Bovine Tuberculosis in Free-Ranging Carnivores from Michigan

Bovine Tuberculosis in Free-Ranging Carnivores from Michigan
of 7
All materials on our website are shared by users. If you have any questions about copyright issues, please report us to resolve them. We are always happy to assist you.
Related Documents
  58 Journal of Wildlife Diseases,  37(1), 2001, pp. 58–64   WildlifeDiseaseAssociation2001 BOVINE TUBERCULOSIS IN FREE-RANGING CARNIVORES FROMMICHIGAN Colleen S. Bruning-Fann, 1,8 Stephen M. Schmitt, 2 Scott D. Fitzgerald, 3 Jean S. Fierke, 2 PaulD. Friedrich, 2 John B. Kaneene, 4 Kathy A. Clarke, 3 Kelly L. Butler, 3 Janet B. Payeur, 5 DianaL. Whipple, 6 Thomas M. Cooley, 2 Janice M. Miller, 6 and Darian P. Muzo 7 1 Veterinary Services, Animal and Plant Health Inspection Service, United States Department of Agriculture,East Lansing, Michigan 48823, USA 2 Wildlife Disease Laboratory, Rose Lake Wildlife Research Station, Michigan Department of Natural Resources,East Lansing, Michigan 48823, USA 3 Animal Health Diagnostic Laboratory and Department of Pathology, College of Veterinary Medicine,Michigan State University, East Lansing, Michigan 48824, USA 4 Population Medicine Center, College of Veterinary Medicine, Michigan State University, East Lansing,Michigan 48824, USA 5 National Veterinary Services Laboratories, United States Department of Agriculture, Ames, Iowa 50010, USA 6 Agricultural Research Service, United States Department of Agriculture, Ames, Iowa 50010, USA 7 Department of Fisheries and Wildlife, College of Agriculture and Natural Resources, Michigan State University,East Lansing, Michigan 48824, USA 8 Corresponding author (email: ABSTRACT : Duringasurveyof carnivoresand omnivoresfor bovinetuberculosisconducted inMichigan (USA) since1996,  Mycobacterium bovis   wascultured fromlymphnodespooledfromsixcoyotes( Canis latrans  )(four adultfemale,twoadultmale),twoadultmaleraccoons( Procyon lotor  ), oneadult malered fox( Vulpes vulpes  ), and one1.5-yr-old maleblack bear ( Ursus amer- icanus  ).Oneadult,malebobcat( Felis rufus  )withhistologiclesionssuggestiveoftuberculosiswasnegativeonculturebutpositivefor organismsbelongingtothe Mycobacterium tuberculosis  com-plex when tested by polymerase chain reaction. All the tuberculous animals were taken fromthreeadjoiningcountieswhere M. bovis  isknowntobeendemicinthefree-rangingwhite-taileddeer ( Odocoileus virginianus  )population.Thereweretwocoyotes,oneraccoon,oneredfox,andonebobcat infected in Alpenacounty. MontmorencyCountyhad two coyotesand oneraccoonwith  M. bovis.  Two coyotesand abear were infected fromAlconaCounty. Thesefree-rangingcarnivores/omnivoresprobablybecameinfectedwith M. bovis   throughconsumptionof tubercu-lous deer. Other speciesincluded in the survey were opossum( Didelphis virginiana  ), grayfox( Urocyon cinereoargenteus  ),andbadger ( Taxidea taxus  );thesewerenegativefor  M. bovis.Key words:   Coyote( Canis latrans  ), raccoon( Procyon lotor  ), blackbear ( Ursus americanus  ),bobcat ( Felis rufus  ), redfox( Vulpes vulpes  ),  Mycobacterium bovis,  survey, tuberculosis. INTRODUCTION Bovinetuberculosiscausedby Mycobac- terium bovis   is endemic in free-rangingwhite-taileddeer ( Odocoileus virginianus  )in five counties (Alcona, Alpena, Mont-morency,Oscoda,andPresqueIsle)inthenortheasternLowerPeninsulaofMichigan(USA) (Schmitt et al., 1997). Since1996,a survey of free-ranging carnivores andomnivores for tuberculosis has been inprogressand resultswerereported previ-ously(Bruning-Fann et al., 1998). Of the62 animals reported in 1998 (15 coyotes,28raccoons, 11opossums, fivefoxes, twobadgers, and one bobcat),  M. bovis   wascultured from three coyotes ( Canis la- trans  ) that werenormal in appearanceonboth gross and histological examination. Thisreportprovidesanupdateofthispro- ject. Three factors provided the impetusfor examiningfree-rangingcarnivoresandomnivoresfor tuberculosisinnortheasternMichiganFirstwastheimplicationofnon-ruminant wildlife as a reservoir of tuber-culosis in New Zealand (de Lisle, 1993),Great Britain (Clifton-Hadley, 1996), andIreland (Collinset al., 1994). Second, thewide host range of   M. bovis   (Francis,1958). Third,thepresenceof endemictu-berculosis in free-ranging deer in north-easternMichigan(Schmitt et al., 1997). MATERIALS AND METHODS Wildlifeincludedinthison-goingstudywerethosecarnivorousand omnivorousmammalianspecies present in the tuberculosis endemicareawhosepopulationdensitywassufficientto  BRUNING-FANN ET AL.—TUBERCULOSIS IN FREE-RANGING CARNIVORES 59 F IGURE  1. Location of   Mycobacterium bovis   in-fected carnivoresandwhite-taileddeer inMichigan,1999. allow collection. Coyote, bobcat ( Felis rufus  ),raccoon ( Procyon lotor  ), black bear ( Ursus americanus  ), red fox( Vulpes vulpes  ), gray fox( Urocyon cinereoargenteus  ), opossum ( Didel- phis virginiana  ), and badger ( Taxidea taxus  )weresurveyed. The area from which omnivores and carni-vores were collected increased since last re-ported(Bruning-Fannetal.,1998) andinclud-ed thefivetuberculosisendemic counties(Al-pena, Alcona, Montmorency, Oscoda, andPresqueIsle)andaboundaryareasurroundingtheseendemiccounties(Fig.1).Theboundaryareawasdefined bytwomajor roadways(I-75and M-55) and contained approximately onehalf of each of the counties (Cheboygan, Ot-sego, Crawford, Roscommon, Ogemaw, andIosco) that border the endemic counties. TheMichigan Department of Natural Resources(MDNR, Lansing, Michigan, USA) recordedthe location where each animal was hunted,trapped,orfounddead.Theageofthecoyotes,bobcats, raccoons, red foxes, grayfoxes, opos-sums,andbadgerswerecategorizedasadultor juvenilebased on thepresenceof adult or ju-venile dentition (Bookhout, 1994). The bearwas aged by cementum annuli analysis (Sto-neberg and Jonkel, 1966; Friedrich et al.,1990).Carcasses of carnivores and omnivores (ex-ceptfor blackbears) werenecropsiedatMich-igan State University (MSU, East Lansing,Michigan, USA). Visiblelesionsandtheparot-id, mandibular, medial retropharyngeal, bron-chial,mediastinal,andmesentericlymphnodeswere collected for histologic examination andmycobacterial culture. Lymph nodes (pooledfromeachanimal) wereculturedfor mycobac-teriaA thorough description of samplecollec-tion, processing, examination, and culture hasbeen reported (Bruning-Fann et al., 1998).Black bear headswere obtained fromtaxider-mists, andtheparotid, mandibular,andmedialretropharyngeallymphnodeswerecollectedbyMSU FisheriesandWildlifestudents.Process-ing, examination and culturingof thesetissueswasthesameasfortheotherspeciessurveyed.We were unable to examine bear viscera be-causethecarcasseswereevisceratedbyhuntersinthefield.Apolymerasechainreaction(PCR)test for identification of   Mycobacterium tuber- culosis   complex organisms in formalin-fixed,paraffin-embeddedtissuewasperformedasde-scribedpreviously(Milleretal.,1997)ontissuefromthebobcat. RESULTS Fromthestart of thesurveyuntil June1999,294carcasseswerecollectedandex-amined grosslyfor tuberculosis(Table1).Gross lesions suspicious of tuberculosiswere seen in two coyotes (both culturepositive), and oneadult malebobcat (cul-turenegative,PCRpositive)(Table2).Notall animalsobtainedinthesurveywereex-amined histologicallyand tissuesculturedfor mycobacteriadue to a variety of rea-sons. Of the270 animalsexamined histo-logically (106 coyotes, 54 opossums, 52raccoons, 42 black bears, five red foxes,onegrayfox, twobadgers, andeight bob-cats), seven had microscopic lesions sug-gestiveoftuberculosis(Table2).Mycobac-terial cultures were performed on tissuesfrom 266 animals (106 coyotes, 54 opos-sums,48raccoons,42blackbears,fivered  60 JOURNAL OF WILDLIFE DISEASES, VOL. 37, NO. 1, JANUARY 2001  T ABLE  1. Species,sex,andageofcarnivoresandomnivoressurveyedfortuberculosisinMichigan,1996–99. SpeciesFemaleAdult Juvenile UnknownMaleAdult Juvenile UnknownSex/AgeUnknown Totals BadgerBlackbearBobcatCoyoteGrayfox——4611——13——14———3—344—1——1——23————5—1—44281101OpossumRaccoonRedfox Total1218234————37391723————1—59646294 T ABLE  2. Summaryof grossandhistologicexaminationandmycobacterial cultureoftuberculosisconfirmedandsuspiciouscasesincarnivoresandomnivoressurveyedinMichigan1996–99. Species IdentificationGrosslesionsHistologiclesions M. bovis  cultured Location BlackbearBobcatCoyote h CoyoteCoyote h 35704987C45C51C58  b  b,f   b,e  g  USA 44  48  N, 83  37  WUSA 45  00  N, 83  30  WUSA 44  50  N, 83  44  WUSA 44  45  N, 83  33  WUSA 44  53  N, 83  56  WCoyote h CoyoteCoyoteCoyoteCoyoteC61C65C88C10031555  b,d  b  d,e  b,f   b,f   USA 44  48  N, 83  50  WUSA 45  11  N, 83  56  WUSA 45  27  N, 84  06  WUSA 44  55  N, 83  35  WUSA 45  00  N, 83  40  WRaccoonRaccoonRaccoonRedfoxC81C83C1194997  a,e  c,f   USA 44  55  N, 84  00  WUSA 45  01  N, 83  47  WUSA 44  58  N, 83  54  WUSA 45  07  N, 83  24  W a  Thoraciclymphnodes. b Mesentericlymphnodes. c Cranial lymphnodes. d Lungs. e Histologiclesionsuggestiveof TB withoutacid-fastbacilli. f  Histologiclesionsuggestiveof TB withacid-fastbacilli seen. g Positivefor  M. tuberculosis  complexbyPCR examinationof paraffintissuesections. h Previouslyreported. foxes,onegrayfox,twobadgers,andeightbobcats). Mycobacterium bovis  wasculturedfromsixcoyotes(four adult females[threepre-viously reported], two adult males), twoadult male raccoons, one adult male redfox, and one 1.5-yr-old male black bear(Table 2). The tuberculous animals weretaken from three adjoining counties innortheastern Michigan (Fig. 1). Tubercu-lous animals in Alpena county includedtwocoyotes,oneraccoon,oneredfox,andonebobcat.Montmorencycountyhadtwocoyotes,andoneraccoon.Twocoyotesandabear fromAlconacountyweretubercu-lous.Of thesixcoyotesfromwhich M. bovis  wascultured, histologic lesionssuggestiveof tuberculosiswere seen in two coyotes.Oneadult malecoyote(C65) had numer-ous 2 to 3 mm firm, white nodules thatwereraisedabovethesurfaceof thelung. The mesenteric lymph nodes were en-larged with gritty, white mottling. Follic-  BRUNING-FANN ET AL.  — TUBERCULOSIS IN FREE-RANGING CARNIVORES 61 ularhyperplasiawithmultiplegranulomas,composed primarily of macrophages andlymphocytes, were seen histologically. Al-though, no acid-fast bacilli wereseen,  M.bovis   wascultured fromthesetissues. Anadult femalecoyote(31555) had no grosslesions, but histologically a mesentericlymphnodecontainedasingle,largefocusof partially mineralized necrotic debris.Lownumbersof acid-fast bacilli wereob-served adjacent to theareaof mineraliza-tion, and  M. bovis   wascultured fromthisanimal. Mycobacterium bovis  wasalsocul-tured from an adult male coyote (C100),which had markedly enlarged pale mes-enteric lymph nodes, but only lymphoidhyperplasiawasobservedhistologically.Aspreviouslyreported, M. bovis  wasculturedfrom coyotes C45, C58, and C61 whichhadnogrossor histologiclesionsoftuber-culosis(Bruning-Fannet al., 1998). Two additional coyotesweresuspiciousof tuberculosis. Although no grosslesionswere seen in these adult female coyotes,histologiclesionssuggestiveoftuberculosiswerefound. Themesentericlymphnodesof coyoteC51containedmultiplenecroticfoci, which werepartiallymineralizedbutacid-fast organisms were not observed.CoyoteC88hadseveral lymphnodescon-taining multiple caseogranulomas withcentral areas of partially mineralized ne-crotic debris. Moderate numbersof acid-fast bacilli werepresent inthecentral de-bris. Mycobacteriawerenot isolatedfromthetissuesof either coyote. Thecauseof the lesions in these coyotescould not bedeterminedasnotissueremainedfortest-ingbyPCR. Threeraccoonsshowed evidenceof tu-berculosis. One raccoon (C119) had bothhistologic lesions and was positive for  M.bovis   on culture. Although presentedinastateof advanceddecompositionandlack-ing abdominal viscera, low numbers of acid-fast bacilli wereseen in necroticfocicontained within thecranial lymph nodesof thisadult maleraccoon. No inflamma-torycellswereassociatedwiththenecroticfoci. An adult female raccoon (C81) hadno gross lesions, but a tracheobronchiallymph node contained caseogranulomascomposedof acentral areaofnecroticde-briswithpartial mineralization.Noorgan-isms were seen on acid-fast staining, nomycobacteriawereisolated, and notissueremained for testing by PCR. RaccoonC83hadnogrossorhistologiclesionssug-gestive of tuberculosis, but  M. bovis   wasisolatedfromthisadult male.One adult, female bobcat (4987) hadenlarged mesenteric lymph nodes (2 cmdiameter) with numerous pale, tan nod-ules (2 mm diameter) on gross examina-tion.Histopathologicexaminationrevealedmultifocal caseogranulomas with partiallymineralizednecroticdebrisinthecenters,surrounded by lymphocytes and macro-phages.Moderatenumbersofacid-fastba-cilli were present in the necrotic debris.Nomycobacteriawereisolatedfromthesetissues. However, aPCR test onDNA ex-tractedfromparaffinsectionsofthetissuesdetected thepresenceof bacteriabelong-ing to the  M. tuberculosis   complex, agroup of organismthat includes M. bovis  (J. M. Miller, pers. comm.). Mycobacterium bovis   wasisolatedfroman adult malered fox(4997) and amale,1.5-yr-old black bear (3570). No gross orhistologic lesionswere observed in eitherof these animals. All opossums and bad-gersweregrosslyandhistologicallynormaland mycobacteriawere not isolated fromanyof theseanimals. DISCUSSION Although bovine tuberculosis has beenreported in a wide variety of animals(Francis, 1958), this report provides thefirst documentation of thisdiseasein twospecies. This is the first report of bovinetuberculosisin abobcat. Thisfindingwasnot unexpected as  M. bovis   has been re-ported in other felids: leopards( Panthera uncia   and Panthera pardus  )(Thorel etal.,1998), lions ( Panthera leo  ) (Keet et al.,1996),acheetah( Acinonyx jubatus  )(Keetet al., 1996), atiger ( Panthera tigris  )(Lu-meij etal.,1987),anddomesticcats(Isaac  62 JOURNAL OF WILDLIFE DISEASES, VOL. 37, NO. 1, JANUARY 2001 etal.,1983).Thisisalsothefirstreportof  M. bovis   in free-rangingraccoons. Bovinetuberculosis has been reported in coatis( Nasua narica  )(Fox,1923)which,likerac-coons, are members of the family Pro-cyonidae. In addition, this is the first re-portof grossandhistologiclesionssugges-tiveoftuberculosisincoyotes,although M.bovis   has previously been cultured fromthisspecies(Rhyan et al., 1995; Bruning-Fannet al., 1998). Thelackof grossorhistologiclesionsinthe culture positive red foxfound in thissurveyissimilartoapreviousreportwhere M. bovis   wascultured fromafoxwithoutlesionsinEngland(Littleetal.,1982).Tu-berculosis has been found in bear, al-thoughthereportfurnishedfewdetailsastospeciesor extentof lesions(Fox,1923).Hadall bear tissuesbeenavailablefor ex-amination and culture, it is possible thatbovinetuberculosiswould havebeen cul-turedfromadditional bearsor thatlesionscouldhavebeenobserved.Restriction fragment length polymor-phism(RFLP) analysishasbeencomplet-ed for the  M. bovis   isolates from five of thesixcoyotes, thetworaccoons, andthebear. TheseRFLP patternswereidenticaltothepredominantRFLP patternseenin M. bovis  isolatedfromfree-rangingwhite-tailed deer taken from the five countieswhere tuberculosis is endemic (D. L.Whipple, pers. comm.). The similarity inRFLP patternsbetween the M. bovis   iso-latesfromthesecarnivores/omnivoresandfree-rangingdeer,andtheclosegeograph-ical proximityof thecases,providesstrongevidenceof alinkbetweenthecases(Fig.1). Thefindingthatmostofthelesionsseengrossly and histologically in the  M. bovis  culturepositivecoyotesand PCR positivebobcat occurred in themesentericlymphnodessuggestsexposurebyingestion.Sev-eral reports of   M. bovis   infection in car-nivores have been attributed to the con-sumption of tuberculous meat (Francis,1958;Isaacetal.,1983;Littleetal.,1982).In view of this evidence, the most likelysource of infection for these carnivores/omnivores was through the consumptionof tuberculouswhite-taileddeer. Thenumber, extent and distribution of tuberculous lesions in an infected animalprovidesanindicationofthatspecies’abil-itytoactasareservoir hostsincesuccess-ful diseasetransmissionrequiresexcretionof the infectious agent from the host.While most mammalian species are sus-ceptible to bovine tuberculosis (Francis1958), only a few non-ruminant speciesare thought to be reservoirs of   M. bovis. Brushtail possums( Trichosurus vulpecula  )andferrets( Mustela furo  )inNewZealand(Pattersonetal.,1995;Sauter andMorris,1995) and European badgers ( Meles me- les  ) in England and Ireland (Nolan andWilesmith, 1994; O’Reilly and Daborn,1995)arebelievedtobereservoirhostsforbovinetuberculosis.Thesespeciesdevelopextensive lesions containing tremendousnumbersof bacilli. Excretion of   M. bovis  hasbeendemonstratedfromthesespecies(Gallagher et al., 1976; Jackson et al.,1995; Morriset al., 1994; Nolan and Wi-lesmith,1994;Raggetal.,1995).Thusfar,disseminatedlesionswithhighnumbersof bacillihavenotbeenfoundassociatedwiththe native Michigan carnivores or omni-vores. The number of tuberculous carni-voresandomnivores,thevarietyofspeciesinvolved, and the geographic spacingbe-tween thecasesismoreindicativeof dis-ease spillover from the free-rangingdeerreservoir to these wildlife species ratherthan endemic tuberculosis in these thecarnivores and omnivores. Although it iscurrently thought that no wildlife otherthanwhite-taileddeer serveasareservoirfor tuberculosis in Michigan, continuedandexpandedwildlifesurveysandexperi-mental inoculationstudiesareinprogress. ACKNOWLEDGEMENTS WethankN.H.LehmanandR.L.Lyonfortechnical assistance with RFLP analysis, S.Winterstein for the collection of bear tissues,theMDNR, MSU, and USDA personnel whohelpedwiththecarnivore/omnivoresurvey,andthe hunters/trappers who participated in the
Similar documents
View more...
Related Search
We Need Your Support
Thank you for visiting our website and your interest in our free products and services. We are nonprofit website to share and download documents. To the running of this website, we need your help to support us.

Thanks to everyone for your continued support.

No, Thanks