OsongPublicHealthResPerspect20123(1),14e18 doi:10.1016/j.phrp.2012.01.002 pISSN2210-9099 eISSN2233-6052 - - ORIGINAL ARTICLE Epidemiologic Features of Animal Bite Cases Occurring in Rabies-Endemic Areas of Korea, 2005 to 2009 Myung Guk Han*, Jung Sang Ryou, Young Eui Jeong, Young Ran Ju, Jung Eun Cho, Jun-Sun Park Division of Arboviruses, Korea National Institute of Health, Osong, Korea. Received:October4, Abstract 2011 Objectives:HumanrabiesisareemerginginfectiousdiseaseinKorea.Therewas Revised:December 15, no human rabies case for 14 years until the disease had reoccurred in 1999. To 2011 prevent occurrence of human rabies, surveillance for animal bite patients in Accepted: January5, rabies endemic areas in Korea was conducted since 2005 as a part of a human 2012 rabies control program. The animal bite cases were analyzed to determine whetherpatientsweretreatedaccordingtothepost-exposureprophylaxis(PEP) KEYWORDS: guidelineofthe KoreaCenters forDisease ControlandPrevention. Methods: Information of animal bite cases that occurred from 2005 to 2009 in animalbite, rabies high-risk regions were collected by cooperation with Regional Public post-exposure Health Centers in18cities/districts of rabiesendemic areas. prophylaxis, Results:Atotalof2458animalbitecaseswerereported.Dogsaccountedfor86% rabies, ofanimalbitesand67%oftheanimalswerenotvaccinatedagainstrabiesvirus. wildanimal ForPEP,amongrabies-vaccinatedanimals,92.7%wereobservedforclinicalsigns and 1.4% underwent necropsy. Among unvaccinated animals, 72.7% were observedforclinicalsignsand4.1%underwentnecropsy.Theremaininganimals werenotavailableforexamination.Oftheanimalbitepatients,32.5%received PEPand51.6% weretreatedby firstaidor by washingthe wound. Conclusions: Given that no human rabies cases were reported since 2005 and animal rabies was continuously reported in endemic areas of Korea, the human rabiescontrolprogramimplementedin2005appearstohaveasignificantrolein the prevention andcontrol ofhuman rabies. 1. Introduction reservoir of rabies virus, but dogs are a predominant animal for transmission. There were no human cases of Rabies is a representative zoonosis and a reemerg- rabies from 1985 to 1998, but the disease reoccurred in ing disease in Korea. In Korea, the raccoon dog 1999, following a new case of animal rabies in 1993 (Nyctereutes procyonoides) is a principal natural [1,2]. *Correspondingauthor. E-mail:[email protected] This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0)whichpermitsunrestrictednon-commercialuse,distribution,andreproductionin anymedium,providedtheoriginalworkisproperlycited. Copyrightª2012KoreaCentersforDiseaseControlandPrevention.PublishedbyElsevierKoreaLLC.Allrightsreserved. Epidemiologic features of animal bites 15 Human rabies can be prevented by avoiding bite Animal Bite Patient Surveillance (NABPS) program of rabid animals, pre-exposure vaccination or post- wasimplementedin2005byguidelinesoftheHRCPto exposure prophylaxis (PEP). The guidelines for prevent human rabies. The NABPS was performed in Human Rabies Prevention and Control (HRPC) by close cooperation with KCDC, the Regional Public Korea Centers for Disease Control and Prevention Health Centers (RPHC), and two Provincial Veterinary (KCDC) recommends PEP based on the anatomical Service Laboratories in the rabies endemic areas. High- locations of the bite, animal species, wound status, and risk and suspect-risk regions were designated by rabies vaccination history of the animal [3]. Patients guidelines of the HRCP. Animal bite patients in the whoacquiredbitesthatwereapplicabletoWorldHealth high-risk region report to RPHC and are received Organization (WHO) Categories II and III in high-risk a proper measurement including PEP. regions should immediately receive PEP, and animals Inthisstudy,weanalyzedanimalbitecasesfromthe shouldbeobservedforclinicalsignsorbeexaminedfor high-risk region from 2005 to 2009 to determine the rabies diagnosis [5]. According to the KCDC rabies current status of animal bites and to determine whether guidelines, PEP should be completed by administering patients were properly treated. We also discuss risk vaccine on Days 0, 3, 7, 14 and 28, with human rabies factors of rabies in the high-risk region and conclude immune globulin (HRIG) on Day 0. Equine rabies that NABPS contributed to human rabies prevention immunoglobulin is not permitted to use for animal bite since 2005, although animal rabies, including wildlife, patients in Korea. If no clinical signs of rabies in an has continuously been reported in the high-risk region. animalwereobservedwithin10daysorifananimalwas negative for rabies diagnosis by molecular and histo- pathological examinations, the remainder of PEP is not 2. Materials and Methods necessary. Alternatively, for animal bites that occur nationwide, including the suspect-risk regions, animals The risk areas of rabies were divided into high-risk should be observed for clinical signs for 10 days. If and suspect-risk regions according to the KCDC animals are clinically normal, PEP is not necessary. guidelineoftheHRCP(Figure1)[4].Thecities/districts However,ifabnormalclinicalsignsareobserved,PEPis where human or animal rabies had occurred since 1993 required,andtheanimalshouldbeconsideredforrabies are designated as high-risk regions. Cities/districts diagnosis. If no animal is available for rabies examina- which are adjacent with the high-risk regions are tion or if the bite is caused by a wild animal regardless assigned tosuspect-risk regions. There are nineteenand ofgeographicallocation,PEPshouldbeadministeredto 14 cities/districts in the high-risk region and in the a patient immediately. suspect-risk region, respectively. Two cities/districts Due toexpandingregions ofanimal rabies outbreaks were switched to the high-risk region from suspect-risk and to increasing public health threats, the National region in 2005 due to the occurrence of rabies in Figure 1. High-risk and suspect-risk regions of human rabies in Korea. The cities/districts where human or animal rabies had occurredsince1993are designatedashigh-riskregions.Theregionsare locatedinthenorthernpartofGyeonggiandGangwon provincesandaresurroundedbytheHanRiver,anexpressway,theEastSeaandthedemilitarizedzone.High-riskandsuspect-risk regions are indicated inblueand lightblue, respectively. 16 M.G. Han, et al raccoon dogs and farm animals. The high-risk region in from the high-risk region located near the DMZ Gangwon province was 1.7 times wider than that in (Table 1) and there were no human rabies case since Gyeonggi province. The human population in the high- 2005. The estimated incubation periods of the patients risk region was 3.5 times higher in Gyeonggi province varied from 3 to 11 weeks. Three patients with facial than in Gangwon province. woundshadshorterincubationperiodsthantwopatients Humanrabiesdatafrom1999to2009werecollected with wounds on their arms. Details of the first case of fromcasereportsofwrittenepidemiologicinvestigations rabiesweremissedbecauseofdelayedreporting.Ofthe intheKCDC.Wealsocollectedanimalbitecasedatafrom sixcases,fourwerecausedbydogsandtwowerecaused high-riskregionsfrom2005to2009andcalculatedanimal by raccoon dogs. Rabies PEP was applied to two cases bite incidences for the city/district and for different age that had wounds around their eyes. One patient was groups.AccordingtotheguidelineoftheHRCP,animal administered rabies vaccine and an inaccurate dose of bite patients should be reported to the RPHCs in the HRIG. Another patient was administered PEP after the patient’s residential region. The information from cases onset of clinical symptoms. reported to the RPHCs was submitted quarterly to the KCDCforanalysis.AllRPHCsin18citiesoftwoprov- 3.2. Animal bite cases incesinthehigh-riskregionparticipatedintheNABPS. A total of 2,458 animal-related potential rabies Information was divided into patient information and exposures in high-risk regions were reported to RPHCs animalinformation.Patientinformationincludeddateand from 2005 to 2009. The annual number of animal bite regionwheretheanimalbiteoccurred,sex,age,location case was ranged from 359 to 658 (mean: 491.6). The of wounds, and types of PEP applied (complete or lowestnumberofannualcaseswasreportedin2005and appropriate). Complete PEP means that both HRIG and the number increased thereafter. A mean bite rates in vaccination were administered. Appropriate PEP means each city/district in the high-risk regions of Gangwon thatvaccinationwasadministeredwithoutHRIG.Animal and Gyeonggi provinces were 61.4 (cid:1) 41.2 (mean (cid:1) data included animal species, rabies vaccination history SD) and 22.0 (cid:1) 21.0, respectively, and ranged from andanalysisofanimalafterbitingincludingobservation 0.3 to 113.7 per 100,000 individuals. An annual mean ofclinicalsignsornecropsy.Animalswereconsideredas incidence rate of more than 50 was recorded in five vaccinated if vaccinated or boostedwithin 1 year of the cities/districts of Gangwon province and in one cities/ biting incident. Clinical signs were observed by veteri- districts of Gyeonggi province. nariansemployedinlocal governments and rabiesdiag- Most patients were bitten in the hand or leg (44.2% noses by animal necropsy were accomplished at the and 33.9%, respectively), followed by the arm (9.6%), Provincial Veterinary Service Laboratories by histopa- foot(4.0%),face(2.5%),andhip(1.1%).Somepatients thology, indirect immunofluorescent assay and reverse (2.8%) were bitten on more than two body sites. Most transcription-polymerasechainreaction(REF). bitepatientshadCategoryIIIexposure,aspertheWHO The study was approved by the KCDC in 2005 and classification and Category II exposure reported in less compliedwiththeguidelinesoftheKCDC.Thedatawere than 5% of the cases. The incidence was highest in submitted to KCDC by the RPHCs without information adults in their 50s (18.0%), followed by 40s (17.6%), about individuals and clinical intervention. Information 60s (15.8%), and 30s (12.5%). Young children under 9 on human rabies cases did not include any personal years of age accounted for 7.2% of all cases. The information.Alldatawereanalyzedanonymously. numberofcaseswashigherinmen(62.4%)thanwomen (37.6%) and there was no significant difference of patient’s sex between two provinces or among different 3. Results ages. The cases of animal bite patients were higher in July and gradually increased from winter and spring to 3.1. Rabies cases summer. Since the reoccurrence of human rabies in 1999, six Dogs were the predominant biting animals and were cases of human rabies were reported to KCDC to 2004 responsiblefor86.0%ofanimalbites.Unprovokedbites Table 1. Human rabiescases from 1999to2004 Year City/district Site ofwound Rabidanimal Incubationperiod (wk) PEP 1999 Paju-si Unknown Dog Unknown Unknown 2001 Hwacheon-gun Arm Raccoon dog 11 No 2002 Yeoncheon-gun Face Dog 5 Yes 2003 Pocheon-si Face Dog 3 Yes 2003 Pocheon-si Face Raccoon dog 8 No 2004 Goyang-si Arm Dog 11 No PEPZpost-exposureprophylaxis. Epidemiologic features of animal bites 17 by stray dogs accounted for 3.2% of animal bites or appropriate PEP. Among patients that were bitten by (Figure 2). Cats, including strays, were responsible for unvaccinated animals (including wildlife), 31.7% 6.2% of animal bites. Wildlife accounted for 3.7% of received PEP in 2005, and gradually increased to animal bites. Raccoon dogs (1.4%) were the common 37.0%, 42.2%, and 47.7% in 2006, 2007, and 2008, wildlifespecies.Fourcaseswerefromcattleinhigh-risk respectively. In 2009, 39.8% of patients received PEP. regions. Wildrats,badgers,otters, wildboars,squirrels, Of430patientsthatwerebittenbyunavailableanimals, weasels, and bats were also involved in producing 272 cases (63.3%) received PEP. Complete PEP was woundsinhumans.Exposuretobatbiteswasreportedin administered in all patients bitten by confirmed rabid onlyonecasein2006.Thespeciesofbitinganimalwas animals. notidentifiedfor96cases,ofwhichwere75casesfrom one city in 2005. Ofthe2,273animalbitecases,67.4%oftheanimals 4. Discussion were not vaccinated against rabies or were vaccinated more than one year before the incident. The ratio of Due to outbreaks of animal rabies in limited areas, animals vaccinated against rabies within 1 year before HRCP focused mainly on management of animal bite biting decreased each year (46.7%, 36.0%, 33.8%, patients and on public education in the endemic areas. 27.7%,and27.2%in2005,2006,2007,2008,and2009, Unexpectedly high number of animal bite cases was respectively). Of 95 cats, only two were vaccinated reported in the first year of HRCP, although PEP data against rabies. A total of 77 animals were examined by were only passively collected by the reporting of necropsy for the rabies and 22 were rabid. These patientstoRPHCsthatwereprovidedPEP.Thismaybe included 16 dogs, three raccoon dogs, and three cattle. because the PEP service was free. The total number of Animals were divided into two groups depending on reported cases gradually increased, although this was rabies vaccination history to analyze whether affected by many factors. This finding may reflect measurements were appropriately applied. Measure- increased knowledge about rabies among the residents ments to vaccinated and unvaccinated animals were to in the high-risk region rather than due to more bite observe clinical signs of rabies for 92.7% and 72.7%, cases. respectively, of the cases and to perform necropsy for HRCPplaysakeyroleinpreventinghumanrabiesin 1.4% and 4.1%, respectively (Table 2). No animals Korea. However, several risk factors should be consid- showedclinicalsignsduringtheobservationperiod.For eredtokeepafreeofhumanrabies.Ahighincidenceof 1.6% and 16.6% of the vaccinated and unvaccinated rabies was reported in dogs, cattle, and raccoon dogs. animals, respectively, no measurements were available More than 70% of the domestic animals causing bites due escape of the animals (including wildlife) or were unvaccinated or had been vaccinated more than improper disposal. Complete or appropriate PEP was one year after the booster. To encourage animal vacci- administered more in patients bitten by unvaccinated nation in high-risk regions, cattle, dogs, and cats have animals (40.6%) than in patients bitten by vaccinated been vaccinated free of cost by public health veteri- animals (13.2%). Of animal bite patients, 21.8% had narians in local governments since 1993. In spite of the complete PEP and 10.7% were treated with appropriate strengthenedanimalvaccinationprogram,thenumberof PEP. Of the patients bitten by vaccinated animals, unvaccinatedbitinganimalsremainshigh.Raccoondog 12.8% ((cid:1)3.4) (from 7.4% to 16.9%) received complete rabies remains high and has resulted in of transmission ofthevirustocattleanddogsintheendemicareas[1,6]. These data suggest that mass vaccination programs should be strengthened in the high-risk regions to prevent rabies outbreaks [2]. After the recurrence of animal rabies in 1993, the virus gradually spread southward and eastward in the twoendemicprovinces.Theendemicareasofrabiesare surroundedbyariverandanexpresswayonthesouthern side, shoreline on eastern and western sides and the demilitarized zone (DMZ) on the northern side. If the rabies virus crosses the southern barrier, it can rapidly spread nationwide. Other factors include possible introductionofthevirusfromendemiccountries[7e11] and misdiagnosis and delayed PEP due to a lack of Figure 2. Animal species causing bites from 2005 to 2009. experience amonghealth care providersandthe general Otheranimalsincludebadger,wildboar,chipmunk,otter,rats, hamster,monkey,andweasel.Dogsandcatsalsoincludestray communityoutsideoftheriskareas[12].Therefore,itis animals.Dogs(86.0%)weretheprimaryanimalscausingbites, necessarytoexpandthe animal bitemonitoringareasto followed bycats. cities/districts adjacent toendemicareasandtostrength 18 M.G. Han, et al Table 2. Animal managementand patient treatment afteranimal bites,2005to2009 Treatment of animalbite case (%)a Animal vaccination Animal to rabies management Woundtreatment Incomplete PEP Appropriate PEP Complete PEP Vaccination Observation 20.1 4.4 1.0 2.1 Necropsy 0.1 0 0 0.3 None 1.0 0.1 0.2 0.4 Nonvaccinated Observation 26.3 9.3 5.1 10.4 Necropsy 0.5 0.2 0.4 1.8 None 3.6 1.8 4.0 6.8 aCompletepost-exposureprophylaxis(PEP)meansthatbothhumanrabiesimmuneglobulin(HRIG)andvaccinationwereadministered.AppropriatePEP meansthatvaccinationwasadministeredwithoutHRIG. PEPZpost-exposureprophylaxis. information, education, campaign and communication This study was supported by an intramural fund of programs in the suspect-risk areas. KoreaNationalInstituteofHealth(No.4800-4834-300). The KCDC guidelines recommend that both HRIC and rabies vaccine are administered to patients in the References high-riskregionwhohadWHOCategoryIIIexposureor wild animal bites as soon as possible, regardless of the 1. 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