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Mycobacterium bovis Pulmonary Tuberculosis after Ritual Sheep Sacrifice in Tunisia.

Mycobacterium bovis is historically responsible for zoonotic, deadly tuberculosis and has seemingly reemerged in countries where it had previously vanished following eradication programs in cattle and the pasteurization of dairy products (1-3). In most cases, M. bovis tuberculosis results from consuming unpasteurized milk; extrapulmonary disease is thus the most frequent clinical manifestation (4-6). Also, M. bovis could be an airborne zoonotic pathogen causing pulmonary tuberculosis (7). In western Europe countries, most of M. bovis human tuberculosis cases are seen in migrants and are associated with travel to the country of origin (4,5,8,9). M. bovis tuberculosis is traced to animal sources, yet reporting of clinical signs and symptoms is often delayed (3). The observation of a woman affected by M. bovis tuberculosis who participated in a precisely dated religious practice involving sheep slaughtering provided an opportunity to shed light on these medical aspects.

A 43-year-old unemployed woman born in Tunisia emigrated to France in 2000, married, and had 2 children. The patient had no underlying chronic condition, no medical history, no treatment, no history of smoking, and no toxic habits. She had received the bacillus Calmette-Guerin vaccine during childhood. Her last trip to Tunis and surrounding areas was during July 10-August 28, 2018. The patient denied any contacts with ill persons during her stay. She participated in the Aid-el-Kebir (the Great Festival) Muslim festivities on August 22-23, 2018. After the ritual, her husband slaughtered a veterinary-uncontrolled sheep outside the house by cutting through its neck in an open place and then insufflating air beneath the skin of the dead animal using bellows before butchering the viscera, including lungs, heart, liver, and kidneys, which were put into a container while the digestive tract was put separately into another container. His wife then washed the lungs and the other viscera for [approximately equal to] 2 hours in a confined kitchen, cooked them, and consumed them with her family; she did not experience any injury while butchering the animal.

After her return to France, the patient was apyretic with productive cough, fatigue, and anorexia, which started exactly 22 days after the Aid-el-Kebir festivities ended. The patient attributed symptoms to allergy and did not consult with a healthcare professional. In December 2018, her respiratory tract symptoms persisted; she also developed fatigue, fever, and night sweats and consulted a general practitioner. In January 2019, a computerized tomodensitometry scan confirmed an abscess in the inferior lobe of the patient's left lung with thick walls and an infiltrate in the lower lobe of the right lung. The patient reported fever, cough, expectoration, and anorexia, and lost 5 kg within 1 month (body mass index 15); we found crackles in both the left inferior and right superior lobes. She did not report hemoptysis, and her physical examination was otherwise unremarkable. Blood examination showed an iron deficiency in microcytic anemia, and her leukocyte count was normal.

We performed a GenExpert assay (Cepheid, https://www.cepheid.com) and detected M. tuberculosis complex DNA in 1 sputum sample; we cultured the M. tuberculosis complex CSURQ0209 strain. None of the patient's other family members had any pulmonary symptoms at any time, and their chest radiographs results were normal. Before the precise M. bovis identification was known, we administered to the patient a daily oral regimen of rifampin (480 mg), isoniazid (200 mg), pyrazinamide (1,200 mg), and ethambutol (1,000 mg) for 2 months, followed by rifampin (600 mg/d) and isoniazid (300 mg/d) for 4 additional months, with favorable clinical and radiological outcomes and excellent tolerance. Whole-genome sequence analysis of strain CSURQ0209 (GenBank accession no. PRJEB39431) showed that it grouped more proximately with 1 M. bovis strain isolated from a patient from Algeria (Figure).

In this case, slaughtering a sheep during the annual ritual Aid-el-Kebir festivities was a probable source of infection, although no animal remains were available to confirm this hypothesis. Genome sequence analysis confirmed the identification of M. bovis, clustering with isolates from Algeria, in the absence of any other sequence from Tunisia. These results reinforced that this patient had been infected in her native country. During previous years, the festivities took place at the time the family was in France, and no animal sacrifice was performed on these occasions.

Transmission of M. bovis may occur during slaughtering through the inhalation of aerosols exhaled by infected animals (9). In this case, the patient was most likely infected by aerosols after prolonged manipulation of the crude viscera. This case potentially concerns millions of Muslim persons worldwide. Our findings indicate that, in countries where ritual animal sacrifices take place, health authorities may want to work with religious authorities to advocate veterinary inspection of slaughtered animals to discard viscera from animals with suspected tuberculosis, in phase with the current World Health Organization roadmap against zoonotic tuberculosis (10).

References

(1.) Good M, Bakker D, Duignan A, Collins DM. The history of in vivo tuberculin testing in bovines: tuberculosis, a "One Health" issue. Front Vet Sci. 2018;5:59. https://doi.org/10.3389/fvets.2018.00059

(2.) Cousins DV. Mycobacterium bovis infection and control in domestic livestock. Rev Sci Tech. 2001;20:71-85. https://doi.org/10.20506/rst.20.1.1263

(3.) Good M, Duignan A. Perspectives on the history of bovine TB and the role of tuberculin in bovine TB eradication. Vet Med Int. 2011;2011:410470. https://doi.org/10.4061/ 2011/410470

(4.) Majoor CJ, Magis-Escurra C, van Ingen J, Boeree MJ, van Soolingen D. Epidemiology of Mycobacterium bovis disease in humans, the Netherlands, 1993-2007. Emerg Infect Dis. 2011;17:457-63. https://doi.org/10.3201/ eid1703.101111

(5.) Scott C, Cavanaugh JS, Pratt R, Silk BJ, LoBue P, Moonan PK. Human tuberculosis caused by Mycobacterium bovis in the United States, 2006-2013. Clin Infect Dis. 2016;63:594-601. https://doi.org/10.1093/cid/ciw371

(6.) Torres-Gonzalez P, Cervera-Hernandez ME, Martinez-Gamboa A, Garcia-Garcia L, Cruz-Hervert LP, Bobadilla-Del Valle M, et al. Human tuberculosis caused by Mycobacterium bovis: a retrospective comparison with Mycobacterium tuberculosis in a Mexican tertiary care centre, 2000-2015. BMC Infect Dis. 2016;16:657. https://doi.org/ 10.1186/s12879-016-2001-5

(7.) Vayr F, Martin-Blondel G, Saval! F, Soulat JM, Deffontaines G, Herin F. Occupational exposure to human Mycobacterium bovis infection: a systematic review. PLoS Negl Trop Dis. 2018;12:e0006208. https://doi.org/ 10.1371/journal.pntd.0006208

(8.) Nebreda-Mayoral T, Brezmes-Valdivieso MF, Gutierrez-Zufiaurre N, Garcia-de Cruz S, Labayru-Echeverria C, Lopez-Medrano R, et al. Human Mycobacterium bovis infection in Castile and Leon (Spain), 2006-2015 [in Spanish]. Enferm Infecc Microbiol Clin. 2019;37:19-24. https://doi.org/10.1016/j.eimc.2017.11.018

(9.) Lepesqueux G, Mailles A, Aubry A, Veziris N, Jaffre J, Jarlier V, et al. Epidemiologie des cas de tuberculose a Mycobacterium bovis diagnostiques en France. Med Mal Infect. 2018;48:S115-6. https://doi.org/10.1016/ j.medmal.2018.04.291

(10.) World Health Organization. Roadmap for zoonotic tuberculosis. 2017 [cited 2019 Nov 29]. https://www.who. int/tb/publications/2017/Roadmap_for_zoonotic_ tuberculosis_med_red.pdf

Address for correspondence: Michel Drancourt, Aix-Marseille Universite IHU Mediterranee Infection, Unite de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR CNRS 6236 IRD 3R198, IFR 48 27 Bd., Jean Moulin, Marseille 13385 CEDEX 05, France; email: michel.drancourt@univ-amu.fr

Mr. Saad is a PhD student at Aix-Marseille Universite, Marseille, France, with interest in developing appropriate methods for the real-time genomics diagnosis of mycobacterial infections, including tuberculosis.

Jamal Saad, Sophie Baron, Jean-Christophe Lagier, Michel Draneourt, Phillipe Gautret

Author affiliations: IHU Mediterranee Infection, Marseille, France (J. Saad); Aix-Marseille-Universite, Marseille (J. Saad, S. Baron, J.-C. Lagier, M. Drancourt, P. Gautret)

DOI: https://doi.org/10.3201/eid2607.191597

Caption: Figure. Pangenome tree of Mycobacterium bovis from a patient in France (bold; GenBank accession no. CSURQ0209) with 11 reference Mycobacterium bovis strains isolated from different regions and hosts. The patient had visited her home country, Tunisia, where she participated in the ritual slaughter of a sheep. Scale bar represents 5% sequence divergence.
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Title Annotation:RESEARCH LETTERS
Author:Saad, Jamal; Baron, Sophie; Lagier, Jean-Christophe; Draneourt, Michel; Gautret, Phillipe
Publication:Emerging Infectious Diseases
Article Type:Letter to the editor
Date:Jul 1, 2020
Words:1329
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