Leprosy: Armadillos in the Amazon are a threat for humans, says Dr. John Spencer and Dr. Moises Silva

Our study calls attention to the possibility of leprosy zoonotic transmission

Leprosy is an infectious disease caused by bacteria Mycobacterium leprae, and affects from two to three million people worldwide according to numbers from the World Health Organization (WHO). In Brazil, the Ministry of Health considers leprosy an endemic disease. In 2017 alone, 23 thousand new cases were diagnosed, from which 5 thousand in the North region, 5 thousand in the Middle-West and 11 in Brazil’s Northeast.

Recently a study entitled “Evidence of zoonotic leprosy in Pará, Brazilian Amazon, and risks associated with human contact or consumption of armadillos” published on specialized journal PLoS Neglected Tropical Diseases called attention to the fact that over half of the studied wild armadillos in Brazil’s Amazon are carriers of the leprosy bacteria.

According to scientists John Spencer from the Colorado State University and Moises Silva, from the Federal University of Pará (UFPA), who talked to the Press Advisory from the Brazilian Society of Tropical Medicine (BSTM), Brazilians, especially in rural areas, hund and kill armadillos as a food source. In the small town of Belterra, Western Pará State, a research among 146 locals revealed that 65% of them had some contact with armadillos, by hunting, manipulating for cooking and eating. Still according to the researchers, a group of people who were served armadillos more frequently (over one time per month) had a significantly higher antibody count and twice the risk of being diagnosed with leprosy, a significant risk.

To know more about this, find below the full interview with scientists Dr. John Spencer and Dr. Moises Silva.

BSTM: How did the interest in this topic and in this region arise?

Dr.John Spencer: I would be happy to answer some of your questions for your article. I have been working with Dr. Claudio Salgado and his team for almost 10 years, mostly on leprosy surveillance of people in Pará state, working there around 3 months per year.  This armadillo project was proposed by a Masters graduate student, Juliana Portela, whose advisor at UFOPA was Antonio Minervino and Claudio at UFPA.  Initially, we had doubts that exposure to armadillos could affect people living in a hyperendemic area, there is already so much exposure to Mycobacterium leprae from human to human contact, and more than 60% are antibody positive to PGL-I antigen from the bacterium.  But when we saw a much higher antibody titer in the group that eats armadillos the most (50% higher) and that there was an almost 2X greater risk of having disease due to this behavior, this is strong evidence that leprosy is a zoonotic disease spreading from armadillos to humans, just like in the southern U.S.

BSTM: was the research performed?

Dr.John Spencer: This was a project that included my long-term collaborators in Brazil (Claudio Salgado, Moises da Silva, Josafá Barreto at UFPA; Marco Andrey Frade at USP-Ribeirão Preto; and Antonio Minervino at UFOPA), Leiden University Medical Center, The Netherlands (Annemiek Geluk); École Polytechnique Fédérale de Lausanne, Switzerland (Stewart Cole and Charlotte Avanzi), and other researchers from my university, Colorado State University.  The research was performed at all of these institutions over a 3 year period.

BSTM: Which are the next steps?

Dr.John Spencer: The evidence for zoonotic transmission of leprosy from armadillos to humans in Louisiana and Texas was proven by using whole genome sequencing of M. leprae isolated from both patients and armadillos, showing there was an exact match of the strain type.  There are two very specific genetic variants of M. leprae in armadillos, one in Texas and Louisiana (SNP type 3I-2-v1) and the other in a cluster of infected armadillos in central Florida in Volusia county (SNP type 3I-2-v15) that was identified in 2015 as crossing over to infect humans.  Recently, the first known case of endemic leprosy in a young child in Florida was reported, with the only known exposure to the disease being contact with armadillos in the backyard. We are attempting to define the genetic type of M. leprae circulating in this area in Pará state to show that the type that is found in armadillos is also found in leprosy patients.

BSTM: How could you explain the fact that over half of the tested armadillos living in the Brazilian Amazon tested positive for Mycobacterium leprae?

Dr.John Spencer: Nine-banded armadillos are native to South America and Brazil. They expanded their range from Mexico into Texas around 1850, and then continued north and east to populate all of the southern states in the U.S. Since it has been found that they have a rate of infection of 15-20%, this has meant that humans infected armadillos with M. leprae first and then they have been giving it back to humans for decades. Because armadillos are native to Brazil and leprosy occurs at much higher rates in the state of Pará, humans likely infected armadillos with M. leprae a over a much longer time-frame, perhaps >300 years ago. This is why armadillos in this region are infected at such high rates (62%), which is 3X higher than in rates in the southern U.S.

BSTM: Can the same happen to armadillos from other Brazilian regions?

Dr.John Spencer: Probably. This is likely because leprosy occurs in all states in Brazil. It is highest in the central-west, northern, and northeastern states, lower in the south.

BSTM: Can other animals in this area carry the Mycobacterium leprae?

Dr.John Spencer: Animals in other states or regions can also test positive. Surveys need to be performed from a wider region to examine this.

BSTM: Regarding transmission in the United States, how did it happen? Wouldn’t a certain pre-disposition be necessary to develop leprosy?

Dr.John Spencer: As mentioned in the paper, 90% of all people all over the world are resistant to infection by mycobacteria that cause tuberculosis, leprosy, and other mycobacterial diseases. People who are susceptible to develop disease caused by these mycobacteria (around 10%) will do so if they are infected and other conditions are met.

BSTM: Considering the high rates of leprosy in the Amazon, it is thought that the animal-human transmission route is not a recent phenomenon in the region. Are there any signs of when this started? And which specific route?

Dr.John Spencer: As I mentioned above, we can only speculate that armadillos were infected by the colonists from Europe and slaves who brought leprosy to North and South America in the last 500 years. Humans with leprosy had to give M. leprae to armadillos first before they started giving it back to humans, but this took at least 100 years, similar to what occurred in Texas and Louisiana in the U.S.

BSTM: How does the transmission happen and how to avoid it?

Dr.John Spencer: Human to human is aerosol transmission by untreated cases that can be reduced by early diagnosis and treatment.  Armadillo to human can be by aerosol, blood, or from contaminated soil.

BSTM: Are authors considering leprosy transmission BEFORE the arrival of Europeans, since the armadillo is an animal of the new world and leprosy was already endemic in the Old World for thousands of years?

Dr. John Spencer: So, as mentioned in the paper, although armadillos originated in South America and co-existed with native Indian people there for 10s of thousands of years, there was no leprosy at all in humans or armadillos until the explorers came from Europe in the 1500’s.  Leprosy had existed in Europe since around at least 700 A.D. in France and moved north to infect all of Europe, the U.K. and Scandinavian countries. When the colonists (Portuguese, English, Dutch, Spaniards, French, etc.) arrived in the New World to North and South America beginning in the 1500’s, they brought leprosy with them and spread it (and other diseases) to the Indians and amongst themselves in colonies they populated in North and South America.  At some time in the last 500 years, armadillos in South America became infected with M. leprae from humans with leprosy. Armadillos only expanded their range into Texas in the 1850’s, so it took a while after that for them to get the disease from humans in the southern U.S. states. It is unclear exactly how they got it, but probably from contaminated soil (they are digging animals). Once it reached a certain infection rate in armadillos (10-20%), then armadillos could give it back to humans, just like they do now in Texas, Louisiana and Florida through contact with humans.

BSTM: Do you think leprosy is an anthroponotic disease in the Old World and a zoonosis only in the New World?

Dr. Moises Silva: No, in the new world leprosy is also an anthroponotic disease, and humans are the core of infection control. Early diagnostic for leprosy cases, impeding the dispersion of the bacteria and avoiding patients to acquire physical inabilities. Zoophilic transmission, in Brazil, is a secondary issue in the transmission process. Wild armadillos naturally and singly infected, are not responsible for the 3 thousand-plus new cases detected every year in Pará state (data from 2016 SINAN). The disease’s control is multifactorial and depends on actions ranging from strategic family health coverage increase – which in Belém, capital of Pará State, is only 22% (2016), to monitoring notified cases and evaluating their reports, to applying supervision, support and training for health professionals to detect initial cases of the disease, including actions in elementary and secondary schools.

BSTM: Would you like to add anything you may find important and that was not approached?

Dr.John Spencer: This paper represents the most significant work I have published in my career, and the publicity supports this.  All of our Brazilian and other collaborators are very proud of this work, it took 3 years of hard effort to complete this study.

Best advice to avoiding contracting leprosy is to limit one’s exposure to armadillos. People who hunt, kill, or prepare the meat for cooking should take precautions not to be exposed to blood, tissues or body fluids (wear gloves while preparing or handling the meat).  Cook the meat fully so as not to consume rare or raw meat.

As discussed in the paper, many people in rural areas in Brazil eat armadillos as a source of protein, but it is also a part of their social and cultural existence, going on for generations. Armadillos for many people are considered a delicacy, and since they are large animals, a hunter who catches one can share it with family and friends, having a feast and a party. For these reasons, it is not likely that this culture or behavior will be changed, even if these people know about armadillos transmitting disease (and we did tell around 75 people in this town at a meeting there about this, and they seemed unperturbed about this fact, stating that they would still eat armadillos).…