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Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and elephants.

Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and... Dispatches Mycobacterium tuberculosis Infection as a Zoonotic Disease: Transmission between Humans and Elephants Kathleen Michalak,* Connie Austin,† Sandy Diesel,* J. Maichle Bacon,* Phil Zimmerman,‡ and Joel N. Maslow§ *McHenry County Department of Health, Woodstock, Illinois, USA; †Illinois Department of Public Health, Springfield, Illinois, USA; ‡University of Illinois, College of Medicine at Rockford, Rockford, Illinois, USA; and §Boston University School of Medicine and the VA Medical Center, Boston, Massachusetts, USA Between 1994 and 1996, three elephants from an exotic animal farm in Illinois died of pulmonary disease due to Mycobacterium tuberculosis. In October 1996, a fourth living elephant was culture-positive for M. tuberculosis. Twenty-two handlers at the farm were screened for tuberculosis (TB); eleven had positive reactions to intradermal injection with purified protein derivative. One had smear-negative, culture-positive active TB. DNA fingerprint comparison by IS6110 and TBN12 typing showed that the isolates from the four elephants and the handler with active TB were the same strain. This investigation indicates transmission of M. tuberculosis between humans and elephants. Mycobacterium tuberculosis and M. bovis, Transmission of M. tuberculosis between animals related organisms of the M. tuberculosis complex, and humans has not been reported. This paper infect a wide variety of mammalian species. M. describes M. tuberculosis transmission from bovis is pathogenic for many animal species, elephants to humans. especially bovidae, cervidae, and occasionally carnivores. Human disease with M. bovis is well The Outbreak described and historically was a common cause of In March 1996, five elephants from an exotic tuberculosis (TB) transmitted by infected dairy animal farm in Illinois were in California as part products. As a result of milk pasteurization and of a circus act. One elephant (with chronic, TB eradication programs in most industrialized unexplained weight loss since October 1995) died countries, zoonotic transmission of M. bovis under anesthesia on August 3, 1996, during a through domestic livestock is now rare. In contrast, diagnostic dental work-up. Necropsy showed a similar eradication program has not been widespread consolidation of lung tissue with conducted for wild or exotic animals, which caseous necrosis of the lungs and mediastinal therefore remain an uncommon source for M. bovis lymph nodes. Short, fat, relatively scant numbers exposure. Zoonotic transmission of M. bovis has of acid-fast bacilli were observed in necropsy been reported from seals, rhinoceros, and elk (1-4). tissues. A presumptive diagnosis of M. tuberculo- M. tuberculosis, the most common species to sis was made. The remaining four elephants were cause TB, classically causes disease in humans. recalled to the farm in Illinois. A second elephant Animal infection with M. tuberculosis, while died en route on August 6, 1996. Necropsy uncommon, has been described among species revealed copious respiratory and trunk exudates (e.g., birds, elephants, and other mammals) with and caseous necrosis of the lung. prolonged and close contact with humans (5-10). To determine the risk for and possibility of infection among the animal trainers and caretakers, an epidemiologic investigation was Address for correspondence: Kathleen Michalak, McHenry County Department of Health, 2200 N. Seminary Avenue, initiated. The remaining elephants in the herd Woodstock, IL 60098, USA; fax: 815-338-7661. and the elephant handlers and trainers who were Vol. 4, No. 2, April–June 1998 Emerging Infectious Diseases 283 Dispatches still traveling were recalled to the farm and analysis. Southern blots of Pvu II restricted examined for evidence of M. tuberculosis whole chromosomal DNA, resolved in 1% agarose infection. All elephants were empirically begun on gels, were probed with a DNA fragment antituberculous therapy in early December 1996. corresponding to the right side of IS6110 and detected by chemiluminescence (11). The number Epidemiologic Investigation and size of the hybridizing fragments for each The exotic animal farm was visited on isolate were compared in the same gel. Isolates numerous occasions to evaluate the type and with identical RFLP patterns or with ≤ 2 band degree of contact between elephants and differences were considered to represent the employees. The farm, located in a rural area and same strain. Additionally, Pvu II digested DNA surrounded by barbed wire and trees, originally was similarly typed after probing with the housed 18 Asian and 2 African elephants. repetitive element TBN12. Thirteen elephants were tethered on a chain in one large barn, four were housed in a separate Epidemiologic Findings large room (two in a common stall), and a baby Elephant handlers worked in very close elephant was in a third room with 5-6 tigers. A proximity with the elephants around the clock, separate barn housed approximately 80 tigers. whereas tiger handlers had little direct contact with the elephants. Most of the elephant handlers TB Screening of Employees lived on the farm in a separate section of the barn; The animal handlers (trainers and caretak- four lived in trailers on the grounds. The handlers’ ers) who had direct contact with the elephants living quarters had a separate ventilation system were administered purified protein derivative from the elephants’; however, the doors between (PPD) skin tests. Initial screening was performed the two quarters were open for unknown periods. in August 1996, with subsequent screenings in Handlers indicated that they held social events in a December 1996 and March, June, and September building connected to the elephant barn. of 1997. Testing was performed by the McHenry Necropsies of elephants were performed on County Department of Health, except in two the farm and were attended by a number of handlers who had subsequent skin tests elephant and tiger handlers (including the performed elsewhere. As part of the screening handler with the active case). The necropsy of process, handlers were questioned about their the elephant that died in 1994, also performed risk factors for TB, including previous bacillus on the farm, showed caseous necrosis of the Calmette-Guérin (BCG) vaccination. lungs and pleural exudates whose culture Handlers were tested by the two-step method yielded M. tuberculosis. using 5 tuberculin units of PPD (0.1 ml) by In addition to the three elephants that died of intradermal injection in the flexor surface of the M. tuberculosis infection, a fourth living elephant forearm. A positive result was defined as an was also infected with the mycobacterium; this induration of >5 mm. Handlers with positive skin infection was diagnosed in late December 1996 tests were evaluated by a TB health-care worker from a trunk culture obtained in October 1996. and had chest radiographs taken. Sputum Subsequent cultures from this and the other samples from any handler with a chest animals have been negative for mycobacteria. radiograph consistent with TB were submitted to Another elephant from this farm died of M. the Illinois Department of Public Health tuberculosis infection in 1981 (5), but contact Laboratory. Samples were examined by direct between this elephant and the present herd or microscopy for acid-fast organisms, stained with any of the handlers could not be established. fluorochrome, and processed for culture by Twenty-two handlers at the exotic animal standard methods. farm had moderate to frequent contact with the infected animals; 12 were elephant handlers and Examination of Isolates 10 were tiger handlers. Initial PPD testing was The human isolate and the four elephant performed for 14 handlers in August 1996, 2 in isolates were sent to the National Tuberculosis October 1996, and 5 in December 1996. One who Genotyping and Surveillance Network at the was PPD-positive in November 1995 reported Michigan Community Public Health Agency for receiving BCG more than 10 years before. restriction fragment length polymorphism (RFLP) Eleven (50%) of 22 handlers were found PPD- Emerging Infectious Diseases Vol. 4, No. 2, April–June 1998 284 Dispatches positive as part of this investigation. Eight of the was reduced to INH and rifampin when the isolate 11 had positive PPD skin test results upon initial showed no resistance to antituberculous medica- testing, with a median induration of 12 mm tions. Subsequent chest radiographs revealed (range, 10 to 19 mm). Four of the eight were improvement or clearing of the initial lesions. Nine elephant handlers and four were tiger handlers. of the remaining 11 PPD-positive handlers were The skin test reaction of three handlers converted prescribed INH prophylaxis; two declined because from negative to positive with a median induration of the risk for adverse reactions. of 12 mm (range, 8 to 15 mm). The three PPD converters were initially tested in August 1996; one Molecular Analysis of Elephant and Human was positive upon retesting in January 1997, and Isolates two tested positive in April 1997 (Table). The sputum isolate from the handler with Eight of the 11 handlers reported that they active TB was compared with the isolates from had negative skin tests in the past and had not the three animals that died and the living received BCG. The other three reported some elephant whose infection was diagnosed during type of reaction from a previous skin test in the the investigation. The isolates had identical past but did not know the results. All three also IS6110 RFLP pattern, differing by ≤ 2 bands reported receiving BCG more than 10 years (Figure 1). Additionally, all isolates had the before. Eight of the 10 handlers with negative identical TBN12 RFLP pattern, except the isolate PPD skin tests had at least one negative follow- from the elephant that died in August 1996, which up test at 3 months; two left the farm and did not demonstrated a shift of one band (Figure 2). receive follow-up testing. The attack rates were approximately equal Conclusions for the elephant and tiger handlers. Of the 12 Infection with M. tuberculosis or M. bovis has elephant handlers tested, 6 (50%) were PPD- not been reported in nondomesticated Asian or positive with two conversions documented in African elephants. M. tuberculosis infection in April 1997; of the 9 tiger handlers, 5 (56%) were domesticated elephants was first reported in PPD-positive, with one conversion documented 1875 by Garrod and has been recognized in the in January 1997. Overall, a very high rate (52%) ancient Ayurvedic literature (10); humans have of handlers tested positive. been considered the source of infection. A trainer All 12 handlers with positive PPDs (including with cavitary TB was suspected as the source of the one with the known positive PPD) received an infection (8) for one Asian elephant that died of evaluation and chest radiograph; one had M. tuberculosis, although subsequent analysis irregular nodules and interstitial changes in the showed the animal and human isolates to be of right apex without retraction of the lungs, two different phage types. consistent with active TB, but no cough, chest This report describes the first case of zoonotic pain, fever, night sweats, weight loss, or fatigue. M. tuberculosis transmission. The epidemiologic Three sputum samples were smear-negative investigation strongly suggests M. tuberculosis for acid-fast bacilli, although one yielded M. transmission between humans and elephants, as tuberculosis upon culture. Isoniazid (INH), rifampin, evidenced by DNA fingerprinting. RFLP analysis pyrazinamide, and ethambutol treatment was comparing Southern blots of chromosomal DNA initiated in September 1996, and after 2 months, probed with IS6110 and TBN12 indicated that four elephant isolates had identical patterns with the human isolate, differing by ≤ 2 bands. The a addition or loss of a single band has been Table. TB PPD skin test results of animal handlers, Aug demonstrated in other outbreak settings, and the 1996–Sep 1997 repetitive element that generates patterns has Positive Negative characteristics of a mobile genetic element (11). Previously positive 1 Eleven (50%) of 22 employees screened were Elephant handlers 4 6 skin-test positive, with no difference between Tiger handlers 4 4 tiger and elephant handlers. This is a higher rate Elephant handlers (converted) 2 Tiger handlers (converted) 1 of positives than documented in animal Total 12 10 handlers exposed to M. bovis-infected animals Tuberculin purified protein derivative. (3,4). Since the handlers had no accurate Vol. 4, No. 2, April–June 1998 Emerging Infectious Diseases 285 Dispatches 1 2 34 56 12 3 4 5 6 Figure 1. IS6110 restriction fragment length polymor- Figure 2. TBN12 restriction fragment length polymor- phism results. Lane1, elephant isolate (died August 6, phism results. Lane1, elephant isolate (died August 6, 1996); Lane 2, elephant isolate (died 1994); Lane 3, liv- 1996); Lane 2, elephant isolate (died 1994); Lane 3, liv- ing elephant trunk culture (October 1996); Lane 4, el- ing elephant trunk culture (October 1996); Lane 4, el- ephant lung tissue isolate (died August 3, 1996); Lane ephant lung tissue isolate (died August 3, 1996); Lane 5, elephant lymph node tissue isolate (died August 3, 5, elephant lymph node tissue isolate (died August 3, 1996); Lane 6, human sputum isolate (September 1996). 1996); Lane 6, human sputum isolate (September 1996). Provided by State of Michigan Community Public Provided by State of Michigan Community Public Health Agency. Health Agency. history of tuberculin skin testing, it was not smear- and culture-negative; the third had low possible to determine when conversions took numbers of acid-fast bacilli manifested by a place. The original source of infection for both negative sputum smear, thus posing a low elephants and humans is unknown. infectivity risk to others. In contrast, the three The possible mechanisms of transmission elephants that died had evidence of widespread include close contact while handling and training pulmonary disease and, therefore, represented elephants, cleaning the barn, participating in a greater risk for dissemination. elephant necropsies, and living in close proximity Three handlers converted from negative to to the elephant barn. positive during the course of the investigation; Human-to-human transmission of TB is their relevant exposure is unknown. The source unlikely because the only handler with active may have been one elephant found antemortem disease did not have cough. Of the three to be culture-positive for M. tuberculosis, sputum samples initially collected, two were although this animal did not return to the farm Emerging Infectious Diseases Vol. 4, No. 2, April–June 1998 286 Dispatches until November. Contact with this animal is Laboratories; and Janet Payeur, National Veterinary Services Laboratory, U.S. Department of Agriculture, MB Section. This unlikely for handlers whose PPD tests converted research was supported in part by the Centers for Disease in December and unknown for the two handlers Control and Prevention, National Tuberculosis Genotyping whose test results were positive in April (the and Surveillance Network cooperative agreement. latter two had not been retested since August). Kathleen Michalak is the Director of Nursing for TB is transmitted through close prolonged McHenry County Department of Health. She has worked contact with a person (or animal) with active TB. to improve the use of community resources, and The risk for TB transmission from an animal with improved service to client, providers, and the community a case of active TB is higher for daily handlers as a whole. than for persons with only brief contact, e.g., members of the public viewing a performance or References receiving elephant rides. In this outbreak, 1. Thoen CO. Tuberculosis (Revised 1995). Zoonosis screening of all persons who had (or thought updates. Journal of the American Veterinary Medical Association 1995;2:155-8. they had) contact with an elephant that died of 2. Thompson PJ, Cousins DV, Gow BL, Collins DM, M. tuberculosis identified three PPD-positive Willamson BH, Dagnia HT. Seals, seal trainers, and cases but no cases of active TB (8). Because the mycobacterial infection. American Review of real risk for transmission to the general public Respiratory Diseases 1993;147:164-7. was poorly understood, this case received 3. Dalovisio JR, Stetter M, Mikota-Wells S. Rhinoceros’ rhinorrhea: cause of an outbreak of infection due to considerable media attention as well as mention airborne Mycobacterium bovis in zookeepers. Clin in the medical literature (7,12). Infect Dis 1992;15:598-600. Veterinary practices should be initiated to 4. Fanning A, Edwards S. Mycobacterium bovis infection reduce the risks for exposure to animals infected in human beings in contact with elk (Cervus elaphus) in with M. tuberculosis. No data are available on TB Alberta, Canada. Lancet 1991;338:1253-5. 5. Saunders G. Pulmonary Mycobacterium tuberculosis incidence among domesticated elephants in the infection in a circus elephant. J Am Vet Med Assoc United States. An estimate can be derived from a 1983;183:1311-2. retrospective study of 379 zoo elephants of which 6. Pinto MRM, Jainudeen MR, Panabokke RG. eight (2.3%) had M. tuberculosis infection (10). Tuberculosis in a domesticated Asiatic Elaphas Reliable diagnosis and prevention of TB in all maximus. Vet Rec 1973;93:662-4. 7. Frankel D. Elephants pack their trunks and leave the domesticated and exhibited animals is ideal. circus. Lancet 1997;349:1675. Short of this, possible ways to prevent and 8. Greenberg AS, Jung RC, Gutter AK. Hazel Elephant is decrease zoonotic spread of any mycobacterial dead (of Tuberculosis). American Review of Respiratory infection (M. tuberculosis or M. bovis) include 1) Diseases 1981;124:341. regular skin testing of handlers or keepers; 2) a 9. Jones WD, Good RC. Hazel elephant redux. American Review of Respiratory Diseases 1982;125:270. high index of suspicion of TB in elephants with 10. Mikota S, Sargent EL, Ranglack GS. Medical unexplained weight loss, cough, or rhinorrhea; 3) management of the elephant. Tuberculosis and public health measures of contact tracing and Tuberculin Testing 1994;33-9. notification; and 4) active and effective treatment 11. Small P, Moss A. Molecular epidemiology and the new of infected personnel and animals (13). tuberculosis. Infect Agents Dis 1993;2:132-8. 12. Furley CW. Tuberculosis in elephants. Lancet 1997;350:224. Acknowledgments 13. Centers for Disease Control and Prevention. Guidelines We thank Stephen Dietrich and Laura Mosher, North for preventing the transmission of Mycobacterium Central Area TB-RFLP Laboratory, Michigan Department of tuberculosis in health-care facilities. MMWR Morb Public Health; George J. Dizikes, Chief of Molecular Mortal Wkly Rep 1994;43:63-4. Diagnostics, Illinois Department of Public Health, Division of Vol. 4, No. 2, April–June 1998 Emerging Infectious Diseases http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Emerging Infectious Diseases Pubmed Central

Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and elephants.

Michalak, K; Austin, C; Diesel, S; Bacon, M J; Zimmerman, P; Maslow, J N
Emerging Infectious Diseases , Volume 4 (2) – Jun 1, 167
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Dispatches Mycobacterium tuberculosis Infection as a Zoonotic Disease: Transmission between Humans and Elephants Kathleen Michalak,* Connie Austin,† Sandy Diesel,* J. Maichle Bacon,* Phil Zimmerman,‡ and Joel N. Maslow§ *McHenry County Department of Health, Woodstock, Illinois, USA; †Illinois Department of Public Health, Springfield, Illinois, USA; ‡University of Illinois, College of Medicine at Rockford, Rockford, Illinois, USA; and §Boston University School of Medicine and the VA Medical Center, Boston, Massachusetts, USA Between 1994 and 1996, three elephants from an exotic animal farm in Illinois died of pulmonary disease due to Mycobacterium tuberculosis. In October 1996, a fourth living elephant was culture-positive for M. tuberculosis. Twenty-two handlers at the farm were screened for tuberculosis (TB); eleven had positive reactions to intradermal injection with purified protein derivative. One had smear-negative, culture-positive active TB. DNA fingerprint comparison by IS6110 and TBN12 typing showed that the isolates from the four elephants and the handler with active TB were the same strain. This investigation indicates transmission of M. tuberculosis between humans and elephants. Mycobacterium tuberculosis and M. bovis, Transmission of M. tuberculosis between animals related organisms of the M. tuberculosis complex, and humans has not been reported. This paper infect a wide variety of mammalian species. M. describes M. tuberculosis transmission from bovis is pathogenic for many animal species, elephants to humans. especially bovidae, cervidae, and occasionally carnivores. Human disease with M. bovis is well The Outbreak described and historically was a common cause of In March 1996, five elephants from an exotic tuberculosis (TB) transmitted by infected dairy animal farm in Illinois were in California as part products. As a result of milk pasteurization and of a circus act. One elephant (with chronic, TB eradication programs in most industrialized unexplained weight loss since October 1995) died countries, zoonotic transmission of M. bovis under anesthesia on August 3, 1996, during a through domestic livestock is now rare. In contrast, diagnostic dental work-up. Necropsy showed a similar eradication program has not been widespread consolidation of lung tissue with conducted for wild or exotic animals, which caseous necrosis of the lungs and mediastinal therefore remain an uncommon source for M. bovis lymph nodes. Short, fat, relatively scant numbers exposure. Zoonotic transmission of M. bovis has of acid-fast bacilli were observed in necropsy been reported from seals, rhinoceros, and elk (1-4). tissues. A presumptive diagnosis of M. tuberculo- M. tuberculosis, the most common species to sis was made. The remaining four elephants were cause TB, classically causes disease in humans. recalled to the farm in Illinois. A second elephant Animal infection with M. tuberculosis, while died en route on August 6, 1996. Necropsy uncommon, has been described among species revealed copious respiratory and trunk exudates (e.g., birds, elephants, and other mammals) with and caseous necrosis of the lung. prolonged and close contact with humans (5-10). To determine the risk for and possibility of infection among the animal trainers and caretakers, an epidemiologic investigation was Address for correspondence: Kathleen Michalak, McHenry County Department of Health, 2200 N. Seminary Avenue, initiated. The remaining elephants in the herd Woodstock, IL 60098, USA; fax: 815-338-7661. and the elephant handlers and trainers who were Vol. 4, No. 2, April–June 1998 Emerging Infectious Diseases 283 Dispatches still traveling were recalled to the farm and analysis. Southern blots of Pvu II restricted examined for evidence of M. tuberculosis whole chromosomal DNA, resolved in 1% agarose infection. All elephants were empirically begun on gels, were probed with a DNA fragment antituberculous therapy in early December 1996. corresponding to the right side of IS6110 and detected by chemiluminescence (11). The number Epidemiologic Investigation and size of the hybridizing fragments for each The exotic animal farm was visited on isolate were compared in the same gel. Isolates numerous occasions to evaluate the type and with identical RFLP patterns or with ≤ 2 band degree of contact between elephants and differences were considered to represent the employees. The farm, located in a rural area and same strain. Additionally, Pvu II digested DNA surrounded by barbed wire and trees, originally was similarly typed after probing with the housed 18 Asian and 2 African elephants. repetitive element TBN12. Thirteen elephants were tethered on a chain in one large barn, four were housed in a separate Epidemiologic Findings large room (two in a common stall), and a baby Elephant handlers worked in very close elephant was in a third room with 5-6 tigers. A proximity with the elephants around the clock, separate barn housed approximately 80 tigers. whereas tiger handlers had little direct contact with the elephants. Most of the elephant handlers TB Screening of Employees lived on the farm in a separate section of the barn; The animal handlers (trainers and caretak- four lived in trailers on the grounds. The handlers’ ers) who had direct contact with the elephants living quarters had a separate ventilation system were administered purified protein derivative from the elephants’; however, the doors between (PPD) skin tests. Initial screening was performed the two quarters were open for unknown periods. in August 1996, with subsequent screenings in Handlers indicated that they held social events in a December 1996 and March, June, and September building connected to the elephant barn. of 1997. Testing was performed by the McHenry Necropsies of elephants were performed on County Department of Health, except in two the farm and were attended by a number of handlers who had subsequent skin tests elephant and tiger handlers (including the performed elsewhere. As part of the screening handler with the active case). The necropsy of process, handlers were questioned about their the elephant that died in 1994, also performed risk factors for TB, including previous bacillus on the farm, showed caseous necrosis of the Calmette-Guérin (BCG) vaccination. lungs and pleural exudates whose culture Handlers were tested by the two-step method yielded M. tuberculosis. using 5 tuberculin units of PPD (0.1 ml) by In addition to the three elephants that died of intradermal injection in the flexor surface of the M. tuberculosis infection, a fourth living elephant forearm. A positive result was defined as an was also infected with the mycobacterium; this induration of >5 mm. Handlers with positive skin infection was diagnosed in late December 1996 tests were evaluated by a TB health-care worker from a trunk culture obtained in October 1996. and had chest radiographs taken. Sputum Subsequent cultures from this and the other samples from any handler with a chest animals have been negative for mycobacteria. radiograph consistent with TB were submitted to Another elephant from this farm died of M. the Illinois Department of Public Health tuberculosis infection in 1981 (5), but contact Laboratory. Samples were examined by direct between this elephant and the present herd or microscopy for acid-fast organisms, stained with any of the handlers could not be established. fluorochrome, and processed for culture by Twenty-two handlers at the exotic animal standard methods. farm had moderate to frequent contact with the infected animals; 12 were elephant handlers and Examination of Isolates 10 were tiger handlers. Initial PPD testing was The human isolate and the four elephant performed for 14 handlers in August 1996, 2 in isolates were sent to the National Tuberculosis October 1996, and 5 in December 1996. One who Genotyping and Surveillance Network at the was PPD-positive in November 1995 reported Michigan Community Public Health Agency for receiving BCG more than 10 years before. restriction fragment length polymorphism (RFLP) Eleven (50%) of 22 handlers were found PPD- Emerging Infectious Diseases Vol. 4, No. 2, April–June 1998 284 Dispatches positive as part of this investigation. Eight of the was reduced to INH and rifampin when the isolate 11 had positive PPD skin test results upon initial showed no resistance to antituberculous medica- testing, with a median induration of 12 mm tions. Subsequent chest radiographs revealed (range, 10 to 19 mm). Four of the eight were improvement or clearing of the initial lesions. Nine elephant handlers and four were tiger handlers. of the remaining 11 PPD-positive handlers were The skin test reaction of three handlers converted prescribed INH prophylaxis; two declined because from negative to positive with a median induration of the risk for adverse reactions. of 12 mm (range, 8 to 15 mm). The three PPD converters were initially tested in August 1996; one Molecular Analysis of Elephant and Human was positive upon retesting in January 1997, and Isolates two tested positive in April 1997 (Table). The sputum isolate from the handler with Eight of the 11 handlers reported that they active TB was compared with the isolates from had negative skin tests in the past and had not the three animals that died and the living received BCG. The other three reported some elephant whose infection was diagnosed during type of reaction from a previous skin test in the the investigation. The isolates had identical past but did not know the results. All three also IS6110 RFLP pattern, differing by ≤ 2 bands reported receiving BCG more than 10 years (Figure 1). Additionally, all isolates had the before. Eight of the 10 handlers with negative identical TBN12 RFLP pattern, except the isolate PPD skin tests had at least one negative follow- from the elephant that died in August 1996, which up test at 3 months; two left the farm and did not demonstrated a shift of one band (Figure 2). receive follow-up testing. The attack rates were approximately equal Conclusions for the elephant and tiger handlers. Of the 12 Infection with M. tuberculosis or M. bovis has elephant handlers tested, 6 (50%) were PPD- not been reported in nondomesticated Asian or positive with two conversions documented in African elephants. M. tuberculosis infection in April 1997; of the 9 tiger handlers, 5 (56%) were domesticated elephants was first reported in PPD-positive, with one conversion documented 1875 by Garrod and has been recognized in the in January 1997. Overall, a very high rate (52%) ancient Ayurvedic literature (10); humans have of handlers tested positive. been considered the source of infection. A trainer All 12 handlers with positive PPDs (including with cavitary TB was suspected as the source of the one with the known positive PPD) received an infection (8) for one Asian elephant that died of evaluation and chest radiograph; one had M. tuberculosis, although subsequent analysis irregular nodules and interstitial changes in the showed the animal and human isolates to be of right apex without retraction of the lungs, two different phage types. consistent with active TB, but no cough, chest This report describes the first case of zoonotic pain, fever, night sweats, weight loss, or fatigue. M. tuberculosis transmission. The epidemiologic Three sputum samples were smear-negative investigation strongly suggests M. tuberculosis for acid-fast bacilli, although one yielded M. transmission between humans and elephants, as tuberculosis upon culture. Isoniazid (INH), rifampin, evidenced by DNA fingerprinting. RFLP analysis pyrazinamide, and ethambutol treatment was comparing Southern blots of chromosomal DNA initiated in September 1996, and after 2 months, probed with IS6110 and TBN12 indicated that four elephant isolates had identical patterns with the human isolate, differing by ≤ 2 bands. The a addition or loss of a single band has been Table. TB PPD skin test results of animal handlers, Aug demonstrated in other outbreak settings, and the 1996–Sep 1997 repetitive element that generates patterns has Positive Negative characteristics of a mobile genetic element (11). Previously positive 1 Eleven (50%) of 22 employees screened were Elephant handlers 4 6 skin-test positive, with no difference between Tiger handlers 4 4 tiger and elephant handlers. This is a higher rate Elephant handlers (converted) 2 Tiger handlers (converted) 1 of positives than documented in animal Total 12 10 handlers exposed to M. bovis-infected animals Tuberculin purified protein derivative. (3,4). Since the handlers had no accurate Vol. 4, No. 2, April–June 1998 Emerging Infectious Diseases 285 Dispatches 1 2 34 56 12 3 4 5 6 Figure 1. IS6110 restriction fragment length polymor- Figure 2. TBN12 restriction fragment length polymor- phism results. Lane1, elephant isolate (died August 6, phism results. Lane1, elephant isolate (died August 6, 1996); Lane 2, elephant isolate (died 1994); Lane 3, liv- 1996); Lane 2, elephant isolate (died 1994); Lane 3, liv- ing elephant trunk culture (October 1996); Lane 4, el- ing elephant trunk culture (October 1996); Lane 4, el- ephant lung tissue isolate (died August 3, 1996); Lane ephant lung tissue isolate (died August 3, 1996); Lane 5, elephant lymph node tissue isolate (died August 3, 5, elephant lymph node tissue isolate (died August 3, 1996); Lane 6, human sputum isolate (September 1996). 1996); Lane 6, human sputum isolate (September 1996). Provided by State of Michigan Community Public Provided by State of Michigan Community Public Health Agency. Health Agency. history of tuberculin skin testing, it was not smear- and culture-negative; the third had low possible to determine when conversions took numbers of acid-fast bacilli manifested by a place. The original source of infection for both negative sputum smear, thus posing a low elephants and humans is unknown. infectivity risk to others. In contrast, the three The possible mechanisms of transmission elephants that died had evidence of widespread include close contact while handling and training pulmonary disease and, therefore, represented elephants, cleaning the barn, participating in a greater risk for dissemination. elephant necropsies, and living in close proximity Three handlers converted from negative to to the elephant barn. positive during the course of the investigation; Human-to-human transmission of TB is their relevant exposure is unknown. The source unlikely because the only handler with active may have been one elephant found antemortem disease did not have cough. Of the three to be culture-positive for M. tuberculosis, sputum samples initially collected, two were although this animal did not return to the farm Emerging Infectious Diseases Vol. 4, No. 2, April–June 1998 286 Dispatches until November. Contact with this animal is Laboratories; and Janet Payeur, National Veterinary Services Laboratory, U.S. Department of Agriculture, MB Section. This unlikely for handlers whose PPD tests converted research was supported in part by the Centers for Disease in December and unknown for the two handlers Control and Prevention, National Tuberculosis Genotyping whose test results were positive in April (the and Surveillance Network cooperative agreement. latter two had not been retested since August). Kathleen Michalak is the Director of Nursing for TB is transmitted through close prolonged McHenry County Department of Health. She has worked contact with a person (or animal) with active TB. to improve the use of community resources, and The risk for TB transmission from an animal with improved service to client, providers, and the community a case of active TB is higher for daily handlers as a whole. than for persons with only brief contact, e.g., members of the public viewing a performance or References receiving elephant rides. In this outbreak, 1. Thoen CO. Tuberculosis (Revised 1995). Zoonosis screening of all persons who had (or thought updates. Journal of the American Veterinary Medical Association 1995;2:155-8. they had) contact with an elephant that died of 2. Thompson PJ, Cousins DV, Gow BL, Collins DM, M. tuberculosis identified three PPD-positive Willamson BH, Dagnia HT. Seals, seal trainers, and cases but no cases of active TB (8). Because the mycobacterial infection. American Review of real risk for transmission to the general public Respiratory Diseases 1993;147:164-7. was poorly understood, this case received 3. Dalovisio JR, Stetter M, Mikota-Wells S. Rhinoceros’ rhinorrhea: cause of an outbreak of infection due to considerable media attention as well as mention airborne Mycobacterium bovis in zookeepers. Clin in the medical literature (7,12). Infect Dis 1992;15:598-600. Veterinary practices should be initiated to 4. Fanning A, Edwards S. Mycobacterium bovis infection reduce the risks for exposure to animals infected in human beings in contact with elk (Cervus elaphus) in with M. tuberculosis. No data are available on TB Alberta, Canada. Lancet 1991;338:1253-5. 5. Saunders G. Pulmonary Mycobacterium tuberculosis incidence among domesticated elephants in the infection in a circus elephant. J Am Vet Med Assoc United States. An estimate can be derived from a 1983;183:1311-2. retrospective study of 379 zoo elephants of which 6. Pinto MRM, Jainudeen MR, Panabokke RG. eight (2.3%) had M. tuberculosis infection (10). Tuberculosis in a domesticated Asiatic Elaphas Reliable diagnosis and prevention of TB in all maximus. Vet Rec 1973;93:662-4. 7. Frankel D. Elephants pack their trunks and leave the domesticated and exhibited animals is ideal. circus. Lancet 1997;349:1675. Short of this, possible ways to prevent and 8. Greenberg AS, Jung RC, Gutter AK. Hazel Elephant is decrease zoonotic spread of any mycobacterial dead (of Tuberculosis). American Review of Respiratory infection (M. tuberculosis or M. bovis) include 1) Diseases 1981;124:341. regular skin testing of handlers or keepers; 2) a 9. Jones WD, Good RC. Hazel elephant redux. American Review of Respiratory Diseases 1982;125:270. high index of suspicion of TB in elephants with 10. Mikota S, Sargent EL, Ranglack GS. Medical unexplained weight loss, cough, or rhinorrhea; 3) management of the elephant. Tuberculosis and public health measures of contact tracing and Tuberculin Testing 1994;33-9. notification; and 4) active and effective treatment 11. Small P, Moss A. Molecular epidemiology and the new of infected personnel and animals (13). tuberculosis. Infect Agents Dis 1993;2:132-8. 12. Furley CW. Tuberculosis in elephants. Lancet 1997;350:224. Acknowledgments 13. Centers for Disease Control and Prevention. Guidelines We thank Stephen Dietrich and Laura Mosher, North for preventing the transmission of Mycobacterium Central Area TB-RFLP Laboratory, Michigan Department of tuberculosis in health-care facilities. MMWR Morb Public Health; George J. Dizikes, Chief of Molecular Mortal Wkly Rep 1994;43:63-4. Diagnostics, Illinois Department of Public Health, Division of Vol. 4, No. 2, April–June 1998 Emerging Infectious Diseases

Journal

Emerging Infectious Diseases – Pubmed Central

Published: Jun 1, 167

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