Armadillos: Vectors of leprosy in the US?

Issue: June 2016

ByDonald Kaye, MD, MACP

ByMatthew E. Levison, MD, FACP

Leprosy, also known as Hansen’s disease, is a chronic bacterial infection caused by Mycobacterium leprae, an obligate intracellular parasite. Although an ancient disease, leprosy continues to be a major health problem in the developing countries of Africa, Asia and Latin America. Several million people worldwide are permanently disabled by Hansen’s disease. Although 95% of the global total of new cases were reported from 14 countries in 2013 (Bangladesh, Brazil, Côte d’Ivoire, Democratic Republic of the Congo, Ethiopia, India, Indonesia, Madagascar, Myanmar, Nepal, Nigeria, Philippines, Sri Lanka and Tanzania), 59% were from India alone. In these countries, infected humans are the only known natural reservoir, and M. leprae are thought to spread person-to-person following long-term, close contact, usually with an infected member of the household who is excreting enormous numbers of leprosy bacilli in their nasal secretions. Nonetheless, only 5% of the world’s population are naturally susceptible to infection with M. leprae.

Donald Kaye

Matthew E. Levison

Although rare, leprosy has been a reportable disease in the United States since 1970. In the past decade for which data are available (2004-2013), the number of new cases reported each year has been mostly fewer than 100 (average, 88.5 new cases yearly; range, 66-105). In the past decade, Hawaii reported a yearly average of 19.2 new cases, Texas 19.1, California 15.3 and Florida 8.4. The average number of new cases per year in Texas and Hawaii is consistent with the historical values for these states, but California shows a decreasing, and Florida an increasing, trend. For example, in the 12 years before 2006, Florida usually reported five or fewer cases yearly; but from 2007 to 2014, the state frequently reported 10 or more cases per year. The Florida Department of Health has recently reported 29 newly diagnosed cases in 2015. This represents a dramatic, almost threefold increase compared with the previous year.

In the laboratory, M. leprae has been grown in mouse footpads and in the 9-banded armadillo (Dasypus novemcinctus), but cannot be cultivated in vitro. The organism favors growth in cooler parts of the human body. Armadillos, due to their unusually low body temperature of 34°C (93°F) — similar to human skin — are particularly susceptible to leprosy, which becomes systemically disseminated. Following the discovery that armadillos were susceptible to M. leprae in the laboratory, leprosy was found to be occurring naturally in free-ranging armadillos. When armadillos first became infected with M. leprae, however, is unknown.

Figure 1. Nine-banded armadillo (Dasypus novemcinctus).

Source: Shutterstock.com

Armadillos are the size of house cats, primarily nocturnal, feed mainly on insects and burrow into the ground. A bony carapace that covers its back and flanks is divided into three sections: a scapular shield, a pelvic shield and a midsection composed of a number of bands separated by flexible skin. Armadillos are found only in the Western Hemisphere.

The 9-banded armadillo, distributed geographically from northern Argentina to the southern U.S., is the only species of 21 that inhabits the South in Texas, Louisiana and Arkansas, where they are believed to have migrated northward from Mexico. A separate population of 9-banded armadillos in Florida is derived from groups that escaped captivity in the 1920s. Cold weather limits the northern extension of the armadillo’s range.

Serological surveys conducted before 2005 on more than 5,000 animals confirmed that M. leprae infection was present among armadillos primarily in the low-lying coastal areas of Texas and Louisiana, where nearly one-third of adult armadillos are infected.

The Florida armadillo population was found, until recently, to be M. leprae-free.

However, a study from the National Hansen’s Disease Program (NHDP) in Baton Rouge, Louisiana, found that M. leprae infection spread from the western Gulf Coast states to affect armadillos in the Southeastern states. M. leprae DNA or antibodies were found in 106 of 645 (16.4%) armadillos obtained at eight locations in the Southeast not known before 2009 to harbor enzootic leprosy — these locations included southern Mississippi, Alabama and Georgia, and the northeastern, east-central and Panhandle regions of Florida). Forty-two of the M. leprae PCR-positive specimens were genotyped. Only two M. leprae genotypes were recovered: 35/42 (83%) of the animals had type 3I-2-v1, which had previously been identified in armadillos in Texas, Louisiana, Mississippi and Arkansas; and seven armadillos from east-central Florida harbored a newly identified genotype, 3I-2-v15. Few studies have addressed the occurrence of M. leprae in armadillos outside the U.S.

Besides M. leprae-infected humans, the 9-banded armadillo is the only natural host of M. leprae and therefore may be a source of infection for some humans in the U.S. About 70% of cases in the country acquired their disease when they lived or worked in leprosy-endemic regions outside the U.S.; however, about 30% of cases in the U.S. report no foreign residence and therefore likely acquired leprosy inside the country. Most of these indigenously acquired cases are not able to recall any known contact with a person who had leprosy. Most reside in states where M. leprae infection occurs naturally in free-ranging armadillos, and case-control studies have shown that contact with M. leprae-infected armadillos is a risk factor for acquisition of leprosy in the U.S.

Human exposure to armadillos is quite common in the Gulf Coast region, where the animals are handled during the process of hunting, cleaning and preparing their meat for food, and eating. Armadillos are also encountered as roadkill, and many homeowners and gardeners trap them because they are a common nuisance around the house due to their extensive digging in search of food and nests.

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Molecular typing of M. leprae from patients and armadillos has been used by Truman and colleagues at the NHDP with great success to confirm transmission pathways. In one study from 2011, NHDP investigators analyzed the genomes of M. leprae collected from 50 unrelated patients with multibacillary leprosy and 33 armadillos that were captured in the wild in five states where the animals are known to harbor M. leprae (Arkansas, Alabama, Louisiana, Mississippi and Texas). Thirty-nine of the 50 patients reported residence in Mexico or the U.S. where leprosy-infected armadillos are found, and 29 of those patients reported no foreign residence. Genotyping confirmed the same highly specific strain of M. leprae in 28 of the 33 armadillos and in 25 of 29 patients who had never lived outside the U.S. and Mexico and who resided in states with leprosy-infected armadillos. This genotype (3I-2-v1) has not been reported previously elsewhere in the world. Interviews with 15 of the leprosy patients further revealed that eight had direct contact with armadillos. In patients whose risk was foreign residence only, the M. leprae genotype was typical for the strains found in that foreign region.

Click on image to enlarge.

In a subsequent study, the M. leprae genotypes were also assessed in biopsy specimens from 52 unrelated leprosy patients residing in the same regions from 2007 to 2012. None had reported contact with another person with leprosy. Twenty-two of the patients (42.3%) were infected with the same unique strains of M. leprae that occurred naturally among wild armadillos in the region and have not been reported elsewhere in the world. Twelve patients were infected with genotype 3I-2-v1, and 10 patients were infected with the strain 3I-2-v15. All 10 patients with M. leprae 3I-2-v15 resided in the same region where armadillos with this same unique M. leprae genotype strain had been found. These data strongly implicate armadillos as their source of infection.

None of the patients interviewed in Mississippi or Florida recalled direct contact with armadillos, but many reported gardening and other outdoor activities that might have provided some exposure to environments possibly contaminated by M. leprae from armadillos. M. leprae, which have a limited capacity for survival extracellularly, have been shown to survive for many months and remain infectious within free-living amoebae, which can be found in soil or water. M. leprae remain viable in encysted amoebae, which can provide a haven for M. leprae in relatively harsh environments between hosts.

Control of leprosy has historically depended on completeness of early detection of patients with contagious, multibacillary leprosy and starting them on multidrug therapy aimed at elimination of the human reservoir of infection. Although acquisition of leprosy in the U.S. remains rare, the results of molecular typing strongly implicate armadillos as another source for some human M. leprae infections in Gulf Coast states. The NHDP notes that although the risk for transmission from armadillos to humans is low, armadillos should be treated with proper precautions. Direct contact with armadillos and cooking and consumption of armadillo meat should be discouraged. Also, people should wear gloves when gardening and otherwise working with soil in regions where armadillos are infected with M. leprae. Physicians caring for patients with perplexing chronic skin lesions in Gulf Coast states should consider leprosy in the differential diagnosis.

Applying genotyping techniques in patients and armadillos in non-U.S. regions of the Western Hemisphere may help elucidate leprosy transmission in additional human populations.

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For more information:
Donald Kaye, MD, MACP, is a professor of medicine at Drexel University College of Medicine, associate editor of ProMED-mail, section editor of news for Clinical Infectious Diseases and an Infectious Disease News Editorial Board member.
Matthew E. Levison, MD, is a ProMED-mail associate editor and bacterial disease moderator, professor of public health, Drexel University School of Public Health, and adjunct professor of medicine and former chief of the division of infectious diseases, Drexel University College of Medicine.

Disclosures: Kaye and Levison report no relevant financial disclosures.