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Abstract. Background Tungiasis is common in resource-poor populations throughout Latin America, the. Caribbean, and sub-Saharan Africa, but epidemiologic ...
Tropical medicine rounds Oxford, UK International IJD Blackwell 0011-9059 45 Publishing Journal Ltd, Ltd of Dermatology 2006

Tungiasis: high prevalence, parasite load, and morbidity in a rural community in Lagos State, Nigeria Tungiasismedicine Ugbomoiko, Tropical in Lagos Ofoezie, rounds State, andNigeria Heukelbach

Uade Samuel Ugbomoiko, BSc MSc PhD, Ifeanyi Emmanuel Ofoezie, BSc MSc PhD, and Jorg Heukelbach, MD PhD

From the Department of Zoology, University of Ilorin, Ilorin, Nigeria, Department of Zoology, University of Nigeria, Nsukka, Nigeria, Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil, and School of Public Health, Tropical Medicine and Rehabilitation Sciences, James Cook University, Townsville, Qld, Australia Correspondence Jorg Heukelbach, MD, PhD Departamento de Saúde Comunitária Faculdade de Medicina Universidade Federal do Ceará Rua Prof Costa Mendes 1608, 5. andar Fortaleza, CE 60430-140 Brazil E-mail: [email protected]

Abstract Background Tungiasis is common in resource-poor populations throughout Latin America, the Caribbean, and sub-Saharan Africa, but epidemiologic data from Africa on this ectoparasitosis are scarce. Methods A cross-sectional study was carried out in a representative sample of a rural community in Lagos State, 54 km west of Lagos (Nigeria). In the dry season, 142 households of the community were randomly selected and visited. Family members were examined for the presence of tungiasis. The localization, number, and stage of penetrated fleas, as well as the associated morbidity, were documented. Results Five hundred and fifty-seven individuals were examined, 299 (53.7%) males and 258 (46.3%) females. In total, 252 (45.2%; 95% confidence interval, 41.1– 49.5) were infested with Tunga penetrans. The prevalence was highest between the ages of 5 and 14 years, decreased in adults, and increased again in the elderly. There was no statistically significant difference between the prevalence in males and females (47.2% vs. 43.0%; P = 0.3). Almost 95% of lesions were localized on the feet. Ten per cent of individuals presented with sand fleas on the hands and elbows. The median parasite load was six (interquartile range, 3–16). Individuals aged 60 years or over had significantly more lesions (median of 41 lesions; P < 0.01). About one-third of the study participants found it difficult to walk; in 10% of cases, fissures were present. Superinfection was common. Conclusions The prevalence of tungiasis and the parasite load were high, and the severity of the disease was considerable. The prevalence and parasite burden showed a characteristic distribution. In western Nigeria, tungiasis needs to be regarded as an important public health problem.

Introduction The jigger flea, Tunga penetrans, causes debilitating disease in resource-poor populations throughout Latin America, the Caribbean, and sub-Saharan Africa.1,2 The disease is a result of the female T. penetrans burrowing into the host’s skin, and thereafter undergoing an impressive hypertrophy. In recent years, the awareness of tungiasis as a public health problem has increased in some communities, but tungiasis is still a neglected disease of underprivileged urban and rural populations.2–4 The parasite originally occurred only in Latin America and the Caribbean. The sand flea was first reported in native indigenous populations from Haiti in 1525, and the first scientific description from Brazil dates back to the 17th century.1 It was probably introduced several times in the 17th, 18th and 19th centuries to West Africa as a result of the slave trade; however, the flea did not spread over the © 2007 The International Society of Dermatology

continent.5–7 Only at the end of the 19th century was T. penetrans dispersed throughout sub-Saharan Africa, after being carried in ballast sand on a ship traveling from Brazil to Angola.1,5,8,9 In subsequent decades, tungiasis has been reported from most countries on the continent, and has even been considered as “the greatest curse that has ever afflicted Africa.”2,7,9–11 Travelers on expeditions to Africa at the end of the 19th and the beginning of the 20th century reported communities in which inhabitants suffered from severe infestation and morbidity, such as suppuration, ulcers, gangrene, and difficulty in walking.9,12–15 Military operations in African colonial times were prejudiced as a result of the heavy infestation of soldiers’ feet, making walking difficult.8,10,16 Recently, severe tungiasis has been described in several deprived communities in Latin American and Caribbean countries, such as Argentina, Brazil, and Haiti.3,17–20 The current epidemiologic situation on the African continent is International Journal of Dermatology 2007, 46, 475–481

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not known in detail, and is mainly based on anecdotal observations and reports from returning travelers.21–23 One recent study from Cameroon reported a high prevalence in different provinces and considered the ectoparasitosis as an important public health problem.24 Several older studies from Nigeria reported a high prevalence and morbidity in the southern part of the country.25–29 Historic reports from Zimbabwe and Congo Brazzaville indicated that tungiasis was a major cause of tetanus infection in unvaccinated individuals.30,31 Thus, there is an urgent need for data from Africa on the epidemiology of the disease and the morbidity it causes in resource-poor populations. To fill this gap, we conducted a cross-sectional study in a representative population of a rural village in western Nigeria. Materials and Methods Study area and population This cross-sectional study was carried out in Erekiti, a rural community in Lagos State, about 54 km west of the city of Lagos, Nigeria (Fig. 1). The inhabitants of Erekiti are mainly subsistence farmers and fishermen. Women are traditional mat weavers. According to the National Population Commission of Lagos State, the total population of the community in 1999 was about 1200 individuals in 250 households. The mean monthly family income was 45US$. Roads leading to the community are unpaved and usually impassable during the rainy season. Housing conditions are precarious; many houses are made of bricks and are supplied with electricity, but about two-thirds of houses have no concrete floor. There is no community water supply; open wells and the nearby river serve as the source of water. In the area, pigs, goats, chickens, dogs, and cats roam freely. Malaria is endemic. The community can be regarded as characteristic of a small rural village in western Nigeria. Study design and data collection The study was conducted in the dry season (March 2006). Anecdotal data from the community under study and published data from elsewhere indicated the highest prevalence during the dry season.20,24 One hundred and forty-two households (643 individuals) of Erekiti were randomly selected using a table of random numbers, visited, and the family members interviewed regarding socio-demographic variables, using a pretested structured questionnaire. Thereafter, all present family members were examined clinically for the presence of tungiasis. To guarantee privacy, only the legs, feet, hands, and arms were examined. This approach has been considered as acceptable as, in hyperendemic communities, more than 99% of tungiasis lesions occur on the feet, legs, hands, and arms.32 If family members were not present, houses were revisited at a time when they were likely to be at home. International Journal of Dermatology 2007, 46, 475–481

Figure 1 Location of Nigeria and Lagos State

The following findings were considered to be diagnostic for tungiasis: an itching red-brownish spot with a diameter of 1–3 mm; a circular lesion presenting as a white patch with a diameter of 4–10 mm with a central black dot; a black crust surrounded by necrotic tissue; and partially or totally removed fleas leaving a characteristic sore in the skin. The location and number of lesions were recorded. They were staged according to the “Fortaleza classification”, in which stages I–III correspond to vital sand fleas © 2007 The International Society of Dermatology

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and stage IV to avital fleas.33 According to this classification, stage I is defined as the presence of adult fleas in the process of penetration (statu penetrandi ), stage II is defined as a developing lesion marked as a dark itching spot encircled by erythema, stage III indicates mature lesions presenting as a white circular area of about 1 cm in diameter with a dark central spot, and stage IV represents a dead parasite defined as a dark circular crust often surrounded by necrotic tissue. In addition, lesions manipulated with a needle, thorn, or similar instrument by the patient or a caregiver were documented. The following symptoms and signs associated with acute and/or chronic sand flea infestation were noted based on clinical examination: edema, ulcer, loss of a toenail, nail deformation, fissure, hyperkeratosis, desquamation of the skin, erythema, pustule, and suppuration. Difficulty in walking, itching, and pain were assessed using a structured questionnaire.

Data analysis Data were checked for entry errors and analyzed using the Epi Info software package (version 6.04d, Centers for Disease Control and Prevention, Atlanta, GA, USA). Ninety-five per cent confidence intervals for prevalences were calculated using the respective Epi Info modules. The chi-squared test was used to determine the differences in relative frequencies. Data not distributed normally were presented as the medians and interquartile ranges; differences in the medians between groups were assessed by the Wilcoxon test.

and 86.6% of the target population. Eighty-six individuals (13.4%) were not encountered at home, even after revisiting the houses, or refused to participate. Of the 557 included in the study, 299 (53.7%) were male and 258 (46.3%) were female. The median age was 12 years (interquartile range, 8– 24 years). Prevalence and localization of the lesions

In total, 252 individuals were infested, resulting in an overall point prevalence of 45.2% (Table 1). In general, tungiasis was more common at a younger age (median age: infested, 10 years; uninfested, 15 years; P < 0.0001). Interestingly, the prevalence followed a characteristic curve: it was highest between the ages of 5 and 14 years, decreased in adults, and increased again in the elderly. Prevalences stratified by age group are depicted in Table 1. Overall, there was no statistically significant difference between the prevalence in males and females (prevalence of 47.2% vs. 43.0%, respectively; P = 0.3). There was no statistically significant difference in the prevalence between the sexes in all age groups. All infested individuals had penetrated fleas on the feet, and almost 95% of the lesions were localized on the feet. About two-thirds of patients had periungual lesions. Ten per cent presented with sand fleas on ectopic sites (hands and elbows) (Table 2). Parasite load

Ethical considerations The study was approved by the Ethical Committee of the Badagary Local Government Public Health Board, which is made up of medical and administrative personnel. The community leaders of Erekiti approved the study. Oral consent was obtained from all study participants or, in the case of minors, from their caregivers. Data were kept strictly confidential.

Results Five hundred and fifty-seven individuals were examined. This represents 45.2% of the total population of the community Table 1 Individuals examined, prevalence,

and parasite load of tungiasis in the study population, stratified by age group

In total, 3111 lesions were counted in the 252 infested individuals (Table 2). The median number of lesions per infested individual was six (interquartile range, 3–16). The maximum number of lesions encountered was 87 penetrated fleas. Sixty-two individuals (24.6%) had one or two lesions, and 89 (35.3%) had 10 or more lesions. Males showed a higher parasite load (median of seven lesions; interquartile range, 3–19) than females (median of four lesions; interquartile range, 2–13); however, this difference was not statistically significant (P = 0.06). The pattern of vital, avital, and manipulated lesions was similar in both sexes.

Age group (years)

Examined n

Positive n

Prevalence (%) (95% confidence interval)

Parasite load* median (interquartile range)

≤4 5–9 10–14 15–19 20–39 40–59 ≥ 60 Total

49 159 121 71 82 58 17 557

19 102 77 9 13 23 9 252

38.8 (25.2–35.8) 64.2 (56.2–71.6) 63.6 (54.4–72.2) 12.7 (6.0–22.7) 15.9 (8.7–25.6) 39.7 (27.0–53.4) 52.9 (27.8–77.0) 45.2 (41.1–49.5)

4 (2–8) 5 (2–11) 9 (2–19) 4 (4–18) 8 (4–13) 9 (3–17) 41 (6–57) 6 (3–16)

*For those infested with tungiasis. © 2007 The International Society of Dermatology

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Table 2 Topographic distribution in individuals with tungiasis

(n = 252)

Topographic site

Number of lesions (% of total number)

Number of individuals with tungiasis at certain sites (%)*

Feet Toes† Periungual Heels Soles/plantar Instep/lateral rim Ectopic sites Fingers Wrists and elbows Total

2946 (94.7) 1362 (43.8) 555 (17.8) 655 (21.1) 242 (7.8) 132 (4.2) 165 (5.3) 100 (3.2) 65 (2.1) 3111 (100)

252 (100) 234 (92.9) 170 (67.5) 147 (58.3) 68 (27.0) 60 (23.8) 26 (10.3) 19 (7.5) 17 (6.7) 252 (100)

*Lesions occurred on more than one site. †Without periungual sites.

Although in the age groups under 59 years, the median parasite load did not differ considerably (overall median of six lesions), individuals aged 60 years or over had significantly more lesions (P < 0.01): a median of 41 lesions per individual (Table 1). Interestingly, the relative number of manipulated lesions in the older age group was considerably lower than in the other age groups, and the number of avital lesions (indicating that the lesions had not been removed by the patient) was higher (Fig. 2). Morbidity

The morbidity associated with tungiasis was considerable and severe in many cases. Itching and erythema were the most common findings (Table 3). About one-third of individuals found it difficult to walk and, in 10% of cases, fissures were

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present. Superinfection indicated by the presence of pustules, suppuration, and erythema was also common (Table 3). Discussion Current epidemiologic data on tungiasis are virtually nonexistent from African countries; however, control measures can only be planned when the burden of disease, transmission dynamics, and risk factors are known in detail. As a first step, we have conducted a cross-sectional study in a typical rural community in western Nigeria. In our study, the overall prevalence (45.2%) and parasite load (median of six lesions) were high, and the severity of disease was considerable; tungiasis-associated morbidity, such as difficulty in walking and deformation of the toenails, was commonly reported. The overt clinical manifestations associated with infestation have been reported in detail by various authors in other endemic areas.3,34,35 Table 3 Tungiasis-associated symptoms and signs (n = 252) n (%) Itching Erythema Difficulty in walking Deformation of toenails Desquamation of skin Loss of toenails Edema Pustule Ulcers Hyperkeratosis Fissures Generalized pain Suppuration

114 (53.2) 111 (44.0) 81 (32.1) 69 (27.4) 48 (19.0) 41 (16.3) 37 (14.7) 35 (13.9) 30 (11.9) 28 (11.1) 27 (10.7) 25 (9.9) 18 (7.1)

Figure 2 Median numbers of vital, avital,

and manipulated lesions per individual, stratified by age group. Vertical bars indicate interquartile ranges International Journal of Dermatology 2007, 46, 475–481

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Several studies have reported tungiasis from Nigeria.25–29,36 The most recent was a small survey in schoolchildren performed in 1991, in which 22% of the children were found to be infested;29 however, the study was not carried out on a representative sample of the population, and the parasite load and associated morbidity were not reported. Our study is the first comprehensive survey on tungiasis and associated morbidity from a representative population in Nigeria. One recent publication has indicated that the ectoparasitosis is a major public health problem in Cameroon.24 Njeumi et al.24 reported a prevalence of about 50% in schoolchildren from different communities in the West Province of this neighboring country to Nigeria. In addition, historic studies have reported high prevalences in humans and pigs from several other sub-Saharan countries.25–31,37–39 It can be assumed that the disease still prevails in many underprivileged communities in Africa. The prevalence found in our study was similar to that reported during the dry season in poor rural communities and urban slums in Brazil,17,18,20 and higher than that reported in communities in Trinidad;40,41 however, the data from Trinidad are difficult to compare, as it is not clear whether these communities were examined during the dry season, when the highest prevalence is expected.20 The S-shaped prevalence pattern, with the highest prevalence in the 5–14-year age group and ≥ 60-year age groups, has been reported previously from a rural community in Brazil.17 Other studies have also reported children to be commonly affected, but have not confirmed the increase in prevalence in the elderly population.18,41,42 The S-shaped curve cannot be explained by acquired immunity, but suggests that the marked increase in the oldest age group is caused by factors other than the host’s immune system. The different prevalence may be influenced to an important degree by the different exposure and behavior with age. For example, middle-aged groups are composed mainly of the working population who spend more time outside the endemic community and may have different disease-related behavior (i.e. remove embedded fleas more rigorously). In contrast, school-aged children and the elderly have a longer duration of interaction with the endemic environment without adopting appropriate protective behavior – the majority of them walk barefoot or, at best, wear slippers. Interestingly, high exposure is correlated with parasite load.43 The high prevalence in children is probably a result of their greater exposure (playing barefoot in the community), whereas older individuals may find it more difficult to remove embedded fleas. Anecdotal observations have revealed that skillful older children carry out flea extraction for their friends and younger children at school (U. S. Ugbomoiko, unpublished observation). Such assistance is rarely rendered to less skillful, poor-sighted, and sometimes even helpless older individuals. Thus, the high proportion of avital lesions and low pro© 2007 The International Society of Dermatology

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portion of manipulated lesions in the elderly, relative to younger age groups (Fig. 2), may be attributed to the fact that fleas are not removed and finish their natural history embedded in the host’s skin. Elderly people of endemic communities are at high risk of severe tungiasis infestation. This is of additional concern, as tungiasis may be a port of entry for Clostridium bacteria, and the elderly usually show the lowest tetanus vaccination coverage. We did not find any difference in the prevalence between males and females. Indeed, data on sex distribution are inconsistent and, similar to age, are probably related to different exposure and disease-related behavior. For example, Carvalho et al.18 observed more females than males to be affected in south Brazil, whereas other studies from Brazil, Trinidad, and Nigeria found more males to be affected,25,25,27,41,42 or no significant difference between the sexes.17 The data on associated pathology show that tungiasis cannot be regarded as a nuisance, but as an important health problem in Nigeria. The ectoparasitosis is a public health problem, not only in Erekiti, but possibly in neighboring communities. Important morbidity has been reported by key informants in these communities. In addition, tungiasis has also been reported from other states in Nigeria (U. S. Ugbomoiko, unpublished observation). Tungiasis is clearly a disease of the very poor, and improvement in housing and hygiene conditions will provide the most effective approach, not only to control tungiasis, but also other parasitic diseases associated with poverty.44 The control of tungiasis requires an integrated approach, including clinicians, public health specialists, veterinarians, and biologists, with a consideration also of the animal reservoirs.4,44 Furthermore, public policies promoting sustainable changes in the quality of life and improved health will reduce the incidence and parasite burden in affected communities. We have shown that tungiasis is extremely common in a resource-poor community in Nigeria, and that the parasite load and morbidity are high. In Nigeria, severely infested schoolchildren and families are socially stigmatized; infested schoolchildren are absent from schools, traders are confined to their houses, and farmers are compelled to suspend agricultural activities (U. S. Ugbomoiko, unpublished observation). Future studies on the risk factors, animal reservoirs, and disease-related behavior of affected populations are needed to design measures to control severe disease caused by T. penetrans in endemic communities in Nigeria. Acknowledgments We are indebted to the Baales of Erekiti and Ajido Erekiti communities for supporting the study, and thank Mr Durotimi Ashade and Mr Ola Avhose for skillful assistance. We thank William Brennan Arden for providing the maps. International Journal of Dermatology 2007, 46, 475–481

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The generous support, by a research leave, from the authority of the University of Ilorin, Nigeria, is acknowledged. J.H. received an Endeavour Australia Research Fellowship.

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20 Heukelbach J, Wilcke T, Harms G, et al. Seasonal variation of tungiasis in an endemic community. Am J Trop Med Hyg 2005; 72: 145 – 149. 21 Swaminathan A, Gosbell IB, Zwar NA, et al. Tungiasis in recently arrived African refugees. Med J Aust 2005; 183: 51. 22 Cantarella C. In Africa, it isn’t Always the Big Game That’s Out to Get You, 1998. URL www.cnn.com/TRAVEL/ PURSUITS/OUTDOORS/9808/Jiggers [accessed on 9 November 2006]. 23 Franck S, Feldmeier H, Heukelbach J. Tungiasis: more than an exotic nuisance. Travel Med Infect Dis 2003; 1: 159 – 166. 24 Njeumi F, Nsangou C, Ndjend AG, et al. Tunga penetrans au Cameroun. Rev Méd Vét 2002; 153: 176 – 180. 25 Ade-Serrano MA, Ejezie GC. Prevalence of tungiasis in Oto-Ijanikin village, Badagry, Lagos State, Nigeria. Ann Trop Med Parasitol 1981; 75: 471– 472. 26 Ejezie GC. The parasitic diseases of school children in Lagos State, Nigeria. Acta Trop 1981; 38: 79 – 84. 27 Arene FO. The prevalence of sand flea (Tunga penetrans) among primary and post-primary school pupils in Choba area of the Niger Delta. Public Health 1984; 98: 282 – 283. 28 Atunrase JO, Awobodu CA, Fawole CA, et al. Some observations on tungiasis in Yorubaland, Western Nigeria. West Afr Med J 1952; 3: 181– 182. 29 Nte AR, Eke FU. Jigger infestation in children in a rural area of Rivers State of Nigeria. West Afr J Med 1995; 14: 56 – 58. 30 Obengui. La tungose et le tétanos au C.H.U. de Brazzaville. Dakar Med 1989; 34: 44 – 48. 31 Tonge BL. Tetanus from chigger flea sores. J Trop Pediatr 1989; 35: 94. 32 Heukelbach J, Wilcke T, Eisele M, et al. Ectopic localization of tungiasis. Am J Trop Med Hyg 2002; 67: 214 – 216. 33 Eisele M, Heukelbach J, van Marck E, et al. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: I. Natural history of tungiasis in man. Parasitol Res 2003; 90: 87 – 99. 34 Feldmeier H, Eisele M, Saboia-Moura RC, et al. Severe tungiasis in underprivileged communities: case series from Brazil. Emerg Infect Dis 2003; 9: 949 – 955. 35 Feldmeier H, Van Eisele MME, Mehlhorn H, et al. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: IV. Clinical and histopathology. Parasitol Res 2004; 94: 275 – 282. 36 Ade-Serrano MA, Olomolehin OG, Adewunmi A. Treatment of human tungiasis with niridazole (Ambilhar): a double-blind placebo-controlled trial. Ann Trop Med Parasitol 1982; 76: 89 – 92. 37 Cooper JE. An outbreak of Tunga penetrans in a pig herd. Vet Records 1967; 80: 365 – 366. 38 Cooper JE. Tunga penetrans infestation in pigs. Vet Records 1976; 98: 472. 39 Goldsmid JM. Tungiasis in Zimbabwe. Cent Afr J Med 1981; 27: 151 – 152. 40 Chadee DD. Distribution patterns of Tunga penetrans within a community in Trinidad, West Indies. J Trop Med Hyg 1994; 97: 167 – 170. © 2007 The International Society of Dermatology

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41 Chadee DD. Tungiasis among five communities in south-western Trinidad, West Indies. Ann Trop Med Parasitol 1998; 92: 107 – 113. 42 Wilcke T, Heukelbach J, Cesar Saboia MR, et al. High prevalence of tungiasis in a poor neighbourhood in Fortaleza, Northeast Brazil. Acta Trop 2002; 83: 255 – 258.

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43 Feldmeier H, Kehr JD, Poggensee G, et al. High exposure to Tunga penetrans (Linnaeus, 1758) correlates with intensity of infestation. Mem Inst Oswaldo Cruz 2006; 101: 65 – 69. 44 Heukelbach J. Revision on tungiasis: treatment options and prevention. Expert Rev Anti Infect Ther 2006; 4: 151–157.

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