Tuberculosis is emerging/re-emerging in captive elephant populations, where it causes morbidity and deaths, although no case of TB in wild African elephants has been reported. In this paper we report the first case of fatal TB in an African elephant in the wild. The infection with Mycobacterium tuberculosis was confirmed by post-mortem and histological examinations of a female sub-adult elephant aged >12 years that died in Tsavo East National Park, Kenya, while under treatment. This case is unique in that during its lifetime the elephant had contact with both humans and wild elephants. The source of the infection was unclear because the elephant could have acquired the infection in the orphanage or in the wild. However, our results show that wild elephants can maintain human TB in the wild and that the infection can be fata

ALASAAD, S.

GAKUYA, F.

MAKUMI, J.

MULEI, I.

NGOTHO, M.

OBANDA, V.

OMONDI, P.

POGHON, J.

SORIGUER, R. C.

Stärk, Katharina D. C.

WAITITU, K.

YONGO, M.

RERO DOC Digital Library

SHORT REPORTFirst reported case of fatal tuberculosis in a wild Africanelephant with past human–wildlife contactV. OBANDA 1,2*, J. POGHON 1, M. YONGO1, I. MULEI 2, M. NGOTHO 3,K. WAITITU 3, J. MAKUMI 4, F. GAKUYA1, P. OMONDI1, R. C. SORIGUER5AND S. ALASAAD 5,6*1 Veterinary Services Department, Kenya Wildlife Service, Nairobi, Kenya2 Faculty of Veterinary Medicine, University of Nairobi, Nairobi, Kenya3 Institute of primate Research, National Museums of Kenya, Karen, Nairobi, Kenya4 School of Pure and Applied Sciences, Biochemistry and Biotechnology Department, Kenyatta University,Nairobi, Kenya5 Estacio´n Biolo´gica de Don˜ana, Consejo Superior de Investigaciones Cientı´ﬁcas (CSIC), Sevilla, Spain6 Institute of Evolutionary Biology and Environmental Studies (IEU), University of Zu¨rich, Zu¨rich, SwitzerlandReceived 18 October 2012; Final revision 11 December 2012; Accepted 2 January 2013;ﬁrst published online 23 January 2013SUMMARYTuberculosis is emerging/re-emerging in captive elephant populations, where it causes morbidityand deaths, although no case of TB in wild African elephants has been reported. In this paperwe report the ﬁrst case of fatal TB in an African elephant in the wild. The infection withMycobacterium tuberculosis was conﬁrmed by post-mortem and histological examinations of afemale sub-adult elephant aged>12 years that died in Tsavo East National Park, Kenya, whileunder treatment. This case is unique in that during its lifetime the elephant had contact with bothhumans and wild elephants. The source of the infection was unclear because the elephant couldhave acquired the infection in the orphanage or in the wild. However, our results show that wildelephants can maintain human TB in the wild and that the infection can be fatal.Key word : Tuberculosis (TB).Tuberculosis (TB) is an old disease that occursworldwide but is mostly endemic in sub-SaharanAfrica, where it continues to threaten public healthand devastate the livestock industry [1, 2]. Bacteriafrom the genus Mycobacterium, particularly Myco-bacterium bovis and M. tuberculosis are the frequentcausal pathogens of animal and human TB, respect-ively [1]. Epidemiology, prevention and treatment ofTB in humans have been complicated by the upsurgeof the HIV epidemic, and the emergence of multidrug-resistant strains [2]. Increased interactions betweenwild animal reservoirs and humans with their livestockcreate opportunities for cross-transmissionofTB [3, 4].Transmission of TB between wildlife and humansis commonly reported in captive conditions [5–7],although infected free-ranging wildlife may cause thespillover of TB to livestock and eventually to humans.However, transmission pathways involving wildlifeare neglected and rarely included in the epidemiologi-cal strategies towards curbing spread of the disease [8].The disease is now prevalent in free-ranging wildlifeand of concern is the involvement of human TB [4].* Author for correspondence: Dr V. Obanda, Veterinary ServicesDepartment, Kenya Wildlife Service, P. O. Box 40241-00100Nairobi, Kenya.(Email : vobanda@kws.go.ke) [V. Obanda](Email : samer@ebd.csic.es) [S. Alasaad]Epidemiol. Infect. (2013), 141, 1476–1480. f Cambridge University Press 2013doi:10.1017/S0950268813000022https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268813000022Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 19:52:35, subject to the Cambridge Core terms of use, available atTB is emerging/re-emerging in elephants where it isassociated with the morbidity and death of captivepopulations [5, 9]. Occupational risks that requireclose and elongated interactions between elephantsand their handlers create the opportunity for bi-directional transmission of TB, a pathway that intro-duced the fatal multidrug-resistant strain into anelephant [10]. Further, elephants infected with humanTB, have been reported to transmit the pathogen totheir human handlers [5], a scenario that has graveimplications for public health [9]. Human TB has onlybeen detected in domesticated elephants, although theprevalence of M. tuberculosis in wild elephants hasnot been evaluated. Wild animals are likely to acquirehuman TB as they scavenge or forage near humansettlements where they may be exposed to TB-contaminated materials [4]. In Kenya, prevalence ofTB infection in elephants (Loxodonta africana) isunknown, although there are both captive and wildpopulations [20]. Of interest are the domesticatedelephant orphans rescued from the wild and reared byhumans until they are released back into the wild.Tsavo East National Park is situated in SouthEastern Kenya at latitude 2x 46k 43a S and longitude38x 46k 18a E. This semi-arid savannah region covers11747 km2 and is mainly plain grassland at an elev-ation of 229 m, but the craggy hills and mountainsreach 2438 m. Within this park, is the Voi elephantstockade, established as an orphanage for rearingrescued elephant calves. The orphans are released intothe wild through a process of habituation and mixingwith wild elephants, a transition that takes 8–10 years(www.sheldrickwildlifetrust.org). Rainfall is unpre-dictable in the park, although long periods of rain areexpected between March and May, while the shortrainy period is between October and December, withan annual average rainfall of 250–500 mm. The Tsavoecosystem which comprises contiguous Tsavo Eastand Tsavo West National parks holds the largestelephant population in Kenya with 10000 animalsaccording to the 2012 census [11]. Tsavo East is alsohome to many small and large herbivores [e.g. impala(Aepyceros melampus), African buﬀalo (Syncerus caf-fer), black rhinoceros (Diceros bicornis), hippopota-mus (Hippopotamus amphibius)] ; carnivores [e.g. lion(Pathera leo), leopard (Panthera pardus)], and non-human primates [e.g. baboon (Papio anubis), vervetmonkey (Cercopithecus aethiops)]. There are severalstreams that water the area, such as the Mbololo riverand the Athi-Galana river. In recent times, pastoralcommunities and their animals [e.g. camels (Camelusdromedarius), sheep (Ovis aries), goats (Capra hircus),cattle (Bos taurus)] have moved into the wildlife dis-persal areas around this park to graze their animals.This has enhanced contact between wildlife, human,and livestock, an interaction that has many negativeramiﬁcations such as frequent human–wildlife con-ﬂicts, resource scarcity and may potentially allow forpathogen and vector exchange.In this short report we describe the case of a femalesub-adult elephant aged >12 years, formerly an or-phan named ‘Loisaba’. The elephant was originallyrescued as an abandoned calf from the Laikipia re-gion of Central Kenya. The calf was raised along withother rescued orphans at the Voi elephant stockade,located within Tsavo East National Park. Alongwith other rehabilitated orphans, Loisaba, then aged7 years, was released back into the wild within theTsavo National Park. Loisaba was in her ﬁfth year inthe wild when gradual loss of body condition was(a) (b)Fig. 1 [colour online]. Gross pathological examination. (a) The thin arrow indicates the nodular whitish substance that coversthe cross-section of the left lung and the thick arrow indicates the infected section of the lung. (b) The thick arrow indicatesthe remaining apparently normal part of the lung.Tuberculosis in a wild African elephant 1477https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268813000022Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 19:52:35, subject to the Cambridge Core terms of use, available atobserved about 3 months before her death. Duringthis period, the monitoring team from the stockadeobserved that the elephant tended to lag behindthe herd. When the elephant was found isolated fromthe herd with a staggering gait, it was rescued andreturned to the stockade for examination and treat-ment (Supplementary Fig. S1).The elephant was examined and the followingwere noted: general malaise, reluctant to move, loss ofbreath, dyspnoea and emaciation. The animal wastentatively diagnosed as having pneumonia and wastreated with long-acting antibiotics and non-steroidalanti-inﬂammatory drugs, which were administeredparenterally via intramuscular injections on 25 June2011. The animal died 2 days later on the night of27 June 2011 and necropsy was performed on themorning of 28 June 2011.A ﬁeld veterinarian performed a general post-mortem on the animal. Sections of the lungs were thenexcised for histology. These samples were frozen andtransported to the Diagnostic Pathology laboratory atthe Institute of Primate Research, Nairobi. At thelaboratory, the lungs were thawed and sliced into thinsections that were then ﬁxed in 10% neutral buﬀeredformalin and processed using routine histologicaltechniques. Sections (4- to 5-mm thick) were preparedfrom the paraﬃn-embedded specimens, stained withhaematoxylin and eosin and analysedmicroscopically.(a) (b)Fig. 2 [colour online]. Histological examination of elephant lung. (a) The thick arrows indicate ﬁbrous encapsulating material.The thin arrow indicates the characteristic stellate formation of a tubercle. Note the lost architectural pattern of the lung dueto collapsed alveoli and the increased mononuclear inﬁltration. (b) Arrow (A) shows a giant cell in the midst of otherinﬂammatory cells while arrow (B) shows cellular debris in an alveolar (H&E stain,r100).Fig. 3 [colour online]. An impression smear from a section of the elephant lung showingMycobacterium tuberculosis (arrows)(Ziehl–Neelsen stain,r1000).1478 V. Obanda and othershttps:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268813000022Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 19:52:35, subject to the Cambridge Core terms of use, available atImpression smears from the thawed lung tissue werealso made and acid fast-stained using Ziehl–Neelsenstain [22].We observed that the elephant was anaemic asdepicted by paleness of the mucus membranes.Sub-mandibular lymph nodes were congested andenlarged. The appearance and texture of the lungswere altered, with about 85% of both right and leftlobes inﬁltrated with whitish nodules that were un-even to the touch. The non-caseated parts lookedmeaty in appearance due to consolidation (Fig. 1).Histology of the lungs showed collapsed alveoli, areasof mononuclear cellular inﬁltration especially plasmacells and cellular debris encapsulated with ﬁbrousmaterial (Fig. 2a) and giant cells (Fig. 2b). An im-pression smear of the lungs showed reddish rods ordots typical of M. tuberculosis (Fig. 3).TB is an emerging/re-emerging zoonotic diseasewith signiﬁcant risks to livestock, wildlife and publichealth. The status of TB in free-ranging elephantsin Kenya and elsewhere is unknown. However, thedetection of human TB in wild mongooses (Mungosmungo) shows that wild animals can maintain humanTB and demonstrates that increased contact betweenhumans and wildlife creates an opportunity for inter-species pathogen exchange [4]. This transmission op-portunity exists in Africa where 29% of the globalburden and 34% of TB-associated deaths occur [23].In the present report, the histological and grosspathology indicate that the elephant had TB infectioncaused by M. tuberculosis. This case is unique in thatduring its lifetime the elephant had contact with bothhumans (orphanage period during the ﬁrst 7 years oflife) and wild elephants (post-release period duringthe last 5 years of life), and hence the source of infec-tion of this elephant is equivocal as it could have ac-quired it from wild conspeciﬁcs post-release, or fromthe orphanage.This case of fatal TB in a wild African elephantraises the following questions regarding the epidemi-ology of TB. (1) ‘Could past years of human contacthave predisposed the elephant to TB?’ If so, then theelephant had a latent infection for over 5 years in thewild. (2) ‘Which factors might have triggered clinicaldisease? ’ Elephants that acquire human TB in cap-tivity may maintain latent infection for many years[13, 14] but when they develop clinical disease they areeither treated or die in captivity. Nevertheless, thepresent scenario is diﬀerent in that if the elephant ac-quired human TB while in contact with humans, uponrelease, it carried the risk of spreading the diseaseto other wild species or conspeciﬁcs. This suggeststhat release of rehabilitated animals, with prolongedhuman contact, may act as a conduit for human-acquired pathogens for wild animal populations. Theperiod for development of delayed hypersensitivity inwild animals varies for diﬀerent species and for indi-vidual animals in a population in which TB hasbeen diagnosed. This has been observed in captiveelephants in which individuals diﬀered in theperiod they harboured latent TB infection [13]. If theelephant was not infected in the orphanage, then itmust have acquired the disease in the wild.We therefore recommend that (a) the release ofdomesticated elephants into the wild requires eﬃcientscreening for TB, and (b) the status of TB in wildelephants should be assessed.Our results show that whatever the source of in-fection, an African elephant living in the wild canharbour latent TB infection, which can become clini-cal and cause death.SUPPLEMENTARY MATERIALFor supplementary material accompanying this papervisit http://dx.doi.org/10.1017/S0950268813000022.ACKNOWLEDGEMENTSWe are grateful to the support of the Director, KenyaWildlife Service (KWS) for authorizing this study. Weacknowledge the technical assistance from staﬀ at theAnimal Sciences Department, Institute of PrimateResearch. We appreciate the work of anonymous re-viewers who have improved the quality of this manu-script.DECLARATION OF INTERESTNone.REFERENCES1. Gagneux S, Small PM. Global phylogeography ofMycobacterium tuberculosis and implications for tu-berculosis product development. Lancet InfectiousDiseases 2007; 7 : 328–373.2. Samper S, et al. Transmission between HIV-infectedpatients of multidrug-resistant tuberculosis caused byMycobacterium bovis. AIDS 1997; 11 : 1237–1242.3. Murphree R, et al. Elephant-to-human transmission oftuberculosis, 2009. Emerging Infectious Diseases 2011;17 : 366–371.Tuberculosis in a wild African elephant 1479https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268813000022Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 19:52:35, subject to the Cambridge Core terms of use, available at4. Alexander KA, et al. Mycobacterium tuberculosis : anemerging disease of free-ranging wildlife. EmergingInfectious Diseases 2002; 8 : 598–601.5. Michalak K, et al. Mycobacterium tuberculosis infectionas a zoonotic disease : transmission between humansand elephants. Emerging Infectious Diseases 1998; 4 :283–287.6. Fanning A, Edwards S. Mycobacterium bovis infectionin human beings in contact with elk (Cervus elaphus) inAlberta, Canada. Lancet 1991; 16 : 1253–1255.7. Kaewamatawong T, et al. Disseminated tuberculosis incaptive Malayan tapir (Tapirus indicus). Thai Journal ofVeterinary Medicine 2010; 40 : 427–431.8. Baker MG, et al. Continuing Mycobacterium bovistransmission from animals to humans in New Zealand.Epidemiology and Infection 2006; 134 : 1068–1073.9. Mikota KS, Maslow NJ. Tuberculosis at the human-animal interface: an emerging disease of elephants.Tuberculosis 2011; 91 : 208–211.10. Lyashchenko KP, et al. A multi-antigen print im-munoassay for the development of serological diagnosisof infectious diseases. Journal of Immunological Meth-ods 2000; 242 : 91–100.11. Kenya Wildlife Service. Conservation and managementstrategy for the elephant in Kenya, 2012–2021. KenyaWildlife Service, 2012, pp. 2–6.12. Chaisson ER, Martinson AN. Tuberculosis in Africa –combating an HIV driven crisis. New England Journalof Medicine 2008; 358 : 1089–1092.13. Lyashchenko PK, et al. Tuberculosis in elephants : anti-body responses to deﬁned antigens of Mycobacteriumtuberculosis, potential for early diagnosis and monitor-ing of treatment. Clinical and Vaccine Immunology2006; 13 : 722–732.14. Verma-Kumar S, et al. Serodiagnosis of tuberculosis inAsian elephants (Elephas maximus) in Southern India:a latent class analysis. PLoS ONE 7 : e49548.1480 V. Obanda and othershttps:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268813000022Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 19:52:35, subject to the Cambridge Core terms of use, available at

First reported case of fatal tuberculosis in a wild African elephant with past human-wildlife contact

http://doc.rero.ch/record/299022/files/S0950268813000022.pdf

First reported case of fatal tuberculosis in a wild African elephant with past human-wildlife contact

Abstract

Similar works

Full text

Available Versions

RERO DOC Digital Library