Next Article in Journal
First Microbial Survey of a Submerged Petrified Forest in the Black Sea: Culture-Based and Metagenomic Insights
Previous Article in Journal
Depth-Dependent Phenotypic Plasticity Differs Between Two Deep-Freshwater Amphipod Scavengers of the Genus Ommatogammarus Despite Similarly Low Genetic Diversity in Ancient Lake Baikal
Previous Article in Special Issue
Phylogeography and Past Distribution of Peripheral Individuals of Large Hairy Armadillo Chaetophractus villosus
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 17
Issue 8
10.3390/d17080582
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Systematic Review

Impacts of Mycobacterium leprae-Infection on Wild Populations of the Nine-Banded Armadillo (Dasypus novemcinctus) Species Complex: A Systematic Review

by
Olivia F. Sciandra
1,*,
Wesley M. Anderson
1,*,
Sarah Zohdy
1 and
Kelly H. Dunning
1,2
1
College of Forestry, Wildlife and Environment, Auburn University, 602 Duncan Dr, Auburn, AL 36849, USA
2
School of Environment and Natural Resources, University of Wyoming Haub, 804 E Fremont St, Laramie, WY 82072, USA
*
Authors to whom correspondence should be addressed.
Diversity 2025, 17(8), 582; https://doi.org/10.3390/d17080582
Submission received: 30 June 2025 / Revised: 1 August 2025 / Accepted: 7 August 2025 / Published: 20 August 2025
(This article belongs to the Special Issue Ecology, Behavior, and Conservation of Armadillos)
Browse Figures
Review Reports Versions Notes

Abstract

Leprosy is a chronically infectious disease caused by infection with Mycobacterium leprae, or the more recently discovered Mycobacterium lepromatosis. In the Americas, wild armadillos of the Dasypus genus are natural hosts. A systematic review evaluated demographics and spatiotemporal patterns of infection with leprosy-causing bacteria in wild populations of the Dasypus novemcinctus species complex. The Web of Science Core Collection, Biosis Citation Index, Dissertations and Theses, and PubMed databases, in addition to Google Scholar, were searched on 16 April 2022. 158 records were recovered, and six peer-reviewed journal articles were selected and summarized that evaluated the effects of M. leprae-infection on mortality, reproduction, age structure, and sex ratio, in addition to seasonal, annual, and spatial infection patterns. Findings indicate that infection with M. leprae has the potential to impact reproduction, mortality, and population age structure. Studies found that the pathogen does not appear to cluster in populations, but consistent temporal findings were not recovered. A limitation of this review is that there was a single reviewer, which may introduce bias. A better understanding of the impacts and distribution of leprosy in wild populations would allow for improved management recommendations for nuisance Dasypus armadillos throughout their range and limit potential zoonotic transmission.

1. Introduction

The nine-banded armadillo (Dasypus novemcinctus) species complex has an extensive range in South and Central America that expanded into North America, including the Southeast United States, in the nineteenth century [1]. As a result of recent genomic findings, this D. novemcinctus species complex has been subdivided into four distinct lineages: D. novemcinctus, D. fenestratus, D. mexicanus, and D. guianensis sp. nov. [2]. In this paper, species within the D. novemcinctus complex are referred to as “armadillo” since distinct lineages and species were not yet determined at the time of this review.
The armadillo has a low tolerance for colder weather, limiting the species’ northward expansion. As a burrowing insectivore, it is also believed that suitable soils and sufficient precipitation are factors limiting the species’ westward expansion in North America [1]. As a result, armadillos are common in South America, Mexico, and the Southeast United States; although, in recent years, they have been found as far north as southern Illinois [1,3].
Armadillos are mainly nocturnal but can be seen during periods of daylight; individuals are also solitary with the exception of females with young offspring [4]. In the late spring and early summer, males disperse further distances than they would typically travel the remainder of the year to find a mate [5]. Once a mate is found, males and females breed annually during the summer in non–monogamous pairs [6]. If fertilization is successful, female armadillos delay implantation of the fertilized egg until the fall, giving birth to identical quadruplets around 18 weeks later in early spring. Among the four littermates, kin selection does not appear to occur, and juveniles typically disperse out of the population, away from siblings, by the following fall [7,8]. According to McDonough and Loughry, the age structure of a wild armadillo population is mainly adults, as most juveniles are depredated before reaching adulthood [9]. If juveniles do reach adulthood, the lifespan for an adult armadillo in the wild is estimated to be between eight and twelve years [9].
Mortality in wild armadillo populations may be a result of extreme environmental conditions such as drought, depredation of juveniles, and vehicular collisions [7]. An additional source of mortality may be disease, specifically leprosy caused by infection with Mycobacterium spp. Leprosy, also known as Hansen’s Disease, is a neglected tropical disease (NTD), that persists in developing nations and mainly affects the peripheral nervous system and mucus membranes [10]. The disease–causing agents of leprosy are acid–fast rod–shaped bacteria, Mycobacterium leprae, and the more recently discovered M. lepromatosis, which are obligate intracellular pathogens [11,12,13]. In the Americas, armadillos are the only known natural reservoirs of the bacteria, outside of humans [14].
Armadillos were discovered to be efficient animal models of leprosy in the 1960s, contributing to the use of the species in clinical research [15]. In 1974 and 1975, wild armadillos in Louisiana were discovered to carry leprosy-causing bacteria [16]. Since the 1970s, M. leprae has been detected in armadillo populations throughout parts of their range in North, Central and South America [17,18,19,20,21]. In the Southeast United States, where most of the research in wild armadillos has occurred, M. leprae prevalence has ranged from 0% to 25%, using a combination of serologic, molecular, and histopathologic detection [17,18,19,22]. The prevalence of leprosy-causing bacteria has also been studied in South America, particularly in Brazil, where nine–banded armadillos are native, and prevalence has ranged from 0% to 63% [20,21,23,24,25,26,27]. However, sample sizes in South American countries have been smaller than in the United States due to legal protections that do not permit the use of many specimens, particularly the limitations of Brazilian laws where most of the research has occurred, as reviewed in [28].
Laboratory studies in armadillos have demonstrated that detectable signs of infection can occur between six months to four years after inoculation with M. leprae, depending on the method of infection [29,30]. Once infected, the bacteria become localized mainly in the reticuloendothelial system, and by 18 to 24 months, an individual has typically developed a severe infection [15]. Balamayooran et al. also discovered that, although armadillos display the full spectrum of disseminated disease, most infections in armadillos are a lepromatous–type response, which is indicative of a poor immune response to the bacteria [15]. Once infected, armadillos with leprosy succumb to the disease within a year or two of infection as a result of bacillated macrophages in the skin, liver, spleen, lungs, and lymph nodes; infection with the bacteria can result in lesions in the lungs and other organs, leading to organ failure, or make an individual more susceptible to concurrent infections, resulting in death [31,32,33].
Armadillos are believed to be highly susceptible to infection with M. leprae; however, one study found that there were different individual-level immune responses, with 15 to 20% of armadillos resisting infection; it is currently believed that resistance to infection may have a genetic basis in armadillos [32]. Genetic resistance is similar in humans with the discovery of genes such as NRAMP1 that control immune response and thus susceptibility [11]. In armadillos, susceptible individuals will likely become infected through the inhalation of infectious aerosols of an infected individual; however, direct and indirect leprosy transmission routes require further investigation, as reviewed in [34].
Armadillos’ susceptibility to infection with M. leprae may be due to a shorter period of co-evolutionary history with the pathogen, as, according to genetic studies, the species was first exposed within the past 500 years [35]. A shorter co-evolutionary period may cause the pathogen, and thus leprosy, to significantly impact the physiology of armadillos. It has been demonstrated that infected armadillos have a metabolic rate that is 23.9% higher than that of uninfected armadillos [36]. The same study suggested that since metabolism is required for reproduction, migration, and foraging, a substantial decrease in metabolic rate of infected individuals may impact an individual’s ability to carry out normal behaviors [36]. As a result, physiological changes due to infection may lead to significant impacts on population dynamics [37].
Much of the previously discussed literature about M. leprae infection in armadillos has involved laboratory populations. Research in wild populations has mainly been limited to leprosy prevalence studies in the Southeast United States and Brazil [18,19,21,26]. Studies that have evaluated the pathogen’s spatiotemporal patterns of infection and impact on wild armadillo population dynamics have yet to be comprehensively reviewed.
Armadillos are also considered nuisance wildlife, causing damage to property that often requires management. Management may take the form of trapping and relocating, dispatching, use of deterrents, and habitat modifications [38]. Additionally, the cultural consumption of armadillo meat is common in parts of the species’ range and may be a source of potential human exposure to leprosy-causing bacteria [39]. Recent genetic and case studies in the Southeast United States and South America have also demonstrated that M. leprae has likely been transferred between humans and armadillos [18,20]. Therefore, because of nuisance armadillo management and cultural consumption of armadillos, exposure to potentially infected individuals may present a zoonotic disease risk.
Evaluating the impact of M. leprae-infection on wild armadillo population dynamics, as well as spatial and temporal patterns of infection, is important in understanding the epidemiology of the disease in wild populations. Additionally, an understanding of how the disease may impact armadillo populations can inform how people interact with the species, decreasing the likelihood of potential zoonotic transmission. This systematic review aimed to characterize studies that have investigated the effects of M. leprae or M. lepromatosis-infection on wild armadillo population dynamics for species in the D. novemcinctus complex, as well as the spatiotemporal patterns of infection. This review identifies research gaps in the geographic distribution of populations that have been previously studied, limited evaluation of temporal infection patterns, and conflicting results related to certain demographic impacts of M. leprae-infection on armadillo populations. Future studies should aim to fill these research gaps to better understand the epidemiology of M. leprae-infection in armadillos, improve management recommendations, and reduce the potential for zoonotic transmission.

2. Materials and Methods

Documents were queried, including peer–reviewed research articles and gray literature such as conference proceedings and theses or dissertations. Our inclusion criteria included papers that analyzed population effects or spatiotemporal patterns of infection with leprosy-causing bacteria in wild armadillos of the nine–banded armadillo species complex. At the time of this research, the species complex was not yet subdivided into distinct species, so the relevant search terms were “nine-banded armadillo” or “Dasypus novemcinctus”. The queried results included all past documents with no defined time period, as our goal was to perform a complete review of all research related to the topic. We were also limited to reports in English or that have been translated to English. Records discussing armadillos in any part of their geographic range or in a laboratory setting were included if an objective was also to investigate the temporal pattern of infection with leprosy-causing bacteria or the impacts on population dynamics. Population dynamics for the purposes of this review include sex ratio, age structure, fecundity or reproduction, and mortality or morbidity.
A structured literature search following PRISMA guidelines was conducted to retrieve records [40]. The search string (‘nine–banded armadillo *’ OR ‘Dasypus novemcinctus’ OR ‘D novemcinctus’) AND (lepro * OR ‘M leprae’ OR ‘M lepromatosis’ OR ‘Mycobacterium leprae’ OR ‘Mycobacterium lepromatosis’ OR ‘Hansen’s Disease’) AND (surviv * OR demograph * OR migrat * OR dispers * OR reproduce * OR breed * OR fecund * OR fertile * OR mortal * OR death OR predate * OR fatal * OR lethal OR ‘population dynamics’ OR ‘life history’ OR size OR density OR ‘sex ratio’ OR age OR spatial * OR temporal *) was used to search the databases of Web of Science Core Collection, Biosis Citation Index, Dissertations and Theses, and PubMed. Google Scholar was also searched to recover any missing reports. Due to character limits, the search string used to query the Google Scholar database was ‘allintitle: leprosy OR leprae OR lepromatosis OR Hansen’s AND nine banded armadillo’. All search queries were conducted on 16 April 2022.
Exclusion criteria included (1) solely clinical trials on leprosy pathogenesis or pathogen susceptibility (2) a focus on a disease other than leprosy (3) a study focused on a different armadillo species outside of the D. novemcinctus species complex (4) clinical trials focused on developing detection methods and (5) pathogen prevalence studies that did not include an analysis of population demographics or spatiotemporal patterns of infection. Commentaries, reviews, and other secondary records were excluded prior to the first screening. Gray literature, including theses, conference proceedings, and technical reports, was included in the first screening. The first screening involved a single researcher reviewing the titles and abstracts of each paper. Papers that were not relevant based on the first screening were removed before the next screening phase. The second screening was a full–text review of each paper by a single reviewer. Records were excluded if the full review revealed that an article did not meet the selection criteria previously described. If the study evaluated multiple populations at multiple sites, the study was included if they evaluated the specified parameters for at least one site. The single reviewer was the same reviewer for the first and second screening; however, the use of strict exclusion criteria that utilized multiple eligibility criteria helped to address potential biases. An official review protocol outside of the methods listed here was not prepared.
The selected records were summarized based on the prevalence of leprosy-causing bacteria recorded in the paper, the detection method used, the study years, and location. From the selected records, findings from one or more of the papers were also summarized into main findings. All relevant and distinct findings from each record were included. Leprosy prevalence was relevant to the summary of the papers and if a total prevalence was not provided, it was calculated from the data presented in each article. These total prevalences were mapped alongside other prevalence studies in the region that were comparable using ArcGIS Pro (v. 3.0.3, ESRI, Redlands, CA, USA) [41].
The impacts of M. leprae infection on population demographics were grouped into four main categories and summarized in a table: reproduction, age structure, sex ratio, and mortality. Reports that included findings of infection patterns were grouped into two broad categories and summarized in a separate table: spatial and temporal. Some records discussed both population demographics and spatiotemporal patterns; in these instances, we separated the same report’s findings into the applicable categories during the review process.

3. Results

The literature search for the effect of M. leprae-infection on wild armadillo population demographics and spatiotemporal patterns of infection revealed a total of 158 articles. Before the first screening we removed 49 records, including 40 duplicates and nine secondary literature sources. During the title and abstract screening, 101 records were removed according to the inclusion and exclusion criteria (Figure 1). Common reasons for exclusion include the clinical study of laboratory armadillos, the study of a disease other than leprosy, or the study of an individual armadillo rather than populations. The final screening of the full text was performed for the remaining 8 records. We removed two records due to their evaluation of D. novemcinctus genetic factors and recording pathogen prevalence without at least one of the topics related to demographic effects or spatiotemporal patterns [42,43]. The result was therefore six relevant records that were included in the review [44,45,46,47,48,49].
All included studies evaluated population dynamics, except for [45], which instead evaluated the prevalence rates from year–to–year and calculated an incidence density for the observed population. Five of the six papers also evaluated spatiotemporal patterns of infection, with the exception of one [49], which only estimated impacts on population dynamics. Additionally, the included studies were all journal articles published in well-established and credible journals. We could not identify potential conflicts of interest for any of the articles included. The oldest article was from 1991 [44] and the most recent article was published in 2017 [49]. Despite identifying only six records in the review process, the findings remain necessary and relevant as they provide critical insights into an underexplored area, potentially guiding future research or policy decisions. A smaller number of publications can still offer high-quality, impactful evidence that addresses specific gaps in knowledge.

3.1. Study Sites

All six of the included studies analyzed wild populations in the Southeast United States and were limited to three states: Louisiana, Mississippi, and Texas. Overall, the studies utilized a total of five unique study sites. Four studies had the same study site of the Yazoo National Wildlife Refuge in Western Mississippi, USA [45,47,48,49]. Additionally, there was one study site included in [44], Welder Wildlife Refuge, which only evaluated prevalence of infection and not the other necessary criteria; therefore, this study site was not included in the following summaries.

3.2. Prevalence of M. leprae

The average sample size of armadillos evaluated across the six studies was 449 (± 34 SE). The studies detected M. leprae infection by either enzyme–linked immunosorbent assay (ELISA) for the M. leprae–specific anti–PGL1 antigen or through the histopathological examination of ear and reticuloendothelial tissues. The result of the ELISA was used to compare prevalence results since all studies used this diagnostic test. The prevalence of M. leprae in the included studies ranged from 10.1% to 23.4% at certain study sites. One study had three included study sites which were averaged together for a study average of 19% (±2.9% SE) [44]. Across all six studies, there was an average M. leprae prevalence of 16.4% (±2.1% SE), as detected using ELISA. We summarized the years of the study, study site locations, diagnostic methods, and average prevalence of leprosy-causing bacteria for each record (Table 1).
Utilizing the prevalence of M. leprae-infection detected via ELISA, these values were compared to other prevalence studies in the region that did not qualify for inclusion in this review [17,19] and were found to have higher prevalence values overall. In these comparable studies, there were duplicate study sites, DeWayne Hayes Recreational area and Pinebloom Plantation, in which the prevalences were averaged across the two studies for comparison [17,19]. It should also be noted that the diagnostic methods of one of these studies utilized both ELISA and polymerase chain reaction (PCR) [17]. We mapped the recorded prevalences of these studies alongside those included in this review for comparison (Figure 2).

3.3. Population Dynamics

The recorded effects of M. leprae-infection on wild armadillo population dynamics in the included papers were summarized (Table 2). There were nine main findings related to the demographic effects of infection, which were further subdivided into reproduction, age structure, sex ratio, and mortality.
Firstly, effects on reproduction included (1) reproducing females were more likely to be seropositive for M. leprae-infection than non-reproducing females and (2) the probability that a seropositive female would reproduce did not vary significantly from females that were not.
The effects of M. leprae-infection on age structure were (3) no yearlings or juveniles were seropositive and (4) older males with increased phenotypic damage (which is often correlated with age) were more likely to be seropositive.
The effects on sex ratio were (5) for seropositive individuals, there was no difference in survival probability between the sexes and (6) there was no significant difference in seropositivity between males and females. However, the latter finding was contradicted by one study where significantly more females were found to be seropositive than males (7).
Lastly, for the effects of infection on mortality, it was found that (8) M. leprae-infection overall reduced the population survivability by 14.5%, (9) seropositive individuals persisted in the population for no more than three years and (10) seropositive individuals had no possibility of recovery from infection.

3.4. Spatiotemporal Patterns of Infection

The spatiotemporal patterns of M. leprae-infection in wild armadillo populations were also reviewed and summarized (Table 3). There were four main findings about infection patterns in wild armadillos with three being categorized as temporal and one as spatial. One spatial finding was recovered and supported by four of the six studies, which was that (1) seropositive individuals were randomly distributed with no significant clumping or clustering of individuals in the areas of study.
Two temporal findings were contradictory with (1) there being no significant annual fluctuations in prevalence and (2) there being annual fluctuations in infection prevalence. The last temporal finding that was found by was (3) a significant seasonal variation in infection prevalence [44], which was not evaluated by the other studies included in this review.

4. Discussion

Previous literature on M. leprae-infection in armadillo species has been primarily limited to basic prevalence studies and clinical laboratory trials. However, a better understanding of leprosy’s epidemiology in wild armadillo populations throughout their range would benefit scientific understanding of the impacts on D. novemcinctus species. Additionally, individuals of the D. novemcinctus species complex are often encountered, handled, and consumed by people. Therefore, understanding patterns of infection in wild armadillos can improve public health recommendations and inform safe management practices of nuisance armadillos, preventing the zoonotic transmission of leprosy-causing bacteria. Our systematic review of the global literature related to leprosy and its impact on wild armadillo populations recovered only six relevant papers, indicating a significant research gap.
Although there were a small number of articles, there were some trends that could be identified as it relates to M. leprae-infection and armadillo population dynamics. Firstly, in wild populations without a detectable infection, no costs of female reproduction have previously been demonstrated [9]. However, in the findings reviewed here, lactating or reproducing females were more likely to be seropositive for M. leprae than non–lactating females [44,46,49]. This finding, however, may be due to the nature of M. leprae as a slow-replicating bacterium, resulting in older females who are more likely to be seropositive for M. leprae while also being of reproductive age [47,50]. Additionally, physiological changes that accompany breeding and gestation may affect female armadillo immune response, making infection detectable and disease potentially more severe; however, no relevant literature on this topic could be recovered. Still, the findings support that M. leprae-positive females are able to reproduce and infection does not decrease the probability of offspring [49]. Further study is required on whether seropositive females face additional costs of reproduction that decreases the number of successful reproductive efforts.
The impacts of M. leprae-infection on male reproductive effort could not be evaluated in the reviewed studies as there is currently no reliable field method for evaluating male reproductive status. One of the reviewed studies [46] did find that seropositive males had more phenotypic damage on the carapace which is often used as a proxy for age, resulting from conspecific aggression and environmental causes [51]. Therefore, it appears that, similar to females, seropositive males were likely to be older; however, further research is needed on whether M. leprae-infection influences male reproductive effort.
A consistent finding across four studies related to age structure impacts was that juveniles and yearlings were not found to be seropositive [46,47,48,49]. This conclusion further supports the finding that leprosy affects older animals as a result of M. leprae’s long incubation period compared to other bacteria [47]. However, recent findings have detected a wild juvenile armadillo that was seropositive and PCR-positive for M. leprae [52]; this armadillo was the first known wild juvenile with an M. leprae infection; therefore, there may be other transmission routes such as vertical transmission from a female to her offspring or indirect environmental transmission through shared burrows. Further research is needed to determine how M. leprae-infection may impact armadillos of different age classes and overall age structure. In general, D. novemcinctus armadillos may live to be eight to twelve years old in the wild, and the studies here only evaluated, at most, six years of population data [6]. Therefore, long–term studies of seropositive females and subsequent litters are needed to better understand potential transmission dynamics and impacts on age structure.
Two of the reviewed studies did not observe a significant difference in the sex ratio of seropositive and seronegative individuals [44,47]. However, Morgan and Loughry observed an uneven sex–ratio of seropositive individuals, with more females compared to males, and this finding was also significant across both years of their study [46]. It is possible that the observed sex ratio by Morgan and Loughry was a result of a small number of seropositive individuals [46]. However, additional studies should be performed to evaluate the sex–ratio of seropositive and seronegative armadillos in other populations. If future studies find additional evidence of uneven sex ratios among infected individuals, it may warrant further investigation into potential physiological explanations that may impact immune response and make female armadillos more susceptible to infection.
The final evaluated parameter of population dynamics was leprosy’s impact on armadillo mortality. One study found a 14.5% reduction in adult survival for those infected with M. leprae, with no possibility of adults recovering [49]. Adult mortality is typically less common than juvenile mortality since juveniles are depredated at a higher frequency than adults [10]. Without a decrease in juvenile mortality, an increase in adult mortality due to M. leprae-infection can thus impact the population growth rate, which was estimated to be a 13% decrease. Therefore, mortality caused by leprosy, in addition to natural mortality, has a substantial effect at the population level [49]. The other included studies did not evaluate mortality rate for a comparison of these findings. Future studies should evaluate how leprosy may impact a population’s mortality rate over a longer time–period using multistate capture–mark–recapture modeling, similar to the methods described in [49].
The second main objective of this review was to summarize the spatiotemporal findings of M. leprae-infection in wild armadillo populations. Across four of the six studies, it was found that seropositive individuals were not spatially clustered and instead, were randomly dispersed throughout a population [44,45,46,48]. In one study, clustering was observed in a portion of the population, but this finding was not statistically significant [46]. The random dispersion of infection observed in the majority of studies may be due to an equal risk of any susceptible individual being infected after exposure to M. leprae [46]. Additionally, the feasibility of environmental transmission has been demonstrated, as reviewed in [34], and the widespread contamination of the environment with M. leprae may result in dispersed infection. However, it should also be noted that the findings of homogenous spatial infection may be limited as the reviewed studies made these conclusions from only five unique study sites that were all in LA and MS, USA, along the Mississippi River. Future studies at additional sites representative of armadillos’ widely diverse habitats may reveal different spatial patterns of infection as a result of genetic variation between populations and habitat factors such as food and water sources, temperature, and soil type.
Temporal patterns of infection also influence wildlife disease systems with changes in prevalence often lagging behind changes in the timing of certain events [53]. Fewer studies included in this review evaluated temporal patterns of infection. In one study that did evaluate temporal findings across seasons at a single study site, the Louisiana Atchafalaya, it was observed that prevalence rates were higher in the winter and summer months compared to the spring [44]. However, other studies did not sample armadillos in different seasons and thus could not support or refute this finding. Still, an explanation for the observation of higher prevalence rates during the summer and winter months may be due to a higher rate of potentially seropositive transient individuals from outside the population during the breeding season [9]. Additionally, there were only two spring sampling seasons compared to a combined four summer and winter seasons which may have caused a bias in the results [44]. Future studies should involve long-term evaluations of the same population over multiple seasons.
In addition to seasonal changes in infection, there were also annual variations observed in two studies. There were conflicting results as in one study, it was found that infection prevalence fluctuated annually [47], whereas in another study, infection prevalence was stable year-to-year [44]. The incidence of M. leprae-infection and leprosy may be impacted by environmental factors contributing to bacteria transmission or environmental changes that apply stressors to the population. Additionally, host and pathogen factors may adapt and change, including host susceptibility and the pathogenecity of M. leprae. Long–term studies are therefore needed to evaluate the annual prevalence of M. leprae in an armadillo population, in addition to further research on biological and environmental factors that may influence disease incidence.
The findings related to leprosy, population dynamics, and spatiotemporal infection patterns in armadillo populations provide an important foundation. However, the papers included in this review also had several limitations. Firstly, the papers were geographically limited to the Southeast United States despite members of the D. novemcinctus species complex having a far greater range. Even within this region, Louisiana and Mississippi were the only two southeastern states in which study sites resided despite Alabama, Texas, Georgia, Florida, and other states east of Mississippi, USA recording a comparable or higher prevalence of M. leprae in wild populations [17,19]. A greater representation of populations from other states is crucial considering the well-accepted fact that armadillo populations first established in Texas, USA, eventually merged with a separately introduced population from Florida near the state of Alabama in the mid-twentieth century [54,55]. Since the studies reviewed in this paper were all along the Mississippi River, these populations may not be genetically representative of other armadillo populations further east. The concentration of study sites to a localized area may also not be representative of different strains of M. leprae with potentially varying impacts on populations. For instance, a distinct strain of M. leprae not found elsewhere in the Southeast United States, 3I–2–v15, has been detected in recent years in Florida; however, the lack of studies evaluating the pathogen’s impact on armadillo populations there and in neighboring states indicates a significant research gap [19].
In addition to being limited to two states, four of the six papers utilized the same population of armadillos at the Yazoo National Wildlife Refuge (YZ) and the studies were conducted in overlapping years, which may also conflate the reported prevalence rates [46,47,48,49]. Further, at YZ and the other study sites included in this review, researchers sampled live armadillos alongside roadways or trails. However, previous studies on roadkill, and thus armadillos found along roadsides, have demonstrated potential biases to the represented age structure with more adults than younger individuals found [56]. In addition to the roadside collection of specimens, all of the represented study sites were natural areas in wildlife refuges or management areas. Therefore, the impacts that M. leprae-infection may have on suburban and urban populations have not been evaluated, despite their increasing expansion into urbanized areas over the last several decades [57]. Several other zoonotic disease systems have demonstrated higher pathogen prevalence in urban populations compared to rural populations such as woodchucks with Toxoplasma gondii in the Midwest, USA [58] and mule deer with chronic wasting disease (CWD) in Colorado, USA [59]. The relationship between wildlife diseases and more human–dominated landscapes, in general, is complex but is an area requiring further study, especially for armadillos with leprosy as the human–wildlife interface is becoming increasingly interconnected [53].
An additional limitation of the included studies is that all six papers utilized the same detection method, enzyme–linked immunosorbent assay (ELISA) to detect IgM antibodies to the phenolic glycolipid–I (PGL–1) antigen of M. leprae. Although ELISA can detect antibodies specific to M. leprae, it is limited in detecting early stages of the disease and paucibacillary–type infections, which are a less severe manifestation of leprosy [60]. Polymerase chain reaction (PCR), on the other hand, detects DNA sequences specific to the M. leprae genome, specifically the 18 kDA protein gene, in infected tissues, at small quantities (100 bacteria) such as with multibacillary infections [61]. For instance, one study detected 16 of the 30 armadillos to be positive for M. leprae via PCR, whereas only 2 of the 30 armadillos were seropositive via ELISA [62]. Due to the higher specificity of PCR, repeating the methods described in the reviewed papers with PCR detection, in addition to ELISA, would be more sensitive and provide a better understanding of M. leprae’s impacts on wild armadillos at different stages of infection.
Lastly, none of the included studies evaluated the prevalence of M. lepromatosis, a recently discovered bacterium that is a causative agent of diffuse lepromatous leprosy [13]. A recent study found that armadillos sampled from eight sites in the Southeast United States from 2003 to 2012 were negative for M. lepromatosis [63]. However, it is possible that over the last decade, armadillos have acquired M. lepromatosis from infected people or other animals with the bacteria, like red squirrels in the UK [64]. The detection of M. lepromatosis should be included in future studies as wild armadillos may serve as a reservoir for this bacterium.
The systematic review itself was limited as a result of our access to only articles in English. Additionally, the query and review were performed by a single reviewer and although strict criteria was followed to address potential biases, a future query and review of records with a secondary reviewer would be beneficial. As a result of the taxonomic changes to the Dasypus novemcinctus species complex, it may also be beneficial to repeat the review for each distinct species to better understand potential impacts to regional populations.
This systematic review underscores the impact that infection with leprosy-causing bacteria may have on wild armadillo populations of the Dasypus novemcinctus species complex. The ecology of the disease in wild populations is complex given the long incubation time of M. leprae and the transmission routes that are not fully understood. Although it appears to impact older adults in armadillo populations and lead to an increased risk of mortality, other important components of population dynamics such as reproduction and sex ratio do not appear to be impacted. Spatially, the disease may be homogenous; however, this was inconclusive in the reviewed studies. Similarly, findings related to temporal patterns of infection, both seasonal and annual, were contradictory and warrant further evaluation. Additionally, the impact that leprosy-causing bacteria has on wild armadillo populations in other regions, states, and habitats, such as human–modified landscapes, requires further study.
In the Southeast United States, where all the reviewed studies were located, the “nine-banded armadillo”, now named the Mexican long-nosed armadillo (Dasypus mexicanus) [2], is a nuisance species. As a result, armadillos in this region often require direct and indirect management, which may put people at an increased risk of zoonotic transmission for M. leprae or M. lepromatosis. In addition, the impact of leprosy on armadillo populations requires consideration when developing management recommendations for property owners. Two common management techniques for many homeowners in the Southeast United States is to trap and relocate or shoot armadillos [41]. These techniques might (1) increase a person’s interaction with a potentially infected individual and (2) result in the translocation of an infected individual into an unaffected population. With additional studies that further evaluate the prevalence and epidemiology of leprosy, global wildlife managers can leverage these findings to develop targeted management strategies that adopt evidence-based practices within a One-Health framework.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/d17080582/s1, Table S1: PRISMA Checklist.

Author Contributions

Conceptualization, O.F.S., W.M.A., S.Z. and K.H.D.; methodology, O.F.S., W.M.A., S.Z. and K.H.D.; validation, O.F.S., W.M.A., S.Z. and K.H.D.; formal analysis, O.F.S. and S.Z.; investigation, O.F.S.; data curation, O.F.S.; writing—original draft preparation, O.F.S. and S.Z.; writing—review and editing, O.F.S., W.M.A., S.Z. and K.H.D.; visualization, O.F.S.; supervision, W.M.A.; project administration, O.F.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Acknowledgments

We would like to thank Patricia Hartman and Auburn University Libraries for their help in developing search queries for this review.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
PRISMAPreferred Reporting Items for Systematic Reviews and Meta-Analyses
ELISAEnzyme-linked immunosorbent assay
PCRPolymerase chain reaction

References

  1. Taulman, J.F.; Robbins, L.W. Range expansion and distributional limits of the nine–banded armadillo in the United States: An update of Taulman & Robbins (1996). J. Biogeogr. 2014, 41, 1626–1630. [Google Scholar] [CrossRef]
  2. Barthe, M.; Rancilhac, L.; Arteaga, M.C.; Feijó, A.; Tilak, M.K.; Justy, F.; Loughry, W.J.; McDonough, C.M.; de Thoisy, B.; Catzeflis, F.; et al. Exon capture museomics deciphers the nine-banded armadillo species complex and identifies a new species endemic to the Guiana Shield. Syst. Biol. 2024, 2, 177–197. [Google Scholar] [CrossRef]
  3. Haywood, C.J.; Jordon, A.M.; Pena, M.; Nielsen, C.K.; Jiménez, F.A. Tissue and gastrointestinal parasites of colonizing nine–banded armadillos at the edge of their northern range. J. Parasitol. 2022, 108, 57–63. [Google Scholar] [CrossRef]
  4. Clark, W.K. Ecological life history of the armadillo in the Eastern Edwards Plateau region. Am. Midl. Nat. 1951, 46, 337–358. [Google Scholar] [CrossRef]
  5. McDonough, C.M. Social organization of nine–banded armadillos (Dasypus novemcinctus) in a riparian habitat. Am. Midl. Nat. 2000, 144, 139–151. [Google Scholar] [CrossRef]
  6. McDonough, C.M. Pairing behavior of the nine–banded armadillo (Dasypus novemcinctus). Am. Midl. Nat. 1997, 138, 290–298. [Google Scholar] [CrossRef]
  7. McDonough, C.M.; Loughry, W.J. Patterns of mortality in a population of nine–banded armadillos, Dasypus novemcinctus. Am. Midl. Nat. 1997, 138, 299–305. [Google Scholar] [CrossRef]
  8. McDonough, C.M.; McPhee, S.A.; Loughry, W.J. Growth rates of juvenile nine–banded armadillos. Southwest. Nat. 1998, 43, 462–468. [Google Scholar]
  9. Loughry, W.J.; Perez–Heydrich, C.; McDonough, C.M.; Oli, M.K. Population ecology of the nine–banded armadillo in Florida. J. Mammal. 2013, 94, 408–416. [Google Scholar] [CrossRef]
  10. Joshi, G.; Quadir, S.S.; Yadav, K.S. Road map to the treatment of neglected tropical diseases: Nanocarriers interventions. J. Control. Release 2021, 339, 51–74. [Google Scholar] [CrossRef]
  11. Scollard, D.M.; Adams, L.B.; Gillis, T.P.; Krahenbuhl, J.L.; Truman, R.W.; Williams, D.L. The continuing challenges of leprosy. Clin. Microbiol. Rev. 2006, 19, 338–381. [Google Scholar] [CrossRef]
  12. Scollard, D.M. Infection with Mycobacterium lepromatosis. Am. J. Trop. Med. Hyg. 2016, 95, 500–501. [Google Scholar] [CrossRef]
  13. Han, X.Y.; Seo, Y.-H.; Sizer, K.C.; Schoberle, T.; May, G.S.; Spencer, J.S.; Li, W.; Nair, R.G. A new Mycobacterium species causing diffuse lepromatous leprosy. Am. J. Clin. Pathol. 2008, 130, 856–864. [Google Scholar] [CrossRef]
  14. Truman, R. Leprosy in wild armadillos. Lepr. Rev. 2005, 76, 198–208. [Google Scholar] [CrossRef]
  15. Balamayooran, G.; Pena, M.; Sharma, R.; Truman, R.W. The armadillo as an animal model and reservoir host for Mycobacterium leprae. Clin. Dermatol. 2015, 33, 108–115. [Google Scholar] [CrossRef]
  16. Centers for Disease Control and Prevention. Leprosy–like disease in wild–caught armadillos—Louisiana. Cent. Dis. Control Prev. 1976, 25, 18–23. [Google Scholar]
  17. Loughry, W.J.; Truman, R.W.; McDonough, C.M.; Tilak, M. –K.; Garnier, S.; Delsuc, F. Is leprosy spreading among nine–banded armadillos in the southeastern United States? J. Wildl. Dis. 2009, 45, 144–152. [Google Scholar] [CrossRef] [PubMed]
  18. Truman, R.W.; Singh, P.; Sharma, R.; Busso, P.; Rougemont, J.; Paniz–Mondolfi, A.; Kapopoulou, A.; Brisse, S.; Scollard, D.M.; Gillis, T.P.; et al. Probable zoonotic leprosy in the southern United States. N. Engl. J. Med. 2011, 364, 1626–1633. [Google Scholar] [CrossRef] [PubMed]
  19. Sharma, R.; Singh, P.; Loughry, W.J.; Lockhart, M.J.; Inman, W.B.; Duthie, M.S.; Pena, M.T.; Marcos, L.A.; Scollard, D.M.; Cole, S.T.; et al. Zoonotic leprosy in the southeastern United States. Emerg. Infect. Dis. 2015, 21, 2127–2134. [Google Scholar] [CrossRef]
  20. da Silva, M.; Portela, J.; Li, W.; Jackson, M.; Gonzalez–Juarrero, M.; Hidalgo, A.; Belisle, J.; Bouth, R.; Gobbo, A.; Barreto, J.; et al. Evidence of zoonotic leprosy in Para A, Brazilian Amazon, and risks associated with human contact or consumption of armadillos. PLoS Negl. Trop. Dis. 2018, 12, e0006532. [Google Scholar] [CrossRef]
  21. Stefani, M.M.A.; Rosa, P.S.; Costa, M.B.; Schetinni, A.P.M.; Manhães, I.; Pontes, M.A.A.; Costa, P.; Fachin, L.R.V.; Batista, I.M.F.D.; Virmond, M.; et al. Leprosy survey among rural communities and wild armadillos from Amazonas state, Northern Brazil. PLoS ONE 2019, 14, e0209491. [Google Scholar] [CrossRef] [PubMed]
  22. Howerth, E.W.; Stallknecht, D.E.; Davidson, W.R.; Wentworth, E.J. Survey for leprosy in nine–banded armadillos (Dasypus novemcinctus) from the southeastern United States. J. Wildl. Dis. 1990, 26, 112–115. [Google Scholar] [CrossRef] [PubMed]
  23. Deps, P.D.D. Pesquisa de Mycobacterium Leprae em Tatus Selvagens da Espécie Dasypus Novencintus do Estado do Espírito Santo. Ph.D. Thesis, Universidade Federal de São Paulo, São Paulo, Brazil, May 2003. [Google Scholar] [CrossRef]
  24. Deps, P.D.; Antunes, J.M.A.d.P.; Faria, C.; Bührer–Sékula, S.; Camargo, Z.P.; Opromola, D.V.; Tomimori, J. Research regarding anti–PGL–I antibodies by ELISA in wild armadillos from Brazil. Rev. Soc. Bras. Med. Trop. 2008, 41 (Suppl. 2), 73–76. [Google Scholar] [CrossRef]
  25. Pedrini, S.C.B.; Rosa, P.S.; Medri, I.M.; Mourão, G.; Bagagli, E.; Lopes, C.A.d.M. Search for Mycobacterium leprae in wild mammals. Braz. J. Infect. Dis. 2010, 14, 47–53. [Google Scholar] [CrossRef]
  26. Frota, C.C.; Lima, L.N.C.; Rocha, A.d.S.; Suffys, P.N.; Rolim, B.N.; Rodrigues, L.C.; Barreto, M.L.; Kendall, C.; Kerr, L.R.S. Mycobacterium leprae in six–banded (Euphractus sexcinctus) and nine–banded armadillos (Dasypus novemcinctus) in Northeast Brazil. Mem. Inst. Oswaldo Cruz. 2012, 107, 209–213. [Google Scholar] [CrossRef]
  27. Souza, D.K.d. Avaliação da Prevalência de Patógenos Zoonóticos de Importância Para a Saúde Pública em Tatus de Vida Livre—Mato Grosso do Sul—Brasil. Master’s Thesis, Instituto de Medicina Tropical de São Paulo, São Paulo, Brazil, 2016. [Google Scholar] [CrossRef]
  28. Deps, P.; Antunes, J.; Santos, A.; Collin, S. Prevalence of Mycobacterium leprae in armadillos in Brazil: A systematic review and meta–analysis. PLoS Negl. Trop. Dis. 2020, 14, e0008127. [Google Scholar] [CrossRef]
  29. Storrs, E.E.; Walsh, G.P.; Burchfield, H.P.; Binford, C.H. Leprosy in the armadillo: New model for biomedical research. Science 1974, 183, 851–852. [Google Scholar] [CrossRef]
  30. Duthie, M.S.; Truman, R.W.; Goto, W.; O’Donnell, J.; Hay, M.N.; Spencer, J.S.; Carter, D.; Reed, S.G. Insight toward early diagnosis of leprosy through analysis of the developing antibody responses of Mycobacterium leprae–infected armadillos. Clin. Vaccine Immunol. 2011, 18, 254–259. [Google Scholar] [CrossRef]
  31. Job, C.K.; Sanchez, R.M.; Hastings, R.C. Effect of repeated lepromin testing on experimental nine–banded armadillo leprosy. Indian. J. Lepr. 1985, 57, 716–727. [Google Scholar] [PubMed]
  32. Truman, R.W.; Ebenezer, G.J.; Pena, M.T.; Sharma, R.; Balamayooran, G.; Gillingwater, T.H.; Scollard, D.M.; McArthur, J.C.; Rambukkana, A. The armadillo as a model for peripheral neuropathy in leprosy. ILAR J. 2014, 54, 304–314. [Google Scholar] [CrossRef]
  33. Vijayaraghavan, R. Nine–banded armadillo Dasypus novemcinctus animal model for leprosy (Hansen’s Disease). Scand. J. Lab. Anim. Sci. 2009, 36, 167–176. [Google Scholar]
  34. Ploemacher, T.; Faber, W.R.; Menke, H.; Rutten, V.; Pieters, T. Reservoirs and transmission routes of leprosy; A systematic review. PLoS Negl. Trop. Dis. 2020, 14, 1–27. [Google Scholar] [CrossRef] [PubMed]
  35. Monot, M.; Honoré, N.; Garnier, T.; Araoz, R.; Coppée, J. –Y.; Lacroix, C.; Sow, S.; Spencer, J.S.; Truman, R.W.; Williams, D.L.; et al. On the origin of leprosy. AAAS 2005, 308, 1040–1042. [Google Scholar] [CrossRef]
  36. Steuber, J.G. The Cost of an Emerging Disease: Mycobacterium Leprae Infection Alters Metabbolic Rate of the Nine-Banded Armadillo (Dasypus novemcinctus). Master’s Thesis, The University of Akron, Akron, OH, USA, December 2007. [Google Scholar]
  37. Tompkins, D.M.; Dunn, A.M.; Smith, M.J.; Telfer, S. Wildlife diseases: From individuals to ecosystems. J. Anim. Ecol. 2011, 80, 19–38. [Google Scholar] [CrossRef]
  38. Gammons, D.J.; Mengak, M.T.; Conner, L.M. Translocation of nine–banded armadillos. Hum.-Wildl. Confl. 2009, 3, 64–71. [Google Scholar]
  39. Deps, P.D.; Alves, B.L.; Gripp, C.G.; Aragao, R.L.; Guedes, B.; Filho, J.B.; Andreatta, M.K.; Marcari, R.S.; Prates, I.; Rodrigues, L.C. Contact with armadillos increases the risk of leprosy in Brazil: A case control study. Indian J. Dermatol. Venereol. Leprol. 2008, 74, 338–342. [Google Scholar] [CrossRef]
  40. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Syst. Rev. 2021, 10, 89. [Google Scholar] [CrossRef]
  41. ESRI 2023. USA Counties—Overview. Available online: https://www.arcgis.com/home/item.html?id=a00d6b6149b34ed3b833e10fb72ef47b (accessed on 1 May 2024).
  42. Job, C.K.; Drain, V.; Truman, R.; Deming, A.T.; Sanchez, R.M.; Hastings, R.C. The pathogenesis of leprosy in the nine-banded armadillo and the significance of IgM antibodies to PGL-1. Indian J. Lepr. 1992, 64, 137–151. [Google Scholar] [PubMed]
  43. Stallknecht, D.E.; Truman, R.W.; Hugh-Jones, M.E.; Job, C.K. Surveillance for naturally acquired leprosy in a nine-banded armadillo population. J. Wild. Dis. 1987, 23, 308–310. [Google Scholar] [CrossRef]
  44. Truman, R.W.; Kumaresan, J.A.; McDonough, C.M.; Job, C.K.; Hastings, R.C. Seasonal and spatial trends in the detectability of leprosy in wild armadillos. Epidemiol. Infect. 1991, 106, 549–560. [Google Scholar] [CrossRef] [PubMed]
  45. Paige, C.F.; Scholl, D.T.; Truman, R.W. Prevalence and incidence density of Mycobacterium leprae and Trypanosoma cruzi infections within a population of wild nine–banded armadillos. Am. J. Trop. Med. Hyg. 2002, 67, 528–532. [Google Scholar] [CrossRef]
  46. Morgan, R.E.; Loughry, W.J. Consequences of exposure to leprosy in a population of wild nine–banded armadillos. J. Mammal. 2009, 90, 1363–1369. [Google Scholar] [CrossRef]
  47. Andrew, J.W.; Loughry, W.J. Temporal aspects of leprosy infection in a wild population of nine–banded armadillos. Southeast. Nat. 2012, 11, 173–182. [Google Scholar] [CrossRef]
  48. Perez–Heydrich, C.; Loughry, W.J.; Anderson, C.D.; Oli, M.K. Patterns of Mycobacterium leprae infection in wild nine–banded armadillos (Dasypus novemcinctus) in Mississippi, USA. J. Wildl. Dis. 2016, 52, 524–532. [Google Scholar] [CrossRef]
  49. Oli, M.K.; Loughry, W.J.; Caswell, H.; Perez–Heydrich, C.; McDonough, C.M.; Truman, R.W. Dynamics of leprosy in nine–banded armadillos: Net reproductive number and effects on host population dynamics. Ecol. Modell. 2017, 350, 100–108. [Google Scholar] [CrossRef]
  50. Loughry, W.J.; McDonough, C.M. The Nine–Banded Armadillo: A Natural History; University of Oklahoma Press: Publishing Division of the University: Norman, OK, USA, 2024; Volume 11, pp. 1–311. [Google Scholar]
  51. Loughry, W.J.; McDonough, C.M.; Robertson, E.G. Patterns of anatomical damage in a population of nine–banded armadillos Dasypus novemcinctus (Xenarthra, Dasypodidae). Mammalia 2002, 66, 111–122. [Google Scholar] [CrossRef]
  52. Sciandra, O.F.S. The Complexities of Living with the Nine-Banded Armadillo (Daypus novemcinctus): Leprosy, Management, and Homeowner Perceptions. Master’ Thesis, Auburn University, Auburn, AL, USA, May 2024. [Google Scholar]
  53. Brearley, G.; Rhodes, J.; Bradley, A.; Baxter, G.; Seabrook, L.; Lunney, D.; Liu, Y.; McAlpine, C. Wildlife disease prevalence in human–modified landscapes. Biol. Rev. 2013, 88, 427–442. [Google Scholar] [CrossRef] [PubMed]
  54. Talmage, R.V.; Buchanan, G.D. The armadillo: A review of its natural history, ecology, anatomy and reproductive physiology. Rice Inst. Pamph. 1954, 41, 16–28. [Google Scholar]
  55. Taulman, J.F.; Robbins, L.W. Recent range expansion and distributional limits of the nine–banded armadillo (Dasypus novemcinctus) in the United States. J. Biogeogr. 1996, 23, 635–648. [Google Scholar] [CrossRef]
  56. Loughry, W.J.; McDonough, C.M. Are road kills valid indicators of armadillo population structure? Am. Midl. Nat. 1996, 135, 53–59. [Google Scholar] [CrossRef]
  57. Hohbein, R.R.; Mengak, M.T. Cooperative extension agents as key informants in assessing wildlife damage trends in Georgia. HWI 2018, 12, 243–258. [Google Scholar]
  58. Lehrer, E.W.; Fredebaugh, S.L.; Schooley, R.L.; Mateus–Pinilla, N.E. Prevalence of antibodies to Toxoplasma gondii in woodchucks across an urban–rural gradient. J. Wildl. Dis. 2010, 46, 977–980. [Google Scholar] [CrossRef]
  59. Farnsworth, M.L.; Wolfe, L.L.; Hobbs, N.T.; Burnham, K.P.; Williams, E.S.; Theobald, D.M.; Conner, M.M.; Miller, M.W. Human land use influences chronic wasting disease prevalence in mule deer. Ecol. Appl. 2005, 15, 119–126. [Google Scholar] [CrossRef]
  60. Gama, R.S.; Leite, L.A.; Colombo, L.T.; Fraga, L.A.d.O. Prospects for new leprosy diagnostic tools, a narrative review considering ELISA and PCR assays. Rev. Soc. Bras. Med. Trop. 2020, 53, e20200197. [Google Scholar] [CrossRef]
  61. Williams, D.; Gillis, T.; Booth, R.; Looker, D.; Watson, J. The use of a specific DNA probe and polymerase chain reaction for the detection of Mycobacterium leprae. J. Infect. Dis. 1990, 162, 193–200. [Google Scholar] [CrossRef]
  62. Job, C.K.; Drain, V.; Williams, D.L.; Gillis, T.P.; Truman, R.W.; Sanchez, R.M.; Deming, A.T.; Hastings, R.C. Comparison of polymerase chain reaction technique with other methods for detection of Mycobacterium leprae in tissues of wild nine–banded armadillos. Lepr. Rev. 1991, 62, 362–373. [Google Scholar] [CrossRef] [PubMed]
  63. Sharma, R.; Singh, P.; McCoy, R.C.; Lenz, S.M.; Donovan, K.; Ochoa, M.T.; Estrada–Garcia, I.; Silva–Miranda, M.; Jurado–Santa Cruz, F.; Balagon, M.F.; et al. Isolation of Mycobacterium lepromatosis and development of molecular diagnostic assays to distinguish Mycobacterium leprae and M. lepromatosis. Clin. Infect. Dis. 2019, 71, e262–e269. [Google Scholar] [CrossRef] [PubMed]
  64. Meredith, A.; Pozo, J.D.; Smith, S.; Milne, E.; Stevenson, K.; McLuckie, J. Leprosy in red squirrels in Scotland. Vet. Rec. 2014, 175, 285–286. [Google Scholar] [CrossRef]
Diversity 17 00582 g001
Figure 1. A PRISMA flowchart detailing the search strategies and selection criteria of eligible articles for this study. Reporting details in PRISMA Checklist (Table S1).
Figure 1. A PRISMA flowchart detailing the search strategies and selection criteria of eligible articles for this study. Reporting details in PRISMA Checklist (Table S1).
Diversity 17 00582 g001
Diversity 17 00582 g002
Figure 2. The study sites of armadillos sampled for M. leprae, a leprosy-causing bacterium, in the six included papers from this global systematic review (purple labeling) compared to other excluded study sites (black labeling) from other prevalence studies in the Southeast United States [17,19], including one study site from [44]: (WEWR) Welder Wildlife Refuge. The abbreviations are: (DSO) DeSoto National Forest, (CON) Conecuh National Forest, (PBH) Pebble Hill Plantation, (VAL) Valdosta, GA, (TLT) Tall Timbers Research Station and Land Conservancy, (CMB) Camp Blanding, (MRI) Merritt Island National Wildlife Refuge, (RS) Riverside, (SC) St. Catherine’s Creek National Wildlife Refuge, (ST) Stimpson Wildlife Sanctuary, (YZ) Yazoo National Wildlife Refuge, (DH) DeWayne Hayes Recreational Area, (PNB) Pinebloom Plantation, (YZ) Yazoo National Wildlife Refuge, (EARL) East Atchafalaya River Levee, (TENS) Tensas River National Wildlife Refuge, (SWMA) Sherbourne Wildlife Management Area, (LNWR) Laccasine National Wildlife Refuge, and.
Figure 2. The study sites of armadillos sampled for M. leprae, a leprosy-causing bacterium, in the six included papers from this global systematic review (purple labeling) compared to other excluded study sites (black labeling) from other prevalence studies in the Southeast United States [17,19], including one study site from [44]: (WEWR) Welder Wildlife Refuge. The abbreviations are: (DSO) DeSoto National Forest, (CON) Conecuh National Forest, (PBH) Pebble Hill Plantation, (VAL) Valdosta, GA, (TLT) Tall Timbers Research Station and Land Conservancy, (CMB) Camp Blanding, (MRI) Merritt Island National Wildlife Refuge, (RS) Riverside, (SC) St. Catherine’s Creek National Wildlife Refuge, (ST) Stimpson Wildlife Sanctuary, (YZ) Yazoo National Wildlife Refuge, (DH) DeWayne Hayes Recreational Area, (PNB) Pinebloom Plantation, (YZ) Yazoo National Wildlife Refuge, (EARL) East Atchafalaya River Levee, (TENS) Tensas River National Wildlife Refuge, (SWMA) Sherbourne Wildlife Management Area, (LNWR) Laccasine National Wildlife Refuge, and.
Diversity 17 00582 g002
Table 1. Summary of included articles listed in reverse chronological order of the publication date with information about study years, location, sample size, prevalence of M. leprae infection based on enzyme–linked immunoassay (ELISA) or histopathological examination, and incidence density. ‘ND’ represents that no data was available.
Table 1. Summary of included articles listed in reverse chronological order of the publication date with information about study years, location, sample size, prevalence of M. leprae infection based on enzyme–linked immunoassay (ELISA) or histopathological examination, and incidence density. ‘ND’ represents that no data was available.
CitationStudy YearsLocation(s), USAAverage Prevalence of M. leprae as Detected by ELISA PGL–1 for AdultsAverage Prevalence of M. leprae as Detected by HistopathologyIncidence Density (New Cases/1000 Animal Days)
(Oli et al. 2017) A [49]2005–2010Yazoo National Wildlife Refuge, MS, USA17.8% (N = 454)NDND
(Perez–Heydrich et al., 2016) [48]2005–2010Yazoo National Wildlife Refuge, MS, USA15.9% (N = 466)NDND
(Andrew and Loughry 2012) B [47]2005–2010Yazoo National Wildlife Refuge, MS, USA16.4% (N = 469)ND0.12–0.61
(Morgan and Loughry 2009) A [45]2007–2008Yazoo National Wildlife Refuge, MS, USA10.1% (N = 317)NDND
(Paige et al., 2002) C [45]1987–1989, 1997Point Coupee Parish, LA, USA19.1% (N = 414)3% (N = 165)0.47–3.5
(Truman et al., 1991) D [44]1984–1989(1) Tensas NWR, Tallulah, LA, USA; (2) Sherbourne WMA, Krots Springs, LA, USA E
(3) Lacassine NWR, Lake Arthur, LA, USA		(1) 23.4% (N = 77)
(2) 13.7% (N = 386)
(3) 20.6% (N = 78)
Average: 19.2% (N = 541)		(1) 6.4% (N = 77)
(2) 3.2% (N = 349)
(3) 1.5% (N = 78)
Average: 3.7%
(N = 504)		ND
A: A total prevalence rate for the population was not provided in the paper but was calculated from the number of “leprous” and “non–leprous” individuals that the paper presented. B: Total sample size was cumulative over the 6 study years. C: Histopathologic examination was performed only on tissue samples collected in 1997. D: Used histopathologic examination on tissue samples collected only at the Louisiana sites. E: The prevalence of M. leprae infection was done for the population at Welder Wildlife Refuge, but the site was excluded from this review as population dynamics or spatiotemporal patterns were not evaluated.
Table 2. Main findings of the demographic impacts of M. leprae-infection on wild armadillos of the D. novemcinctus species complex.
Table 2. Main findings of the demographic impacts of M. leprae-infection on wild armadillos of the D. novemcinctus species complex.
FindingsCitation(s)
Reproduction
1
Lactating—and therefore reproducing—females were much more likely to be seropositive than non–lactating females A
(Truman et al., 1991; Morgan and Loughry 2009; Perez–Heydrich et al., 2016) [44,46,48]
2
No decrease in the probability for a seropositive female to reproduce
(Oli et al., 2017) [49]
Age structure
3
No yearlings/juveniles were seropositive
(Morgan and Loughry 2009; Andrew and Loughry 2012; Perez–Heydrich et al., 2016; Oli et al., 2017) [46,47,48,49]
4
Seropositive males exhibited more phenotypic damage than seronegative males B
(Morgan and Loughry 2009) [46]
Sex ratio
5
There was no evidence that survival probability of seropositive individuals differed between the sexes
(Andrew and Loughry 2012; Oli et al., 2017) [47,49]
6
There was no significant difference in seropositivity between sexes
(Truman et al., 1991; Andrew and Loughry 2012) [44,47]
7
More females were positive than males C
(Morgan and Loughry 2009) [46]
Mortality
8
M. leprae-infection reduced the survival of adults by 14.5%
(Oli et al., 2017) [49]
9
Infected individuals persisted in the population for no more than 3 years
(Andrew and Loughry 2012) [47]
10
Infected individuals have no possibility of recovery from leprosy
(Oli et al., 2017) [49]
A: This finding could also be classified as age structure since reproducing females are typically older females [46]. B: Phenotypic damage is often used as a proxy for age in male armadillos [50]. C: This result was statistically significant in one year of the study, 2008, and when both 2007 and 2008 were combined [46].
Table 3. Summary of the reviewed papers regarding the spatiotemporal patterns of M. leprae-infection in wild armadillos of the Dasypus novemcinctus species complex.
Table 3. Summary of the reviewed papers regarding the spatiotemporal patterns of M. leprae-infection in wild armadillos of the Dasypus novemcinctus species complex.
FindingsCitation(s)
Spatial
  • Seropositive individuals were randomly distributed with no significant clumping or clustering A
(Truman et al., 1991; Paige et al., 2002; Morgan and Loughry 2009; Perez–Heydrich et al., 2016) [44,45,46,48]
Temporal
  • There were annual fluctuations in infection prevalence
(Andrew and Loughry 2012) [47]
2
Infection prevalence was relatively stable year–to–year
(Truman et al., 1991) [44]
3
There were significantly higher prevalence rates in the winter and summer months than in the spring
(Truman et al., 1991) [44]
A: Findings suggested spatial clumping, but it was not statistically significant [46].
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sciandra, O.F.; Anderson, W.M.; Zohdy, S.; Dunning, K.H. Impacts of Mycobacterium leprae-Infection on Wild Populations of the Nine-Banded Armadillo (Dasypus novemcinctus) Species Complex: A Systematic Review. Diversity 2025, 17, 582. https://doi.org/10.3390/d17080582

AMA Style

Sciandra OF, Anderson WM, Zohdy S, Dunning KH. Impacts of Mycobacterium leprae-Infection on Wild Populations of the Nine-Banded Armadillo (Dasypus novemcinctus) Species Complex: A Systematic Review. Diversity. 2025; 17(8):582. https://doi.org/10.3390/d17080582

Chicago/Turabian Style

Sciandra, Olivia F., Wesley M. Anderson, Sarah Zohdy, and Kelly H. Dunning. 2025. "Impacts of Mycobacterium leprae-Infection on Wild Populations of the Nine-Banded Armadillo (Dasypus novemcinctus) Species Complex: A Systematic Review" Diversity 17, no. 8: 582. https://doi.org/10.3390/d17080582

APA Style

Sciandra, O. F., Anderson, W. M., Zohdy, S., & Dunning, K. H. (2025). Impacts of Mycobacterium leprae-Infection on Wild Populations of the Nine-Banded Armadillo (Dasypus novemcinctus) Species Complex: A Systematic Review. Diversity, 17(8), 582. https://doi.org/10.3390/d17080582

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop