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By Willem Schaftenaar DVM

Tuberculosis in zoos

Based on positive cultures of trunk washing samples or necropsy results the median point prevalence within the Asian elephant in the USA zoo population between 1997 and 2011 increased was 5.1%, with a range from 0.3% to 6.7%. Similarly, the average annual incidence was 2.4 cases per year, with a range from 0 to 7. Since 1960, a total of 45 cases of MTBC (45 M. tuberculosis) were tabulated in Asian elephants in comparison to only 5 cases in African elephants (4 M. tuberculosis and 1 M. bovis), suggesting a difference in species susceptibility (Feldman et al, 2013).

The results of a survey on necropsy reports of 301 Asian elephants and 196 African elephants kept in European zoos in the period from 1980 to 2024 is shown in table 1(Hess, 2021, updated by Willem Schaftenaar, 2024).

MTBC cases confirmed at necropsy in elephants kept in European zoos from 1980-2024.

Table 1. MTBC cases confirmed at necropsy in elephants kept in

European zoos from 1980-2024.

One case of M. caprae has been reported in a Bornean elephant housed in a zoo in Japan. Another M.caprae case in a European zoo is included in table 1.

Tuberculosis in range-countries

In countries where contact between man and elephant is close, tuberculosis forms a health risk for both humans and elephants.

In a study in Malaysia under 60 elephants in 6 different facilities, the overall seroprevalence of TB amongst the elephants was 23.3% and the risk of seroconversion was significantly higher among elephants with assigned mahouts. The percentage of positive responders among wildlife staff was 24.8% and the risk of infection was observed to be significantly associated with being a zoo employee or elephant handler. These findings revealed a potential risk of TB infection in captive elephants and handlers in Malaysia (Yakubu, 2016).

Tuberculosis in free ranging elephants

Paudel et al (2020) gave an overview of tuberculosis in free ranging elephants. The first report of TB in wild Asian elephants was from Sri Lanka in 2014. A 35-year-old female elephant was found in a moribund condition in the corridor between Udawalawe and Lunugamwehera National Parks. Three wild male Asian elephants that died between 2007 and 2013 in a wildlife sanctuary in southern India were confirmed to be TB positive. One wild Asian elephant that died of suspected TB lesions in the forest of Rajiv Gandhi National Park, Karnataka, India in 2016, was confirmed as TB positive.

The first case of TB infection in wild African elephants was reported in Kenya in. This elephant was an orphaned calf rescued from a national park in Kenya and raised with other rescued orphans and then was eventually released back into the wild. Serology, using STAT-PAK on banked serum samples collected from free-ranging African elephants between 2004 and 2018 in Kruger National Park (KNP) in South Africa showed that 9.3% of 161 elephants tested were MTBC positive (Kerr et al, 2019). MTBC was isolated for the first time from a wild African elephant from KNP in South Africa in 2016 (Miller et al, 2019).

Zoonotic aspects

Transmission of tuberculosis to elephant caretakers, mahouts or zoo visitors should always be considered as a threat to human health. Once an elephant is suspected of tuberculosis, caretakers should seek medical assistance and be checked for this disease on a regular basis.

Transmission to other mammalian species

The pathogen can be transmitted to humans and other mammalian species by direct contact, contaminated food and materials. Zoo animals treated by the same animal caretakers can transmit MTBC from a shedding elephant to other species (and vice versa). In a Swedish zoo 4 different M. tuberculosis strains were found in different elephants and other zoo animals in the same period (see diagram below): strain A was present in an Asian elephant, a gibbon and a group of South American tapirs. Strain B was found in 4 Asian elephants, while strain C was detected in a giraffe and one of the elephants that also harbored strain B. Strain D was found in an Asian elephant that also carried strain B (Sternberg et al, 2005).

In an Australian zoo, a diseased chimpanzee was diagnosed with tuberculosis caused by a MTBC-strain that was indistinguishable from a strain found in an Asian elephant at the same zoo. Investigations included staff and animal screening. Four staff had tuberculin skin test conversions associated with spending at least 10 hours within the elephant enclosure; none had disease (Stephans et al, 2013).

TB-suspected elephants should not be in contact with animals that are considered TB-free. Separate cleaning materials and equipment must be used for TB-suspected elephants.

Symptoms

Tuberculosis is a slow developing disease. Most elephants with TB are older than 5 years. One of the first signs of clinical disease is persistent weight loss. Often this is the only symptom seen. If no explanation can be found for this chronic weight loss, one should consider TB as its possible cause. Although the lungs are usually the first organs that are affected, respiratory signs are usually not observed. Other organs can also become affected, like kidneys, urinary bladder, GI-tract, uterus, liver pancreas and mesenteries. Metastatic MTBC-granulomas are often found in lymph nodes that drain the affected organ system.

The lesions caused by MTBC consist of granulomas. If the immune system of the elephant is functioning well, such granulomatous inflammation can be contained, and a buffer zone of defensive cells can produce a capsula around this process. In old granulomas, the original inflammation tissue can become calcified. Even in such a calcified granuloma, vital Mycobacteria can still be present. The presence of such ‘inactive’ granulomas may go completely unnoticed without causing any visible discomfort. Only immunological diagnostic assays will detect such a silent carrier.

Unfortunately, many elephants that become infected with MTBC will develop multiple granulomas often with metastasis to regional lymph nodes. Once a granuloma breaks through into the air-containing space of the lung alveoli or bronchi, the elephant can spread the disease to other elephants, humans or other mammals by direct and indirect contact. Sputum that has entered the lower airways can be brought up into the higher airways and, when swallowed, reach the stomach and intestines. MTBC has been detected in fecal samples.

If the infection route is orally, granulomas can develop in the GI tract. MTBC-granulomas in the kidneys, urinary tract, uterus or other organs are the result of bacteremia.

Granulomas caused by M.tuberculosis in an adult African elephant bull.

Figure 1. Granulomas caused by M.tuberculosis in an adult African elephant bull. Courtesy: Christian Wenker

Sputum collected from the same elephant bull tested positive for M. tuberculosis in PCR and culture.

Figurs 2. Sputum collected from the same elephant bull tested positive for M. tuberculosis in PCR and culture. Courtesy: Christian Wenker

Transmission

When the granulomas affect the excretion system of the organs, the pathogens can contaminate the environment (sputum, urine, feces, fetal fluids) and transmit the disease to other animals. Transmission by breeding has never been documented in elephants. The trunk is considered a major transmission organ of Mycobacterium spp. originating from the lungs. Nevertheless, it is very difficult to find TB-organisms in trunk washes (see trunk wash procedure). There are several anecdotal reports that a sputum sample found on the floor was confirmed TB-positive while numerous trunk wash samples from the same elephant had been tested negative.

Diagnosis

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Test samples

Any granulomatous lesion that is found at necropsy should be suspected of MTBC.

Trunk wash samples are frequently used to monitor elephants for MTBC. The elephant needs to be trained for this procedure. For the description of the procedure, click here. Fluids recovered from the trunkwash must be submitted for PCR and culture. The sensitivity of this procedure is extremely low (1-2%) (Sternberg et al. 2005, Vogelnest et al. 2015), which makes the trunkwash a questionable diagnostic tool.

Samples obtained by Broncho Alveolar Lavage (BAL) are considered more sensitive than trunk wash samples. However, one should realize that the probability to target an infected bronchus by the BAL-method depends on the number and severity of the lesions. An elephant suspected of carrying MTBC based on immunological tests, can harbor just one or a few encapsulated granulomas in the lung; BAL-samples taken from the area of such granulomas will yield no MTBC. Click here to read more about BAL. A disadvantage of the procedure is that it requires standing sedation or general anesthesia.

Excretions like sputum (see figure 2) urine, feces and fetal fluids in MTBC-suspected elephants (chronic weight loss) should be submitted for culture and PCR.

Direct tests

  • The golden standard method to diagnose MTBC is culturing of the pathogen. This requires a lab that is certified to culture this microbe. The culturing procedure can take as long as 6 -10 weeks. The cultured isolates must be spoligotyped and preferably submitted for multilocus, variable-number of tandem repeat analysis (MLVA) and whole-genome sequencing, as described previously (Ruetten et al, 2020, Ghielmetti, 2017).

  • PCR is next in reliability and usually carried out in conjunction with culture. Results can be obtained within one day. Positive results should still be cultured.

  • Acid-fast stain (Zhiel-Neelson) on tissue or swab samples can demonstrate the presence of acid-fast bacteria. Confirmation needs to come from culture.

 

Indirect tests (immunological tests)

1. Tests based on cellular immunity. The WHO recommends the following immunological tests as the first choice (for humans):

  • Interferon Gamma Release Assay (IGRA): PBMCs are stimulated with antigens of MTBC. After incubation the amount of elephant interferon is measured in the supernatant (Angkawanish et al, 2013). This assay is currently being practiced at the Utrecht University for monitoring TB in the European elephant population. Another IGRA has been developed in Japan (Paudel et al, 2016).

  • Skin test: in individuals that have been in contact or still carry MTBC intra-cutaneous injection of MTBC- derived antigens can cause a local reaction of the skin (swelling, redness, warm) after 72 hours. Due to the unique properties of the very thick elephant’s skin, this test is not recommended for elephants (Mikota et.al. 2001).

 

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Dual Path Platform Assay VetTB Assay for elephants

2. Tests based on humoral immunity

  • DPP = Dual Path Platform Assay VetTB Assay for elephants: antibodies against several MTBC-antigens can be demonstrated in a quick test, which is based on ELISA-technology.

  • Multi Antigene Print Immuno Assay (MAPIA). This test is offered by Chembio (USA) as a confirmation test of the DPP VetTB Assay for elephants. Each antigen that is present in the DPP is individually tested in the MAPIA.

  • ELISA- some local labs had developed their own in-house ELISA. Currently they are not being used.

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Note: A study in Japan concluded that the discrepancies between serological and IGRA highlight that the two methods may detect different stages of elephant TB. Therefore, employing both tests may enable them to complement each other in correctly identifying elephants that have been exposed to MTBC (Songthammanuphap et al, 2020).

Cross reactions

Immunological tests have the disadvantage that they do not detect the pathogen itself, but only the immunological reaction of the host to MTBC. Unfortunately, several non-tuberculous Mycobacterium spp (such as M. kansasii, M. fortuitum) have some antigens in common with MTBC. Therefore, one should always take additional circumstances into account when an immunological test turns out positive for MTBC. Chronic weight loss, a history of MTBC in the herd, a caretaker suffering from tuberculosis are factors that can help form a stronger diagnosis than just the outcome of an immunological test.

 

Non-tuberculous Mycobacterium spp.

Several non-tuberculous Mycobacteria (NTM) have been identified, e.g. M. intracellulare, M. hominnisuis, M. fortuitum, M.avium, M. flehi, M kansasii. In one study, isolates of M. avium, M. peregrinum, and M. novocastrense, three NTM species, were detected in samples from the lung or mouth (Hermes et al, 2018). One NTM, Mycobacterium szulgai, was associated with mortality in two captive African elephants (Loxodonta africana) (Lacasse et al, 2007).

Treatment

Treatment of MTBC has been an option when MTBC is confirmed by culture. One should realize, however, that the complete elimination of the pathogen by treatment is not guaranteed. Like in humans, MTBC can remain present in encapsulated foci and relapses after several years have occurred. Treating tuberculosis is expensive, laborious, and needs to be sustained for a long period. As some of the drugs are (nephro)toxic, negative side effects of the drugs need to be monitored closely. The elephant protocol is based on treatment regimens that are used to treat TB in humans. The basic protocol calls for 3-4 drugs for 2 months followed by 2 drugs for 10 months. Isoniazid, rifampin, ethambutol, and pyrazinamide are the first line drugs that are typically used. Administration is oral or rectal although rectal Rx has some limitations. If at all possible, serum drug levels should be monitored. Treatment details can be found in chapter 9 and 10 of the Guidelines for the control of tuberculosis in elephants 2010 .

Surveillance

Monitoring elephants that have been in contact with other animals suffering of MTBC (including humans) by regular TB-testing is the most effective way to detect an infection. Elephants with a TB-history (treated or in contact with MTBC-positive animals) should not be moved to a TB-free facility. Annual TB-screening of caretakers should be part of the elephant management in zoos.

Moving elephants

Elephants that will be moved from one zoo to another should be checked before the transfer. Click here for TB-recommendation for European zoos and click here for TB-recommendation for USA zoos.

The release of orphaned elephants after rehabilitation in a management system under human care, carries a risk of transmission of tuberculosis to free ranging elephants. The disease may have been present unnoticed during the rehab period. Testing for MTBC prior to release should be a requirement without which no release should take place.

Prevention

A vaccine against tuberculosis in elephants is not available. The value of BCG-vaccination, used to vaccinate humans in endemic areas, has not been tested in elephants.  Even in humans, it only prevents the childhood meningitis form of TB and does not protect against pulmonary TB.

Government regulations

Though M. bovis is just one of the MTB-complex group, for economic reasons related to the cattle industry, most governments only have strong regulations for cases of tuberculosis caused by M. bovis. In those countries, tuberculosis caused by M. bovis in elephants is notifiable. Because of the zoonotic aspects of the disease it is, however, strongly recommended to contact government officials in any case of confirmed tuberculosis.

References

  • Hess A. 2021. Lesions found in the post-mortem reports of the Asian (Elephas maximus) and African (Loxodonta africana) elephants of the European Association of Zoos and Aquaria. Thesis at the Department of Exotic Animal and Wildlife Medicine University of Veterinary Medicine Budapest, Hungary. Updated by Schaftenaar W. 2024. Unpublished data EAZA elephant TAG studbook.

  • Paudel S, Sreevatsan S. 2020. Tuberculosis in elephants: Origins and evidence of interspecies transmission. Science direct: Tuberculosis 123 (2020) 101962.

  • Ruetten M, Steinmetz HW, Thiersch M, Kik M, Vaughan L, Altamura S, Muckenthaler MU and Gassmann M. 2020. Iron regulation in elderly Asian elephants (Elephas maximus) chronically infected with Mycobacterium tuberculosis. Front. Vet. Sci. 7:596379. doi: 10.3389/fvets.2020.596379

  • Songthammanuphap S, Puthong S, Pongma C, BuakeawA, Prammananan T, Warit S, Tipkantha W, Kaewkhunjob E, Yindeeyoungyeon W, and Palaga T. 2020. Detection of Mycobacterium tuberculosis complex infection in Asian elephants (Elephas maximus) using an interferon gamma release assay in a captive elephant herd. Scientific Reports (2020) 10:14551; https://doi.org/10.1038/s41598-020-71099-3

  • Kerr TJ, de Waal CR, Buss PE, Hofmeyer J, Lyashchenko KP, Miller M.A. 2019. Seroprevalence of Mycobacterium tuberculosis Complex in Free-ranging African Elephants (Loxodonta africana) in Kruger National Park, South Africa. J Wildl Dis (2019) 55 (4): 923–927.

  • Miller MA, Buss P, Roos EO, Hausler G, Dippenaar A, Mitchell E, van Schalkwyk L, Robbe-Austerman S, Waters WR, Sikar-Gang A, Lyashchenko KP, Parsons SDC, Warren R and van Helden P. (2019). Fatal Tuberculosis in a Free-Ranging African Elephant and One Health Implications of Human Pathogens in Wildlife. Front. Vet. Sci. 6:18. doi: 10.3389/fvets.2019.00018

  • R. Hermes R, Saragusty J, Holtze S, Nieter J, Sachse K, Voracek T, Bouts T, Göritz F, and Hildebrandt TB. 2018. Bronchoalveolar lavage for diagnosis of tuberculosis infection in elephants. Epidemiology and Infection 146, 481–488. https://doi.org/10.1017/S0950268818000122

  • Ghielmetti G, Coscolla M, Ruetten M, Friedel U, Loiseau C, Feldmann J. 2017. Tuberculosis in Swiss captive Asian elephants: microevolution of Mycobacterium tuberculosis characterized by multilocus variable-number tandem-repeat analysis and whole-genome sequencing. Sci Rep. (2017) 7:14647. doi: 10.1038/s41598-017-15278-9

  • Paudel S, Villanueva M.A, Mikota S.K, Nakajima C, Gairhe K.P, Subedi S, Rayamajhi N, Sashika M, Shimozuru M, Matsuba T, ySuzuki Y and Tsubota T. 2016. Development and evaluation of an interferon-γ release assay in Asian elephants (Elephas maximus). J. Vet. Med. Sci. 78(7): 1117–1121, 2016

  • Yakubua Y, Onga B.L., Zakaria Z, Hassan L, Mutalib A.R., Ngeowc Y.F., Verasahib K, Razak M.F.A.A. 2016. Evidence and potential risk factors of tuberculosis among captive Asian elephants and wildlife staff in Peninsular Malaysia. Preventive Veterinary Medicine Volume 125, 1 March 2016, Pages 147-153.

  • Vogelnest L, Hulst F, Thompson P, Lyashchenko K.P., Vinette Herrin K.A. 2015. Diagnosis and management of tuberculosis (Mycobacterium tuberculosis) in an Asian elephant (Elephas maximus) with a newborn calf. Journal of Zoo and Wildlife Medicine 46(1): 77–85, 2015.

  • Angkawanish T, Morar D, van Kooten P, Bontekoning I, Schreuder J, Maas M, Wajjwalku W, Sirimalaisuwan A, Michel A, Tijhaar E and Rutten V. 2013. The Elephant Interferon Gamma Assay: A Contribution to Diagnosis of Tuberculosis in Elephants. Transboundary and Emerging Diseases. 60 (Suppl. 1) (2013) 53–59.

  • Feldman M, Isaza R, Prins C, Hernandez J. 2013.Point prevalence and incidence of Mycobacterium tuberculosis complex in captive elephants in the United States of America. Vet Q 2013; 33:25–9.

  • Stephans N, Vogelnest L, Lowbridge C, Christensen A, Marks G.B., Sintchenko V, McAnulty J. 2013. Transmission of Mycobacterium tuberculosis from an Asian elephant (Elephas maximus) to a chimpanzee (Pan troglodytes) and humans in an Australian zoo. Epidemiol. Infect. (2013), 141, 1488–1497. © Cambridge University Press 2013

  • Lacasse C, Terio K, Kinsel M.J, Farina L.L, Travis D.A. D.A, Rena Greenwald, Konstantin P. Lyashchenko, Miller M, Gamble K.C. 2007. Two cases of atypical mycobacteriosis caused by Mycobacterium szulgai associated with mortality in captive African elephants (Loxodonta africana). J. of Zoo and Wildlife Medicine, 38(1):101-107 (2007).

  • Sternberg Lewerin S, Olsson S-L, Eld K, Röken B, Ghebremichael S, Koivula T, Källenius G, Bölske G. 2005. Outbreak of Mycobacterium tuberculosis infection among captive Asian elephants in a Swedish zoo. Veterinary Record (2005) 156, 171-175.

  • Mikota SK, Peddie L, Peddie J, Isaza R, Dunker F, West G, Lindsay L, Larsen RS. 2001. Epidemiology and diagnosis of M. tb in captive Asian elephants. J. Zoo Wildl. Med. 32: 1-16

Tuberculosis

Tuberculosis is an infectious zoonotic disease with a ubiquitous distribution, caused by Mycobacterium species. The most relevant species that affect mammals belong to the group of Mycobacterium tuberculosis-complex (MTBC), including M. tuberculosis, M. bovis, M. pinnipedi, M. africanum, M. microti, M. canetii, M.caprae and Bacillus Calmette-Guérin (vaccine). The disease is relevant for elephants under human care, as transmission from man to elephant and vice versa is possible. TB is a chronic disease with a long incubation period, and the initial stages of the disease are often missed.

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