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doi:10.1016/j.jv

Journal of Veterinary Behavior (2012) 7, 233-237

RESEARCH

A survey of animal bites on humans in Bursa, Turkey

Ebru Yalcina, Havva Kentsub, Hasan Batmaza

aDepartment of Internal Medicine, Faculty of Veterinary Medicine, Animal Teaching Hospital, Uludag University, Nilufer,Bursa, Turkey; andbDepartment of Infectious Diseases, Bursa State Hospital, Bursa, Turkey.

KEYWORDS: Abstract Animal bites are a major public health problem. The aim of this study was to conduct a survey

animal bite;dog;epidemiology;public health;children;

bite location

of animal bites in Bursa, Turkey. Patients who sought medical care for animal bites over an 18-monthperiod were included in our study (n 5 1,715). Data were obtained from the registry of the Bursa StateHospital; 71.84% of the patients were men and 28.16% were women. Bites were most frequent amongpatients who were .18 years of age (comprising 60.83% of all bites). The anatomical site of the bitewas recorded in all 1,715 cases, and 1,778 bite locations on the body were reported. The upper extrem-ities were the most frequent sites of animal bites (53.83%), followed by the lower extremities (38.03%).Bites were most frequently inflicted by dogs (68.04%), followed by cats (28.45%), mice (2.56%), andother animals (hamsters, donkeys, horses, foxes, and rabbits together comprised 0.95% of the bites). Asa result, bite incidents were mostly associated with males aged .18 years and occurred in the upperextremities. This study showed that dog bites constitute a major animal bite problem in Bursa, Turkey.� 2012 Elsevier Inc. All rights reserved.

Introduction

Animal bites, particularly dog bites, are a major publichealth problem throughout the world for some major reasonssuch as tissue injury, secondary infections, and rare possi-bility of contracting rabies (Morgan and Palmer, 2007).Animal bites and scratches, even when they are minor, canbecome infected and spread bacteria to other parts of thebody. The microorganisms involved tend to originate fromthe oral cavity of the offending biter and the environmentwhere the injury occurred. The other major health risk ofanimal bites, rabies, is still common among stray animalsin Turkey and institutes a significant public health risk forthe country (Buyuk et al., 2007; Vos et al., 2009).

reprint requests and correspondence: Ebru Yalcin, PhD,

nternal Medicine, Faculty of Veterinary Medicine, Animal

al, Uludag University, 16059 Nilufer, Bursa, Turkey; Tel:

11; Fax: 190 224 294 0873.

ine@uludag.edu.tr

ee front matter � 2012 Elsevier Inc. All rights reserved.

eb.2011.08.008

In Turkey, between 1995 and 2004, 240 animal bite-related deaths occurred, and 39,511 patients requiredhospitalization in state hospitals (Turkish StatisticalInstitute: Health Statistics, 2008). In a retrospective studyconducted in Turkey, animal-related injuries contributedto 0.2% of all emergency department admittances. Of those,dog bites were most commonly encountered (30%),followed by horse- (22%) and livestock-related injuries(12%). Males were more frequently (73.2%) involved,and bites occurred often during summer months (16.5%in July and 18.5% in August). Hospitalization was signifi-cantly higher in mammal-related injuries (67.9%) com-pared with nonmammal injuries (32.1%) (Emet et al.,2009). Just to make a comparison, an average of 0.655fatalities per million per year was recorded in the UnitedStates of America (Langley, 2005), whereas this rate wasalmost half (approximately 0.364 fatalities per million peryear) in Turkey (Turkish Statistical Institute: HealthStatistics, 2008).

Table 1 Details of 1,715 animal bites treated in the State Hospital in Bursa, Turkey: Species of the aggressor

Animal n (%)

Patient sex Patient age (years)

Male (%) Female (%) 0-5 (%) 6-12 (%) 13-18 (%) .18 (%)

Dog 1,167 (68.04) 900 (77.12) 267 (22.87) 103 (8.82) 211 (18.08) 141 (12.08) 712 (60.83)Cat 488 (28.45) 296 (60.65) 192 (39.34) 53 (10.86) 109 (22.33) 40 (8.19) 286 (58.60)Mouse 44 (2.56) 29 (65.90) 15 (34.09) 1 (2.27) 1 (2.27) 8 (18.18) 34 (77.27)Hamster 8 (0.46) 4 4 – 2 2 4Donkey 3 (0.17) 1 2 – – – 3Horse 2 (0.11) 1 1 – – – 2Rabbit 1 (0.11) – 1 – 1 – –Fox 2 (0.05) 1 1 – – 1 1Total 1,715 1,232 (71.84) 483 (28.16) 157 (9.15) 324 (18.90) 192 (11.20) 1,042 (60.75)

234 Journal of Veterinary Behavior, Vol 7, No 4, July/August 2012

Dogs are most commonly responsible for animal bites. Inthe literature (Overall and Love, 2001), the frequency of dogbites has been estimated to be approximately 18 per1,000 subjects. In Ireland (O’Sullivan et al., 2008),21% of 234 dog bite incidents were considered to be serious,whereas 2% were considered to be life-threatening. Afterdogs, cats account for approximately 25% of the reportedbites. Twenty to fifty percent of cat bites become infected,with the risk of infection based on bite location, host factors,and local wound care (Loar, 1987). Furthermore, cats aremore likely than dogs to be exposed to rabid bats and lesslikely to be vaccinated against rabies, which increases therisk of rabies among cat bite victims (Hoff et al., 1993).Other animals, including rodents, rabbits, horses, monkeys,fox, and sheep, comprise the remaining 5%-10% of bitecases (Moore et al., 2000; Eslamifar et al., 2008).

Children are the most frequent victims of animal bitesworldwide (Sacks et al., 1996; Weiss et al., 1998; Overalland Love, 2001) and are at least 3-5 times more likely toexperience dog bites than adults (Overall and Love,2001). Data from reported bites requiring medical attentionindicate that children younger than 15 years of age in theUnited States of America are the most commonly affectedgroup (Sacks et al., 1996; Weiss et al., 1998). Most fatali-ties from dog bites are observed in young children andare due to head and neck injuries (Cleaveland et al.,2002; Monroy et al., 2009; Rosado et al., 2009).

The objective of this study was to determine whichanimal species were responsible for bites, their origin andownership status, and to describe the population of peoplebitten and the anatomical location of bites among patientsreferred to a major hospital in Bursa, Turkey. This is thefirst study of this nature performed in this region.

Materials and methods

Study type

This retrospective study was performed on patients withanimal bites who were referred to the State Hospital in

Bursa, Turkey, between January 1, 2004 and June 30, 2005(18 months).

Study site

Study victims and aggressors all resided in Bursaprovince city center or rural areas. Similar to Rosadoet al. (2009), we assessed the distribution of animal bitesbased on residence in urban versus rural settings; patientswere categorized as living either in high-population areas(average density: .5,000 inhabitants/km2) or in low-population areas (average density: ,50 inhabitants/km2).

Data collection

Data were obtained from the registry of the Bursa StateHospital and included age, sex, address, anatomic locationof bite(s), the species of the biting animals, and the owner-ship status. Bite victims were categorized into the following4 age groups:,6, 6-12, 13-18, and.18 years. Bite locationswere grouped into the following 4 categories: upper extrem-ities, lower extremities, thorax and abdomen, and head. Dataregarding the animals’ breed, age, and sex were not readilyavailable and therefore were not included in this study.

Results

A total of 1,715 victims treated for animal bites (1,778 bites;some victims were bitten at more than 1 anatomic location)were included in our study. The distribution of the animalspecies is shown in Table 1. The data show that dog biteswere the most frequent (68.04%) animal bites. Of allanimal bite victims, 71.84% of the animal bite victimswere men and 28.16% were women. Bites were mostfrequent in the .18 years age group (60.75%), followed bythe 6-12 years age group (18.90%), the 13-18 years age group(11.20%), and the 0-5 years age group (9.15%). The upperextremities were the most frequent bite site (53.83%),followed by the lower extremities (38.03%), the head(4.83%), and the thorax and abdomen (3.31%) (Table 2).

Table 2 Distribution of the injury sites

Animal

Bite locations

Upperextremities

Lowerextremities

Thorax andabdomen Head

Dog 561 (44.03) 612 (48.03) 53 (4.16) 48 (3.76)Cat 351 (79.77) 55 (12.50) 5 (1.13) 29 (6.59)Mouse 31 (67.39) 7 (15.21) 1 (2.17) 7 (15.21)Hamster 8 – – –Donkey 3 1 – 1Horse 1 – – 1Rabbit – 1 – –Fox 2 – – –Total 957 (53.83%) 676 (38.03) 59 (3.31) 86 (4.83)

Yalcin et al Animal bite problem in Bursa, Turkey 235

Data on the ownership status and residence area of theanimals are presented in Table 3. Although most (72.15%)of the dogs included in the study were owned, most of thecats (58.12%) were feral. Majority of the animal bites(61.98%) occurred in nonurban areas.

Discussion

Animal bites comprise an important public health problem(Weiss et al., 1998). In a previous study conducted in Turkey,animal-related injuries comprised 0.2% of all emergency de-partment admittances and mostly involved mammal-relatedbites occurring in males during summer (Emet et al., 2009).In the current study, men were the victims in 71.84% of theanimal bites, similar to some other studies (Kilic et al., 2006;Emet et al., 2009). In contrast, in a study conducted in PuertoRico (Quiles-Cosme et al., 2000), the distribution of animalbites was equal in both men and women.

In the current study, when the overall animal bites wereexamined, we observed that people aged .18 years hadthe highest frequency of animal bites. Upper extremitieswere the most frequent bite region. Similar findings wereobserved by other researchers regarding the affected agegroup (Rasania et al., 2004; Kilic et al., 2006; Emet al.,2009) and location of the bite (Quiles-Cosme et al., 2000).

Table 3 Distribution of the ownership status and residence area

Animal

Ownership

Yes No

Dog 842 (72.15) 325 (27.84Cat 188 (41.87) 261 (58.12Mouse 3 (6.81) 41 (93.18Hamster 6 2Donkey 2 1Horse 1 1Rabbit 1 –Fox – –Total 1,043 (60.82) 672 (39.18

In this study, regarding the aggressor species, most biteswere inflicted by dogs (68.04%), followed by cats (28.45%),mice (2.56%), and other species (0.95%). This distributionof biting species is similar to other studies (Moore et al.,2000; Kilic et al., 2006; Emet et al., 2009). The ratio ofmale victims bitten by cats was 60.65% in this study.Although some researchers have found similar results(Patrick and O’Rourke, 1998), most studies suggest thatwomen are more likely than men to be bitten by cats(Underman, 1987; MacBean et al., 2007). Thirty of themouse bites (68.18%) reported in the hospital data occurredin city centers, likely because of the increased density ofmice in these areas. We assume that unreported cases thatoccur in rural areas also play an important role in this result.

In this study, the highest percentages of dog and cat bites(60.83% and 58.60%, respectively) that required medicaltreatment in a hospital occurred in people.18 years of age,whereas the second highest percentages (18.08% and22.33%, respectively) occurred in the 6-12 years age group.Dog attacks on children are thought to be attributed to theirsmaller size and the proximity of their face to the dog’smouth, and attacks are generally related to interactionswith the dog (possibly provocative) before the attack(MacBean et al., 2007; Ozanne-Smith et al., 2001). Theundeveloped motor skills of children and the relativelylarge size of the head in comparison with the body arealso contributing factors. In addition, children often demon-strate willingness to bring their faces within the area per-ceived as an intimate and threatening distance by dogs,which increases the likelihood of an attack. Finally, faceand neck biting of children may be an extension of theface and mouth biting behavior of dogs with each otherin learning dominance behavior (Brogan et al., 1995). Bitesin children can be decreased by increasing awareness ofrisk situations with dogs and by adult supervision. Pro-grams such as the Blue Dog are a valuable adjunct in thiscontext (Meints and de Keuster, 2009).

Dog bites most frequently occurred on the lowerextremities (48.03%), followed by the upper extremities.Patrick and O’Rourke (1998) found that dog bites occurredall over the body: face/head (16.1%), hands/arms (36.7%),

Residence area

Nonurban Urban

) 516 (54.25) 435 (45.74)) 351 (89.76) 40 (10.23)) 27 (69.23) 12 (30.76)

6 0– 3– 21 –2 –

) 1,063 (61.98) 652 (38.02)

236 Journal of Veterinary Behavior, Vol 7, No 4, July/August 2012

trunk (8.0%), feet/legs (33.2%), and at multiple sites(5.9%). This distribution may be a result of the small sizeof many dogs, which may result in increased accessibilityto the lower extremities. Injuries to the upper extremitiesare often associated with large-sized dogs, which attackupward, or with the upper extremities being used in defenseby the victims. Cornelissen and Hopster (2010) found thatmost bites occurred on the upper extremities (58%), fol-lowed by the lower extremities (29%). Head injuries mostfrequently occurred in bite victims younger than 12 yearsof age (71.04%), which is in accordance with findings ofother studies (Kahn et al., 2004; Monroy et al., 2009).

In the current study, cat bites were most frequentlyobserved on the upper extremities (79.77%). Patrick andO’Rourke (1998) found that the majority of cat bites(78.9%) occurred only on the hands or arms, and thatvictims were likely to have provoked the cat by trying topick it up or pet it. Cats are agile and are often contactedwith the hands, which may be a reason for the majority ofcat bites occurring on the hands (Patrick andO’Rourke, 1998).

Approximately 72% of biting dogs in this study hadowners, which is consistent with previous reports (Kahnet al., 2003; Schalamon et al., 2006).

Studies in Europe suggest that the majority of bites occurin the child’s home by a pet (Kahn et al., 2004; Morgan andPalmer, 2007; Cornelissen and Hopster, 2010). In some cul-tures, as in Turkey, there may be a significant free-roamingdog population (De Keuster and Butcher, 2008). It is inter-esting to note that these free-roaming dogs constitute alower risk than the owned dogs regarding the animal bites.

Turkey is the only country in Europe where urban dog-mediated rabies persists. Control measures in recent decadeshave reduced the burden of rabies to relatively low levels,but rabies still persists in certain areas, particularly urbanareas. Occasional human cases result from this persistence,although the source of these cases appears to involve bothdogs and wildlife reservoirs (Johnson et al., 2010).

This study shows that animal bites are a major healthproblem in Bursa, Turkey. It is likely that uncomplicatedanimal bites are not referred for medical care and that theactual ratio of animal bites could be greater than that reportedin this study. Further studies are required to investigate otheraspects of the animal bite problem, such as the diseasestransmitted through these bites and the economic burden theproblem poses on the health industry. As rabies is stillcommon in Turkey, application of strict vaccination pro-grams for the eradication of the disease and publicwidewarnings about the risk of animal bites are needed.

References

Brogan, T.V., Bratton, S.L., Dowd, M.D., Hegenbarth, M.A., 1995. Severe

dog bites in children. Pediatrics 96, 947-950.

Buyuk, Y., Uzun, I., Aybar, Y., Kurnaz, G., Ozaras, R., 2007. Rabies in

Turkey: three human cases illustrating the importance of suspecting

exposure. Wilderness Environ. Med. 18, 214-217.

Cleaveland, E., Fevre, E., Kaare, M., Coleman, P.G., 2002. Estimating hu-

man rabies mortality in the United Republic of Tanzania from dog bite

injuries. Bull. World Health Org. 80, 304-310.

Cornelissen, J.M., Hopster, H., 2010. Dog bites in The Netherlands: a

study of victims, injuries, circumstances and aggressors to support

evaluation of breed specific legislation. Vet. J. 186, 292-298.

De Keuster, T., Butcher, R., 2008. Preventing dog bites: risk factors in

different cultural settings. Vet. J. 177, 155-156.

Emet, M., Beyhun, N.E., Kosan, Z., Aslan, S., Uzkeser, M., Cakir, Z.G.,

2009. Animal-related injuries: epidemiological and meteorological

features. Ann. Agric. Environ. Med. 16, 87-92.

Eslamifar, A., Ramezani, A., Razzaghi-Abyaneh, M., Fallahian, V.,

Mashayekhi, P., Hazrati, M., Askari, T., Fayaz, A., Aghakhan, A.,

2008. Animal bites in Tehran, Iran. Arch. Iranian Med. 11, 200-202.

Hoff, G., Mellon, G., Thomas, M., Giedinghasen, D., 1993. Bats, cats, and

rabies in an urban community. South Med. J. 86, 1115-1118.

Johnson, N., Un, H., Fooks, A.R., Freuling, C., Muller, T., Aylan, O.,

Vos, A., 2010. Rabies epidemiology and control in Turkey: past and

present. Epidemiol. Infect 138, 305-312.

Kahn, A., Bauch, P., Lamoureux, J., 2003. Child victims of dog bites trea-

ted in emergency departments. Eur. J. Ped. 162, 254-258.

Kahn, A., Rober, E., Piett, D., De Keuste, T., Lamoureux, J., Leveque, A.,

2004. Prevalance of dog bites in children. A telephone survey.

Eur. J. Ped. 163, 424.

Kilic, B., Unal, B., Semin, S., Konakci, S.K., 2006. An important public

health problem: rabies, suspected bite, and post-exposure prophylaxis

in a health district in Turkey. Int. J. Infect. Dis. 10, 248-254.

Langley, R.L., 2005. Animal-related fatalities in the United States-an

update. Wilderness Environ Med. 16, 67-74.

Loar, M., 1987. Risks of pet ownership: the family practitioner’s view-

point. In: August, J., Loar, A. (Eds.), The Veterinary Clinics of North

America: Small Animal Practice. W.B. Saunders Co., Philadelphia,

PA, pp. 17-25.

MacBean, C.E., Taylor, D.M., Ashby, K., 2007. Animal and human bite

injuries in Victoria, 1998–2004. Med. J. Aust. 186, 38-40.

Meints, K., de Keuster, T., 2009. Brief report: don’t kiss a sleeping dog: the

first assessment of "the blue dog" bite prevention program. J. Pediatr.

Psychol. 34, 1084-1090.

Monroy, A., Behar, P., Nagy, M., Poje, C., Pizzuto, M., Brodsky, L., 2009.

Head and neck dog bites in children. Otolaryngol. Head Neck Surg.

140, 354-357.

Moore, D.A., Sischo, V.M., Hunter, A., Miles, T., 2000. Animal bite epi-

demiology and surveillance for rabies postexposure prophylaxis.

J. Am. Vet. Med. Assoc. 217, 190-194.

Morgan, M., Palmer, J., 2007. Dog bites. Br. Med. J. 334, 413-417.

O’Sullivan, E.N., Jones, B.R., O’Sullivan, K., Hanlonn, A.J., 2008. Char-

acteristics of 234 dog bite incidents in Ireland during 2004 and 2005.

Vet. Rec. 163, 37-42.

Overall, K., Love, M., 2001. Dog bites to humans: demography, epidemi-

ology, injury and risk. J. Am. Vet. Med. Assoc. 218, 1923-1934.

Ozanne-Smith, J., Ashby, K., Stathakis, V.Z., 2001. Dog bite and injury

preventiondanalysis, critical review, and research agenda. Inj. Prev.

7, 321-326.

Patrick, G.R., O’Rourke, K.M., 1998. Dog and cat bites: epidemiologic

analyses suggest different prevention strategies. Public Health Rep.

113, 252-257.

Quiles-Cosme, G.M., Perz-Cardona, C.M., Aponte-Orti, F.I., 2000.

Descriptive study of animal attacks and bites in the municipality of

San Juan, Puerto Rico, 1996-1998. P. R. Health Sci. J. 19, 39-47.

Rasania, S.K., Bhall, S., Khandekar, J., Pathi, S., Matta, S., Singh, S.,

2004. Postexposure management of animal bite cases attending

a primary health center of Delhi. J. Common Dis. 36, 195-198.

Rosado, B., Garcia-Belenguer, S., Leon, M., Palacio, J., 2009. A

comprehensive study of dog bites in Spain 1995-2004. Vet. J. 179,

383-391.

Sacks, J.J., Kresnow, M., Houston, B., 1996. Dog bites: how big a prob-

lem? Inj. Prev. 2, 52-54.

Yalcin et al Animal bite problem in Bursa, Turkey 237

Schalamon, J., Ainoedhofer, H., Singer, G., Petnehazy, T., Mayr, J.,

Kiss, K., Hollwarth, M.E., 2006. Analysis of dog bites in children

who are younger than 17 years. Pediatrics 117, 374-379.

Turkish Statistical Institute: Health Statistics, 2008. Data according to rea-

son of diseases. Available at: http://www.tuik.gov.tr/VeriBilgi.do?

tb_id56&ust_id51. Accessed June 3, 2008.

Underman, A., 1987. Bite wounds inflicted by dogs and cats. In:

August, J., Loar, A. (Eds.). The Veterinary Clinics of North America:

Small Animal Practice. W. B. Saunders Co., Philadelphia, PA,

pp. 195-207.

Vos, A., Freuling, C., Eskiizmirliler, S., Un, H., Aylan, O., Johnson, N.,

Gurbuz, S., Muller, W., Akkoca, N., Muller, T., Fooks, A.R.,

Askaroglu, H., 2009. Rabies in foxes, Aegean region, Turkey. Emerg.

Infect. Dis. 15, 1620-1622.

Weiss,H.B., Friedman,D.I., Coben, J.H., 1998. Incidence of dog bite injuries

treated in emergency departments. J. Am. Med. Assoc. 279, 51-53.