J. Microbiol. Infect. Dis., (2024), Vol. 14(4): 143–145

Letter to the Editor

10.5455/JMID.20241207081335

Avian botulism: An update

P. Shaik Syed Ali

Assistant Professor, School of Medicine, The Maldives National University, Maldives

*Corresponding Author: P. Shaik Syed Ali. School of Medicine, The Maldives National University, Maldives. Email: shaik.syed [at] mnu.edu.mv

Submitted: 07/12/2024 Accepted: 09/12/2024 Published: 31/12/2024

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ABSTRACT

Avian botulism is a neuromuscular disease that causes paralysis in both wild and captive bird populations. On a global scale, it is probably the most important disease of migratory birds. The disease is caused by botulinum, a neurotoxin produced by Clostridium botulinum.

Keywords: Avian, Birds, Botulism

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Dear Editor,

Avian botulism is a neuromuscular disease that causes paralysis in both wild and captive bird populations. On a global scale, it is probably the most important disease of migratory birds. The disease is caused by botulinum, a neurotoxin produced by Clostridium botulinum. There are seven types of botulinum toxins, A—H and X (Zhang et al. 2017). There are several subtypes of botulinum toxins such as A1—A8, B1—B8, mosaic C/D, F1—F8, and E1—E12 with no subtypes identified for the other toxinotype. Wild bird populations are most commonly affected by types C and E (Rocke et al. 2000). C.botulinum is ubiquitously found in water and terrestrial habitats, such as lakes, ponds, and marshes, respectively. The bacteria produce toxins under certainconditions, such as low oxygen content, high watertemperatures, and the availability of protein-rich substrates. Human activities might additionally contributeto the multiplication of bacteria through actions such asdraining wetlands, displacing pesticides, and removingagricultural pollutants that kill aquatic life, thus providing more protein substrate for toxins. This phenomenon stimulates toxin production because the bacteria are anaerobic, and some strains are proteolytic and favorablygrow at temperatures above 10^°C by proteolyzing theorganic substrates (Lynt et al. 1982).

Avian botulism has been recorded globally, with high prevalence in the marshlands of North America. Types C and E are the most common strains of avian botulism. Type C most commonly affects waterfowl, shorebirds, and gulls, and less commonly affects upland game birds, herons, raptors, and songbirds. Type E most commonly affects gulls and loons and less commonly affects waterfowl (Rocke and Friend 1999—2001). C. botulinum type E is found in aquatic habitats in the Canadian-American Great Lakes region, which includes the U.S. states of Illinois, Indiana, Michigan, Minnesota, New York, Ohio, Pennsylvania, and Wisconsin, as well as the Canadian province of Ontario (Leclair et al. 2013; Austin and Leclair 2011). C. botulinum types C and D are predominantly found in Australia and several European countries (Masters and Palmer 2021; Souillard et al. 2014). In the Pacific region, type C is predominantly found in Indonesia, whereas both types C and E are present in Japan (Suhadi et al. 1981; Yamakawa and Nakamura 1992; Maeda et al. 2023). In Asian countries, types C and D that cause animal intoxication are commonly found in Southern China (Gao et al. 1990). In India, type C is predominantly found in fish and aquatic environments in tropical regions (Lalitha and Gopakumar 2000). Recent outbreaks were recorded in India in 2019 and 2024. In 2019, over 18,000 migratory birds were found dead at Sambhar Lake in Rajasthan, and over 500 migratory birds have been found dead since October 26, 2024 (TOI 2024). However, the specific types of botulism associated with bird deaths due to avian botulism have not been investigated.

Horizontal transmission (i.e., bird-to-bird transmission) is not observed in avian botulism. Several hypotheses have been proposed regarding its transmission. One hypothesis suggests that in the wild, the disease is transmitted from dead fish and invertebrates to birds. Fish and invertebrates ingest the bacteria, and when environmental conditions — such as low oxygen levels and high temperatures — kill the fish and invertebrates, the bacteria multiply in their carcasses and produce the toxins. Birds consume these dead fish and invertebrates and die from the neuromuscular effects of the toxins. The toxins then undergo biomagnification in maggots feeding on dead birds. When these maggots are consumed by waterfowl, they contract the disease and die. This is referred to as the “carcass-maggot cycle” of avian botulism. Interestingly, some scavenger birds, such as vultures, exhibit resistance to this toxin, specifically type C (Zepeda Mendoza et al. 2018). Another hypothesis suggests that wild birds ingest bacteria from dead fish and invertebrates, and the bacteria later multiply in the cecum, producing the neurotoxin that causes clinical signs of avian botulism (Anza et al. 2016).

Botulinum toxin is synthesized as a single chain with a molecular weight of 150 kDa, which undergoes proteolytic cleavage to form light and heavy chains. The heavy chain facilitates light chain translocation across the endosomal membrane. The light chain then acts on the soluble N-ethylmaleimide-sensitive factor attachment proteins (SNARE) in vesicles containing acetylcholine, preventing its release and causing neuromuscular paralysis, specifically flaccid paralysis. A typical sign of an avian botulism outbreak is the presence of dozens or even hundreds of freshwater bird carcasses. Sick birds exhibit signs of progressive weakness and ascending flaccid paralysis of the skeletal muscles, affecting the legs, wings, and neck. An additional important sign is the closure of the eyes due to paralysis of the nictitating membrane (Circella et al. 2019; Anniballi et al. 2013). This results in the bird’s inability to fly, clumsy walking, and difficulty landing. In the advanced stages of the disease, neck paralysis occurs, leading to death due to drowning or cardiorespiratory failure. Among all the clinical manifestations, paralysis of the neck and nictitating membrane are the distinguishing signs of avian botulism (Le Gratiet 2020).

The most widely used tests to diagnose avian botulism are the mouse protection test and enzyme-linked immunosorbent assay (ELISA). The in vitro ELISA test specifically detects type C toxins. A presumptive diagnosis is made by observing the characteristic signs of avian botulism, such as neck and nictitating membrane paralysis, in sick birds. Additionally, the absence of lesions in the internal organs of dead birds should be noted for differential diagnosis. Confirmatory diagnosis is achieved through mouse protection tests or ELISA (Rocke and Friend 1999—2001). However, it is best to confirm the presence of type C toxins using ELISA. If the results are negative, then a mouse protection test can be performed by challenging the bird with toxins after previous prophylaxis with antitoxin. Compared with the in vivo mouse protection test, in vitro ELISA is easier to perform in the field. However, ELISA tests to detect other types of toxins other than type C must be developed.

Rehabilitation efforts have a 90% success rate in waterfowl, compared to birds such as coots, shorebirds, gulls, and grebes, which often die despite treatment. Sick birds are treated by providing water, food, shade, and injection of antitoxin (Rocke and Friend 1999—2001; Anza et al. 2016). The prevention of avian botulism is challenging because the spores of C. bot ulinum are ubiquitous in nature. However, avian botulism can be transmitted by taking measures such as removing carcasses to prevent maggot infestation and disrupt the carcass-maggot cycle. In addition, constant monitoring of wetlands, especially in areas with recurring outbreaks (e.g., “hot spots”), is necessary. Furthermore, fertilizer and pollutant disposal should be avoided. The prevention and control of avian botulism are critical for the protection of endangered migratory birds from extinction.

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SOURCES OF SUPPORT AND FUNDING

None.

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PATIENT CONSENT FORM

This is not applicable.

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ETHICAL APPROVAL AND/OR INSTITUTIONAL REVIEW BOARD (IRB) APPROVAL

Not required.

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CONFLICT OF INTEREST

The author declares no conflicts of interest.

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ACKNOWLEDGMENTS

None.

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REFERENCES

Anniballi, F., Fiore, A., Löfström,, C., Skarin, H., Auricchio, B., Woudstra, C., Bano, L., Segerman, B., Koene, M., Båverud, V., Hansen, T., Fach. P., Tevell Aberg, A., Hedeland, M., Olsson Engvall, E. and De Medici, D. 2013. Management of animal botulism outbreaks: from clinical suspicion to practical countermeasures to prevent or minimize outbreaks. Biosecur. Bioterror. 11, S191–199. https://doi.org/10.1089/bsp.2012.0089

Anza, I., Vidal, D., Feliu, J., Crespo, E. and Mateo, R. 2016. Differences in the vulnerability of waterbird species to botulism outbreaks in Mediterranean wetlands: an assessment of ecological and physiological factors. Appl. Environ. Microbiol. 82(10), 3092–3099. https://doi.org/10.1128/AEM.00119-16

Austin, J.W. and Leclair, D. 2011. Botulism in the North: A disease without borders. Clin. Infect Dis. 52(5), 593–594. https://doi.org/10.1093/cid/ciq256

Circella, E., Camarda, A., Bano, L., Marzano, G., Lombardi, R., D’Onghia, F. and Greco, G. 2019. Botulism in wild birds and changes in environmental habitat: a relationship to be considered. Animals. 9(12), 1034. https://doi.org/10.3390/ani9121034

Gao, Q.Y., Huang, Y.F., Wu, J.G., Liu, H.D. and Xia, H.Q. 1990. A review of botulism in China. Biomed. Env. Sci. 3(3), 326–336.

Lalitha, K. and Gopakumar, K. 2000. Distribution and ecology of Clostridium botulinum in fish and aquatic environments of a tropical region. Food Microbiol. 17(5), 535–541. https://doi.org/10.1006/fmic.2000.0346

Le Gratiet, T., Poezevara, T., Rouxel, S., Houard, E., Mazuet, C., Chemaly, M. and Maréchal, C.L. 2020. Development of an innovative and quick method for the isolation of clostridium botulinum strains involved in avian botulism outbreaks. Toxins (Basel). 12(1), 42. https://doi.org/10.3390/toxins12010042

Leclair, D., Farber, J.M., Doidge, B., Blanchfield, B., Suppa, S., Pagotto, F. and Austin, J.W. 2013. Distribution of Clostridium botulinum type E strains in Nunavik, Northern Quebec, Canada. Appl. Environ. Microbiol. 79(2), 646–654. https://doi.org/10.1128/AEM.05999-11

Lynt, R.K., Kautter, D.A. and Solomon, H.M. 1982. Differences and similarities among proteolytic and nonproteolytic strains of Clostridium bot ulinum types A, B, E and F: a review. J. Food Prot. 45(5), 466–474. https://doi.org/10.4315/0362-028X-45.5.466

Maeda, R., Mori, M., Harada, S., Izu, I., Hirano, T., Inoue, Y., Yahiro, S. and Koyama, H. 2023. Emergence of novel type C botulism strain in household outbreak, Japan. Emerg Infect Dis. 29(10), 2175–2177. https://doi.org/10.3201/eid2910.230433

Masters, A.M. and Palmer, D.G. 2021. Confirmation of botulism diagnosis in Australian bird samples by ELISA and RT rtPCR. J. Vet. Diagn. Invest. 33(4), 684–694. https://doi.org/10.1177/10406387211014486

Rocke, T. and Friend, M. 1999–2001. Avian botulism. In: Field Manual Of Wildlife Diseases: General Field Procedures and Diseases of Birds, U.S. Geological Survey. 271–281.

Rocke, T.E., Samuel, M.D., Swift, P.K. and Yarris, G.S. 2000. Efficacy of a type C botulism vaccine in green-winged teal. J. Wildl. Dis. 36(3), 489–493. https://doi.org/10.7589/0090-3558-36.3.489

Souillard, R., Woudstra, C., Le Maréchal, C., Dia, M., Bayon-Auboyer, M.H., Chemaly, M., Fach, P. and Le, Bouquin, S. 2014. Investigation of Clos tridium botulinum in commercial poultry farms in France between 2011 and 2013. Avian Pathol. 43(5), 458–464. https://doi.org/10.1080/03079457.2014.957644

Suhadi, F., Thayib, S.S. and Sumarsono, N. 1981. Distribution of Clostridium botulinum around fishing areas of the western part of Indonesian waters. Appl. Environ. Microbiol. 41(6), 1468–1471. https://doi.org/10.1128/aem.41.6.1468-1471.1981

TOI. 2024. What is Avian Botulism, that has killed over 500 migratory birds at Rajasthan’s Sambhar Lake? Available via https://timesofindia.indiatimes.com/india/what-is-avian-botulism-that-has-killed-over-500-migratory-birds-at-rajasthans-sambhar-lake/articleshow/115104126.cms (Accessed 12 November 2024).

Yamakawa, K. and Nakamura, S. 1992. Prevalence of Clostridium botulinum type E and coexistence of C. botulinum nonproteolytic type B in the river soil of Japan. Microbiol. Immunol. 36(6), 583–591. https://doi.org/10.1111/j.1348-0421.1992.tb02058.x

Zepeda Mendoza, M.L., Roggenbuck, M., Manzano Vargas, K., Hansen, L.H., Brunak, S., Gilbert, M.T.P. and Sicheritz-Pontén, T. 2018. Protective role of the vulture facial skin and gut microbiomes aid adaptation to scavenging. Acta Vet. Scand. 60, 61. https://doi.org/10.1186/s13028-018-0415-3

Zhang, S., Masuyer, G., Zhang, J., Shen, Y., Lundin, D., Henriksson L., Miyashita, S.I., Martínez-Carranza, M., Dong, M. and Stenmark, P. 2017. Identification and characterization of a novel botulinum neurotoxin. Nat Commun. 8, 14130. https://doi.org/10.1038/ncomms14130