and the total hatch rate (120588 = +065119875 gt 005) (Table 5)

The embryonic mortality rate was not significantlyaffected (119875 gt 005) by the doses of the essential oil usedHow-ever it tends to decrease with essential oil whatever the dosecompared to the controlThe lowest embryonicmortality ratewas recorded in quails treated with 100 120583lkg bw The gingeressential oil whatever the dose induced a nonsignificant(119875 gt 005) increase in chickrsquos weight compared to the con-trol However the highest chick weight was recorded with100 120583lkg bw of the essential oil (Table 6)

4 Discussion

The present study revealed that feed intake live body weightand body weight gain were not significantly affected by theginger essential oil treatments over the 12-week period Thisobservation agreed with the findings of Dieumou et al [23]who recorded no significant differences in feed intake bodyweight gain and feed conversion ratio with 10 20 and40mgkg bw of ginger essential oil for seven consecutiveweeks in broilers The findings of Fakhim et al [5] alsorevealed no improvement in body weight gain of chickens fed

on ginger supplements compared to the control group Feedconversion ratio decreased nonsignificantly and linearly withthe increasing doses of essential oil compared to the controlThis effect could be explained by the various properties ofphenolic and flavonoid compounds of the ginger essential oilin the digestive system of the animal These bioactive com-pounds possess antimicrobial and antioxidant properties thatallow them to reduce the free radical and pathogenic micro-bersquos attacks and a better use of the nutrients in the digestivetract

The present study revealed that the oral administrationof essential oil whatever the dose increased significantly theserum content in total protein and globulin compared tothe control This result is consistent with the findings ofZhang et al [24] with 5 gkg of ginger rhizomes powder inbroiler feed The present results contradicted the findings ofmany other studies which recorded a significant decrease inserum protein and globulin levels in chickens fed on diet sup-plemented with ginger rhizomes powder [25 26] The differ-ences between these studies could be the result of differencein the doses used the shape of the plant (powder essentialoil etc) the route of administration and the experimentalconditions The increase in total protein and globulin maybe due to phenolic components including gingerol shogaolsgingerdiol gingerdione and some related phenolic ketonederivatives of ginger essential oil [4] which have powerfulantioxidant and immunostimulatory properties that allowthem to improve immune responses

Serum content in aspartate aminotransferase (AST) andalanine aminotransferase (ALT) significantly decreased inquails fed on ginger rhizomes essential whatever the dosecompared to the control birds These results are consistentwith the findings of Malekizadeh et al [27] who reporteda significant decrease in serum AST and ALT levels inHyline leghorns (W-36) fed on diet supplemented with3 ginger rhizome powder for 9 weeks The decrease in

6 Veterinary Medicine International

Table 6 Effects of graded levels of ginger essential oil on fertility rate and hatchability traits in Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Fertility () 8189 plusmn 491a 8214 plusmn 311a 9071 plusmn 490b 8854 plusmn 202b 001Hatchability of fertile eggs () 6500 plusmn 1401 7893 plusmn 653 8429 plusmn 1119 7250 plusmn 1509 018Total hatchability () 6071 plusmn 2143 7143 plusmn 1016 7857 plusmn 2736 6714 plusmn 1447 063Embryonic mortality () 1008 plusmn 223 948 plusmn 372 946 plusmn 119 966 plusmn 059 099Chickrsquos weight (g) 808 plusmn 104 817 plusmn 107 842 plusmn 122 833 plusmn 076 040abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails

the transaminases levels suggested that the doses of oiladministered were not toxic and regulated the liver activityof the quails According to Zounongo [28] an increase inserum transaminase levels indicates hepatic cytolysis In factthe weight of the liver in the present study tends to decreasein treated quails at the doses of 100 and 150 120583lkg bw

The malondialdehyde (MDA) as an indicator of lipidperoxidation and oxidative stress significantly decreased in alltreatments groups compared to the control The activities ofthe antioxidant enzymes (superoxide dismutase catalase andreduced glutathione) increased with the oral administrationof this essential oil in quails Antioxidant activity is one of themain defense systems of the body against the harmful effectsof reactive oxygen species in animals The antioxidant actionof ginger has been attributed to the protective actions ofginger bioactive substances against free radical attack [29 30]This antioxidant action of ginger essential oil subsequentlyreduced the lipid peroxidation responsible for apoptosis inspermatogenic cells Indeed the testicular histology in quailstreated with ginger rhizomes essential oil revealed structuralimprovements compared to the control birds that showedmild necrosis In accordance with this result Zancan etal [31] revealed that ginger has protective effects againstcisplatin-induced testicular damage and oxidative stress inanimals Shanoon [32] mentioned that the ginger rhizomesbioactive molecules improve testicular structure by increas-ing the thickness of the seminiferous tubules and the germcell membrane and consequently increase testicular weightviability and motility of the spermatozoa

All the above-mentioned properties contribute to thefertility of the quail treated with different doses of the gingerroots essential oil resulting in an increase in the fertility rateThe present results are consistent with the findings of Ezzatet al [33] in Cobb 500 parent broiler treated with gingerrhizome powder at the doses of 25 and 5 gkg of feed for14 weeks This elevating effect can be attributed to the gin-ger essential oil active compounds (alkaloids and terpenes)which improve the characteristics of the spermatozoa andconsequently make them more active in the female genitaltract According to Froman et al [34] a higher proportionof highly motile spermatozoa enter the sperm storage tubulesof female birds resulting in a high proportion of fertile eggsThe ginger rhizomes essential oil whatever the dose increasedthe hatching rate of fertile eggsThis effect could be related tosperm characteristics (membrane and DNA integrity viabil-ity andmobility) enhanced by the phenolic compounds of theessential oil Indeed the sperm cell membrane is particularly

rich in polyunsaturated fatty acid which predisposes themto lipid peroxidation by reactive oxygen species which isassociated withmale infertility [35] Large amounts of radicaloxygen species have been shown to interferewith the integrityof sperm DNA and thereby influence embryo development[36] The supplementation of the male bird diet with gingerrhizomes essential oil rich in antioxidant property couldreduce the impairment in sperm membrane and DNA Inaccordance with the present result Hoe et al [37] mentionedthat the ginger essential oil protects the DNA from oxidationby hydrogen peroxide and from the harmful effects of thereactive oxygen species This ginger essential oil activityconsequently increases the fertility and hatching rate andreduces the mortality rate The present results revealed apositive correlation between the fertility and the hatching rateof fertile eggs suggesting an improvement in this parameterwith the increasing rate of the fertility

5 Conclusion

The present results revealed that ginger rhizome essentialoil can be used in quails to reduce the lipid peroxidationin reproductive cells and promote fertility without adverseeffects on growth performances

Data Availability

Thedata sets used during the current study are available fromthe corresponding author on reasonable request

Conflicts of Interest

The authors certify that no conflicts of interest exist

References

[1] ldquoAssessment of the risks associated with the presence of myco-toxins in human and animal food chainsrdquoMaisons-Alfort 2009Federation Senegalaise des Societes drsquoAssurances (FSSA)

[2] F Alleman I Gabriel VDufourcq F Perrin and J-FGabarrouldquoEssential oils in poultry feeding 1 Growth performances andregulation aspectsrdquo Productions Animales vol 26 no 1 pp 3ndash12 2013

[3] C Wenk ldquoWhy all the discussion about herbs Biotechnolgyin the feed industryrdquo in Proceedings of the Alltechrsquos 16th AnnualSympsium Alltech Technical Puplications pp 79ndash96 Notting-ham Universty Press Nicholasville 2000

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

Veterinary MedicineJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

International Journal of

Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y

ScienticaHindawiwwwhindawicom Volume 2018

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom

Page 4: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

4 Veterinary Medicine International

ICSPZ

N

N

IC0

ST

IC

IC

150100

50

L

LL

ST

ST

SPZ

Figure 1 Histological structure of Japanese quail testes as affected by ginger roots essential oil (400x) 0 (control) 50 100 and 150 doses ofginger roots essential oil (120583lkg body weight) SPZ spermatozoa ST seminiferous tubules IC interstitial cells L lumen and N necrosis

Table 3 Effects of graded level of ginger roots essential oil on growth characteristics and relative organ weightsof male Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Growth characteristicsFeed intake (g) 907 plusmn 4354 91013 plusmn 4819 85763 plusmn 4783 88915 plusmn 3775 017Live body weight (g) 20927 plusmn1502 20745 plusmn 2490 20427 plusmn 1527 20225 plusmn 1772 080Body weight gain (g) 22529 plusmn 4675 22786 plusmn 3798 21943 plusmn 4659 23314 plusmn 4547 095FCR 598 plusmn 207 579 plusmn 179 511 plusmn 069 463 plusmn 089 039Organ weights (g100 g bw)Liver 155 plusmn 033 157 plusmn 029 146 plusmn 039 147 plusmn 036 085Pair of testes 201 plusmn 048a 208 plusmn 016a 263 plusmn 021b 254 plusmn 032b 001Right testis 100 plusmn 024 104 plusmn 016 118 plusmn 023 114 plusmn 022 056Left testis 101 plusmn 026a 105 plusmn 017a 146 plusmn 007b 141 plusmn 033b 001abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails FCR = feed conversion ratio

treated with essential oil at 100 and 150120583lkg bw werecomparable and significantly (119875 lt 005) higher than activitiesrecorded in control group and the group of quails treatedwith50 120583lkg bw The catalase (CAT) activities were comparablewith 100 and 150120583lkg bw but significantly higher (119875 lt 005)than CAT activity recorded in the control group (Table 4)

35 Histological Structure of the Testes The testes of thequails in the control group showed slight alterations of theseminiferous tubules with necrosis The oral administrationof the essential oil whatever the dose improved the histo-logical structure of the testes compared to the control Thehistological changes observed in the testes of the treatedquails whatever the dose were almost identical (Figure 1)

36 Fertility and Hatchability Traits The fertility rate ofquails treated with the essential oil except the lowest dose(50 120583lkg bw) significantly increased (119875 lt 005) compared tothe control group However the fertility rate of quails treatedwith 100 120583lkg bw is comparable to the fertility of quailstreated with the highest dose of essential oil (150 120583lkg bw)The relative weight of the testes is positively and significantlycorrelated to the fertility rate (120588 = +099 119875 lt 001) the sameobservation was made between GSH and the fertility rate (120588= +095 119875 lt 005) (Table 5)

The oral administration of ginger rhizome essential oil atthe entire used dose tends to increase the hatching rate offertile eggs and the total hatch rate compared to the control(Table 6) However the highest fertile egg hatched and total

Veterinary Medicine International 5

Table 4 Effects of graded levels of ginger essential oil on serum biochemical and testes oxidative stress characteristics

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Serum metabolitesSerum proteins (gdl) 206 plusmn 004a 238 plusmn 019b 266 plusmn 019c 270 plusmn 035c 000Globulins (gdl) 016 plusmn 005a 031 plusmn 006b 049 plusmn 007c 048 plusmn 016c 000AST (UL) 16800 plusmn 2024b 14624 plusmn 1511ab 16324 plusmn 1129ab 13749 plusmn 1688a 000ALT (UL) 5750 plusmn 1049b 4285 plusmn 346a 4000 plusmn 1014a 3343 plusmn 607a 000Total cholesterol (mgdl) 12727 plusmn 798d 11809 plusmn 541c 11006 plusmn 583b 10027 plusmn 198a 000Triglycerides (mgdl) 7346 plusmn 1039b 5718 plusmn 443a 5691 plusmn 649a 5607 plusmn 616a 000Testes oxidative stress (gram of tissue)MDA 9779 plusmn 960c 8220 plusmn 993b 5249 plusmn 839a 5057 plusmn 1783a 000SOD 292 plusmn 048a 347 plusmn 033a 344 plusmn 055a 408 plusmn 023b 000GSH 18373 plusmn 3515a 20147 plusmn 1774a 26507 plusmn 4825b 27402 plusmn 5416b 000CAT 282 plusmn 031a 336 plusmn 073ab 378 plusmn 063b 360 plusmn 089b 004abcdOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails MDA = malondialdehyde GSH = reducedglutathione CAT = catalase SOD = superoxide dismutase AST = aspartate aminotransferase ALT = alanine aminotransferase values are presented as meansplusmn standard deviation

Table 5 Correlations between testes weight GSH sperm motilitytotal hatch and fertility rate

Parameters Pair of testesrelative weight Fertility rate Total hatch rate

Fertility rate 099lowastlowast - 065Sperm motility 099lowast 099lowastlowast -GSH 098lowast 095lowast -lowastThe correlation is significant at the 005 level lowastlowastThe correlation is signifi-cant at the 001 level

hatch rates were recorded in quails treated with 100 120583lkgbw A positive and nonsignificant correlation was recordedbetween the fertility rate and the total hatch rate (120588 = +065119875 gt 005) (Table 5)

The embryonic mortality rate was not significantlyaffected (119875 gt 005) by the doses of the essential oil usedHow-ever it tends to decrease with essential oil whatever the dosecompared to the controlThe lowest embryonicmortality ratewas recorded in quails treated with 100 120583lkg bw The gingeressential oil whatever the dose induced a nonsignificant(119875 gt 005) increase in chickrsquos weight compared to the con-trol However the highest chick weight was recorded with100 120583lkg bw of the essential oil (Table 6)

4 Discussion

The present study revealed that feed intake live body weightand body weight gain were not significantly affected by theginger essential oil treatments over the 12-week period Thisobservation agreed with the findings of Dieumou et al [23]who recorded no significant differences in feed intake bodyweight gain and feed conversion ratio with 10 20 and40mgkg bw of ginger essential oil for seven consecutiveweeks in broilers The findings of Fakhim et al [5] alsorevealed no improvement in body weight gain of chickens fed

on ginger supplements compared to the control group Feedconversion ratio decreased nonsignificantly and linearly withthe increasing doses of essential oil compared to the controlThis effect could be explained by the various properties ofphenolic and flavonoid compounds of the ginger essential oilin the digestive system of the animal These bioactive com-pounds possess antimicrobial and antioxidant properties thatallow them to reduce the free radical and pathogenic micro-bersquos attacks and a better use of the nutrients in the digestivetract

The present study revealed that the oral administrationof essential oil whatever the dose increased significantly theserum content in total protein and globulin compared tothe control This result is consistent with the findings ofZhang et al [24] with 5 gkg of ginger rhizomes powder inbroiler feed The present results contradicted the findings ofmany other studies which recorded a significant decrease inserum protein and globulin levels in chickens fed on diet sup-plemented with ginger rhizomes powder [25 26] The differ-ences between these studies could be the result of differencein the doses used the shape of the plant (powder essentialoil etc) the route of administration and the experimentalconditions The increase in total protein and globulin maybe due to phenolic components including gingerol shogaolsgingerdiol gingerdione and some related phenolic ketonederivatives of ginger essential oil [4] which have powerfulantioxidant and immunostimulatory properties that allowthem to improve immune responses

Serum content in aspartate aminotransferase (AST) andalanine aminotransferase (ALT) significantly decreased inquails fed on ginger rhizomes essential whatever the dosecompared to the control birds These results are consistentwith the findings of Malekizadeh et al [27] who reporteda significant decrease in serum AST and ALT levels inHyline leghorns (W-36) fed on diet supplemented with3 ginger rhizome powder for 9 weeks The decrease in

6 Veterinary Medicine International

Table 6 Effects of graded levels of ginger essential oil on fertility rate and hatchability traits in Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Fertility () 8189 plusmn 491a 8214 plusmn 311a 9071 plusmn 490b 8854 plusmn 202b 001Hatchability of fertile eggs () 6500 plusmn 1401 7893 plusmn 653 8429 plusmn 1119 7250 plusmn 1509 018Total hatchability () 6071 plusmn 2143 7143 plusmn 1016 7857 plusmn 2736 6714 plusmn 1447 063Embryonic mortality () 1008 plusmn 223 948 plusmn 372 946 plusmn 119 966 plusmn 059 099Chickrsquos weight (g) 808 plusmn 104 817 plusmn 107 842 plusmn 122 833 plusmn 076 040abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails

the transaminases levels suggested that the doses of oiladministered were not toxic and regulated the liver activityof the quails According to Zounongo [28] an increase inserum transaminase levels indicates hepatic cytolysis In factthe weight of the liver in the present study tends to decreasein treated quails at the doses of 100 and 150 120583lkg bw

The malondialdehyde (MDA) as an indicator of lipidperoxidation and oxidative stress significantly decreased in alltreatments groups compared to the control The activities ofthe antioxidant enzymes (superoxide dismutase catalase andreduced glutathione) increased with the oral administrationof this essential oil in quails Antioxidant activity is one of themain defense systems of the body against the harmful effectsof reactive oxygen species in animals The antioxidant actionof ginger has been attributed to the protective actions ofginger bioactive substances against free radical attack [29 30]This antioxidant action of ginger essential oil subsequentlyreduced the lipid peroxidation responsible for apoptosis inspermatogenic cells Indeed the testicular histology in quailstreated with ginger rhizomes essential oil revealed structuralimprovements compared to the control birds that showedmild necrosis In accordance with this result Zancan etal [31] revealed that ginger has protective effects againstcisplatin-induced testicular damage and oxidative stress inanimals Shanoon [32] mentioned that the ginger rhizomesbioactive molecules improve testicular structure by increas-ing the thickness of the seminiferous tubules and the germcell membrane and consequently increase testicular weightviability and motility of the spermatozoa

All the above-mentioned properties contribute to thefertility of the quail treated with different doses of the gingerroots essential oil resulting in an increase in the fertility rateThe present results are consistent with the findings of Ezzatet al [33] in Cobb 500 parent broiler treated with gingerrhizome powder at the doses of 25 and 5 gkg of feed for14 weeks This elevating effect can be attributed to the gin-ger essential oil active compounds (alkaloids and terpenes)which improve the characteristics of the spermatozoa andconsequently make them more active in the female genitaltract According to Froman et al [34] a higher proportionof highly motile spermatozoa enter the sperm storage tubulesof female birds resulting in a high proportion of fertile eggsThe ginger rhizomes essential oil whatever the dose increasedthe hatching rate of fertile eggsThis effect could be related tosperm characteristics (membrane and DNA integrity viabil-ity andmobility) enhanced by the phenolic compounds of theessential oil Indeed the sperm cell membrane is particularly

rich in polyunsaturated fatty acid which predisposes themto lipid peroxidation by reactive oxygen species which isassociated withmale infertility [35] Large amounts of radicaloxygen species have been shown to interferewith the integrityof sperm DNA and thereby influence embryo development[36] The supplementation of the male bird diet with gingerrhizomes essential oil rich in antioxidant property couldreduce the impairment in sperm membrane and DNA Inaccordance with the present result Hoe et al [37] mentionedthat the ginger essential oil protects the DNA from oxidationby hydrogen peroxide and from the harmful effects of thereactive oxygen species This ginger essential oil activityconsequently increases the fertility and hatching rate andreduces the mortality rate The present results revealed apositive correlation between the fertility and the hatching rateof fertile eggs suggesting an improvement in this parameterwith the increasing rate of the fertility

5 Conclusion

The present results revealed that ginger rhizome essentialoil can be used in quails to reduce the lipid peroxidationin reproductive cells and promote fertility without adverseeffects on growth performances

Data Availability

Thedata sets used during the current study are available fromthe corresponding author on reasonable request

Conflicts of Interest

The authors certify that no conflicts of interest exist

References

[1] ldquoAssessment of the risks associated with the presence of myco-toxins in human and animal food chainsrdquoMaisons-Alfort 2009Federation Senegalaise des Societes drsquoAssurances (FSSA)

[2] F Alleman I Gabriel VDufourcq F Perrin and J-FGabarrouldquoEssential oils in poultry feeding 1 Growth performances andregulation aspectsrdquo Productions Animales vol 26 no 1 pp 3ndash12 2013

[3] C Wenk ldquoWhy all the discussion about herbs Biotechnolgyin the feed industryrdquo in Proceedings of the Alltechrsquos 16th AnnualSympsium Alltech Technical Puplications pp 79ndash96 Notting-ham Universty Press Nicholasville 2000

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

Veterinary MedicineJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

International Journal of

Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y

ScienticaHindawiwwwhindawicom Volume 2018

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom

Page 5: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

Veterinary Medicine International 5

Table 4 Effects of graded levels of ginger essential oil on serum biochemical and testes oxidative stress characteristics

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Serum metabolitesSerum proteins (gdl) 206 plusmn 004a 238 plusmn 019b 266 plusmn 019c 270 plusmn 035c 000Globulins (gdl) 016 plusmn 005a 031 plusmn 006b 049 plusmn 007c 048 plusmn 016c 000AST (UL) 16800 plusmn 2024b 14624 plusmn 1511ab 16324 plusmn 1129ab 13749 plusmn 1688a 000ALT (UL) 5750 plusmn 1049b 4285 plusmn 346a 4000 plusmn 1014a 3343 plusmn 607a 000Total cholesterol (mgdl) 12727 plusmn 798d 11809 plusmn 541c 11006 plusmn 583b 10027 plusmn 198a 000Triglycerides (mgdl) 7346 plusmn 1039b 5718 plusmn 443a 5691 plusmn 649a 5607 plusmn 616a 000Testes oxidative stress (gram of tissue)MDA 9779 plusmn 960c 8220 plusmn 993b 5249 plusmn 839a 5057 plusmn 1783a 000SOD 292 plusmn 048a 347 plusmn 033a 344 plusmn 055a 408 plusmn 023b 000GSH 18373 plusmn 3515a 20147 plusmn 1774a 26507 plusmn 4825b 27402 plusmn 5416b 000CAT 282 plusmn 031a 336 plusmn 073ab 378 plusmn 063b 360 plusmn 089b 004abcdOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails MDA = malondialdehyde GSH = reducedglutathione CAT = catalase SOD = superoxide dismutase AST = aspartate aminotransferase ALT = alanine aminotransferase values are presented as meansplusmn standard deviation

Table 5 Correlations between testes weight GSH sperm motilitytotal hatch and fertility rate

Parameters Pair of testesrelative weight Fertility rate Total hatch rate

Fertility rate 099lowastlowast - 065Sperm motility 099lowast 099lowastlowast -GSH 098lowast 095lowast -lowastThe correlation is significant at the 005 level lowastlowastThe correlation is signifi-cant at the 001 level

hatch rates were recorded in quails treated with 100 120583lkgbw A positive and nonsignificant correlation was recordedbetween the fertility rate and the total hatch rate (120588 = +065119875 gt 005) (Table 5)

The embryonic mortality rate was not significantlyaffected (119875 gt 005) by the doses of the essential oil usedHow-ever it tends to decrease with essential oil whatever the dosecompared to the controlThe lowest embryonicmortality ratewas recorded in quails treated with 100 120583lkg bw The gingeressential oil whatever the dose induced a nonsignificant(119875 gt 005) increase in chickrsquos weight compared to the con-trol However the highest chick weight was recorded with100 120583lkg bw of the essential oil (Table 6)

4 Discussion

The present study revealed that feed intake live body weightand body weight gain were not significantly affected by theginger essential oil treatments over the 12-week period Thisobservation agreed with the findings of Dieumou et al [23]who recorded no significant differences in feed intake bodyweight gain and feed conversion ratio with 10 20 and40mgkg bw of ginger essential oil for seven consecutiveweeks in broilers The findings of Fakhim et al [5] alsorevealed no improvement in body weight gain of chickens fed

on ginger supplements compared to the control group Feedconversion ratio decreased nonsignificantly and linearly withthe increasing doses of essential oil compared to the controlThis effect could be explained by the various properties ofphenolic and flavonoid compounds of the ginger essential oilin the digestive system of the animal These bioactive com-pounds possess antimicrobial and antioxidant properties thatallow them to reduce the free radical and pathogenic micro-bersquos attacks and a better use of the nutrients in the digestivetract

The present study revealed that the oral administrationof essential oil whatever the dose increased significantly theserum content in total protein and globulin compared tothe control This result is consistent with the findings ofZhang et al [24] with 5 gkg of ginger rhizomes powder inbroiler feed The present results contradicted the findings ofmany other studies which recorded a significant decrease inserum protein and globulin levels in chickens fed on diet sup-plemented with ginger rhizomes powder [25 26] The differ-ences between these studies could be the result of differencein the doses used the shape of the plant (powder essentialoil etc) the route of administration and the experimentalconditions The increase in total protein and globulin maybe due to phenolic components including gingerol shogaolsgingerdiol gingerdione and some related phenolic ketonederivatives of ginger essential oil [4] which have powerfulantioxidant and immunostimulatory properties that allowthem to improve immune responses

Serum content in aspartate aminotransferase (AST) andalanine aminotransferase (ALT) significantly decreased inquails fed on ginger rhizomes essential whatever the dosecompared to the control birds These results are consistentwith the findings of Malekizadeh et al [27] who reporteda significant decrease in serum AST and ALT levels inHyline leghorns (W-36) fed on diet supplemented with3 ginger rhizome powder for 9 weeks The decrease in

6 Veterinary Medicine International

Table 6 Effects of graded levels of ginger essential oil on fertility rate and hatchability traits in Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Fertility () 8189 plusmn 491a 8214 plusmn 311a 9071 plusmn 490b 8854 plusmn 202b 001Hatchability of fertile eggs () 6500 plusmn 1401 7893 plusmn 653 8429 plusmn 1119 7250 plusmn 1509 018Total hatchability () 6071 plusmn 2143 7143 plusmn 1016 7857 plusmn 2736 6714 plusmn 1447 063Embryonic mortality () 1008 plusmn 223 948 plusmn 372 946 plusmn 119 966 plusmn 059 099Chickrsquos weight (g) 808 plusmn 104 817 plusmn 107 842 plusmn 122 833 plusmn 076 040abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails

the transaminases levels suggested that the doses of oiladministered were not toxic and regulated the liver activityof the quails According to Zounongo [28] an increase inserum transaminase levels indicates hepatic cytolysis In factthe weight of the liver in the present study tends to decreasein treated quails at the doses of 100 and 150 120583lkg bw

The malondialdehyde (MDA) as an indicator of lipidperoxidation and oxidative stress significantly decreased in alltreatments groups compared to the control The activities ofthe antioxidant enzymes (superoxide dismutase catalase andreduced glutathione) increased with the oral administrationof this essential oil in quails Antioxidant activity is one of themain defense systems of the body against the harmful effectsof reactive oxygen species in animals The antioxidant actionof ginger has been attributed to the protective actions ofginger bioactive substances against free radical attack [29 30]This antioxidant action of ginger essential oil subsequentlyreduced the lipid peroxidation responsible for apoptosis inspermatogenic cells Indeed the testicular histology in quailstreated with ginger rhizomes essential oil revealed structuralimprovements compared to the control birds that showedmild necrosis In accordance with this result Zancan etal [31] revealed that ginger has protective effects againstcisplatin-induced testicular damage and oxidative stress inanimals Shanoon [32] mentioned that the ginger rhizomesbioactive molecules improve testicular structure by increas-ing the thickness of the seminiferous tubules and the germcell membrane and consequently increase testicular weightviability and motility of the spermatozoa

All the above-mentioned properties contribute to thefertility of the quail treated with different doses of the gingerroots essential oil resulting in an increase in the fertility rateThe present results are consistent with the findings of Ezzatet al [33] in Cobb 500 parent broiler treated with gingerrhizome powder at the doses of 25 and 5 gkg of feed for14 weeks This elevating effect can be attributed to the gin-ger essential oil active compounds (alkaloids and terpenes)which improve the characteristics of the spermatozoa andconsequently make them more active in the female genitaltract According to Froman et al [34] a higher proportionof highly motile spermatozoa enter the sperm storage tubulesof female birds resulting in a high proportion of fertile eggsThe ginger rhizomes essential oil whatever the dose increasedthe hatching rate of fertile eggsThis effect could be related tosperm characteristics (membrane and DNA integrity viabil-ity andmobility) enhanced by the phenolic compounds of theessential oil Indeed the sperm cell membrane is particularly

rich in polyunsaturated fatty acid which predisposes themto lipid peroxidation by reactive oxygen species which isassociated withmale infertility [35] Large amounts of radicaloxygen species have been shown to interferewith the integrityof sperm DNA and thereby influence embryo development[36] The supplementation of the male bird diet with gingerrhizomes essential oil rich in antioxidant property couldreduce the impairment in sperm membrane and DNA Inaccordance with the present result Hoe et al [37] mentionedthat the ginger essential oil protects the DNA from oxidationby hydrogen peroxide and from the harmful effects of thereactive oxygen species This ginger essential oil activityconsequently increases the fertility and hatching rate andreduces the mortality rate The present results revealed apositive correlation between the fertility and the hatching rateof fertile eggs suggesting an improvement in this parameterwith the increasing rate of the fertility

5 Conclusion

The present results revealed that ginger rhizome essentialoil can be used in quails to reduce the lipid peroxidationin reproductive cells and promote fertility without adverseeffects on growth performances

Data Availability

Thedata sets used during the current study are available fromthe corresponding author on reasonable request

Conflicts of Interest

The authors certify that no conflicts of interest exist

References

[1] ldquoAssessment of the risks associated with the presence of myco-toxins in human and animal food chainsrdquoMaisons-Alfort 2009Federation Senegalaise des Societes drsquoAssurances (FSSA)

[2] F Alleman I Gabriel VDufourcq F Perrin and J-FGabarrouldquoEssential oils in poultry feeding 1 Growth performances andregulation aspectsrdquo Productions Animales vol 26 no 1 pp 3ndash12 2013

[3] C Wenk ldquoWhy all the discussion about herbs Biotechnolgyin the feed industryrdquo in Proceedings of the Alltechrsquos 16th AnnualSympsium Alltech Technical Puplications pp 79ndash96 Notting-ham Universty Press Nicholasville 2000

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

Veterinary MedicineJournal of

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Hindawiwwwhindawicom Volume 2018

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Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

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Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

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Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

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Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom

Page 6: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

6 Veterinary Medicine International

Table 6 Effects of graded levels of ginger essential oil on fertility rate and hatchability traits in Japanese quail

Parameters Essential oil doses (120583lkg body weight)Control (119899 = 12) 50 (119899 = 12) 100 (119899 = 12) 150 (119899 = 12) 119875 value

Fertility () 8189 plusmn 491a 8214 plusmn 311a 9071 plusmn 490b 8854 plusmn 202b 001Hatchability of fertile eggs () 6500 plusmn 1401 7893 plusmn 653 8429 plusmn 1119 7250 plusmn 1509 018Total hatchability () 6071 plusmn 2143 7143 plusmn 1016 7857 plusmn 2736 6714 plusmn 1447 063Embryonic mortality () 1008 plusmn 223 948 plusmn 372 946 plusmn 119 966 plusmn 059 099Chickrsquos weight (g) 808 plusmn 104 817 plusmn 107 842 plusmn 122 833 plusmn 076 040abOn the same line means with the same letter were not significantly different (119875 gt 005) 119899 = number ofquails

the transaminases levels suggested that the doses of oiladministered were not toxic and regulated the liver activityof the quails According to Zounongo [28] an increase inserum transaminase levels indicates hepatic cytolysis In factthe weight of the liver in the present study tends to decreasein treated quails at the doses of 100 and 150 120583lkg bw

The malondialdehyde (MDA) as an indicator of lipidperoxidation and oxidative stress significantly decreased in alltreatments groups compared to the control The activities ofthe antioxidant enzymes (superoxide dismutase catalase andreduced glutathione) increased with the oral administrationof this essential oil in quails Antioxidant activity is one of themain defense systems of the body against the harmful effectsof reactive oxygen species in animals The antioxidant actionof ginger has been attributed to the protective actions ofginger bioactive substances against free radical attack [29 30]This antioxidant action of ginger essential oil subsequentlyreduced the lipid peroxidation responsible for apoptosis inspermatogenic cells Indeed the testicular histology in quailstreated with ginger rhizomes essential oil revealed structuralimprovements compared to the control birds that showedmild necrosis In accordance with this result Zancan etal [31] revealed that ginger has protective effects againstcisplatin-induced testicular damage and oxidative stress inanimals Shanoon [32] mentioned that the ginger rhizomesbioactive molecules improve testicular structure by increas-ing the thickness of the seminiferous tubules and the germcell membrane and consequently increase testicular weightviability and motility of the spermatozoa

All the above-mentioned properties contribute to thefertility of the quail treated with different doses of the gingerroots essential oil resulting in an increase in the fertility rateThe present results are consistent with the findings of Ezzatet al [33] in Cobb 500 parent broiler treated with gingerrhizome powder at the doses of 25 and 5 gkg of feed for14 weeks This elevating effect can be attributed to the gin-ger essential oil active compounds (alkaloids and terpenes)which improve the characteristics of the spermatozoa andconsequently make them more active in the female genitaltract According to Froman et al [34] a higher proportionof highly motile spermatozoa enter the sperm storage tubulesof female birds resulting in a high proportion of fertile eggsThe ginger rhizomes essential oil whatever the dose increasedthe hatching rate of fertile eggsThis effect could be related tosperm characteristics (membrane and DNA integrity viabil-ity andmobility) enhanced by the phenolic compounds of theessential oil Indeed the sperm cell membrane is particularly

rich in polyunsaturated fatty acid which predisposes themto lipid peroxidation by reactive oxygen species which isassociated withmale infertility [35] Large amounts of radicaloxygen species have been shown to interferewith the integrityof sperm DNA and thereby influence embryo development[36] The supplementation of the male bird diet with gingerrhizomes essential oil rich in antioxidant property couldreduce the impairment in sperm membrane and DNA Inaccordance with the present result Hoe et al [37] mentionedthat the ginger essential oil protects the DNA from oxidationby hydrogen peroxide and from the harmful effects of thereactive oxygen species This ginger essential oil activityconsequently increases the fertility and hatching rate andreduces the mortality rate The present results revealed apositive correlation between the fertility and the hatching rateof fertile eggs suggesting an improvement in this parameterwith the increasing rate of the fertility

5 Conclusion

The present results revealed that ginger rhizome essentialoil can be used in quails to reduce the lipid peroxidationin reproductive cells and promote fertility without adverseeffects on growth performances

Data Availability

Thedata sets used during the current study are available fromthe corresponding author on reasonable request

Conflicts of Interest

The authors certify that no conflicts of interest exist

References

[1] ldquoAssessment of the risks associated with the presence of myco-toxins in human and animal food chainsrdquoMaisons-Alfort 2009Federation Senegalaise des Societes drsquoAssurances (FSSA)

[2] F Alleman I Gabriel VDufourcq F Perrin and J-FGabarrouldquoEssential oils in poultry feeding 1 Growth performances andregulation aspectsrdquo Productions Animales vol 26 no 1 pp 3ndash12 2013

[3] C Wenk ldquoWhy all the discussion about herbs Biotechnolgyin the feed industryrdquo in Proceedings of the Alltechrsquos 16th AnnualSympsium Alltech Technical Puplications pp 79ndash96 Notting-ham Universty Press Nicholasville 2000

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

Veterinary MedicineJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

International Journal of

Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y

ScienticaHindawiwwwhindawicom Volume 2018

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom

Page 7: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

Veterinary Medicine International 7

[4] X Zhao Z B Yang W R Yang Y Wang S Z Jiang and GG Zhang ldquoEffects of ginger root (Zingiber officinale) on lay-ing performance and antioxidant status of laying hens and ondietary oxidation stabilityrdquo Poultry Science vol 90 no 8 pp1720ndash1727 2011

[5] R Fakhim Y Ebrahimnezhad H R Seyedabadi and T Vah-datpour ldquoEffect of different concentrations of aqueous extractof ginger (Zingiber officinale) on performance and carcasscharacteristics of male broiler chickens in wheat-soybean mealbased dietsrdquo Journal of Bioscience and Biotechnology vol 2 no2 pp 95ndash99 2013

[6] B H Ali G Blunden M O Tanira and A Nemmar ldquoSomephytochemical pharmacological and toxicological properties ofginger (Zingiber officinale Roscoe) a review of recent researchrdquoFood and Chemical Toxicology vol 46 no 2 pp 409ndash420 2008

[7] S McGary I Estevez M R Bakst and D L Pollock ldquoPhe-notypic traits as reliable indicators of fertility in male broilerbreedersrdquo Poultry Science vol 81 no 1 pp 102ndash111 2002

[8] S Leeson and J D Summers Broiler Breeder Production Uni-versity Books Guelph Ontario Canada 2000

[9] M FerroukN Boukenaoui I Smaili I AbdAl Samad and JMExbrayat ldquoMorphometric and histological Study of the testis ofJapanese quail (Corturnix japonica) during post-natal growthrdquoBulletin de la Societe Zoologique de France vol 140 no 1 pp45ndash60 2015

[10] RU Khan SNaz ZNikousefat et al ldquoPotential applications ofginger (Zingiber officinale) in poultry dietsrdquoWorldrsquos Poultry Sci-ence Journal vol 68 no 2 pp 245ndash252 2012

[11] L Wang and C L Weller ldquoRecent advances in extraction ofnutraceuticals from plantsrdquo Trends in Food Science amp Technol-ogy vol 17 no 6 pp 300ndash312 2006

[12] A Banso and J E Ngbede ldquoPhytochemical screening and invitro antifungal properties of Fagara zanthoxyloidesrdquo Journal ofFood Agriculture and Environment (JFAE) vol 4 no 3-4 pp8-9 2006

[13] J Ngbede R A Yakubu and D A Nyam ldquoPhytochemicalScreening for Active Compounds in Canarium scheinfurthii(Atile) leaves fromrdquoMedwell Research Journal of Biological Sci-ence vol 3 no 9 pp 1076ndash1078 2008

[14] P McDonald R A Edwards J F D Greenhalgh C A MorganL A Sinclair and R G Wilkinson Animal Nutrition PrenticeHall London 7th edt edition 2011

[15] R Jourdain ldquoPoultry in tropical environmentrdquo InternationalCouloumiers pp 43ndash45 1980

[16] A G Gornal G S Bardwil and M M David ldquoDeterminationof serum proteins by mean of Biuret reactionsrdquo Journal of Bio-logical Chemistry vol 177 no 2 pp 751ndash766 1989

[17] S A Abdel-Fattah M H El-Sanhoury N M El-Mednay andF Abdel-Azeem ldquoThyroid activity some blood constituentsorgans morphology and performance of broiler chicks fed sup-plemental organic acidsrdquo International Journal of Poultry Sci-ence vol 7 no 3 pp 215ndash222 2008

[18] U A Nilsson L-I Olsson G Carlin and A-C Bylund-Fell-enius ldquoInhibition of lipid peroxidation by spin labels Relation-ships between structure and functionrdquoThe Journal of BiologicalChemistry vol 264 no 19 pp 11131ndash11135 1989

[19] H P Misra and I Fridovich ldquoThe generation of superoxideradical during the autoxidation of hemoglobinrdquo The Journal ofBiological Chemistry vol 247 no 21 pp 6960ndash6962 1972

[20] A K Sinha ldquoColorimetric assay of catalaserdquo Analytical Bio-chemistry vol 47 no 2 pp 389ndash394 1972

[21] G L Ellman and F T Fiches ldquoQuantitative determination ofpeptides by sulfhydryl groups Archrdquo Archives of Biochemistryand Biophysics vol 80 no 2 pp 70ndash72 1959

[22] K Wolfang Histology Pocket Atlas Collection Atlas de poche4th edition 2009 Edition Medicine Sciences Flammarion

[23] F E Dieumou A Teguia J R Kuiate J D Tamokou N BFonge and M C Dongmo ldquoEffects of ginger (Zingiber offici-nale) and garlic (Allium sativum) essential oils on growth per-formance and gut microbial population of broiler chickensrdquoLivestock Research for Rural Development vol 21 no 8 131pages 2009

[24] G F Zhang Z B Yang Y Wang W R Yang S Z Jiang andG S Gai ldquoEffects of ginger root (Zingiber officinale) processedto different particle sizes on growth performance antioxidantstatus and serum metabolites of broiler chickensrdquo PoultryScience vol 88 no 10 pp 2159ndash2166 2009

[25] S Erkelenz W F Mueller M S Evans et al ldquoEfficacy of usingdifferent sources and levels of Allium sativum and Zingiberofficinale on broiler chicks performancerdquo Saudi Journal of Bio-logical Sciences vol 12 no 1 pp 96ndash102 2013

[26] S Nahed A Tamer A E l Amera and G Emad ldquoThe effectsof dietary supplementation of different levels of thyme (Thy-mus vulgaris) and ginger (Zingiber officinale) essential oils onperformance hematological biochemical and immunologicalparameters of broiler chickensrdquo Global Veterinaria vol 12 no6 pp 736ndash744 2014

[27] M Malekizadeh M M Moeini and S Ghazi ldquoThe effects ofdifferent levels of ginger (Zingiber officinaleRosc) and Turmeric(Curcuma longa Linn) rhizomes powder on some blood meta-bolites and production performance characteristics of layinghensrdquo Journal of Agricultural Science and Technology vol 14 no1 pp 127ndash134 2012

[28] MZ ZounongoDetermination of usual biochemical parametersin small ruminants in Burkina Faso and their variation innaturally infected subjects by trypanosomiasis [Thesis for the rankof veterinary doctor] Ecole interetats des sciences et medecineveterinaire 2013

[29] G C Jagetia M S Baliga P Venkatesh and J N Ulloor ldquoInflu-ence of Ginger Rhizome (Zingiber officinale Rosc) on SurvivalGlutathione and Lipid Peroxidation in Mice after Whole-BodyExposure to Gamma Radiationrdquo Journal of Radiation Researchvol 160 no 5 pp 584ndash592 2003

[30] A Haksar A Sharma R Chawla et al ldquoZingiber officinaleexhibits behavioral radioprotection against radiation-inducedCTA in a gender-specific mannerrdquo Pharmacology Biochemistryamp Behavior vol 84 no 2 pp 179ndash188 2006

[31] K C Zancan M O M Marques A J Petenate and M AA Meireles ldquoExtraction of ginger (Zingiber officinale roscoe)oleoresin with CO2 and co-solvents A study of the antioxidantaction of the extractsrdquo The Journal of Supercritical Fluids vol24 no 1 pp 57ndash76 2001

[32] A K Shanoon ldquoEffects of Zingiber officinale powder on semencharacteristic and blood serum sex hormones concentration inbroilers breeder malerdquo International Journal of Poultry Sciencevol 10 no 11 pp 863ndash866 2011

[33] W Ezzat A E El-Slamony A M A Bealish M M M OudaandMM Sabry ldquoEffect of adding dried ginger rhizome to dietson semen quality and fertility rate in aged local cocks underEgyptian hot summer conditionrdquo Egypt Poultry Science Journalvol 37 no 1 pp 233ndash249 2017

[34] D P Froman A J Feltmann M L Rhoads and J D KirbyldquoSperm mobility a primary determinant of fertility in the

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

Veterinary MedicineJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

International Journal of

Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y

ScienticaHindawiwwwhindawicom Volume 2018

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom

Page 8: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

8 Veterinary Medicine International

domestic fowl (Gallus domesticus)rdquoBiology of Reproduction vol61 no 2 pp 400ndash405 1999

[35] P F SuraiN Fujihara B K Speake J BrillardG JWishart andN H Sparks ldquoPolyunsaturated fatty acids lipid peroxidationand antioxidant protection in avian semenrdquo Asian-AustralasianJournal of Animal Sciences vol 14 no 7 pp 1024ndash1050 2001

[36] C Paul A AMurray N Spears and P T K Saunders ldquoA singlemild transient scrotal heat stress causes DNA damage sub-fertility and impairs formation of blastocysts in micerdquo Repro-duction vol 136 no 1 pp 73ndash84 2008

[37] S Y Hoe K H Dong R K Jung and C S Jae ldquoEffects of120572-tocopherol on cadmium-induced toxicity in rat testis andspermatogenesisrdquo Journal of KoreanMedical Science vol 21 no3 pp 445ndash451 2006

Veterinary MedicineJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

International Journal of

Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y

ScienticaHindawiwwwhindawicom Volume 2018

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom

Page 9: Growth Performance, Serum Biochemical Profile, Oxidative Status, …downloads.hindawi.com/journals/vmi/2018/7682060.pdf · Testes and liver of slaughtered quails were carefully removed,

Veterinary MedicineJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

International Journal of

Microbiology

Veterinary Medicine International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

EcologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

PsycheHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

Hindawiwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2018

Biotechnology Research International

Hindawiwwwhindawicom Volume 2018

Agronomy

Hindawiwwwhindawicom Volume 2018

International Journal of

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y

ScienticaHindawiwwwhindawicom Volume 2018

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Case Reports in Veterinary Medicine

Submit your manuscripts atwwwhindawicom