Animal Reservoirs of Zoonotic Tungiasis in Endemic Rural Villages of Uganda

Abstract

BackgroundAnimal tungiasis is believed to increase the prevalence and parasite burden in humans. Animal reservoirs of Tunga penetrans differ among endemic areas and their role in the epidemiology of tungiasis had never been investigated in Uganda.Methods and FindingsTo identify the major animal reservoirs of Tunga penetrans and their relative importance in the transmission of tungiasis in Uganda, a cross sectional study was conducted in animal rearing households in 10 endemic villages in Bugiri District. T. penetrans infections were detected in pigs, dogs, goats and a cat. The prevalences of households with tungiasis ranged from 0% to 71.4% (median 22.2) for animals and from 5 to 71.4% (median 27.8%) for humans. The prevalence of human tungiasis also varied among the population of the villages (median 7%, range 1.3–37.3%). Pig infections had the widest distribution (nine out of 10 villages) and highest prevalence (median 16.2%, range 0–64.1%). Pigs also had a higher number of embedded sand fleas than all other species combined (p<0.0001). Dog tungiasis occurred in five out of 10 villages with low prevalences (median of 2%, range 0–26.9%). Only two goats and a single cat had tungiasis. Prevalences of animal and human tungiasis correlated at both village (rho = 0.89, p = 0.0005) and household (rho = 0.4, p<0.0001) levels. The median number of lesions in household animals correlated with the median intensity of infection in children three to eight years of age (rho = 0.47, p<0.0001). Animal tungiasis increased the odds of occurrence of human cases in households six fold (OR = 6.1, 95% CI 3.3–11.4, p<0.0001).ConclusionAnimal and human tungiasis were closely associated and pigs were identified as the most important animal hosts of T. penetrans. Effective tungiasis control should follow One Health principles and integrate ectoparasites control in animals.

Tungiasis-associated morbidity in pigs and dogs in endemic villages of Uganda

“…Tungiasis also occurs in a wide range of domestic, peri-domestic and wild animals [ 12 – 14 ] usually alongside human tungiasis in endemic communities of South America and sub-Saharan Africa [ 12 – 15 ]. With the increasing number of international journeys with pets, animal tungiasis is also being detected in non-endemic countries [ 16 ].…”

“…Pigs and dogs have been reported as the major domestic animal hosts of zoonotic sand fleas in endemic countries [ 13 – 15 ]. In the study area, the odds of occurrence of animal tungiasis in a household increased with presence of human tungiasis, presence of pigs, with the number of animal species kept and with the size of the homestead [ 14 ]. This study aimed to systematically document the clinical pathology associated with sand flea infections in pigs and dogs in endemic villages in Uganda.…”

Mapping the Geographic Distribution of Tungiasis in Sub-Saharan Africa

“…These regional designations will serve as the basis for reporting the total population living in environmentally suitable areas. Tungiasis occurrences records (n = 86) (please see Supplementary Materials : Table S2 ) were assembled through a search of the literature from 1324–2019 [ 23 , 24 , 25 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 , 75 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 83 , 84 , …”

“…Thus, livestock densities were obtained from the Gridded Livestock of the World (v2.01) database at a 1~kilometer resolution from the Food and Agricultural Organization of the United Nations (FAO) (livestock.geo-wiki.org). These data include the densities of chickens [ 110 ], goats [ 24 ], and pigs [ 110 ]. Domestic animals serving as reservoirs for T. penetrans are numerous and include cats, dogs, chickens, goats, pigs, cattle, monkeys, and rats [ 7 , 15 ].…”

“…Ectopic infections of the genitals [ 21 ], eyelids [ 22 ], and tongue [ 23 ] have been documented. In resource-poor communities with low tetanus vaccination coverage, evidence points to an association between tungiasis and tetanus [ 16 , 24 ]. Individuals living with the disease often face social stigmatization and marginalization.…”