Mycobacterium leprae Infection in Ticks and Tick-Derived Cells.

Natthida Tongluan,Maria Pena,J Hunter Collins,Richard W Truman,Linda B Adams,Layne T Shelton,Kevin R Macaluso,Rahul Sharma,Gregory Mccormick,Patrick Ingraffia,Ramanuj Lahiri

doi:10.3389/fmicb.2021.761420

Abstract

Leprosy is a zoonosis in the southern United States involving humans and wild armadillos. The majority of patients presenting with zoonotic strains of Mycobacterium leprae note extensive outdoor activity but only rarely report any history of direct contact with wild armadillos. Whether M. leprae is transmitted to new vertebrate hosts through the environment independently or with the aid of other organisms, e.g., arthropod vectors, is a fundamental question in leprosy transmission. The objectives of this study were to assess the potential for ticks to transmit M. leprae and to test if viable M. leprae can be maintained in tick-derived cells. To evaluate tick transmission, nymphal Amblyomma maculatum ticks were injected with isolated M. leprae. Infection and transmission were assessed by qPCR. Ticks infected as nymphs harbored M. leprae through vertical transmission events (nymph to adult and adult to progeny); and, horizontal transmission of M. leprae to a vertebrate host was observed. Mycobacterium leprae DNA was detected in multiple tick life cycle stages. Likewise, freshly isolated M. leprae (Thai-53) was used to infect a tick-derived cell line, and enumeration and bacterial viability were assessed at individual time points for up to 49 days. Evaluations of the viability of long-term cultured M. leprae (Thai-53 and Br4923) were also assessed in a mouse model. Tick-derived cells were able to maintain viable M. leprae over the 49-day course of infection and M. leprae remained infectious within tick cells for at least 300 days. The results of this study suggest that ticks themselves might serve as a vector for the transmission of M. leprae and that tick cells are suitable for maintenance of viable M. leprae for an extended period of time.

Highlights

Hansen’s Disease, more commonly known as leprosy, is caused by an obligate intracellular bacillus, Mycobacterium leprae
None of the ticks assessed at 3 days of feeding (n = 4) were determined to be infected with M. leprae
For injected as nymphs (IAN) ticks feeding on mice, 50% (n = 18) of the skin samples at the tick feeding site were positive for M. leprae

Summary

Introduction

Hansen’s Disease, more commonly known as leprosy, is caused by an obligate intracellular bacillus, Mycobacterium leprae. Presenting as a granulomatous infection that involves the skin and peripheral nerves, leprosy can deform and disable individuals if not properly and promptly treated (Walker and Lockwood, 2006). Current disease control strategies depend on the early diagnosis and treatment of new leprosy cases. Poor diagnostic criteria for leprosy and the stigma that surrounds it act as barriers to both diagnosis and treatment. A lack of understanding of how leprosy is spread confounds efforts to eliminate the disease, as transmission is thought to occur mainly through exposure of susceptible individuals to bacilli shed from untreated or asymptomatic cases, though as yet the exact mechanisms are still unclear (Davey, 1974; Scollard, 2005). Environmental contamination and zoonotic transmission from non-human reservoirs have been implicated (Blake et al, 1987; Desikan and Sreevatsa, 1995; Truman and Fine, 2010; Truman et al, 2011; Sharma et al, 2015; Avanzi et al, 2016; Mohanty et al, 2016; Tio-Coma et al, 2019)

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