Broad diversity of Mycobacterium tuberculosis complex strains isolated from humans and cattle in Northern Algeria suggests a zoonotic transmission cycle

Abstract

Mycobacterium tuberculosis complex (MTBC) comprises closely related species responsible for human and animal tuberculosis (TB). Efficient species determination is useful for epidemiological purposes, especially for the elucidation of the zoonotic contribution. In Algeria, data on MTBC genotypes are largely unknown. In this study, we aimed to investigate the occurrence and diversity of MTBC genotypes causing human and bovine TB in Northern Algeria. During a two-year sampling period (2017-2019) in two regions of Northern Algeria, we observed an overall prevalence of 6.5% of tuberculosis (TB) among slaughtered cattle, which is higher than previous Algerian data yet comparable to neighboring countries. A total of 296 Mycobacterium tuberculosis complex (MTBC) isolates were genotyped by spoligotyping: 181 from tissues with TB-like lesions collected from 181 cattle carcasses and 115 from TB patients. In human isolates, we identified 107 M. tuberculosis, seven M. bovis and one "M. pinnipedii-like", while for bovine samples, 174 isolates were identified as M. bovis, three as M. caprae, three as "M. pinnipedii-like" and one as "M. microti-like". The majority of isolates (89.2%) belonged to 72 different known Shared International Types (SIT) or M. bovis spoligotypes (SB), while we also identified seven new SB profiles (SB2695 to SB2701). Twenty-eight of the SB profiles were new to Algeria. Our data suggest zoonotic transmission in Sétif, where significantly more TB was observed among cattle (20%) compared to the slaughterhouses from the three other regions (5.4%-7.3%) (p < 0.0001), with the isolation of the same M. bovis genotypes from TB patients. The present study showed a high genetic diversity of MTBC isolated from human and cattle in Northern Algeria. Even though relatively small in terms of numbers, our data suggest the zoonotic transmission of TB from cattle to humans, suggesting the need for stronger eradication strategies for bovine TB.

Fig 1. Granulomatous alterations of pulmonary lymph nodes.

(A) Multiple small circumscribed tubercles with yellow content in the left tracheobronchial lymph node in a cow aged more than 5 years. (B) Transverse section showing several white-yellowish, irregular foci in the medial mediastinal lymph node in a calf aged <2 years.

Fig 2. Suspected lesions of bovine tuberculosis in extra-pulmonary organs.

(A) A large focus of yellow caseating necrosis in the liver tissue. (B) Numerous small, grey to white-yellowish, confluent tubercles in the uterus (miliary tuberculosis). (C) Round tuberculous granuloma containing a yellow, dry caseous necrosis central, surrounded by a thin brown zone and an outer broader, white-grey zone in the testis lymph node.

Fig 3. Generalized tuberculosis lesions in different bovine organs.

(A) Small tubercles that are grey to white-yellowish on parietal pleura (miliary disease). (B) Multiple tubercles that resemble pearls of a gray-reddish color in the lung tissue (pearl disease). (C) Large caseous mass in the lung tissue.

Fig 4. Schematic representation of the human and bovine sample analysis strategy.

Fig 5. Distribution of M. bovis spoligotypes among bovine and human samples from two departments in Algeria (2017–2019).