Presence of Mycobacterium sp in the feces of captive wild birds in three municipalities of the State of Jalisco

De La Cruz Baltazar, Eliab

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Journal of the Selva Andina Animal Science

versión impresa ISSN 2311-3766versión On-line ISSN 2311-2581

J.Selva Andina Anim. Sci. v.8 n.1 La Paz 2021

https://doi.org/10.36610/j.jsaas.2021.080100022x

Short Communication

Presence of Mycobacterium sp in the feces of captive wild birds in three municipalities of the State of Jalisco

Presencia de Mycobacterium sp en las heces de aves silvestres cautivas en tres municipios del Estado de Jalisco

De La Cruz Baltazar Eliab^*

Rancho Bonito Zoo. Jalisco Mexico. Old road to Tonalá.

*Contact address: Rancho Bonito Zoo. Jalisco Mexico. Old road to Tonalá.

Eliab De La Cruz Baltazar
E-mail address: aiser_76@yahoo.com.mx

Record from the article
Received September 2020.
Returned November 2020.
Accepted January 2021.
Available online, April 2021

ID of article: 082/JSAAS/2020

J. Selva Andina Anim. Sci. 2021; 8(1):22-29.

Abstract

To determine the presence of Mycobacterium sp in captive wild birds in the state of Jalisco, Mexico, an experimental study was carried out in private hatcheries of three municipalities in the state of Jalisco, covering Guadalajara, Tesistan, and Tonala to identify the presence of alcohol-acid resistant bacilli (ABB) in stool samples stained with the use of the Ziehl-Neelsen stain, stool samples were taken from 76 birds under captive conditions. Of the 33 birds analyzed in the municipality of Guadalajara, 4 tested positive for Mycobacterium sp., Giving 0.12 % positivism in this municipality, while, in Tesistan, of 21 birds analyzed, only one specimen tested positive for Mycobacterium sp., Giving 0.4 % positivism. In the municipality of Tonala, a positive specimen was found out of 22 birds analyzed, giving 0.45 % of bird’s positive for Mycobacterium sp. Of the 76 birds analyzed, 0.7 % were positive for Mycobacterium sp. Species such as Eupsittula canicularis, Amazona autumnalis, Ara militaris, Alopochen aegyptica, and Pavo cristatus tested positive for Mycobacterium sp. This work contributes to documenting the cases of Mycobacterium sp., In captive wild birds to take measures that guarantee the health of wild birds.

Keywords: Ziehl-Neelsen, zoonosis, resistant alcohol-acid bacilli, Mycobacterium sp.

Resumen

Con el objetivo de determinar la presencia de Mycobacterium sp en aves silvestres cautivas del estado de Jalisco, México se realizó un estudio de tipo experimental en criaderos particulares de tres municipios del estado de Jalisco, abarcando Guadalajara, Tesistán y Tonalá con el fin de identificar la presencia de bacilos alcohol-acido resistentes (BAAR) en muestras de heces teñidas con el uso de la tinción Ziehl-Neelsen, se tomaron muestras de excremento de 76 aves en condiciones de cautiverio. De las 33 aves analizadas en el municipio de Guadalajara, 4 dieron positivo a Mycobacterium sp., dando un 0.12 % de positivismo en este municipio, mientras que, en Tesistán, de 21 aves analizadas solo un ejemplar dio positivo a Mycobacterium sp., dando un 0.4 % de positivismo. En el municipio de Tonalá de 22 aves analizadas se encontró un ejemplar positivo, dando 0.45 % de aves positivas a Mycobacterium sp. De las 76 aves analizadas el 0.7 % dio positivo a Mycobacterium sp. Especies como Eupsittula canicularis, Amazona autumnalis, Ara militaris, Alopochen aegyptica y Pavo cristatus dieron positivo a Mycobacterium sp. Este trabajo contribuye a documentar los casos de Mycobacterium sp., en aves silvestres cautivas para tomar medidas que garanticen la salud de las aves silvestres.

Palabras clave: Ziehl-Neelsen, zoonosis, bacilos alcohol-acido resistentes, Mycobacterium sp.

Introduction

Many species of birds have been the cause of Mycobacterium avium disease¹, according to Bernarde-lli et al.² M. avium is common where there are a large number of birds, such as zoological institutions, since the presence of an infected bird in captivity, such as a zoo exhibitor, can increase the number of mycobacteria in that environment³, according to Chiodini et al.⁴, the incidence is high in intensively reared birds and can be commonly detected in animal feces. infected⁵, the source of infection is unknown and variable, such as bird remains, which depends on the species, and whether the birds are in captivity or free⁶, in bird necropsies it ranges from 0.5 % to 14 %^7-9, including parrots¹⁰, to confirm the presence of M. avium¹¹, the Ziehl-Neelsen (ZN) stain allows the observation of alcohol-acid resistant bacilli (ABB), according to VanDerHeyden⁹, mycobacterial infections detected at autopsy of pet birds, M. avium is considered the most important pathogen a cause of tuberculosis in domestic birds¹², the diagnosis of M. avium is based on the demonstration of ABB by microscopy¹³, as M. avium has a thick cell wall, rich in mycolic acids, mycosides, glycolipids, and sulpholipids. makes it hydrophobic and impervious to aqueous stains without heat, so heat must be applied in ZN staining¹⁴.

One of the potential sources of contamination of M. avium is fecal matter¹⁵. M. avium is a Gram-positive ABB¹⁶, as ZN staining is a quick, easy, and low-cost technique¹⁷, it allows us to differentiate bacteria into two groups: those that resist discoloration with alcohol-acid and those that are not¹⁸, to Selvakumar et al.¹⁹, the sensitivity of this stain to identify ABB is 74 % and a specificity of 98 %. In humans, M. avium is capable of first producing lymphadenitis, lung disease, and the spread of the infection, particularly in immunosuppressed individuals or under transplant therapy²⁰. According to Aranaz et al.²¹, the stress experienced by birds in captivity triggers the incidence of M. avium, it is also considered by Kriz et al.²² as a potential zoonotic risk due to contact with infected animals.

With insufficient data on the pathogenic potential of Mycobacterium sp., in captive animals and given that the information regarding Mycobacterium sp., infection in birds is relatively limited and incomplete, due to a lack of information on the apparently long incubation, an inadequate identification test, and the difficulty of discovering infected birds²³It is intended that this study be focused on providing information about the presence of Mycobacterium sp in wild birds under captive conditions in the state of Jalisco and the use of tools for its diagnosis as an efficient and economical method for the diagnosis of this zoonotic disease²⁴.

Materials and methods

Study Design. From June to December 2019, an experimental study²⁵ was carried out, based on the samples of feces from captive birds from hatcheries belonging to individuals, which are dedicated to the reproduction, maintenance, and commercialization of birds. with the permits of SEMARNAT (Secretary of the Environment and Natural Resources) for its operation.

Study zone. The study was carried out in the state of Jalisco, covering the municipalities of Guadalajara, Tesistan, and Tonala, located in the center of the country and located within the metropolitan area of Guadalajara.

Collection and transfer of samples. 33 birds from Guadalajara, 21 from Tesistan and 22 from Tonala, their excreta were evaluated. The presence of mycobacteria in the faeces²⁶, for this reason, the excrement samples were taken from the soil, which was previously cleaned and disinfected, it was preferred to make the collections in the morning after feeding, we waited for the birds to defecate and with a sterile swab was stored in a test tube, for transfer to the laboratory, following the Biosafety recommendations Jorge et al.²⁷, later they were stored in thermal coolers with cooling gel inside and kept at a temperature of 4 °C until processed, as this technique is easy to perform, it was preferred to carry out each test in each hatchery, that is, the staining equipment and the microscope were taken to each place in order to reduce the transfer times of the samples. After being collected, they were processed within 20 min.

Identification of Alcohol Acid Resistant Bacilli (ABB). Smears were made of the feces that were previously collected and stained with it with the indicated staining, which is made up of a set of reagents and the ZN reagent ²⁸^,29, it was observed under a microscope with 100X magnification in oil immersion, following the recommended technique³⁰^,31. The description of the bacilli was followed according to Bartos et al.³², following the WHO recommendations³³.

Results

Table 1 indicates that of the 21 birds analyzed, only one Egyptian goose (A. aegyptica) tested positive for Mycobacterium sp, which represents 0.4 % positivism.

Table 1 Bird species with the presence of Mycobacterium sp in their fecal material, municipality of Tesistan, in 2019

Table 2 0.12 % of the stool samples were positive for Mycobacterium sp.

Table 2 Bird species with the presence of Mycobacterium sp in their fecal material, municipality of Guadalajara, in 2019

Table 3 shows 0.45 % of birds positive for Mycobacterium sp, specimens of S. camelus were negative.

Table 3 Bird species with the presence of Mycobacterium sp in their fecal material, municipality of Tonala, in 2019

Discussion

Several types of Mycobacterium sp., the disease occurs in vertebrates, both in mammals, birds, reptiles, amphibians, and fish, it is considered that they contribute to its global distribution since there are few studies published so far³⁴. Mycobacterium sp., the infection has been reported in parrots³⁵, raptors³⁶, pigeons, and ducks³⁷.

To prevent wild animals in captivity from becoming sources of infection for humans and other species, it is necessary to carry out routine diagnostic tests, supplemented with management measures to detect and eliminate sick animals, thus avoiding the disease spread³⁸.

In aquatic species, Cromie et al.³⁹ observed a 70 % reduction in mortality. In the municipality of Guadalajara, 0.12 % of the stool samples were positive for Mycobacterium sp., while in the municipality of Guadalajara, out of 33 birds sampled, 4 were positive for Mycobacterium sp., and in the municipality of Tesistan de in the 21 birds analyzed, only one specimen of Al. aegyptiacus tested positive for Mycobacterium sp., giving 0.4 % positivism. In the municipality of Tonala, out of 22 birds analyzed, 0.45 % of birds were positive for Mycobacterium sp., one of them being S. camelus itself, which has been reported in this species by García et al.⁴⁰.

Species such as E. canicularis, A. autumnalis, A. militaris, A. aegyptica and P. cristatus were positive for Mycobacterium sp., coinciding with what was reported by Fowler⁴¹.

A 0.7 % positivism is reported to Mycobacterium sp of the 76 birds analyzed.

Finally, mycobacteria have inhabited our environment and even more so in animals in captivity, apparently, with the data provided in this research work, it seems that the mere fact of a rapid diagnosis would be the first initiative that allows us to give foot to collect data of its incidence.

But I must also emphasize that a ZN stain is not an accurate diagnosis of M. avium identification, but it would allow us to control the spread of the disease and why not say it, it could even be an initiative that avoids infection to human.

The data are alarming since the sample collection sites are animals that are exposed or commercialized and if there is an infection we could with this technique and in the measure that it is carried out with relative frequency we would help to avoid the spread of this pathogen.

Funding source

The work presented was funded by the Rancho Bonito Zoo with the contribution of reagents and dyes, as well as the required laboratory equipment, a non-profit project.

Conflicts of interest

There were no conflicts of interest between the author and the institution to develop the work interventions.

Acknowledgments

The author thanks the owners of the hatcheries in the three municipalities for the facility granted for the collection of samples for their support of this research project.

Ethical considerations

During the work carried out, each captive wild bird was treated with dignity and respect, and in each enclosure where the samples were collected, it was avoided to alter their environment.

Cited Literature

1. Tell LA, Woods L, Cromie RL. Mycobacteriosis in birds. Rev Sci Tech 2001;20(1):180-203. DOI: https://doi.org/10.20506/rst.20.1.1273

2. Bernardelli A, Nader AJ, Loureiro J, Michelis H, Debenedetti R. Mycobacteriosis in sea mammals and birds. Rev Sci Tech 1990;9(4):1121-9. DOI: https://doi.org/10.20506/rst.9.4.530

3. Dvorska LL, Matlova L, Ayele WY, Fischer OA, Amemori T, Weston RT, et al. Avian tuberculosis in naturally infected captive water birds of Ardeideae and Threskiornithidae families studied by serotyping, IS901 RFLP typing and virulence for poultry. Vet Microbiol 2007;119(2-4):366-74. DOI: https://doi.org/10.1016/j.vetmic.2006.09.010

4. Chiodini RJ, Van Kruiningen HJ, Merkal RS. Ruminant paratuberculosis (Johne´s disease): the current staus and future prospects. Cornell Vet 1984;74(3):218-62.

5. Ayele WY, Svastova P, Roubal P, Bartos M, Pavlik I. Mycobacterium avium, subspecies paratuberculosis cultured from locally and commercially pasteurized cow´s milk in the Czech Republic. Appl Environ Microbiol 2005;71(3):1210-4. DOI: https://doi.org/10.1128/AEM.71.3.12101214.2005

6. Gerhold RW, Fischer JR. Avian tuberculosis in a wild turkey. Avian Dis 2005;49(1):164-6. DOI: https://doi.org/10.1637/7245-072204R

7. Keymer IF, Jones DM, Pugsley SL, Wadsworth PF. A survey of tuberculosis in birds in the regent's park gardens of the zoological society of London. Avian Pathol 1982;11:563-9. DOI: https://doi.org/10.1080/03079458208436131

8. Montali RJ, Bush M, Thoen CO, Smith E. Tuberculosis in captive exotic birds. J Am Vet Med Assoc 1976;169(9):920-7.

9. VanDerHeyden N. Clinical manifestations of mycobacteriosis in pet birds. Semin Avian Exot Pet 1997;6(1):18-24. DOI: https://doi.org/10.1016/ S1055-937X(97)80037-0

10. Ackerman LJ, Benbrook SC, Walton BC. Mycobacterium tuberculosis infection in a parrot (Amazona farinosa). Am Rev Respir Dis. 1974;109(3): 388-90. DOI: https://doi.org/10.1164/arrd.1974.109.3.388

11. De Kantor IN, Kim SJ, Frieden T, Laszlo A, Luelmo F, Norval PY, et al. Laboratory services in tuberculosis control. Microscopy. Part II [Internet]. Geneva: World Health Organization; 1998 [citado 22 de octubre de 2019]. 34 p. Recuperado a partir de: https://apps.who.int/iris/bitstream/handle/10665/65942/WHO_TB_98.258_%28part2%29.pdf?sequence=2&isAllowed=y

12. VanDerHeyden N. Clinical manifestations of mycobacteriosis in pet birds. Semin Avian Exot Pet 1997;6(1):18-24. DOI: https://doi.org/10.1016/S1055-937X(97)80037-0

13. Saito H, Tomioka H, Sato K, Tasaka H, Dawson DJ. Identification of various serovar strains of Mycobacterium avium complex by using DNA probes specific for Mycobacterium avium and Mycobacterium intracellulare. J Clin Microbiol 1990;28(8):1694-7. DOI: https://doi.org/10.1128/JCM.28.8.1694-1697

14. Carter G, Wise D. Mycobacterium. In: Carter G, Wise D, editors. Essentials of Veterinary Bacteriology and Mycology. New York: John Wiley & Sons, Inc.; 2003, p. 103-10.

15. Daniels MJ, Hutchings MR, Beard PM, Henderson D, Greig A, Stevenson K, et al. Do non-ruminant wildlife pose a risk of paratuberculosis to domestic livestock and vice versa in Scotland? J Wildl Dis 2003;39(1):10-5. DOI: https://doi.org/10.7589/0090-3558-39.1.10

16. Harris NB, Barletta RG. Mycobacterium avium subsp paratuberculosis in Veterinary Medicine. Clin Microbiol Rev 2001;14(3):489-512. DOI: https://doi.org/10.1128/CMR.14.3.489-512.2001

17. Selvakumar N, Rahman F, Rajasekaran S, Narayanan PR, Frieden TR. Inefficiency of 0.3 % carbol fuchsin in ziehl-neelsen staining for detecting acid-fast bacilli. J Clin Microbiol 2002;40(8): 3041-3. DOI: https://doi.org/10.1128/jcm.40.8.3041-3043.2002

18. Prescott LM, Harley JP, Klein DA. Microbiology. 5^th ed. Utah: McGraw-Hill; 2002.

19. Selvakumar N, Sekar MG, Rahman F, Syamsunder A, Duraipandian M, Wares F, et al. Comparison of variants of carbol-fuchsin solution in Ziehl-Neelsen for detection of acid-fast bacilli. Int J Tuberc Lung Dis 2005;9(2):226-9.

20. Hoop RK. Public health implications of exotic pet avian mycobacteriosis. Semin Avian Exot Pet 1997;6(1):3-8. DOI: https://doi.org/10.1016/S10 55-937X(97)80035-7

21. Aranaz A, Liébana E, Mateos A, Domínguez L. Laboratory diagnosis ofavianmycobacteriosis. Semin Avian Exot Pet 1997;6(1):9-17. DOI: https://doi.org/10.1016/S1055-937X(97)80036-9

22. Kríz P, Slaný M, Shitaye JE, Pavlík I. Aviárnímyobakteriózy u lidí-stálehrozícínebezpe-cí v Ceskérepublice [Avian mycobacteriosis in humans remains a threat in the Czech Republic]. KlinMikrobiolInfekc Lek 2010;16(1):10-7.

23. de Lisle GW, Bengis RG, Schmitt SM, O'Brien DJ. Tuberculosis in free-ranging wildlife: detection, diagnosis and management. Rev Sci Tech 2002;21(2):317-34. DOI: https://doi.org/10.20506/rst.21.2.1339

24. Cooley G, Etheridge RD, Boehlke C, Bundy B, Weatherly DB, Minning T, et al. High throughput selection of effective serodiagnostics for Trypanosoma cruzi infection. PLoSNegl Trop Dis 2008; 2(10):e316. DOI: https://doi.org/10.1371/jounal.pntd.0000316

25. León G. Diseños de estudios en epidemiologia. 3ª ed. España: Mosby; 2005

26. Smith SL, West DM, Wilson PR, de Lisle GW, Collett MG, Heuer C, et al. The prevalence of disseminated Mycobacterium avium subsp. paratuberculosis infection in tissues of healthy ewes from a New Zealand farm with Johne's disease present. N Z Vet J 2013;61(1):41-4. DOI: https://doi.org/10.1080/00480169.2012.704627

27. Jorge M, Alito A, Bernardelli A, Canal A, Cataldi A, Cicuta M, et al. Manual de diagnóstico de micobacterias de importancia en medicina veterinaria. Buenos Aires: Comisión Científica de Micobacterias, Asociación Argentina de Veterinarios de Laboratorio de Diagnóstico; 2005. p. 1-132.

28. Kusznierz GF, Latini OA, Sequeira MD. Quality assessment of smears microscopy for acid-fast bacilli in the Argentine tuberculosis laboratory network, 1983-2001. Int J Tuberc Lung Dis 2004;8(10):1234-41.

29. Rohit S, Neeta S, Mukerjee S, Sharma PP. RNTCP: Quality control of sputum microscopy at sub-district level. Ind J Tub 2002; 49:143-6.

30. Singh SV, Singh PK, Singh AV, Gupa S, Chaubey KK, Singh B, et al. Bio-burden and Bio-type profiles of Mycobacterium avium subspecies paratuberculosis infection in suspected population of domestic livestock in India. Int J Curr Res 2013;5(7):1897-901.

31. Bernardelli A. Manual de procedimiento técnico: Diagnostico de paratuberculosis [Internet]. México: Servicio Nacional de Sanidad y Calidad Agroalimentaria; 2000 [citado 22-de octubre de 2019]. 47 p. Recuperado a partir de:https://www.aavld.org.ar/publicaciones/paratub.pdf

32. Bartos M, Hlozek P, Svastova P, Dvorska L, Bull T, Matlova L, et al. Identification of members of Mycobacterium avium species by Accu-Probes, serotyping, and single IS900, IS901, IS1245 and IS901-flanking region PCR with internal standards. J Microbiol Methods 2006;64(3):333-45. DOI: https://doi.org/10.1016/j.mimet.2005.05.009

33. Organización Mundial de la Salud. Los servicios de laboratorioen el control de la tuberculosis. MicroscopíaII. Ginebra: WHO/TB/98.258;1998.

34. Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 2004;40(4):639-59. DOI: https://doi.org/10.7589/0090-3558-40.4.639

35. Bougiouklis P, Brellou G, Fragkiadaki E, Iordanidis P, Vlemmas I, Georgopoulou I. Outbreak of avian mycobacteriosis in a flock of two-year-old domestic pigeons (Columba livia f. domestica). Avian Dis 2005;49(3):442-5. DOI: http://doi.org/10.1637/7325-011005R.1

36. Silveira L, Fowler M. Order Anseriformes (Ducks, Geese, Swans): Diseases: Infectious Diseases: Bacterial Diseases. In: Fowler M, Cubas Z. Biology, Medicine, and Surgery of South American Wild Animals. Iowa: Iowa State University Press; 2001. p. 191. DOI: http://doi.org/10.1002/9780470376980.ch11

37. Pocknell AM, Miller BJ, Neufeld JL, Grahn BH. Conjunctival Mycobacteriosis in two emus (Dromaius novaehollandiae). Vet Pathol 1996;33(3):346-8. DOI: https://doi.org/10.1177/030098589603300314

38. Fowler M. Miscellaneous Avian Infectious Diseases: Mycobacteriosis. In: Fowler M. Zoo and Wild Animal Medicine. 2nd ed. Philadelphia: W.B. Saunders Company; 1986. p. 230.

39. Cromie R, Ash NJ, Brown MJ, Stanford J. Avian immune responses to Mycobacterium avium: the wildfowl example. Dev Comp Immunol 2000; 24(2-3):169-85. DOI: https://doi.org/10.1016/s0145-305x(99)00071-3

40. García A, LeClear CT, Gaskin JM. Mycobacterium avium infection in an ostrich (Struthio camelus). J Zoo WildlMed 2001;32(1):96-100. DOI: https://doi.org/10.1638/1042-7260(2001)032[0096:MAIIAO]2.0.CO;2

41. Fowler M. Zoo and wild animal medicine. 2^nd ed. Philadelphia: W.B. Saunders Company. 1986; 17, 65, 351. p.

______________

Editor's Note:

Journal of he Selva Andina Animal Science (JSAAS) remains neutral with respet to jurisdictional claims published on maps and institutional affiliations.

1. Tell LA, Woods L, Cromie RL. Mycobacteriosis in birds. Rev Sci Tech 2001;20(1):180-203. DOI: https://doi.org/10.20506/rst.20.1.1273 [ Links ]

2. Bernardelli A, Nader AJ, Loureiro J, Michelis H, Debenedetti R. Mycobacteriosis in sea mammals and birds. Rev Sci Tech 1990;9(4):1121-9. DOI: https://doi.org/10.20506/rst.9.4.530 [ Links ]

4. Chiodini RJ, Van Kruiningen HJ, Merkal RS. Ruminant paratuberculosis (Johne´s disease): the current staus and future prospects. Cornell Vet 1984;74(3):218-62. [ Links ]

6. Gerhold RW, Fischer JR. Avian tuberculosis in a wild turkey. Avian Dis 2005;49(1):164-6. DOI: https://doi.org/10.1637/7245-072204R [ Links ]

8. Montali RJ, Bush M, Thoen CO, Smith E. Tuberculosis in captive exotic birds. J Am Vet Med Assoc 1976;169(9):920-7. [ Links ]

9. Van Der Heyden N. Clinical manifestations of mycobacteriosis in pet birds. Semin Avian Exot Pet 1997;6(1):18-24. DOI: https://doi.org/10.1016/ S1055-937X(97)80037-0 [ Links ]

11. De Kantor IN, Kim SJ, Frieden T, Laszlo A, Luelmo F, Norval PY, et al. Laboratory services in tuberculosis control. Microscopy. Part II [Internet]. Geneva: World Health Organization; 1998 [citado 22-de octubre de 2019]. 34 p. Recuperado a partir de: https://apps.who.int/iris/bitstream/handle/10665/65942/WHO_TB_98.258_%28part2%29.pdf?sequence=2&isAllowed=y

12. VanDerHeyden N. Clinical manifestations of mycobacteriosis in pet birds. Semin Avian Exot Pet 1997;6(1):18-24. DOI: https://doi.org/10.1016/S1055-937X(97)80037-0

14. Carter G, Wise D. Mycobacterium. In: Carter G, Wise D, editors. Essentials of Veterinary Bacteriology and Mycology. New York: John Wiley & Sons, Inc.; 2003, p. 103-10.

16. Harris NB, Barletta RG. Mycobacterium avium subsp paratuberculosis in Veterinary Medicine. Clin Microbiol Rev 2001;14(3):489-512. DOI: https://doi.org/10.1128/CMR.14.3.489-512.2001 [ Links ]

18. Prescott LM, Harley JP, Klein DA. Microbiology. 5^th ed. Utah: McGraw-Hill; 2002. [ Links ]

20. Hoop RK. Public health implications of exotic pet avian mycobacteriosis. Semin Avian Exot Pet 1997;6(1):3-8. DOI: https://doi.org/10.1016/S10 55-937X(97)80035-7 [ Links ]

21. Aranaz A, Liébana E, Mateos A, Domínguez L. Laboratory diagnosis ofavianmycobacteriosis. Semin Avian Exot Pet 1997;6(1):9-17. DOI: https://doi.org/10.1016/S1055-937X(97)80036-9 [ Links ]

25. León G. Diseños de estudios en epidemiologia. 3ª ed. España: Mosby; 2005 [ Links ]

29. Rohit S, Neeta S, Mukerjee S, Sharma PP. RNTCP: Quality control of sputum microscopy at sub-district level. Ind J Tub 2002; 49:143-6. [ Links ]

33. Organización Mundial de la Salud. Los servicios de laboratorioen el control de la tuberculosis. MicroscopíaII. Ginebra: WHO/TB/98.258;1998.

34. Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 2004;40(4):639-59. DOI: https://doi.org/10.7589/0090-3558-40.4.639 [ Links ]

37. Pocknell AM, Miller BJ, Neufeld JL, Grahn BH. Conjunctival Mycobacteriosis in two emus (Dromaius novaehollandiae). Vet Pathol 1996;33(3):346-8. DOI: https://doi.org/10.1177/030098589603300314 [ Links ]

38. Fowler M. Miscellaneous Avian Infectious Diseases: Mycobacteriosis. In: Fowler M. Zoo and Wild Animal Medicine. 2nd ed. Philadelphia: W.B. Saunders Company; 1986. p. 230. [ Links ]

41. Fowler M. Zoo and wild animal medicine. 2^nd ed. Philadelphia: W.B. Saunders Company. 1986; 17, 65, 351. p. [ Links ]