- Email: [email protected]
Identifying risk factors for tungiasis and heavy infestation in a resource-poor community in northeast Brazil
Transactions of the Royal Society of Tropical Medicine and Hygiene (2006) 100, 371—380
Identifying risk factors for tungiasis and heavy infestation in a resource-poor community in northeast Brazil Marion Muehlen a,b,∗, Hermann Feldmeier a, Thomas Wilcke a, Benedikt Winter a, J¨ org Heukelbach c,d a
Department of Medical Microbiology, Institute of Infectious Medicine, Charit´ e University Medicine Berlin, Campus Benjamin Franklin, Berlin, Germany b Department of Infectious Disease Epidemiology, Robert Koch Institute, Seestrasse 10, 13353 Berlin, Germany c Mandacaru Foundation, Fortaleza, Brazil d Department of Community Health, Medical Faculty, Federal University of Cear´ a, Fortaleza, Brazil Received 11 April 2005 ; received in revised form 18 June 2005; accepted 21 June 2005 Available online 17 November 2005 KEYWORDS Tungiasis; Tunga penetrans; Sand flea; Epidemiology; Risk factor; Brazil
Summary Tungiasis is a neglected parasitic skin disease caused by penetration of female sand fleas into the epidermis. The ectoparasitosis is widespread in resourcepoor communities in South America, the Caribbean and sub-Saharan Africa. To identify risk factors for the presence of sand fleas and severe infestation in an endemic community, we examined the entire population of a traditional fishing village for the presence of embedded sand fleas and determined the number and type of lesions. Demographic, behavioural and environmental characteristics of the population were assessed using a structured questionnaire. Multivariable analysis showed that both occurrence of tungiasis and heavy infestation were significantly related to poor housing conditions (odds ratio [OR] = 4.7, 95% CI 1.4—15.8), lack of health education (OR = 4.1, 95% CI 2.0—8.6) and presence of animals on the compound (OR = 1.9, 95% CI 1.1—3.4). Contrary to common belief, a protective effect of frequent use of closed footwear could not be demonstrated. Based on the population attributable fractions calculated for the major risk factors identified, we conclude that several low-cost interventions would have a considerable impact on the occurrence of tungiasis and heavy infestation. © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
1. Introduction ∗
Corresponding author. Tel.: +49 1888 7543910; fax: +49 1888 7543533. E-mail address: [email protected] (M. Muehlen).
Tungiasis is a neglected parasitic disease caused by the penetration of the female sand flea Tunga
0035-9203/$ — see front matter © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2005.06.033
372 penetrans (jigger flea) into the epidermis of its host. The ectoparasitosis occurs in Central and South America, the Caribbean and sub-Saharan Africa (Macias and Sashida, 2000). In Brazil, it is widespread in economically depressed communities from Rio Grande do Sul State in the south to Roraima in the north of the country (Matias, 1989). In typical endemic areas, age-specific prevalence follows an S-shaped curve, increasing sharply in children 5 to 14 years old, declining in prevalence during adolescence and increasing again in older individuals (Wilcke et al., 2002). The parasite burden is unevenly distributed within an affected population. Whereas the majority of infested individuals harbour between one and ten fleas, a minority may carry up to 150 embedded parasites (Muehlen et al., 2003). Tungiasis is associated with considerable morbidity, such as intense local inflammation, deformation and auto-amputation of digits, deformation and loss of nails, formation of fissures and ulcers, gangrene, difficulty walking and gripping (when lesions are located on the hands), as well as sleep disturbances due to severe itching and pain (Chadee, 1998; Feldmeier et al., 2002; Matias, 1989). Tungiasis may serve as an entry port for Clostridium tetani (Greco et al., 2001), rendering non-immunized individuals susceptible to tetanus. Individuals with a high parasite burden are therefore more vulnerable to severe disease. Why some individuals are heavily parasitized, but others harbour only a few sand fleas remains unknown. Environmental or behavioural factors, which could explain disease occurrence and severity of infestation at community level, have never been studied. To identify risk factors for infestation by T. penetrans and severe disease, a cross-sectional survey was performed in a traditional fishing village in Cear´ a State, as part of a comprehensive study on parasitic skin diseases in resource-poor communities in northeast Brazil. All individuals were interviewed and examined for embedded sand fleas. Demographic, behavioural, socio-economic and environmental risk factors were recorded and analysed.
2. Materials and methods 2.1. Study area and population sThe study was performed in Balbino village, municipality of Cascav´ el, Cear´ a State, northeast Brazil. The village is a traditional fishing community situated 60 km south of Fortaleza and was relatively isolated until recently. It is inhabited by 139
M. Muehlen et al. families with a total population of 620 with little fluctuation. Houses are located on relatively large compounds surrounded by wire fences. The village is covered by the government’s Family Health Program (Programa de Sa´ ude da Fam´ılia) and has two health agents, one for children and the other for the population in general. The health agents are responsible for health education and referral of patients to the health centre in Cascav´ el town.
2.2. Study design During a preparatory phase, we made contact with community leaders and held meetings with local ˜o dos moradores) at which associations (associac¸a the objectives of the study were explained. It was made clear that participation in the study was totally voluntary and that nobody who refused to participate would face a disadvantage. All inhabitants of the village were eligible for the study, provided they had spent at least 4 days per week, on average, in the village during the previous 3 months. A census was performed and each house was mapped using geographic positioning system methods. Data were collected by a door-to-door survey. If family members were absent during the survey, the house was revisited on two further occasions. Missing individuals were invited to come to the local health centre on the following days. Family members absent on all three occasions and who did not present for examination at the health centre were not included in the survey. In order to identify risk factors for the presence of tungiasis and severe infestation, relevant demographic, socio-economic, behavioural, educational and environmental information was collected from household heads (usually the mothers) in the form of structured interviews using a pre-tested questionnaire. Demographic, behavioural and educational risk factors were assessed for each household member, whereas environmental and socio-economic factors were assessed at the household level. Data were collected between June 20 and July 30, 2001, i.e. at the beginning of the dry season. Each individual was thoroughly examined for newly penetrated and embedded sand fleas and lesions were staged using a protocol developed previously (Muehlen et al., 2003). In order not to overlook fleas embedded at ectopic sites, the whole body (except the genital region) was examined. An arbitrarily defined number of lesions (viable, dead or manipulated) was used to classify the infestation as weak (1—5 lesions), moderate (6—30 lesions) and heavy (>30 lesions).
Risk factors for tungiasis in northeast Brazil
2.3. Ethical considerations The study protocol was reviewed by the Ethical Committee of the Cascavel Municipality Board, comprising health professionals, administrative authorities and community representatives. Individuals were only enrolled if they, or, in the case of minors, the legal carers, gave informed oral consent. Family leaders were assured that all data would be handled confidentially. Risk factors identified were explained during a community meeting at the end of the study and villagers were encouraged to modify behaviour and environmental determinants putting them at risk for tungiasis. As more than 50% of the villagers were known to be infected with intestinal helminths and/or ectoparasites, all inhabitants were offered free anthelminthic treatment at the end of the study (Heukelbach et al., 2004b).
2.4. Bias To avoid inter-observer bias, the clinical examination and the interviews were always performed by the same investigators (T.W. and M.M., respectively). The clinical examination was performed first and the interviews were carried out some days later. The interviewer remained blinded to the results of the clinical examination. As the whole study was conducted within a period of 5 weeks, intra-observer bias was negligible. Non-response bias was reduced by active recruitment and nonparticipation bias was minimized by a door-to-door survey. In an effort to reduce selection bias, we defined the whole village as our target population. Although households were visited up to three times, 13.1% of the inhabitants, mainly adult males who were out fishing, were missed. This resulted in an underrepresentation of males aged 20—39 years. Recall bias was reduced by limiting the recall period to 3 months prior to the survey. However, for questions referring to events occurring at irregular intervals, such as having received anthelminthic treatment, a recall bias cannot be excluded.
2.5. Statistical analysis Data was entered in EpiInfo version 6.04d (CDC, Atlanta, GA, USA) and checked for data entry errors, then transferred to SPSS 11.0 (SPSS Inc., Chicago, IL, USA) for data analysis. The 2 test and Fisher’s exact test were used to determine the significance of differences of relative frequencies. Putative risk factors were first assessed by univariate analysis, and odds ratios (OR) and the respective 95% CI were calculated. Variables
373 significantly (P < 0.05) related to the occurrence of tungiasis or severity of infestation in the univariate analysis were entered into a logistic regression analysis model with stepwise forward inclusion of each variable. Factors significantly associated with the occurrence of tungiasis in the univariate analysis but assessed only in individuals older than 15 years, such as level of education, were not included in the model. To determine the potential impact of reducing the prevalence of certain exposures on the occurrence of tungiasis in this community, population attributable fractions (PAF) were calculated for the risk factors with the highest odds ratios and for those exposure variables for which an intervention seems feasible (Kleinbaum et al., 1982).
3. Results The village consisted of 139 families with a total of 620 individuals. Of these, 605 fulfilled the inclusion criterion, i.e. having been present in the village at least 4 days per week during the previous 3 months. Eighty-one individuals (66 males and 15 females) were not encountered on any of three survey visits, reducing the study population to 524. All 524 individuals consented to being interviewed, and 496 agreed to being examined for the presence of sand fleas. Thus, the number of individuals available for the assessment of risk factors was 496, belonging to 132 families (95.0% of all families). There was a significant difference between males (42.7%) and females (57.3%) in the study population (P = 0.05). This was due to an overrepresentation of females >20 years of age. The socio-economic characteristics of the study population are summarized in Table 1. Of adolescents 15 years and older and adults, 26.3% were wholly illiterate, and only 16.4% had completed primary school. Only 57.2% had some basic knowledge of reading and writing. Of the 132 households, 99 (75%) had electricity, but only 26 (19.7%) had a shower in the house. The overall prevalence of tungiasis was 51.0%; 70.4% of the infested individuals had between one and five lesions, 20.6% between six and 30 lesions and 9.1% were considered heavily infested (>30 lesions). The proportion of mild, moderate and heavy infestation changed similarly with increasing age (Figure 1). The results of univariate analysis are shown in Table 2. Age <15 and ≥60 years were highly significant risk factors for tungiasis (P < 0.001 and P = 0.002 respectively). Houses located on dunes, consisting of crude adobe walls or palm stems and leaves, with a floor of sand and without
374
M. Muehlen et al.
Table 1 Geographic and socio-economic characteristics of the study population (132 households) Frequency Location House situated next to/on: Laterite road Road with sand surface Swamp Dune
43.2 39.4 3.0 14.4
Distance to beach (m) >300 100—300 <100
108 21 3
81.8 15.9 2.3
Housing Type of construction Brick Plastered adobe Crude adobe Palm stems and leaves
65 21 31 15
49.2 15.9 23.5 11.4
87 34 11
65.9 25.8 8.3
110 18 4
83.3 13.6 3.0
Waste disposal Public collection Thrown on compound Burned and buried
55 5 72
41.7 3.8 54.5
Water Own well Public supply system Public well
112 4 16
84.8 3.0 12.1
125 111 91 47
94.7 84.1 68.9 35.6
Healthcare Health agent visits to the household Monthly 67 Every 3 months 31 No visit at all 34
50.8 23.5 25.8
Economy Monthly income per household (R$)b 0—180 80 >180 52
60.6 39.4
Age (years) 0—4 5—9
10.1 15.3
Sanitation Toilet Latrine on compound Defecation on compound Sewage system connection
Animals Animals on compound Dogs Cats Othersa
50 76
10—14 15—19 20—39 40—59 ≥60
(%)
57 52 4 19
Type of floor Concrete/tiles Clay soil Sand
Table 1 (Continued ) Frequency
(%)
66 65 111 80 48
13.3 13.1 22.4 16.1 9.7
a
Cows, horses, donkeys, goats, pigs. R$180 corresponds to the minimal Brazilian wage at the time of the survey and is equivalent to ∼90US$. b
electricity were significantly related to infestation by T. penetrans (all P < 0.001). Other significant risk factors were inappropriate waste disposal (P < 0.001), absence of latrines (P = 0.01), as well as overcrowding (≥7 persons/household, P < 0.02). Income was also a significant determinant of tungiasis. In households with a per capita income of ≤60 R$/month, the odds of being affected by tungiasis were twice as high as in individuals with a per capita income >60R$ (P = 0.001). Illiterate individuals were approximately five times more likely to be affected by tungiasis than others (P < 0.001). In persons 15 years and older, the regular use of a deodorant or a body lotion after bathing seemed to have a protective effect (P < 0.001). In households reporting insecticide use in the house during the three previous months, individuals were significantly less affected by tungiasis (OR = 0.36, 95% CI 0.24—0.54, P < 0.001). On the other hand, the regular use of traditional remedies intended to prevent the penetration of sand fleas was associated with seven-fold odds for tungiasis (P < 0.001). The presence of dogs and cats on the compound were also significant risk factors for tungiasis (P < 0.01).
Figure 1 Prevalence of tungiasis in the respective age groups according to severity of infestation. Column height indicates overall prevalence in the age group.
Univariable analysis of demographic, socio-economic, behavioural, educational and environmental risk factors (n = 496)
Exposure variable Demographic characteristics Sex Age group (years)
Persons/household
Housing House situated next to/on:
Distance to beach (m)
Type of construction
Type of floor
Rooms/house
Electricity Water supply
Toilet
Waste disposal
Frequency of tungiasis
Any degree of infestation
n
(%)
OR (95% CI)
Female Male 0—4 5—9 10—14 15—19 20—39 40—59 ≥60 1—3 4—6 ≥7
284 212 50 76 66 65 111 80 48 86 258 152
48.2 54.7 58.0 76.3 69.7 29.2 35.1 42.5 58.3 43.0 49.2 58.6
Reference 1.30 (0.89—1.88) 3.34 (1.44—7.85) 8.23 (3.62—19.02) 5.57 (2.47—12.69) Reference 1.31 (0.64—2.68) 1.79 (0.85—3.81) 3.39 (1.44—8.04) Reference 1.14 (0.76—2.16) 1.36 (1.06—3.31)
Laterite road Road with sand surface Swamp Dune <100 100—300 >300 Brick Plastered adobe Crude adobe Palm stems and leaves Concrete/tiles Clay soil Sand ≥6 4—5 1—3 Yes No Public supply system Own well Public wella Sewage system connection Defecation on compound Latrine on compound Public collection Burned and buried Thrown on compound
213 192 15 76 10 94 392 232 81 133 50 310 157 29 132 300 64 373 123 16 433 47 11 68 417 201 274 21
40.8 49.0 53.3 84.2 30.0 41.5 53.8 34.5 58.0 69.9 66.0 42.3 61.8 86.2 40.9 51.3 70.3 43.7 73.2 56.3 48.0 76.6 27.3 70.6 48.4 42.3 55.1 81.0
Reference 1.39 (0.92—2.10) 1.66 (0.52—5.30) 7.72 (3.78—16.10) Reference 1.65 (0.35—8.69) 2.7 (0.6—13.47) Reference 2.63 (1.52—4.56) 4.42 (2.72—7.18) 3.69 (1.85—7.40) Reference 2.21 (1.46—3.34) 8.54 (2.74—29.71) Reference 1.52 (0.99—2.36) 3.42 (1.73—6.83) Reference 3.51 (2.19—5.64) Reference 0.72 (0.24—2.15) 2.55 (0.66—9.94) Reference 6.40 (1.34—34.4) 2.51 (0.6—12.1) Reference 1.68 (1.14—2.46) 5.80 (1.75—21.21)
Presence of heavy infestation P value
OR (95% CI)
0.15 0.002 <0.001 <0.001
2.24 2.74 1.29 3.74
(0.94—5.43) (0.41—22.63) (0.17—11.49) (0.67—27.22)
P value
0.047 0.40 1.00 0.16
0.42 0.10 0.002
1.49 (0.25—11.43) 0.00 (0.00—3.31) 3.66 (0.59—28.74)
1.00 0.20 0.13
0.32 0.02
0.88 (0.31—2.62) 0.36 (0.08—1.50)
0.80 0.11
0.10 0.34 <0.001
3.99 (0.75—28.15) 16.23 (1.47—180.65) 25.94 (5.45—169.12)
Risk factors for tungiasis in northeast Brazil
Table 2
0.065 0.02 < 0.001
0.74 0.20
Undefined Undefined
1.00 1.00
0.0002 <0.001 <0.001
Undefined Undefined Undefined
0.02 < 0.001 < 0.001
<0.001 <0.001
3.91 (1.42—11.08) 11.29 (3.05—41.69)
0.002 0.0003
0.046 0.001
4.15 (0.91—26.27) 6.72 (1.18—49.80)
0.04 0.016
<0.001
6.49 (2.64—16.26)
< 0.001
0.52 0.20
0.16 (0.04—0.77) 0.89 (0.17—5.00)
0.02 1.00
0.014 0.17
0.60 (0.09—4.84) 0.18 (0.003—1.31)
0.62 0.07
0.006 0.0007
1.60 (0.63—4.12) 1.21 (0.03—9.81)
0.30 0.60
375
376
Table 2 (Continued ) Exposure variable Shower in the house Socio-economic characteristics Monthly income per household (R$)b
Income/capita (R$/month) Educationc
Behaviour characteristics Use of shoes Health care Washes daily Use of soap Use of deodorant/body lotionc Use of traditional medicine Insecticide use in last 90 days Health agent visits the household
Domestic animals Dogs Cats Other animalsd
Any degree of infestation
Presence of heavy infestation
Yes No
n 84 412
(%) 26.2 56.1
OR (95% CI) Reference 3.60 (2.07—6.29)
>200 101—200 0—100 >60 ≤60 Primary school completed Primary school not completed Illiterate
182 185 129 112 384 50 240 80
45.6 46.5 65.1 37.5 54.9 6.6 45.4 57.5
Reference 1.04 (0.67—1.60) 2.23 (1.36—3.64) Reference 2.03 (1.29—3.21) Reference 2.01 (0.91—4.51) 4.80 (2.01—11.64)
0.06 <0.001
Frequent Seldom/never
170 326
43.5 54.9
Reference 1.58 (1.07—2.34)
Yes No Yes No Yes No No Yes No Yes Monthly Once in the last 3 months Never
492 4 476 20 267 37 420 76 308 188 308 105 83
50.8 75.0 50.4 65.0 35.2 70.3 44.8 85.5 60.4 35.6 51.9 43.8 56.6
Reference 2.90 (0.27—72.93) Reference 1.83 (0.67—5.16) Reference 4.35 (1.95—9.85) Reference 7.29 (3.61—15.08) Reference 0.36 (0.24—0.54) Reference 0.72 (0.45—1.15) 1.21 (0.72—2.03)
No Yes No Yes No Yes
81 415 134 36 326 170
33.3 54.5 41.8 54.4 53.7 45.9
Reference 2.39 (1.41—4.07) Reference 1.66 (1.09—2.54) Reference 0.73 (0.50—1.08)
P value
OR (95% CI)
P value
<0.001
Undefined
0.02
0.87 0.0007
2.54 (0.72—9.82) 4.56 (1.32—17.22)
0.11 0.005
0.001
1.24 (0.43—3.84)
0.67
Undefined Undefined
0.34 0.08
0.016
6.68 (1.51—41.38)
0.003
0.34
6.23 (0.11—80.14)
0.2
0.2
5.16 (1.33—18.41)
0.016
<0.001
2.53 (0.51—10.92)
0.17
<0.001
7.68 (3.17—18.69)
<0.001
<0.001
0.20 (0.05—0.72)
0.004
0.15 0.45
0.73 (0.16—2.83) 3.77 (1.48—9.59)
0.77 0.003
0.0005
2.42 (0.54—15.16)
0.28
0.012
2.96 (0.83—12.61)
0.068
0.099
0.84 (0.33—2.11)
0.70
There were three public wells, two of which were functioning. One was in front of the school and health centre, the other in a poorer part of the village where most houses did not have a well on the compound. Water was supplied by the municipality free of charge. b At the time of the survey 1US$ was equivalent to ∼2R$. c Only for individuals ≥15 years of age. d Cows, horses, mules, goats and pigs.
M. Muehlen et al.
a
Frequency of tungiasis
Risk factors for tungiasis in northeast Brazil Table 3
377
Multivariable analysis after adjustment for age and sexa Presence of tungiasis AOR (95% CI)
Being of female sex House built on dune or swamp House built of adobe/palm leaves Floor made of sand Floor of clay soil Having a dog on the compound Use of traditional medicine Insecticide use in last 3 months
Presence of heavy infestation P value
2.44 (1.21—4.94) 1.87 (1.16—3.00) 4.71 (1.41—15.78)
0.031 0.010 0.012
1.89 (1.06—3.36) 4.07 (1.93—8.56) 0.55 (0.36—0.85)
0.031 <0.001 0.007
AOR (95% CI)
P value
0.36 (0.14—0.92) 12.73 (2.76—58.71)
0.032 0.001
10.29 (2.71—39.06) 3.41 (1.21—9.61)
0.001 0.021
4.96 (2.01—12.22)
<0.001
AOR: adjusted odds ratio. a Only statistically significant values are given.
Table 4
Population attributable fraction
House built on dune or near swamp House built of crude adobe House built of palm stems/leaves House with clay/sand floor Defecation on compound Waste on compound Not wearing shoes Dog on compound
OR
AR
% exposed among cases
PAF (%)
4.7 3.0 2.0 2.6 2.6 4.3 1.6 2.4
0.787 0.667 0.50 0.615 0.615 0.767 0.375 0.583
28.5 36.8 13.0 48.2 19.0 66.4 70.8 89.3
22.44 24.53 6.50 29.66 11.69 50.96 26.55 52.09
OR: odds ratio. AR: attributable risk, calculated as (OR−1)/OR, is the risk of tungiasis in the exposed due to the exposure (also termed ‘excess risk’). PAF: population attributable fraction, calculated as % exposed among cases × (OR−1)/OR, is the fraction of cases which would not have occurred if an exposure had been avoided, assuming the exposure is casual and the other risk factors in the population remain unchanged (according to Kleinbaum et al., 1982, to adjust for confounding).
Several risk factors remained highly significant after multivariate analysis (Table 3). Poor housing conditions, having a dog on the compound and use of traditional remedies were identified as independent risk factors for tungiasis. Being of female sex and insecticide use in the previous three months were protective factors. The highest population-attributable fractions (PAF) calculated were having a dog (52%) and disposing of waste on the compound (51%). The PAF for the risk variables associated with housing conditions was 22.4% for houses built on dunes or on swamp land; 24.5% for houses made of crude adobe walls; 6.5% for houses built of palm stems and leaves; and 29.7% for houses with sand floors (Table 4).
4. Discussion Tungiasis is an important but neglected health problem of resource-poor communities in South America, the Caribbean and sub-Saharan Africa
(Arene, 1984; Chadee, 1998; Heukelbach et al., 2001; Matias, 1989; Nte and Eke, 1995). Prevalences of up to 50% in the general population and the considerable morbidity, particularly in severely infested individuals, make this parasitic skin disease an important public health issue. Epidemiological knowledge about tungiasis is rudimentary, and epidemiological studies performed so far only describe the distribution of infestation in selected age-groups and a few economically depressed urban communities (Arene, 1984; de Carvalho et al., 2003; Chadee, 1998; Matias, 1989; Nte and Eke, 1995). Before the present study, nothing was known about risk factors associated with infestation or predisposing to severe disease. This lack of information has made it impossible to devise methods for controlling disease occurrence or morbidity. As a first step towards solving this problem, we systematically examined the entire population in an endemic village and assessed environmental, behavioural and socio-economic factors which might be related to tungiasis. Most individuals had lived in the village since birth and
378 population changes were very low, rendering the site an optimal setting for understanding the local web of causation of this disease which affects half of the population at the beginning of the dry season, when prevalence is still increasing. Conditions related to housing were the most important factors associated with presence of tungiasis and with severe infestation. Living in a house built on a dune or next to a swamp, made of adobe or palm stems and leaves, or having a floor of sand or mud clay increased the odds for presence of tungiasis by a factor of 1.9 to 4.7 and that for heavy infestation by a factor of 1.9 to 12.7 (Table 3). The free-living stages of T. penetrans usually develop in dry and sandy soil. Therefore, if the floor of a house consists of sand or dried mud, development of larvae and adults may even take place within the confines of the house. Houses made of crude adobe walls may have an additional advantage for the replication of T. penetrans. There are always cracks and crevices in the wall, which — in analogy to triatoma bugs — may provide shelters for adult fleas until a suitable host presents. Similarly, walls and roofs of palm stems and leaves are likely to be suitable niches for maturing fleas to hide. For houses located on the dunes, access is only possible on foot and takes much more time than a house next to a road, thereby increasing the exposure to fleas thriving on the sand. In this community, a simple and relatively inexpensive intervention such as cementing the floors of those houses which have sand or clay floors would reduce the prevalence of tungiasis by approximately 30% (Table 4). The observation that living in a house built next to a swamp increased the odds for severe infestation by a factor of ten seems to be in contradiction with the assumption that T. penetrans requires dry and sandy soils for its development. However, high infestation intensities have been observed under very humid conditions in the Amazon basin (Grossmann and Parinaud, 1979). As the soil of the small swamp adjacent to the village was densely covered with leaves shed from the mangroves, it is conceivable that free-living stages of T. penetrans may also develop in this environment. Being a zoonosis, tungiasis affects animals and humans alike. Among domestic animals, dogs, cats, pigs, cattle, goats and others, have been found infested (Heukelbach et al., 2001; Verhulst, 1976). In a study on the animal reservoirs of T. penetrans in two endemic communities, Heukelbach et al. (2004a) found that up to 67% of dogs and 50% of cats were infested. This finding corresponds to our observation that the presence of a dog on the compound increased the odds for tungiasis
M. Muehlen et al. 1.9-fold (Table 3). Considering the PAF for this risk factor, keeping dogs away from the compound could reduce the prevalence of tungiasis by approximately 52%, corroborating the hypothesis of Heukelbach et al. (2001), who speculated that dogs contribute to high attack rates among humans. In Balbino, a mixture of rancid coconut and oil pressed from the mamona (Ricinus communis) seed is smeared on the feet and sometimes hands, for it is believed to keep fleas away. The use of this traditional mixture to repel sand fleas was a strong predictor for the presence of tungiasis and severe infestation alike. We observed that in households with a massive presence of T. penetrans, family members were more likely to apply these traditional repellents on their skin than in less affected houses. Apparently though, the substances used had no protective effect. After multivariate analysis, two exposure variables remained statistically significant protective factors, namely female sex and previous use of an insecticide inside the house (Table 3). In the few studies on infestation intensity performed so far, females consistently have been found to carry fewer embedded fleas than males (Chadee, 1998; Heukelbach et al., 2001; Muehlen et al., 2003; Wilcke et al., 2002). In rural northeast Brazil, girls and women are more settled, keeping to the house more often than boys and men. As being a female reduced the risk of severe infestation by about 66%, this would point to a predominantly peridomicillary transmission. Behavioural characteristics also play an important role in tungiasis-associated morbidity. The mothers usually remove penetrated fleas on a daily basis. In a setting where this does not occur, lesions develop further to advanced stages and the number of penetrated ectoparasites rapidly accumulates, leading to severe infestation and greater morbidity. In communities like the one studied, houses are infested by a great variety of insects and other arthropods. Therefore, many households use commercially available insecticides, either sporadically or regularly. It can therefore be supposed that certain products may have an insecticidal effect against larvae and adults of T. penetrans. In a preliminary study in dogs with porpoxur, fenthion and flumethrin either spotted on or used as impregnated collars, we found a reduction in prevalence rates of tungiasis in dogs observed for a period of 3 months (J. Heukelbach et al., unpublished data). Several other factors were associated with tungiasis and/or severe infestation in univariable analysis (Table 2). Factors indicating low family income (house with fewer than three rooms, no shower,
Risk factors for tungiasis in northeast Brazil no electricity, monthly income per capita ≤60 R$) were significantly associated with the presence of tungiasis. Although houses of crude adobe walls and those without a concrete floor are indicators of a low-income household, it seems that the physical characteristics of such houses — and not primarily the financial situation of the owners — make individuals susceptible to severe infestation. Thus, in this community, poverty per se did not seem to be a determinant for the presence of disease nor the occurrence of severe infestation. The absence of a pit latrine associated with defecation on the compound as well as waste thrown away rather than burned and buried was a significant predictor of tungiasis (OR = 6.4 and 5.8 respectively). In a study conducted in an urban slum where waste and faecal material littered the entire area, we found a prevalence of tungiasis of 34% (Wilcke et al., 2002). Stray dogs, cats, and rodents — important reservoirs for T. penetrans — are particularly attracted to such areas. Organic material contaminating the soil may therefore increase the risk in two independent ways: by attracting animals that can act as suitable hosts for T. penetrans and by providing a sheltered environment for the development of the free-living stages. A low educational level, and particularly illiteracy, is associated with infections as different as helminthic disease and leprosy (Bundy and Guyatt, 1996; Ponnighaus et al., 1994). It is therefore not surprising that in individuals with no or only basic reading and writing ability, the odds of being affected by tungiasis were 4.8 and 2.0 respectively. In contrast, if shoes were worn only irregularly, the odds for tungiasis increased only marginally (OR = 1.6, 95% CI 1.1—2.3). This might be explained by the fact that resource-poor people in northeast Brazil wear almost exclusively flip-flops, which by the very nature of their design cannot protect against penetrating sand fleas. On the other hand, even the use of closed shoes and stockings cannot completely protect against tungiasis. An important finding is that households not visited by the health agent were associated with a four-fold increase in the odds for severe infestation. Health agents of the national family health program are trained to instruct their clients in many ways and could for example encourage family decision-makers to construct a pit latrine or to burn and bury their waste instead of disposing of it somewhere on the compound. As morbidity is directly related to the number of embedded sand fleas found on a person, education on proper hygienic behaviour could become an effective means of reducing tungiasis-associated morbidity.
379 Taken together, these observations show, for the first time, that there is a web of causation in which tungiasis thrives in resource-poor communities, leading to a prevalence of over 50% in the population studied and severe infestations in almost 10% of those infested. Population attributable fractions for the most important risk factors identified showed that better housing conditions, particularly replacing sand and mud floors with concrete or tiled floors, improving waste and garbage disposal by building latrines and offering public garbage collection, and keeping dogs off the compound would each have a considerable impact on both disease occurrence and severity. The possibility of supplying commercially available insecticides appropriate for domestic use should also be explored. This would require government support, as the most infected households are the poorest and hence unlikely to be able to afford insecticides. As the community studied is in many aspects similar to other resource-poor rural communities, at least in Brazil, we believe that risk factors identified here are equally pertinent to other endemic areas. Conflicts of interest statement The authors have no conflicts of interest concerning the work reported in this paper.
Acknowledgments ¨ This study was supported by the Arztekommittee f¨ ur die Dritte Welt, Frankfurt, Germany, the DAAD/CAPES PROBRAL academic exchange programme, the WHO (grant CPE/PVC B2/181/195), and a donation from Mr and Mrs Hertz, Reinbek, Germany. We thank the people of the community of Balbino, who so willingly agreed to participate in this survey. We are also greatly indebted to Anto˜o Santos for her skilful assisnia Val´ eria Assunc ¸a tance. Data are part of the master’s thesis of Marion Muehlen and the medical thesis of Thomas Wilcke.
References Arene, F., 1984. The prevalence of sand flea (Tunga penetrans) among primary and post-primary school pupils in Choba area of the Niger Delta. Public Health 98, 282—283. Bundy, D.A., Guyatt, H.L., 1996. Schools for health: Focus on health, education and the school-age child. Parasitol. Today 12, 1—14. Chadee, D.D., 1998. Tungiasis among five communities in southwestern Trinidad, West Indies. Ann. Trop. Med. Parasitol. 92, 107—113. de Carvalho, R.W., de Almeida, A.B., Barbosa-Silva, S.C., Amorim, M., Ribeiro, P.C., Serra-Freire, N.M., 2003. The patterns of tungiasis in Araruama township, state of Rio de Janeiro, Brazil. Mem. Inst. Oswaldo Cruz 98, 31—36.
380 Feldmeier, H., Heukelbach, J., Eisele, M., Sousa, A.Q., Barbosa, L.M., Carvalho, C.B., 2002. Bacterial superinfection in human tungiasis. Trop. Med. Int. Health 7, 559—564. Greco, J.B., Sacramento, E., Tavares-Neto, J., 2001. Chronic ulcers and myiasis as ports of entry for Clostridium tetani. Braz. J. Infect. Dis. 5, 319—323. Grossmann, E.M., Parinaud, R., 1979. Dermatologie in Franz¨ osisch Guyana. Hautarzt 30, 443—445. Heukelbach, J., de Oliveira, F.A., Hesse, G., Feldmeier, H., 2001. Tungiasis: a neglected health problem of poor communities. Trop. Med. Int. Health 6, 267—272. Heukelbach, J., Costa, A.M., Wilcke, T., Mencke, N., Feldmeier, H., 2004a. The animal reservoir of Tunga penetrans in severely affected communities of north-east Brazil. Med. Vet. Entomol. 18, 329—335. Heukelbach, J., Winter, B., Wilcke, T., Muehlen, M., Albrecht, S., de Oliveira, F.A., Kerr-Pontes, L.R., Liesenfeld, O., Feldmeier, H., 2004b. Selective mass treatment with ivermectin to control intestinal helminthiases and parasitic skin diseases in a severely affected population. Bull. World Health Organ. 82, 563—571. Kleinbaum, D.G., Kupper, L.L., Mogernstern, H., 1982. Epidemiologic Research: Principles and Quantitative Methods. Lifetime Learning Publications, Belmont, California.
M. Muehlen et al. Macias, P.C., Sashida, P.M., 2000. Cutaneous infestation by Tunga penetrans. Int. J. Dermatol. 39, 296—298. Matias, R.S., 1989. [Epidemics of tungiasis in Rio Grande do Sul.] Rev. Soc. Bras. Med. Trop. 22, 137—142 [in Portuguese]. Muehlen, M., Heukelbach, J., Wilcke, T., Winter, B., Mehlhorn, H., Feldmeier, H., 2003. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. II. Prevalence, parasite load and topographic distribution of lesions in the population of a traditional fishing village. Parasitol. Res. 90, 449—455. Nte, A.R., Eke, F.U., 1995. Jigger infestation in children in a rural area of Rivers State of Nigeria. West Afr. J. Med. 14, 56—58. Ponnighaus, J.M., Fine, P.E., Sterne, J.A., Malema, S.S., Bliss, L., Wilson, R.J., 1994. Extended schooling and good housing conditions are associated with reduced risk of leprosy in rural Malawi. Int. J. Lepr. Other Mycobact. Dis. 62, 345—352. Verhulst, A., 1976. Tunga penetrans (Sarcopsylla penetrans) as a cause of agalactia in sows in the Republic of Zaire. Vet. Rec. 98, 384. Wilcke, T., Heukelbach, J., Cesar Saboia Moura, R., Regina Sansigolo Kerr-Pontes, L., Feldmeier, H., 2002. High prevalence of tungiasis in a poor neighbourhood in Fortaleza, Northeast Brazil. Acta Trop. 83, 255—258.
Identifying risk factors for tungiasis and heavy infestation in a resource-poor community in northeast Brazil Marion Muehlen a,b,∗, Hermann Feldmeier a, Thomas Wilcke a, Benedikt Winter a, J¨ org Heukelbach c,d a
Department of Medical Microbiology, Institute of Infectious Medicine, Charit´ e University Medicine Berlin, Campus Benjamin Franklin, Berlin, Germany b Department of Infectious Disease Epidemiology, Robert Koch Institute, Seestrasse 10, 13353 Berlin, Germany c Mandacaru Foundation, Fortaleza, Brazil d Department of Community Health, Medical Faculty, Federal University of Cear´ a, Fortaleza, Brazil Received 11 April 2005 ; received in revised form 18 June 2005; accepted 21 June 2005 Available online 17 November 2005 KEYWORDS Tungiasis; Tunga penetrans; Sand flea; Epidemiology; Risk factor; Brazil
Summary Tungiasis is a neglected parasitic skin disease caused by penetration of female sand fleas into the epidermis. The ectoparasitosis is widespread in resourcepoor communities in South America, the Caribbean and sub-Saharan Africa. To identify risk factors for the presence of sand fleas and severe infestation in an endemic community, we examined the entire population of a traditional fishing village for the presence of embedded sand fleas and determined the number and type of lesions. Demographic, behavioural and environmental characteristics of the population were assessed using a structured questionnaire. Multivariable analysis showed that both occurrence of tungiasis and heavy infestation were significantly related to poor housing conditions (odds ratio [OR] = 4.7, 95% CI 1.4—15.8), lack of health education (OR = 4.1, 95% CI 2.0—8.6) and presence of animals on the compound (OR = 1.9, 95% CI 1.1—3.4). Contrary to common belief, a protective effect of frequent use of closed footwear could not be demonstrated. Based on the population attributable fractions calculated for the major risk factors identified, we conclude that several low-cost interventions would have a considerable impact on the occurrence of tungiasis and heavy infestation. © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
1. Introduction ∗
Corresponding author. Tel.: +49 1888 7543910; fax: +49 1888 7543533. E-mail address: [email protected] (M. Muehlen).
Tungiasis is a neglected parasitic disease caused by the penetration of the female sand flea Tunga
0035-9203/$ — see front matter © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2005.06.033
372 penetrans (jigger flea) into the epidermis of its host. The ectoparasitosis occurs in Central and South America, the Caribbean and sub-Saharan Africa (Macias and Sashida, 2000). In Brazil, it is widespread in economically depressed communities from Rio Grande do Sul State in the south to Roraima in the north of the country (Matias, 1989). In typical endemic areas, age-specific prevalence follows an S-shaped curve, increasing sharply in children 5 to 14 years old, declining in prevalence during adolescence and increasing again in older individuals (Wilcke et al., 2002). The parasite burden is unevenly distributed within an affected population. Whereas the majority of infested individuals harbour between one and ten fleas, a minority may carry up to 150 embedded parasites (Muehlen et al., 2003). Tungiasis is associated with considerable morbidity, such as intense local inflammation, deformation and auto-amputation of digits, deformation and loss of nails, formation of fissures and ulcers, gangrene, difficulty walking and gripping (when lesions are located on the hands), as well as sleep disturbances due to severe itching and pain (Chadee, 1998; Feldmeier et al., 2002; Matias, 1989). Tungiasis may serve as an entry port for Clostridium tetani (Greco et al., 2001), rendering non-immunized individuals susceptible to tetanus. Individuals with a high parasite burden are therefore more vulnerable to severe disease. Why some individuals are heavily parasitized, but others harbour only a few sand fleas remains unknown. Environmental or behavioural factors, which could explain disease occurrence and severity of infestation at community level, have never been studied. To identify risk factors for infestation by T. penetrans and severe disease, a cross-sectional survey was performed in a traditional fishing village in Cear´ a State, as part of a comprehensive study on parasitic skin diseases in resource-poor communities in northeast Brazil. All individuals were interviewed and examined for embedded sand fleas. Demographic, behavioural, socio-economic and environmental risk factors were recorded and analysed.
2. Materials and methods 2.1. Study area and population sThe study was performed in Balbino village, municipality of Cascav´ el, Cear´ a State, northeast Brazil. The village is a traditional fishing community situated 60 km south of Fortaleza and was relatively isolated until recently. It is inhabited by 139
M. Muehlen et al. families with a total population of 620 with little fluctuation. Houses are located on relatively large compounds surrounded by wire fences. The village is covered by the government’s Family Health Program (Programa de Sa´ ude da Fam´ılia) and has two health agents, one for children and the other for the population in general. The health agents are responsible for health education and referral of patients to the health centre in Cascav´ el town.
2.2. Study design During a preparatory phase, we made contact with community leaders and held meetings with local ˜o dos moradores) at which associations (associac¸a the objectives of the study were explained. It was made clear that participation in the study was totally voluntary and that nobody who refused to participate would face a disadvantage. All inhabitants of the village were eligible for the study, provided they had spent at least 4 days per week, on average, in the village during the previous 3 months. A census was performed and each house was mapped using geographic positioning system methods. Data were collected by a door-to-door survey. If family members were absent during the survey, the house was revisited on two further occasions. Missing individuals were invited to come to the local health centre on the following days. Family members absent on all three occasions and who did not present for examination at the health centre were not included in the survey. In order to identify risk factors for the presence of tungiasis and severe infestation, relevant demographic, socio-economic, behavioural, educational and environmental information was collected from household heads (usually the mothers) in the form of structured interviews using a pre-tested questionnaire. Demographic, behavioural and educational risk factors were assessed for each household member, whereas environmental and socio-economic factors were assessed at the household level. Data were collected between June 20 and July 30, 2001, i.e. at the beginning of the dry season. Each individual was thoroughly examined for newly penetrated and embedded sand fleas and lesions were staged using a protocol developed previously (Muehlen et al., 2003). In order not to overlook fleas embedded at ectopic sites, the whole body (except the genital region) was examined. An arbitrarily defined number of lesions (viable, dead or manipulated) was used to classify the infestation as weak (1—5 lesions), moderate (6—30 lesions) and heavy (>30 lesions).
Risk factors for tungiasis in northeast Brazil
2.3. Ethical considerations The study protocol was reviewed by the Ethical Committee of the Cascavel Municipality Board, comprising health professionals, administrative authorities and community representatives. Individuals were only enrolled if they, or, in the case of minors, the legal carers, gave informed oral consent. Family leaders were assured that all data would be handled confidentially. Risk factors identified were explained during a community meeting at the end of the study and villagers were encouraged to modify behaviour and environmental determinants putting them at risk for tungiasis. As more than 50% of the villagers were known to be infected with intestinal helminths and/or ectoparasites, all inhabitants were offered free anthelminthic treatment at the end of the study (Heukelbach et al., 2004b).
2.4. Bias To avoid inter-observer bias, the clinical examination and the interviews were always performed by the same investigators (T.W. and M.M., respectively). The clinical examination was performed first and the interviews were carried out some days later. The interviewer remained blinded to the results of the clinical examination. As the whole study was conducted within a period of 5 weeks, intra-observer bias was negligible. Non-response bias was reduced by active recruitment and nonparticipation bias was minimized by a door-to-door survey. In an effort to reduce selection bias, we defined the whole village as our target population. Although households were visited up to three times, 13.1% of the inhabitants, mainly adult males who were out fishing, were missed. This resulted in an underrepresentation of males aged 20—39 years. Recall bias was reduced by limiting the recall period to 3 months prior to the survey. However, for questions referring to events occurring at irregular intervals, such as having received anthelminthic treatment, a recall bias cannot be excluded.
2.5. Statistical analysis Data was entered in EpiInfo version 6.04d (CDC, Atlanta, GA, USA) and checked for data entry errors, then transferred to SPSS 11.0 (SPSS Inc., Chicago, IL, USA) for data analysis. The 2 test and Fisher’s exact test were used to determine the significance of differences of relative frequencies. Putative risk factors were first assessed by univariate analysis, and odds ratios (OR) and the respective 95% CI were calculated. Variables
373 significantly (P < 0.05) related to the occurrence of tungiasis or severity of infestation in the univariate analysis were entered into a logistic regression analysis model with stepwise forward inclusion of each variable. Factors significantly associated with the occurrence of tungiasis in the univariate analysis but assessed only in individuals older than 15 years, such as level of education, were not included in the model. To determine the potential impact of reducing the prevalence of certain exposures on the occurrence of tungiasis in this community, population attributable fractions (PAF) were calculated for the risk factors with the highest odds ratios and for those exposure variables for which an intervention seems feasible (Kleinbaum et al., 1982).
3. Results The village consisted of 139 families with a total of 620 individuals. Of these, 605 fulfilled the inclusion criterion, i.e. having been present in the village at least 4 days per week during the previous 3 months. Eighty-one individuals (66 males and 15 females) were not encountered on any of three survey visits, reducing the study population to 524. All 524 individuals consented to being interviewed, and 496 agreed to being examined for the presence of sand fleas. Thus, the number of individuals available for the assessment of risk factors was 496, belonging to 132 families (95.0% of all families). There was a significant difference between males (42.7%) and females (57.3%) in the study population (P = 0.05). This was due to an overrepresentation of females >20 years of age. The socio-economic characteristics of the study population are summarized in Table 1. Of adolescents 15 years and older and adults, 26.3% were wholly illiterate, and only 16.4% had completed primary school. Only 57.2% had some basic knowledge of reading and writing. Of the 132 households, 99 (75%) had electricity, but only 26 (19.7%) had a shower in the house. The overall prevalence of tungiasis was 51.0%; 70.4% of the infested individuals had between one and five lesions, 20.6% between six and 30 lesions and 9.1% were considered heavily infested (>30 lesions). The proportion of mild, moderate and heavy infestation changed similarly with increasing age (Figure 1). The results of univariate analysis are shown in Table 2. Age <15 and ≥60 years were highly significant risk factors for tungiasis (P < 0.001 and P = 0.002 respectively). Houses located on dunes, consisting of crude adobe walls or palm stems and leaves, with a floor of sand and without
374
M. Muehlen et al.
Table 1 Geographic and socio-economic characteristics of the study population (132 households) Frequency Location House situated next to/on: Laterite road Road with sand surface Swamp Dune
43.2 39.4 3.0 14.4
Distance to beach (m) >300 100—300 <100
108 21 3
81.8 15.9 2.3
Housing Type of construction Brick Plastered adobe Crude adobe Palm stems and leaves
65 21 31 15
49.2 15.9 23.5 11.4
87 34 11
65.9 25.8 8.3
110 18 4
83.3 13.6 3.0
Waste disposal Public collection Thrown on compound Burned and buried
55 5 72
41.7 3.8 54.5
Water Own well Public supply system Public well
112 4 16
84.8 3.0 12.1
125 111 91 47
94.7 84.1 68.9 35.6
Healthcare Health agent visits to the household Monthly 67 Every 3 months 31 No visit at all 34
50.8 23.5 25.8
Economy Monthly income per household (R$)b 0—180 80 >180 52
60.6 39.4
Age (years) 0—4 5—9
10.1 15.3
Sanitation Toilet Latrine on compound Defecation on compound Sewage system connection
Animals Animals on compound Dogs Cats Othersa
50 76
10—14 15—19 20—39 40—59 ≥60
(%)
57 52 4 19
Type of floor Concrete/tiles Clay soil Sand
Table 1 (Continued ) Frequency
(%)
66 65 111 80 48
13.3 13.1 22.4 16.1 9.7
a
Cows, horses, donkeys, goats, pigs. R$180 corresponds to the minimal Brazilian wage at the time of the survey and is equivalent to ∼90US$. b
electricity were significantly related to infestation by T. penetrans (all P < 0.001). Other significant risk factors were inappropriate waste disposal (P < 0.001), absence of latrines (P = 0.01), as well as overcrowding (≥7 persons/household, P < 0.02). Income was also a significant determinant of tungiasis. In households with a per capita income of ≤60 R$/month, the odds of being affected by tungiasis were twice as high as in individuals with a per capita income >60R$ (P = 0.001). Illiterate individuals were approximately five times more likely to be affected by tungiasis than others (P < 0.001). In persons 15 years and older, the regular use of a deodorant or a body lotion after bathing seemed to have a protective effect (P < 0.001). In households reporting insecticide use in the house during the three previous months, individuals were significantly less affected by tungiasis (OR = 0.36, 95% CI 0.24—0.54, P < 0.001). On the other hand, the regular use of traditional remedies intended to prevent the penetration of sand fleas was associated with seven-fold odds for tungiasis (P < 0.001). The presence of dogs and cats on the compound were also significant risk factors for tungiasis (P < 0.01).
Figure 1 Prevalence of tungiasis in the respective age groups according to severity of infestation. Column height indicates overall prevalence in the age group.
Univariable analysis of demographic, socio-economic, behavioural, educational and environmental risk factors (n = 496)
Exposure variable Demographic characteristics Sex Age group (years)
Persons/household
Housing House situated next to/on:
Distance to beach (m)
Type of construction
Type of floor
Rooms/house
Electricity Water supply
Toilet
Waste disposal
Frequency of tungiasis
Any degree of infestation
n
(%)
OR (95% CI)
Female Male 0—4 5—9 10—14 15—19 20—39 40—59 ≥60 1—3 4—6 ≥7
284 212 50 76 66 65 111 80 48 86 258 152
48.2 54.7 58.0 76.3 69.7 29.2 35.1 42.5 58.3 43.0 49.2 58.6
Reference 1.30 (0.89—1.88) 3.34 (1.44—7.85) 8.23 (3.62—19.02) 5.57 (2.47—12.69) Reference 1.31 (0.64—2.68) 1.79 (0.85—3.81) 3.39 (1.44—8.04) Reference 1.14 (0.76—2.16) 1.36 (1.06—3.31)
Laterite road Road with sand surface Swamp Dune <100 100—300 >300 Brick Plastered adobe Crude adobe Palm stems and leaves Concrete/tiles Clay soil Sand ≥6 4—5 1—3 Yes No Public supply system Own well Public wella Sewage system connection Defecation on compound Latrine on compound Public collection Burned and buried Thrown on compound
213 192 15 76 10 94 392 232 81 133 50 310 157 29 132 300 64 373 123 16 433 47 11 68 417 201 274 21
40.8 49.0 53.3 84.2 30.0 41.5 53.8 34.5 58.0 69.9 66.0 42.3 61.8 86.2 40.9 51.3 70.3 43.7 73.2 56.3 48.0 76.6 27.3 70.6 48.4 42.3 55.1 81.0
Reference 1.39 (0.92—2.10) 1.66 (0.52—5.30) 7.72 (3.78—16.10) Reference 1.65 (0.35—8.69) 2.7 (0.6—13.47) Reference 2.63 (1.52—4.56) 4.42 (2.72—7.18) 3.69 (1.85—7.40) Reference 2.21 (1.46—3.34) 8.54 (2.74—29.71) Reference 1.52 (0.99—2.36) 3.42 (1.73—6.83) Reference 3.51 (2.19—5.64) Reference 0.72 (0.24—2.15) 2.55 (0.66—9.94) Reference 6.40 (1.34—34.4) 2.51 (0.6—12.1) Reference 1.68 (1.14—2.46) 5.80 (1.75—21.21)
Presence of heavy infestation P value
OR (95% CI)
0.15 0.002 <0.001 <0.001
2.24 2.74 1.29 3.74
(0.94—5.43) (0.41—22.63) (0.17—11.49) (0.67—27.22)
P value
0.047 0.40 1.00 0.16
0.42 0.10 0.002
1.49 (0.25—11.43) 0.00 (0.00—3.31) 3.66 (0.59—28.74)
1.00 0.20 0.13
0.32 0.02
0.88 (0.31—2.62) 0.36 (0.08—1.50)
0.80 0.11
0.10 0.34 <0.001
3.99 (0.75—28.15) 16.23 (1.47—180.65) 25.94 (5.45—169.12)
Risk factors for tungiasis in northeast Brazil
Table 2
0.065 0.02 < 0.001
0.74 0.20
Undefined Undefined
1.00 1.00
0.0002 <0.001 <0.001
Undefined Undefined Undefined
0.02 < 0.001 < 0.001
<0.001 <0.001
3.91 (1.42—11.08) 11.29 (3.05—41.69)
0.002 0.0003
0.046 0.001
4.15 (0.91—26.27) 6.72 (1.18—49.80)
0.04 0.016
<0.001
6.49 (2.64—16.26)
< 0.001
0.52 0.20
0.16 (0.04—0.77) 0.89 (0.17—5.00)
0.02 1.00
0.014 0.17
0.60 (0.09—4.84) 0.18 (0.003—1.31)
0.62 0.07
0.006 0.0007
1.60 (0.63—4.12) 1.21 (0.03—9.81)
0.30 0.60
375
376
Table 2 (Continued ) Exposure variable Shower in the house Socio-economic characteristics Monthly income per household (R$)b
Income/capita (R$/month) Educationc
Behaviour characteristics Use of shoes Health care Washes daily Use of soap Use of deodorant/body lotionc Use of traditional medicine Insecticide use in last 90 days Health agent visits the household
Domestic animals Dogs Cats Other animalsd
Any degree of infestation
Presence of heavy infestation
Yes No
n 84 412
(%) 26.2 56.1
OR (95% CI) Reference 3.60 (2.07—6.29)
>200 101—200 0—100 >60 ≤60 Primary school completed Primary school not completed Illiterate
182 185 129 112 384 50 240 80
45.6 46.5 65.1 37.5 54.9 6.6 45.4 57.5
Reference 1.04 (0.67—1.60) 2.23 (1.36—3.64) Reference 2.03 (1.29—3.21) Reference 2.01 (0.91—4.51) 4.80 (2.01—11.64)
0.06 <0.001
Frequent Seldom/never
170 326
43.5 54.9
Reference 1.58 (1.07—2.34)
Yes No Yes No Yes No No Yes No Yes Monthly Once in the last 3 months Never
492 4 476 20 267 37 420 76 308 188 308 105 83
50.8 75.0 50.4 65.0 35.2 70.3 44.8 85.5 60.4 35.6 51.9 43.8 56.6
Reference 2.90 (0.27—72.93) Reference 1.83 (0.67—5.16) Reference 4.35 (1.95—9.85) Reference 7.29 (3.61—15.08) Reference 0.36 (0.24—0.54) Reference 0.72 (0.45—1.15) 1.21 (0.72—2.03)
No Yes No Yes No Yes
81 415 134 36 326 170
33.3 54.5 41.8 54.4 53.7 45.9
Reference 2.39 (1.41—4.07) Reference 1.66 (1.09—2.54) Reference 0.73 (0.50—1.08)
P value
OR (95% CI)
P value
<0.001
Undefined
0.02
0.87 0.0007
2.54 (0.72—9.82) 4.56 (1.32—17.22)
0.11 0.005
0.001
1.24 (0.43—3.84)
0.67
Undefined Undefined
0.34 0.08
0.016
6.68 (1.51—41.38)
0.003
0.34
6.23 (0.11—80.14)
0.2
0.2
5.16 (1.33—18.41)
0.016
<0.001
2.53 (0.51—10.92)
0.17
<0.001
7.68 (3.17—18.69)
<0.001
<0.001
0.20 (0.05—0.72)
0.004
0.15 0.45
0.73 (0.16—2.83) 3.77 (1.48—9.59)
0.77 0.003
0.0005
2.42 (0.54—15.16)
0.28
0.012
2.96 (0.83—12.61)
0.068
0.099
0.84 (0.33—2.11)
0.70
There were three public wells, two of which were functioning. One was in front of the school and health centre, the other in a poorer part of the village where most houses did not have a well on the compound. Water was supplied by the municipality free of charge. b At the time of the survey 1US$ was equivalent to ∼2R$. c Only for individuals ≥15 years of age. d Cows, horses, mules, goats and pigs.
M. Muehlen et al.
a
Frequency of tungiasis
Risk factors for tungiasis in northeast Brazil Table 3
377
Multivariable analysis after adjustment for age and sexa Presence of tungiasis AOR (95% CI)
Being of female sex House built on dune or swamp House built of adobe/palm leaves Floor made of sand Floor of clay soil Having a dog on the compound Use of traditional medicine Insecticide use in last 3 months
Presence of heavy infestation P value
2.44 (1.21—4.94) 1.87 (1.16—3.00) 4.71 (1.41—15.78)
0.031 0.010 0.012
1.89 (1.06—3.36) 4.07 (1.93—8.56) 0.55 (0.36—0.85)
0.031 <0.001 0.007
AOR (95% CI)
P value
0.36 (0.14—0.92) 12.73 (2.76—58.71)
0.032 0.001
10.29 (2.71—39.06) 3.41 (1.21—9.61)
0.001 0.021
4.96 (2.01—12.22)
<0.001
AOR: adjusted odds ratio. a Only statistically significant values are given.
Table 4
Population attributable fraction
House built on dune or near swamp House built of crude adobe House built of palm stems/leaves House with clay/sand floor Defecation on compound Waste on compound Not wearing shoes Dog on compound
OR
AR
% exposed among cases
PAF (%)
4.7 3.0 2.0 2.6 2.6 4.3 1.6 2.4
0.787 0.667 0.50 0.615 0.615 0.767 0.375 0.583
28.5 36.8 13.0 48.2 19.0 66.4 70.8 89.3
22.44 24.53 6.50 29.66 11.69 50.96 26.55 52.09
OR: odds ratio. AR: attributable risk, calculated as (OR−1)/OR, is the risk of tungiasis in the exposed due to the exposure (also termed ‘excess risk’). PAF: population attributable fraction, calculated as % exposed among cases × (OR−1)/OR, is the fraction of cases which would not have occurred if an exposure had been avoided, assuming the exposure is casual and the other risk factors in the population remain unchanged (according to Kleinbaum et al., 1982, to adjust for confounding).
Several risk factors remained highly significant after multivariate analysis (Table 3). Poor housing conditions, having a dog on the compound and use of traditional remedies were identified as independent risk factors for tungiasis. Being of female sex and insecticide use in the previous three months were protective factors. The highest population-attributable fractions (PAF) calculated were having a dog (52%) and disposing of waste on the compound (51%). The PAF for the risk variables associated with housing conditions was 22.4% for houses built on dunes or on swamp land; 24.5% for houses made of crude adobe walls; 6.5% for houses built of palm stems and leaves; and 29.7% for houses with sand floors (Table 4).
4. Discussion Tungiasis is an important but neglected health problem of resource-poor communities in South America, the Caribbean and sub-Saharan Africa
(Arene, 1984; Chadee, 1998; Heukelbach et al., 2001; Matias, 1989; Nte and Eke, 1995). Prevalences of up to 50% in the general population and the considerable morbidity, particularly in severely infested individuals, make this parasitic skin disease an important public health issue. Epidemiological knowledge about tungiasis is rudimentary, and epidemiological studies performed so far only describe the distribution of infestation in selected age-groups and a few economically depressed urban communities (Arene, 1984; de Carvalho et al., 2003; Chadee, 1998; Matias, 1989; Nte and Eke, 1995). Before the present study, nothing was known about risk factors associated with infestation or predisposing to severe disease. This lack of information has made it impossible to devise methods for controlling disease occurrence or morbidity. As a first step towards solving this problem, we systematically examined the entire population in an endemic village and assessed environmental, behavioural and socio-economic factors which might be related to tungiasis. Most individuals had lived in the village since birth and
378 population changes were very low, rendering the site an optimal setting for understanding the local web of causation of this disease which affects half of the population at the beginning of the dry season, when prevalence is still increasing. Conditions related to housing were the most important factors associated with presence of tungiasis and with severe infestation. Living in a house built on a dune or next to a swamp, made of adobe or palm stems and leaves, or having a floor of sand or mud clay increased the odds for presence of tungiasis by a factor of 1.9 to 4.7 and that for heavy infestation by a factor of 1.9 to 12.7 (Table 3). The free-living stages of T. penetrans usually develop in dry and sandy soil. Therefore, if the floor of a house consists of sand or dried mud, development of larvae and adults may even take place within the confines of the house. Houses made of crude adobe walls may have an additional advantage for the replication of T. penetrans. There are always cracks and crevices in the wall, which — in analogy to triatoma bugs — may provide shelters for adult fleas until a suitable host presents. Similarly, walls and roofs of palm stems and leaves are likely to be suitable niches for maturing fleas to hide. For houses located on the dunes, access is only possible on foot and takes much more time than a house next to a road, thereby increasing the exposure to fleas thriving on the sand. In this community, a simple and relatively inexpensive intervention such as cementing the floors of those houses which have sand or clay floors would reduce the prevalence of tungiasis by approximately 30% (Table 4). The observation that living in a house built next to a swamp increased the odds for severe infestation by a factor of ten seems to be in contradiction with the assumption that T. penetrans requires dry and sandy soils for its development. However, high infestation intensities have been observed under very humid conditions in the Amazon basin (Grossmann and Parinaud, 1979). As the soil of the small swamp adjacent to the village was densely covered with leaves shed from the mangroves, it is conceivable that free-living stages of T. penetrans may also develop in this environment. Being a zoonosis, tungiasis affects animals and humans alike. Among domestic animals, dogs, cats, pigs, cattle, goats and others, have been found infested (Heukelbach et al., 2001; Verhulst, 1976). In a study on the animal reservoirs of T. penetrans in two endemic communities, Heukelbach et al. (2004a) found that up to 67% of dogs and 50% of cats were infested. This finding corresponds to our observation that the presence of a dog on the compound increased the odds for tungiasis
M. Muehlen et al. 1.9-fold (Table 3). Considering the PAF for this risk factor, keeping dogs away from the compound could reduce the prevalence of tungiasis by approximately 52%, corroborating the hypothesis of Heukelbach et al. (2001), who speculated that dogs contribute to high attack rates among humans. In Balbino, a mixture of rancid coconut and oil pressed from the mamona (Ricinus communis) seed is smeared on the feet and sometimes hands, for it is believed to keep fleas away. The use of this traditional mixture to repel sand fleas was a strong predictor for the presence of tungiasis and severe infestation alike. We observed that in households with a massive presence of T. penetrans, family members were more likely to apply these traditional repellents on their skin than in less affected houses. Apparently though, the substances used had no protective effect. After multivariate analysis, two exposure variables remained statistically significant protective factors, namely female sex and previous use of an insecticide inside the house (Table 3). In the few studies on infestation intensity performed so far, females consistently have been found to carry fewer embedded fleas than males (Chadee, 1998; Heukelbach et al., 2001; Muehlen et al., 2003; Wilcke et al., 2002). In rural northeast Brazil, girls and women are more settled, keeping to the house more often than boys and men. As being a female reduced the risk of severe infestation by about 66%, this would point to a predominantly peridomicillary transmission. Behavioural characteristics also play an important role in tungiasis-associated morbidity. The mothers usually remove penetrated fleas on a daily basis. In a setting where this does not occur, lesions develop further to advanced stages and the number of penetrated ectoparasites rapidly accumulates, leading to severe infestation and greater morbidity. In communities like the one studied, houses are infested by a great variety of insects and other arthropods. Therefore, many households use commercially available insecticides, either sporadically or regularly. It can therefore be supposed that certain products may have an insecticidal effect against larvae and adults of T. penetrans. In a preliminary study in dogs with porpoxur, fenthion and flumethrin either spotted on or used as impregnated collars, we found a reduction in prevalence rates of tungiasis in dogs observed for a period of 3 months (J. Heukelbach et al., unpublished data). Several other factors were associated with tungiasis and/or severe infestation in univariable analysis (Table 2). Factors indicating low family income (house with fewer than three rooms, no shower,
Risk factors for tungiasis in northeast Brazil no electricity, monthly income per capita ≤60 R$) were significantly associated with the presence of tungiasis. Although houses of crude adobe walls and those without a concrete floor are indicators of a low-income household, it seems that the physical characteristics of such houses — and not primarily the financial situation of the owners — make individuals susceptible to severe infestation. Thus, in this community, poverty per se did not seem to be a determinant for the presence of disease nor the occurrence of severe infestation. The absence of a pit latrine associated with defecation on the compound as well as waste thrown away rather than burned and buried was a significant predictor of tungiasis (OR = 6.4 and 5.8 respectively). In a study conducted in an urban slum where waste and faecal material littered the entire area, we found a prevalence of tungiasis of 34% (Wilcke et al., 2002). Stray dogs, cats, and rodents — important reservoirs for T. penetrans — are particularly attracted to such areas. Organic material contaminating the soil may therefore increase the risk in two independent ways: by attracting animals that can act as suitable hosts for T. penetrans and by providing a sheltered environment for the development of the free-living stages. A low educational level, and particularly illiteracy, is associated with infections as different as helminthic disease and leprosy (Bundy and Guyatt, 1996; Ponnighaus et al., 1994). It is therefore not surprising that in individuals with no or only basic reading and writing ability, the odds of being affected by tungiasis were 4.8 and 2.0 respectively. In contrast, if shoes were worn only irregularly, the odds for tungiasis increased only marginally (OR = 1.6, 95% CI 1.1—2.3). This might be explained by the fact that resource-poor people in northeast Brazil wear almost exclusively flip-flops, which by the very nature of their design cannot protect against penetrating sand fleas. On the other hand, even the use of closed shoes and stockings cannot completely protect against tungiasis. An important finding is that households not visited by the health agent were associated with a four-fold increase in the odds for severe infestation. Health agents of the national family health program are trained to instruct their clients in many ways and could for example encourage family decision-makers to construct a pit latrine or to burn and bury their waste instead of disposing of it somewhere on the compound. As morbidity is directly related to the number of embedded sand fleas found on a person, education on proper hygienic behaviour could become an effective means of reducing tungiasis-associated morbidity.
379 Taken together, these observations show, for the first time, that there is a web of causation in which tungiasis thrives in resource-poor communities, leading to a prevalence of over 50% in the population studied and severe infestations in almost 10% of those infested. Population attributable fractions for the most important risk factors identified showed that better housing conditions, particularly replacing sand and mud floors with concrete or tiled floors, improving waste and garbage disposal by building latrines and offering public garbage collection, and keeping dogs off the compound would each have a considerable impact on both disease occurrence and severity. The possibility of supplying commercially available insecticides appropriate for domestic use should also be explored. This would require government support, as the most infected households are the poorest and hence unlikely to be able to afford insecticides. As the community studied is in many aspects similar to other resource-poor rural communities, at least in Brazil, we believe that risk factors identified here are equally pertinent to other endemic areas. Conflicts of interest statement The authors have no conflicts of interest concerning the work reported in this paper.
Acknowledgments ¨ This study was supported by the Arztekommittee f¨ ur die Dritte Welt, Frankfurt, Germany, the DAAD/CAPES PROBRAL academic exchange programme, the WHO (grant CPE/PVC B2/181/195), and a donation from Mr and Mrs Hertz, Reinbek, Germany. We thank the people of the community of Balbino, who so willingly agreed to participate in this survey. We are also greatly indebted to Anto˜o Santos for her skilful assisnia Val´ eria Assunc ¸a tance. Data are part of the master’s thesis of Marion Muehlen and the medical thesis of Thomas Wilcke.
References Arene, F., 1984. The prevalence of sand flea (Tunga penetrans) among primary and post-primary school pupils in Choba area of the Niger Delta. Public Health 98, 282—283. Bundy, D.A., Guyatt, H.L., 1996. Schools for health: Focus on health, education and the school-age child. Parasitol. Today 12, 1—14. Chadee, D.D., 1998. Tungiasis among five communities in southwestern Trinidad, West Indies. Ann. Trop. Med. Parasitol. 92, 107—113. de Carvalho, R.W., de Almeida, A.B., Barbosa-Silva, S.C., Amorim, M., Ribeiro, P.C., Serra-Freire, N.M., 2003. The patterns of tungiasis in Araruama township, state of Rio de Janeiro, Brazil. Mem. Inst. Oswaldo Cruz 98, 31—36.
380 Feldmeier, H., Heukelbach, J., Eisele, M., Sousa, A.Q., Barbosa, L.M., Carvalho, C.B., 2002. Bacterial superinfection in human tungiasis. Trop. Med. Int. Health 7, 559—564. Greco, J.B., Sacramento, E., Tavares-Neto, J., 2001. Chronic ulcers and myiasis as ports of entry for Clostridium tetani. Braz. J. Infect. Dis. 5, 319—323. Grossmann, E.M., Parinaud, R., 1979. Dermatologie in Franz¨ osisch Guyana. Hautarzt 30, 443—445. Heukelbach, J., de Oliveira, F.A., Hesse, G., Feldmeier, H., 2001. Tungiasis: a neglected health problem of poor communities. Trop. Med. Int. Health 6, 267—272. Heukelbach, J., Costa, A.M., Wilcke, T., Mencke, N., Feldmeier, H., 2004a. The animal reservoir of Tunga penetrans in severely affected communities of north-east Brazil. Med. Vet. Entomol. 18, 329—335. Heukelbach, J., Winter, B., Wilcke, T., Muehlen, M., Albrecht, S., de Oliveira, F.A., Kerr-Pontes, L.R., Liesenfeld, O., Feldmeier, H., 2004b. Selective mass treatment with ivermectin to control intestinal helminthiases and parasitic skin diseases in a severely affected population. Bull. World Health Organ. 82, 563—571. Kleinbaum, D.G., Kupper, L.L., Mogernstern, H., 1982. Epidemiologic Research: Principles and Quantitative Methods. Lifetime Learning Publications, Belmont, California.
M. Muehlen et al. Macias, P.C., Sashida, P.M., 2000. Cutaneous infestation by Tunga penetrans. Int. J. Dermatol. 39, 296—298. Matias, R.S., 1989. [Epidemics of tungiasis in Rio Grande do Sul.] Rev. Soc. Bras. Med. Trop. 22, 137—142 [in Portuguese]. Muehlen, M., Heukelbach, J., Wilcke, T., Winter, B., Mehlhorn, H., Feldmeier, H., 2003. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. II. Prevalence, parasite load and topographic distribution of lesions in the population of a traditional fishing village. Parasitol. Res. 90, 449—455. Nte, A.R., Eke, F.U., 1995. Jigger infestation in children in a rural area of Rivers State of Nigeria. West Afr. J. Med. 14, 56—58. Ponnighaus, J.M., Fine, P.E., Sterne, J.A., Malema, S.S., Bliss, L., Wilson, R.J., 1994. Extended schooling and good housing conditions are associated with reduced risk of leprosy in rural Malawi. Int. J. Lepr. Other Mycobact. Dis. 62, 345—352. Verhulst, A., 1976. Tunga penetrans (Sarcopsylla penetrans) as a cause of agalactia in sows in the Republic of Zaire. Vet. Rec. 98, 384. Wilcke, T., Heukelbach, J., Cesar Saboia Moura, R., Regina Sansigolo Kerr-Pontes, L., Feldmeier, H., 2002. High prevalence of tungiasis in a poor neighbourhood in Fortaleza, Northeast Brazil. Acta Trop. 83, 255—258.