International Journal of Food Sciences and Nutrition (1998) 49, 101-108

Nutritional quality of lactic fermented bitter gourd and fenugreek leaves

Uma Gupta', Rudramma', E.R. Rati2 and R. Joseph2

'Department of studies in Food Science and Nutrition Universizy of Mysore, Mysore-570 006, and ZDepartment of Microbiology Central Food Technological Research Institute, Mysore-570 013, India

Pediococcus pentosaceus was selected from isolates obtained from the naturally fermenting bitter gourd and fenugreek leaves based on its high titre and broad spectrum of inhibitory activity against spoilage organisms. This strain was then employed for fermentation of bitter gourd and fenugreek which resulted in a more acceptable product having enhanced fat, pyridoxine and ascorbic acid levels. It was of interest to note that vitamin B12 was formed in the fenugreek as a result of the fermentation.

Introduction

Fermented foods have a positive image among consumers because of the desirable organoleptic quality, better nutritional attributes and improved shelf-life without the added chemical preservatives (Joshi et aL, 1993). Lactic fermen- tation of vegetables is a well-known process and green olives, cabbage and cucumbers are the most popular lactic fermented vegetables (Vaughn, 1982). In Indian medicinal systems of naturopathy and ayurveda, extracts of veget- ables, particularly those of bitter gourd, cabbage, etc, are used as health-based adjuvants. Cooked and uncooked juice of bitter gourd is popularly consumed for its hypoglycemic properties by diabetics. Lactic fermented vegetable juices such as tomato, pumpkin, ash gourd, bottle gourd, carrot, cabbage, cauliflower, drumstick (Ninnala Devi et aL, 1992) and black carrot juice (Sethi, 1990) have been developed for desirable organo- leptic properties and nutritive values. The present work was therefore undertaken to assess the suitability of lactic fermentation of bitter gourd (Momordica charantia) and fenugreek (Trigonella foenum graecum) leaves in terms of desirable organoleptic properties, acceptability and nutritive values.

Materials and methods

Isolation, screening, maintenance and identification of potent lactic acid bacteria (LAB) from bitter gourd and fenugreek leaves Bitter gourd (BG) and fenugreek leaves (FL) procured from the local market were incubated for 24h at 37°C in lactobacillus MRS broth (Speck, 1984) (ingredients g/L: proteose pep- tone 10.0, beef extract 10.0, yeast extract 5.0, dextrose 20.0, Tween-80 1 .O ml, ammonium citrate 2.0, sodium acetate 5.0, magnesium sulphate 0.1, manganese sulphate 0.05, dipo- tassium phosphate 2.0 and final pH 6.k0.2). The lactic acid bacteria (LAB) in the fermenting MRS broth was enumerated using lactobacillus streptococcus differential agar (LSDM) (HiMe- dia, 1989) (ingredientsa: tryptone 10.0, beef extract 10.0, soy peptone 5.0, yeast extract 5.0, dextrose 20.0, sodium chloride 5.0, L-cystein HCI 0.3, agar 15.0, and lOOml of 10.0% (w/v) solution of antibiotic-free skimined milk and 1O.Oml of 2.0% (w/v) triphenyl tetrazolium chloride filter sterilised solution were mixed before pouring into the plates). LAB appearing on the plates were counted and expressed as cfdml. The LAB isolates were screened for the production of antimicrobial activity against B.

Correspondence to E. R. Rati.

0963-7486/98/020101-8 Q 1998 Carfax Publishing Ltd

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cereus F-4433 (courtesy Dr J. Kramer, UK) by agar diffusion well assay method (Shahani et al., 1976), and expressed as zone of inhibition inmm (ZI). Identification of LAB isolates was canied out by standard methods (Sneath et al., 1986). Heat stability of the antimicrobial factor was assessed by heating the culture filtrate at 8O"C, 100°C and 121°C for 30min each and then testing the antimicrobial activity (Shahani et al., 1976) against foodbome pathogenic bacteria Staphylococcus aureus FR1722 (cour- tesy Dr E. Noterman, The Netherlands), B. cereus F4433 and Escherichia coli D21 (cour- tesy Dr Linggood, Uniliver Research, UK) and foodbome spoilage bacteria KZebsielZu spp. (CFI'RI isolate).

Pure culture fermentation studies The vegetable pulp to water ratio was fixed at 1: 1 after initial trials. The natural fermentation vs the pure culture fermentation was compared by measuring the pH, estimating the acidity and the antimicrobial factor in the fermented juice samples. The critical cultural parameters stan- dardised for the desirable end product were:

Vegetables

1 Cut, wash and blanch

1 Cool and grind

1 Mix vegetable pulp and 2% dextrose

solution (1 : 1 wh)

1 Inoculate with I? pentosaceus for pure

culture fermentation process*

1 Incubate at 37°C

Centrifuge and filter 1 1

Bottle, seal and pasteurise (7OoC/15 min)

*For natural fermentation process lactic inoculurn is not added

Figure 1. Lactic beverage preparation.

level of inoculum of I? pentosaceus (at 0.5, 1.0, 2.0, 4.0 and 5.0%), dextrose concentration (at 0.5, 1 .O, 152.0 and 4.0%) and sodium chloride concentration (at 0.0, 0.5, 1.0, 1.5 and 2.0%). The time required for optimum fermentation was derived by the time course study, wherein analysis for fermentation assessment was con- ducted at regular intervals (after 12, 18,24,30, 36,42, and 48 h). Protocol for the preparation of fermented juice is given in Figure 1.

Nutrient analysis Proximate composition of freshly procured vegetable and lactic fermented product were determined (Ranganna, 1986). Vitamin BI2, folic acid, riboflavin and pyridoxine were estimated by microbiological assay (Freed, 1966) and vitamin C by dye method (Ranganna, 1986).

Sensory evaluation and storage studies The sensory evaluation of the fresh, natural and culture fermented vegetable juice samples were carried out by a trained panel of 20 judges. The sensory scores for comparison of the treatments were analysed by two-way analysis of variance followed by Duncan's new multiple range test (Indian Standards Institution, 1975). The fer- mented juice samples were bottled, sealed, pasteurised (70°C/15 min) and stored at ambient conditions. The pH, acidity and antimicrobial activity were determined after 15, 30 and 45 d of storage.

ReSUltS Screening, identijication and properties of LAB The avera e lactic count in bitter gourd was

X lo6 cNml after their incubation in MRS broth for 24 h, which reflect the magnitude of the naturally inhabiting LABS in vegetables. Of the 20 LAB isolates selected at random from the vegetables, three were found to be homofermentative and the rest, heterofermen- tative, as evinced by trapping of gas in Dur- ham's tube. The pH of the broth after growth of the isolates varied from 3.5 to 5.0. On screening for antimicrobial activity the culture filtrates of nine LAB isolates showed inhibi- tory activity against B. cereus. One of the homofermentative isolate from bitter gourd

150 X 10 IF cNml and in fenugreek leaves 450

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Lactic fermented bitter gourd and fenugreek leaves 103

Table 1. Inhibitory activity of Pediococcus pentosaceus culture filtrate and fermented juice against pathogenic and spoilage microbe

S1 No S. uureus B. cereus Klebsiella E. coli

MRS Culture broth 16 19 13 15

Fermented juice 15 18 11 14 bitter gourd

fenugreek leaves Fermented juice 12 16 10 12

Inhibition zone diameter in nun. Soul of culture filtrate/fermented juice per agar well.

whose culture filtrate showed maximum Z1 and low acid production was identified as Pediococcus pentosaceus. The inhibitory fac- tor of E pentosaceus retained complete activ- ity in the range of 3.5 to 5.0 when heated at 121°C for 30min, but above pH 5.0 the factor lost the inhibitory activity. The inhibitory factor also showed broad spectrum of anti- microbial activity against gram positive patho- gens B. cereus, S. aureus and gram negative spoilage bacteria Klebsiella spp. and pathogen E. coli. The Z1 ranged from 13 to 19mm (Table 1).

Lactic beverage standardisation Fermentation was assessed by changes in pH, acidity and the production of antimicrobial activity. Both the Z1 and acidity were sig- nificantly higher for cultured fermented juices than for naturally fermented juices (Figure 2). The acidity was low for naturally fermented BG and FL juices which were 0.1 and 0.2% respectively, while pure culture fermented jui- ces fermented with P. pentasaceus had higher acidity viz. 0.7 and 0.9% for BG and FL respectively. With increase in the level of inoculum of J? pentosaceus from 0.5 to 5.0% corresponding increase in acidity from 0.2 to 0.7% and from 0.2 to 0.9% was recorded in BG and FL respectively. The pH decreased from 3.9 to 3.2. Maxium Z1 (21 and 22mm) along with increased acidity was found when 5.0% inocu- lum was employed for both the vegetables BG and FL respectively. The level of inoculum was kept constant at 5.0% for all the subsequent trials.

Both the vegetables are low in fermentable carbohydrates, therefore dextrose had to be supplemented for the rapid growth of LAB. As the dextrose concentration increased there was Corresponding increase in acidity resulting in a slight decrease in pH. A pH of 3.2, acidity of 0.7 and 0.9% and Z1 of 20 mrn were attained in

. -1 I '

6

5

10

8

Ql 3

E P € 6

3 r D R 4

2

1 2

0 0

4 %

Y

BGUF BGNF BGCF FLUF FLNF FLCF

rn Zl(mm) Em PH LA (%)

ZI - Zone of inhibition, LA - Lactic acid Figure 2. Comparison of natural fermentation vs culture fermentation. BGUF - bitter gourd unfermented; BGNF - bitter gourd naturally fermented; BGCF - bitter gourd culture unfermented; FLUF - fenugreek leaves unfermented, FLNF - fenugreek leaves naturally fermented, FLCF - fenugreek leaves culture fermented.

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104 U. Gupta et al.

12 18 24 30 36 42 3.2 I I I I I I

12 18 24 30 36 42 Time (h)

l m O 1

01 I I I I I 12 18 24 30 36 42

Time (h) 2ow 15

lo[ 5

E o W 12 18 24 30 36 42

Time (h)

4.0

3.0 I I I I I I 12 18 24 30 36 42 4

Time (h)

h

Ei - 0.2 0 - u r " h

0- 12 18 24 30 36 42 48

Time (h)

25 I

l o 1 5

12 18 24 30 36 42 Time (h)

+ Control + 2%dextrose+ 2% sodium chloride

--c 2%dextrose

+ Control -D- 2% dextrose +

+ 2%dextrose

2% sodium chloride

Figure 3. Tie-course study of bitter gourd. Figure 4. Timecourse study of fenugreek leaves.

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Lactic fermented bitter gourd and fenugreek leaves 105

a 36h fermentation period with 5% level of inoculum and 2% dextrose. There was no appreciable change in acidity and antimicrobial activity at 4% dextrose level for both the vegetables.

In the traditional studies with lactic fermenta- tion of vegetables, sodium chloride is included in the fermenting medium as it is known to regulate the quantity of microflora by encourag- ing the establishment of LABS and preventing the proliferation of undesirable microorganisms during the prolonged natural fermentation peri- ods (Vaughn, 1982). The effect of sodium chloride was studied in fermentation employing pure culture of R pentosaceus. The Z1 was found to be reduced as the concentration of sodium chloride (0.5 to 1.0%) or complete elimination of sodium chloride brought about effective fermentation (indicating pH around 3.3, acidity 0.7% and Z1 20mm in both the vegetables). Fermented juice prepared without the sodium chloride was clearer than those prepared with salt at 2% levels.

The progress of fermentation was assessed in both the vegetables using 2% dextrose solution and with the addition of 2% sodium chloride. The 2% dextrose control sample (without addition of vegetable pulps) was also main- tained. Data on the progress of fermentation are presented in Figure 3 and 4. As discussed earlier, addition of sodium chloride gave lower acidity and Z1. The fermented juice without sodium chloride gave better acidity and had higher levels of antimicrobial factor. The pH and acidity of the control sample remained unchanged after a 12 h period and antimicrobial factor was absent.

Based on the above studies, the level of vegetable pulp to water ratio at 1:1, dextrose

concentration at 2% level, inoculum of R pentosaceus at 5.0% level and a fermentation period of 36 h were optimised to prepare lactic fermented juices. The juices were bottled, sealed, pasteurised and stored at ambient condition.

Nutritional evaluation of lactic fermented beverages The proximate analysis of the fermented and unfermented vegetable juices is given in the Table 2. It was revealed that the ash and carbohy- drate contents were reduced by 37 and 3.0% respectively, while protein content increased by 37% in BG due to fermentation. In FL the rela- tive reduction of ash was 18% and carbohydrate was 12% while protein content increased by 58% (Table 2). The relative increase in protein content may be attributed to bacterial bio-mass and con- version of inorganic nitrogen to organic nitro- gen. The fermentable carbohydrates and mineral salts were utilised by the LAB for their growth and hence there was decrease in carbohydrate. The decrease in ash content may be attributed to solubilisation of minerals.

From Table 3 it can be seen that vitamin B 12 appeared only in the fenugreek leaves fer- mented product, and there was slight reduction in folic acid (15-20%) in both bitter gourd and fenugreek leaves after fermentation. Riboflavin was not produced during fermentation. There was relative increase in pyridoxine and sig- nificant increase in vitamin C in fermented juice samples (Table 3).

Sensory evaluation and storage studies The sensory mean scores for fenugreek and bitter gourd juices are presented in Table 4 and 5 respectively. The fermented beverages

Table 2. Proximate composition of unfermented and fermented bitter gourd and fenugreek leaves juice (on dry weight basis)

Bitter gourd (g%) Fenugreek leaves (g%)

Constituents Unfermented Fermented Unfermented Fermented

Ash 6.4 Proteins 12.3 Fats 0.6 Carbohydrates 80.6

4. i 16.9 0.9 78.0

9.9 15.6 1.8 72.1

8.2 24.6 3.9 63.3

Results are the average of four estimations.

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106 U. Gupta et al.

Table 3. Vitamin contents of juice samples

Bitter gourd juice Fenugreek leaves juice (per 1oOml) (per I00 ml)

Fresh Fermented Fresh Fermented

Vitamin B12 Riboflavin Folic acid Pyridoxine Vitamin C*

nil nil 1.3

25.0 1.3

nil nil 1.1

37.5 37.7

nil 12.5 nil nil 1.5 1.2

17.8 44.0 0.8 18.8

All results are mean of two independent estimations. *Value in mg.

showed significantly better acceptability than the control. The F? pentosaceus fermented juices scored significantly better in all over quality parameters than either the control or the natu- rally fermented juice samples. Bitterness was reduced in the fermented products.

The juice samples analysed after 15, 30 and 45 days of storage showed that there was a

slight reduction in acidity from 0.64 to 0.57% and from 0.62 to 0.52%, and antimicrobial activity from 20 to 1 8 m (ZI) and 22 to 18mm (ZI) in bitter gourd and fenugreek fermented beverages respectively (Table 6). These values indicate that the juices can be stored at room conditions without any visible sign of spoilage since acidity with natural biopreservatives in

Table 4. The sensory mean scores (max 5) for fenugreek leaves juice

Fresh juice Naturally fermented Cultured fermented Parameters (control) juice juice i S E , (38 dfl

Physical appearance 3.0b Aroma 2.2' Mouth feel 2.28 Taste 1.9" Overall 2.P

2.4" 2.6b 2.4' 2.2' 2.2'

3.7' 3.8' 3.8b 3.8b 3.8b

0.17 0.12 0.16 0.12 0.12

Any two mean scores bearing Merent superscripts ', b, ', differ significantly (P>0.05). SE,,, (df) = standard errors of mean (degrees of freedom). Limits for mean scores: 1.5-2.5 = poor; 2.6-3.5 = fair, 3.6-4.5 = good.

Table 5. Sensory mean scores (max 5) for bitter gourd juice

Fresh juice Naturally fermented Cultured fermented Parameters (control) juice juice i S E , (3Sdfl

Physical appearance Aroma Mouth feel TaSte Overall quality

3 .P 2.4' 1.5" 1.8" 1.8'

2.5' 2.5' 2.1b 2.0b 2.1b

3.8' 0.15 3.2b 0.16 3.2' 0.10 3.3= 0.10 3.4c 0.09

Any two mean scores bearing different superscripts ', ', ', differ significantly (P>0.05). SE, (df) = standard errors of mean (degrees of freedom). Limits for mean scores: 1.5-2.5 = poor; 2.6-3.5 = fair, 3.6-4.5 = good.

\

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Lactic fermented bitter gourd and fenugreek leaves 107

'Igble 6. Storage studies of lactic fermented juices

Sample

Antimicrobial activity

ZZ in (mm) Storage period Lactic acid against B. cereus

(days) PH (96)

Bitter gourd

Fenugreek

0 15 30 45 0 15 30 45

3.4 3.1 3.1 3.1

3.2 3.1 3.1 3.1

0.64 0.58 0.57 0.57

0.62 0.55 0.53 0.52

20 18 18 18 22 20 19 18

the fermented juice check the spoilage of the product.

Discussion The pure culture fermentation studies on cucumbers, olives and other vegetables using Lactobacillus plantarum showed that the fer- mentation was completed in 7 to 12 days when incubated at 25 to 30°C (Ethchells et al., 1966). In order to aid the rapid fermentation process by lowering pH to 3.8 or less and acidity produc- tion from 0.7 to 1.0% glucose had been supplemented to the fermenting broth (Vaughn, 1975). The concentration of sodium chloride added varied with the type of vegetable, for example, lactic fermentation of cabbage to produce sauerkraut juice, a low level of salt (2.2 to 3.0%) was desirable (Vaughn, 1982), and in olive fermentation higher concentrations (8.0 to 10.0%) of salt was desirable, while in pickling fermentation of cucumbers a range of 5.0 to 15.0% salt was preferred (Joshi et al., 1993). In sauerkraut product colour retention was ach- ieved with low (1 .O%) sodium chloride concen- tration (Vaughn, 1982). Considerable work on lactic fermented vegetable juices such as carrot, ash gourd, pumpkin, drumstick and other veget- ables using L. plantarum has been conducted in India (Nirmala Devi et al., 1992) and they successfully preserved lactic fermented vegeta- ble juices at room conditions. In our study with pure culture of P pentosaceus and supplementa- tion of glucose the fermentation time was drastically reduced to 36h by incubating the broth at 37°C.

Bitter gourd, a popular vegetable extensively consumed in India, is also used in the indige- nous system of medicine to treat a number of diseases. It is known as vegetable insulin as it contains a glycopeptide with insulinometric property (Ng et al., 1986). It retards retinopathy in rats (Srivatsava et al., 1987) and is a scavenger of superoxide and hydroxy radicals. The anti-diabetic activity seemed to be medi- ated through the scavenging of toxic oxygen radicals (Sreejayan Rao, 1990). Similarly, fenu- greek is a popular leafy vegetable that contain trigonelline, an alkaloid known to have an effect on glycosuria (Rao & Sharma, 1987). The hypoglycemic principle isolated from fenugreek seems to act at pancreatic and extra-pancreatic sites (Moorthy et al., 1989). Fenugreek leaves contain a good amount of mucilage and fibre effective for management of diabetes. The fermented juice with nutritive, therapeutic and storage properties is sure to find use in health- associated benefit application.

In food preservation, it is important to assure that most of the nutritive value of the fresh food is retained in the processed product. In the present study, it was found that pyridoxine and vitamin C increased relatively in both the products and vitamin B12 appeared only in fermented fenugreek leaves product after lactic fermentation. The reduction of bitter taste in both the vegetables may have been due to degradation of bitter principles as reported in olives (Etchells et al., 1966). There was also relative increase in protein and fat in the fermented products. The only anti-microbial factor produced by LAB and currently used in

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108 U. Gupta et al.

food industry is nisin which is produced by Lactococcus lactis ssp. lactis and has a limited applicability because of its narrow range of antibacterial activity and its instability at neutral and alkaline pH conditions (Bemdge, 1949). Our studies highhght that the LAB I! pentosu- ceus brought about fermentation of both the vegetables, and the product remained stable

without any sign of deterioration at ambient conditions in relation to microbial safety and sensory attributes due to natural biopreservative.

Acknowledgement-The authors express their sincere gmh- tude to the D i t o r , CFllU, Mysore for pviding the facilities.

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