1. Introduction
The dimorphic intracellular hemoflagellate protozoan parasites of the genus Leishmania are transmitted to vertebrates by the bite of the phlebotomine sandfly, which are vectors and can cause Leishmaniasis. Most infected humans and animals do not display symptoms or clinical signs, but when they do, they can present in one of three clinical forms: cutaneous leishmaniasis (CL), mucocutaneous leishmaniasis (ML), or visceral leishmaniasis (VL) in humans, and
Leishmania spp. can also cause mucocutaneous lesions in animals [
1]. As per the World Health Organization’s (WHO) estimates, 92 countries and 83 regions are believed to be endemic for CL and VL or have had reported incidences of these diseases in the past. Today, almost 1 billion people are at risk of contracting leishmaniasis. Annually, there are more than 1 million new cases of CL and 30,000 new cases of VL, respectively [
2]. India accounted for 18% of the global kala-azar burden in 2020. Since the accelerated elimination program began in 1992, kala-azar cases in India have decreased by 97%. Reported deaths dropped from 1419 in 1992 to 58 in 2018, and only 37 deaths were recorded in 2020 [
3]. Leishmaniasis predominantly affects isolated rural areas with poor housing and limited medical access, often linked to poverty. Diagnosing the disease in endemic regions places a significant financial strain on individuals and society. As a serious global public health concern, controlling leishmaniasis is challenging and can lead to epidemic outbreaks. Key focus areas include prevention and management, such as early detection, appropriate treatment, vector control, and managing animal reservoirs to reduce prevalence and prevent deaths and disabilities [
4]. There are two epidemiological patterns for kala-azar, or visceral leishmaniasis (VL). The first type of VL is anthroponotic visceral leishmaniasis (AVL) (
Figure 1), and it spreads mainly among humans but can also circulate between animals and human beings. The second type of VL is zoonotic visceral leishmaniasis (ZVL) (
Figure 2), which spreads from infected animals to people, with domestic dogs serving as the main reservoir host; both manifest epidemiologically as VL.
L. donovani, which is present in East Africa, Bangladesh, India, and Nepal, is known to cause the first pattern of VL [
5].
The most severe form of leishmaniasis, known as visceral leishmaniasis (VL, sometimes called kala-azar), can be fatal if left untreated. Without any known animal reservoirs, the
Leishmania donovani complex of parasites that cause VL in the Indian subcontinent (ISC) transfer from person to person via the sandfly
Phlebotomus argentipes [
6]. The reservoir hosts play a crucial role in the life cycle of the leishmanial parasites. The principal vector of visceral leishmaniasis in India prefers to accumulate in and around animal shelters, where the steady microclimate and easy access to blood samples may modify the dynamics of the infection by affecting the rates of vector–host contact [
7]. The complicated interaction between the pathogen vector and reservoir shows geographical and temporal variations [
8]. Comparable to any other host–parasite system, the host factors, parasite characteristics, exposure, and local environmental conditions where the host–parasite system occurs, can precisely determine the
Leishmania infection patterns in any mammalian host organism [
9,
10]. Few studies have suggested that cats are also infected in endemic areas and act as reservoirs to transmit the infection, which is considered to be the most important risk factor predisposing humans to disease. Dogs and humans are considered the natural hosts of leishmaniasis and the primary reservoir for zoonotic visceral leishmaniasis (ZVL) [
11].
Leishmania spp. infect a variety of wild, domestic, and synanthropic species, including dogs, cats, rats, foxes, pigs, and rock hyraxes [
12,
13,
14,
15]. Sandflies (
Phlebotomus,
Lutzomyia) transmit Leishmania parasites through bites, injecting the parasites into the host’s skin, initiating infection and disease spread. A reservoir species is defined as one or more populations with a strong epidemiological bond, where a disease can establish a chronic infection and from which an infecting organism is transmitted to the target population. Significant increases in human susceptibility to leishmaniasis are a result of human activities, such as migration, deforestation, uncontrolled urbanization, or changes in infection vulnerability brought on by immunosuppression and malnutrition [
5,
16,
17]. The aim of this systemic research was to investigate and identify possible domestic animal reservoirs for VL infection in India, as investigating domestic animal reservoirs is crucial for understanding leishmaniasis transmission, vector–host dynamics, epidemiological surveillance, and developing comprehensive control strategies, thus informing effective public health policies.
5. Results and Discussion
A flowchart for conducting the literature search is presented in
Figure 3. Implementing the search technique provided 530 potentially important references, of which 507 were prohibited because of copy avoidance, irrelevant titles, research publications from countries other than India, or modified compositions. Later, in the remaining 23 investigations, 20 were not considered due to having unmatched data during the full-text review. According to the set parameters, three research studies were considered, along with infection in domestic animals in VL-endemic countries, which were also presented for this meta-analysis. The combined data of all the animals that showed the ability to act as reservoirs for leishmaniasis has been given in
Table 1.
Table 1.
Leishmaniasis in numerous species of animals from various parts of India.
Table 1.
Leishmaniasis in numerous species of animals from various parts of India.
Host | Method of Detection | No. of Animals Tested | No. of Positive Cases | Reference |
---|
Cattle (Bos primigenius indicus) | Serologic examination (recombinant protein rK39) and PCR amplification | 161 | 1 | [18] |
Goats (Capra hircus aegagrus) | Serologic examination (recombinant protein rK39) and PCR amplification | 867 | 31 | [18] |
Buffalo (Bubalus bubalis) | Serologic examination (recombinant protein rK39) and PCR amplification | 3 | 0 | [18] |
Rats (Rattus rattus) (Bandicoota bengalensis) (Rattus norvegicus) | ELISA/aldehyde test/culture, serologic examination (recombinant protein rK39), and PCR-RFLP analysis | 309 | 6 | [18,19,20] |
Chickens (Gallus gallus domesticus) | Serologic examination (recombinant protein rK39) and PCR amplification | 106 | 0 | [18] |
Dogs (Canis familiaris) | ELISA/aldehyde test/culture, serologic examination (recombinant protein rK39), and PCR-RFLP analysis | 406 | 5 | [18,19,20,21] |
Sheep (Ovis orientalis vignei) | Serologic examination (recombinant protein rK39) and PCR amplification | 26 | 0 | [18] |
A number of potential animal reservoirs for Indian kala-azar, including dogs and rats (Rattus rattus and Bandicoota bengalensis), were examined regarding the disease’s 1983 epidemic in India. After morphological and serological examination, anti-leishmanial antibodies were found in 5 out of 226 B. bengalensis samples.
In a study by Singh et al. [
18] in India from seven different parts of Bihar, where anthroponotic VL is endemic, blood samples from 1220 domesticated animals and 54 wild rats were collected in 2008 and 2009. Domestic animal samples were collected from both owned and individual animals at abattoir veterinarian clinics. Rats were caught using live traps (box or chamber traps that allow mice to enter but prevent them from exiting), and the antibodies found using a recombinant kinetoplast antigen (the rK39 antigen test detects antibodies against the K39 antigen, a repetitive immunodominant region of a kinesin-related protein from
L. donovani) in amastigotes of the visceralizing Leishmania species,
L. donovani complex, were examined in serum samples from 1220 animals from seven districts with endemic human VL. Additionally, samples that were identified as positive by rK39 antigen serology were examined using the PCR. A total of 33 out of 1220 animals had antibodies to rK39, which is indicative of VL. A total of 31 out of 867 goats, 1 out of 161 cattle, and 1 out of 54 wild rats tested positive for rK39 serology. Using the rK39 serology, none of the 106 chickens, 26 sheep, three water buffaloes, or three canines tested positive. In 20 rK39-positive goat blood samples and one positive cow blood sample,
Leishmania donovani DNA was found using the PCR.
In another study, it was confirmed that dogs serve as
L. donovani reservoirs in the Kani tribe village communities in the Thiruvananthapuram district of Kerala, which are situated in the southernmost portion of the Western Ghats; with the assistance of a veterinarian, rodents and domestic dogs in the communities were checked in 2014. In order to guard against the predatory behavior of wild animals, the tribes domesticate dogs. There were 194 dogs in all, ranging from 1 to 7 dogs in each family, whereby peripheral blood samples from 25 wild rats and 47 domestic dogs were examined for leishmaniasis. It was concluded that Leishmaniasis cases with cutaneous symptoms and a high sandfly population are common in this region. Using PCR-RFLP analysis of the UTR region of the heat shock protein 70 (hsp70) gene and the diagnostic kinetoplast mini-circle DNA,
Leishmania donovani parasite DNA was only found in three of the blood samples taken from domestic dogs. None of the rat blood samples that were taken had any positive results.
L. donovani infection in dogs was proven via sequencing [
20]. This study by Jambulingam et al. [
20] concluded that, despite being asymptomatic, the domestic dogs had molecular evidence of
L. donovani infection when their blood samples were examined. While canine blood samples subjected to PCR assays revealed parasite DNA, none of the blood smears from the positive samples revealed LD bodies (
Leishman-Donovan bodies are the intracellular form of the Leishmania parasite seen in human and animal tissues). This is the result of Leishmania parasites being discovered using the traditional method and the fact that the parasites multiply in the macrophages of the spleen, liver, and bone marrow. However, a PCR technique could be used to find parasite DNA fragments in disintegrating blood cells or tissue samples. Leishmaniasis diagnosis has been demonstrated to benefit from the PCR test, especially in samples with low parasite loads.
L. donovani DNA has also been found in the blood of local dogs, goats, and cows in Bangladesh [
22], Nepal [
23], Sri Lanka [
24], Ethiopia [
14,
25,
26], and Sudan, which are considered to be VL-endemic locations, indicating that these animals serve as significant animal reservoirs of VL. In a region of active VL transmission in Nepal, a few researchers used blood samples from humans, goats, cows, and buffaloes in the Terai region of eastern Nepal to map Leishmania infections among healthy people and animals. Leishmania infections were then identified using the PCR. The results showed that only 37 of the 105 residences in Survey-I had 188 domestic animals (goats, buffaloes, and cows). Goats were responsible for 16% of the 13.3% Leishmania-positive percentages, followed by cows with 5% and buffaloes with 4%. Animals that were
Leishmania spp. positive were found in 15 households. Only goats were sampled during survey II from six of these families; 2 goats (from different houses) out of 24 (8.34%) tested positive for Leishmania spp. Furthermore, a Leishmania-specific sequence was present in all sequenced amplicons, which were validated. By a classification tree analysis, the presence of
Leishmania spp.-positive goats nearby in Nepal is the main risk factor for human leishmaniasis. Additionally, these findings do not necessarily imply that goats are a reservoir host of
L. donovani; however, they do point to the necessity for further research into the potential contribution of goats to the transmission of VL [
23].
There are few studies looking into how domestic animals serve as a reservoir for VL in Bangladesh. Although the exact number of stray dogs in Bangladesh is unclear, the population is extremely large. These canines frequently reside in or close to human residences, and as a result, they may help spread serious zoonotic diseases like leishmaniasis domestically. According to Akter and other scientists [
27], endemic areas of Bangladesh have visceral leishmaniasis, which can be contracted by stray dogs. In Bangladesh’s Trishal and Fulbaria upazila (subdistricts), which are two VL-endemic regions, 50 stray dogs—30 males and 20 females—were discovered. A total of 6 out of 50 (12%) dog blood samples tested positive for anti-Leishmania antibodies, and we saw moderately strong bands in the test line region for four samples but faint bands in the rK39 dipstick test for two samples. Researchers have discovered that dogs in the Bangladeshi region, where leishmanial parasites are endemic, have a leishmanial infection, which supports these parasites’ survival. In other studies, serological and molecular testing in Bangladesh’s VL-endemic regions identified leishmania infections in stray dogs. Anti-leishmanial antibodies were present in cattle from a Bangladeshi endemic area; however, the PCR was unable to detect any parasite DNA [
22].
S.S.K. Nawaratna et al. [
24] conducted a study that supports the proposal that the Cutaneous leishmaniasis disease prevalent in Sri Lanka may be a zoonosis. A total of 15 villages covered the three provinces of Central, North Western, and North Central. Sample collection was conducted concurrently with patient studies and animals that included domestic dogs and rats from the regions where CL patients were identified. By prior arrangement, residence visits were made with the veterinarians in the target areas to collect samples from the dogs. Before the examination, the owner provided a brief history of the animal. If there were any ulcers, needle samples from the skin and the ulcers were taken for smears and a PCR. Blood from the vena cava was drawn for the PCR and smears. Over the course of a year, traps were placed in and around homes and nearby crops to capture field rodents. Upon each visit, 15–20 traps were set and taken to the lab for analysis. The rodents that had been caught were taken to the lab for analysis. After being euthanized with chloroform, they were closely reviewed for cutaneous lesions. According to the data acquired, 2 of the 151 dogs examined in Sri Lanka—one from the skin and one in peripheral blood—showed Leishmania amastigotes in Giemsa-stained smears. None of the examined rodents were positive for Leishmania infection.
Rodents are believed to play a part in the transmission of leishmaniasis in Ethiopia, possibly acting as reservoir hosts, and according to A. Kassahun et al. [
25], there is eco-epidemiological significance of rodents in these hotspots of leishmaniasis. In another research study by Wossenseged Lemma et al. [
26],
A. niloticus,
A. cahirinus,
Gerbilliscus nigricaudus, and
M. erythroleucus may be involved in the cycle of transmission of the zoonotic kala-azar infection caused by
L. donovani in parts of Ethiopia where it is endemic. In Ethiopia, in a different study conducted by Rohousova et al. [
14], 546 animals were tested, and 32 (5.9%) of those tested were positive for Leishmania DNA. Positive animals were found in all the species examined. Although sequencing was unable to differentiate between
L. infantum and
L. donovani, it did reveal that the animals were infected with parasites of the
L. donovani complex. In all, 18.9% of the animals tested positive for anti-
L. donovani IgG, and 23.1% tested positive for anti-P. orientalis saliva IgG, with dogs and sheep showing the highest seroprevalence. Anti-
P. orientalis saliva and anti-
L. donovani IgGs in cows, goats, and sheep were found to be positively correlated. A possible risk factor for VL in the Sudan is the presence of serologically and parasitological positive dogs in an area with a history of VL due to their capacity to present and their role as a major supply of organisms for sandflies (
Table 2).
Table 2.
Identification of L. donovani infection in domestic animals in VL-endemic countries.
Table 2.
Identification of L. donovani infection in domestic animals in VL-endemic countries.
Country | Suspected Species of Potential Reservoir | Reference |
---|
Bangladesh | Dog, Domestic Cattle, Goat | [22,27] |
Nepal | Buffalo, Cow, Goat, Dog | [23] |
Sri Lanka | Dog | [24] |
Ethiopia | Cow, Goat, Dog, Sheep, Rodents | [14,25,26] |
A similar systemic study was conducted in Iran, where the distribution of VL caused by
Leishmania infantum in domestic and wild canines in different geographical areas of the county was reviewed [
28]. According to the data provided by Mohebali et al. [
28], a total of 24,884 animals were evaluated for this research, of which 94.23% were dogs that were either owned pets or stray dogs, with the remaining animals being other wild species. A total of 90% of the dogs tested were sheepdogs and pets, and 10% of those were stray dogs. Leishmanial parasite infection rates were 14.18% in domestic dogs and 6.35% in wild dogs. Domestic dogs are the primary and probable reservoir hosts of canine visceral leishmaniasis, which is endemic in several regions of Iran. In the endemic regions of the disease, other predators, including domestic cats and several species of desert rodents, appear to be maintaining the transmission cycle of
L. infantum.
Many studies in East Africa and the Indian subcontinent have investigated wild and domestic reservoir hosts of human visceral leishmaniasis (VL). This systemic analysis study is to confirm Leishmania infection in domestic animals that acted as a reservoir of VL in the endemic area, linked to
P. argentipes vector transmission using xenodiagnosis. Host-targeted surveillance, including sandfly infection and blood meal tracking, is crucial for monitoring and sustaining the elimination efforts and for VL diagnosis clinical symptoms and positive serological/parasitological tests, with rK39 RDT widely used in the ISC [
29]. Domestic livestock in Bangladesh, Ethiopia, and Nepal have shown higher Leishmania prevalence than in India, influenced by varying sandfly infection rates and environmental factors.
Epidemiological reports around the world have reported signs of infection or exposure to L. donovani in several domestic species, suggesting that L. donovani may be zoonotic. For the purpose of implementing control measures or monitoring programs, it is crucial to understand the function of wild animals as ideal hosts or reservoirs of the Leishmania zoonotic species. In India, the kala-azar is thought to be anthroponotic, and earlier efforts to find an animal reservoir host, although employing insensitive techniques, have failed. India has recorded a small number of instances of visceral leishmaniasis in several animal species, but none have been determined to be zoonotic VL. The extent to which L. donovani infection of domestic animals promotes transmission to other animals or humans in India is not recognized. Evidence from prior vector-borne disease eradication methods showed that domestic species’ developing diseases hampered elimination. Public health and veterinary researchers have neglected the role that few animals have in the maintenance and transmission of VL, and this aspect of the epizootiology of VL needs to be critically examined to update prevention and treatment programs in the kala-azar endemic areas.
Assessing Leishmania donovani infection in domestic and wild animal reservoir hosts is crucial. Firstly, identifying these reservoirs helps us to elucidate the transmission dynamics of zoonotic visceral leishmaniasis (VL), as these animals can harbor and spread the parasite to sandflies, which then transmit it to humans. Simultaneously, understanding which animals are involved allows for more targeted surveillance and control strategies. As reported in various studies, cattle, goats, dogs, and rats acted as hosts to these parasites. Additionally, knowledge of the reservoir hosts can inform vector control measures by identifying the key hosts that contribute to the persistence of the disease in the environment. This approach also helps us to predict and manage outbreaks, as changes in animal infection rates can signal shifts in disease risk. Furthermore, integrating animal reservoir data into public health strategies supports a one-health approach, addressing both human and animal health to control VL effectively.
6. Conclusions
According to the evaluations, although there is less data, CVL is endemic in several regions of India, and goats are both the disease’s primary host and possible reservoir. Goats have higher CVL infection rates than other animals, which raises the possibility that people could contract the disease from them. Goats may be involved in the evolution of VL, according to our results, but this does not necessarily mean that they are the reservoir hosts of
L. donovani.
Leishmania reservoir hosts have been taken into consideration when evaluating certain “reservoir criteria” from an ecological standpoint [
9]. Evaluating the condition of the sandflies, which consume blood from diseased reservoir hosts, is also crucial to limiting the disease’s spread. Leishmaniasis may have been presented for at-risk domestic animals as well as humans, due to a lack of surveillance and inaccurate diagnosis in the country. Evidence also suggests that this disease may be further emerging as a result of environmental changes and increased contact between pets and various organisms in the ecosystems. It is strongly advised that thorough measures need to be adopted to prevent and control this disease, especially in endemic areas, due to the rising trend of CVL in India.
An estimated 12 million people globally are thought to be affected by the significant cutaneous disease leishmaniasis. With an increase in travel to endemic areas, dermatologists must consider this entity in the differential diagnosis of any chronic skin lesion in patients who may have had a possible exposure for any length of time. The symptoms might vary and even be subclinical, making a diagnosis difficult. Although there are several treatment alternatives, they are far from optimal because of toxicity, access issues, low care rates, and growing resistance. If parasites are unable to multiply or reside inside a particular host, it is difficult to detect parasite DNA using molecular diagnostic techniques. Leishmania parasite DNA was discovered in domestic mammals after the period of highest transmission. Additional scientific and clinical research like host–pathogen interactions, genetic and proteomic analyses, drug resistance, immune responses, vaccine development, and integrated control strategies, along with epidemiological studies and improved animal models, are required to better understand the complicated host–species relation that underlies the many clinical presentations and to generate more potent treatments. The mammals’ infectious epidemiology still needs to be widely recognized. Public health and veterinary researchers have neglected the role of some animals in the maintenance and transmission of VL, and this aspect of the epizootiology of VL needs to be critically examined to update prevention and treatment programs in kala-azar endemic areas. Numerous investigations have been conducted on the transmission pathways, reservoir hosts, and ZVL regulation. While it is still obvious that domestic animals are the primary source of sandfly transmission, several possible transmission pathways and reservoir hosts have been discovered. There is currently no proof that non-sandfly transmission can continue an infection, with the possible exception of a small number of animals. Although sylvatic reservoirs are believed to exist in the old world, there is no compelling evidence that reservoir hosts other than domestic animals constitute a significant source of human infection. An accurate indicator of infectiousness would be a very helpful epidemiological tool, and further quantitative research on the prevalence of infectiousness in prospective reservoir hosts is required.
The goal of this analysis was to evaluate studies that looked at domestic animals’ potential for transmitting L. donovani in endemic regions, with a focus on how proximity and animal density may affect the incidence of human leishmaniasis. In the endemic environments found in India and in a few different countries that are endemic to visceral leishmaniasis, domestic animals play a significant role in domestic life. In various regions of the world, it has been shown that other animals, particularly dogs, are important reservoir species for the zoonotic transmission cycle of other visceralizing Leishmania parasites. To determine the involvement of dogs in L. donovani transmission in endemic countries, more research is required, including xenodiagnosis (sandflies can be used to detect Leishmania parasites in hosts). This leads us to the conclusion that these species only play a small part in the spread of L. donovani to humans. Infection in animal species should be observed during outbreaks as observatories and potential parasite sources because sandflies often feed on domestic mammals.