Travel Medicine and Infectious Disease (2012) 10, 220e223
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Outbreak of tungiasis following a trip to Ethiopia M. Grupper*, I. Potasman Infectious Disease Unit, Bnai Zion Medical Center, 47 Golomb St., P.O. Box 9490, Haifa 31048, Israel Received 23 March 2012; received in revised form 4 September 2012; accepted 10 September 2012 Available online 30 September 2012
KEYWORDS Tungiasis; Outbreak; Travel
Summary Tungiasis is a skin disease caused by the ectoparasite sand flea Tunga penetrans. Although tungiasis is an important health problem in endemic areas, mainly South America and sub-Saharan Africa, it is reported uncommonly in travelers. We describe an outbreak of tungiasis in a group of travelers to Ethiopia. Following the diagnosis of tungiasis in a member of a group of 17 Israeli travelers to Ethiopia, other affected members were identified by photograph assisted self diagnosis. The characteristics, including relevant demographic and epidemiologic data were recorded using a telephone interview and computerized questionnaire, and analyzed subsequently. The attack rate of tungiasis in the travel group was 53% (9 patients). Most of the patients (89%) wore open sandals during prolonged periods of their journey, but the pattern of shoeware use was similar in unaffected group members. An insect bite was not felt by any patient. The median number of skin lesions was one, and most lesions were located on the foot (7 of 9 travelers), but the hands were also affected in 2 travelers. All skin lesions healed without a need for a major intervention and without major sequela within 5 weeks of their appearance. Tungiasis may be underdiagnosed in travelers. Medical personnel should include tungiasis in pre-travel recommendations, and post-travel assessment. ª 2012 Elsevier Ltd. All rights reserved.
Introduction Tungiasis is a skin disease caused by the ectoparasite sand flea Tunga penetrans, also known as the jigger flea. This parasite burrows into human skin, usually on the feet. Besides humans, various domestic and sylvatic animals are affected.1,2 Highest parasite load was found in pigs, followed by dogs and rats
* Corresponding author. Tel./fax: þ97248359755. E-mail address:
[email protected] (M. Grupper).
(prevalence of 54.8%, 45.5% and 29.4%, respectively).3 Tungiasis is present on the American continent from Mexico to northern Argentina, on several Caribbean islands, and in almost every country of sub-Saharan Africa. The prevalence, parasite burden and occurrence of severe disease are closely related to poverty.1,2,4,5 After skin penetration, the parasite settles in the epidermis. It immediately starts with an impressive abdominal hypertrophy (volume increment by a factor of 2000e3000) and massive eggs expulsion within 5e7 days. Following, an involution of the skin lesion begins, and after about 3 weeks the flea dies, and the remnants are managed
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Outbreak of tungiasis by host defense mechanisms. Secondary infections may be acquired through entry points in the route of penetration.6e9 Most skin lesions are confined to the feet, as the parasite has limited jumping ability, but ectopic localization of lesions (on hands, elbows, thighs and gluteal region) have been reported.10 Prompt diagnosis is facilitated by prior acquaintance with the disease. Treatment is simple and is based on complete surgical extraction of the flea. Closed shoes and socks seem to prevent tungiasis, although total protection is not achieved.1,2,4,5 Tungiasis has been uncommonly reported in travelers. The low incidence of about 6% of all skin lesions in returning travelers has been attributed to the avoidance of this population from economically depressed areas.11,12 We describe an outbreak of tungiasis in a group of travelers visiting Ethiopia.
Methods This is a descriptive study of tungiasis cases that were all part of a group of travelers returning to Israel from an organized 21-day trip during December, 2011in Ethiopia. The trip began in Addis Ababa, and from that point various localities in the northern and southern parts of Ethiopia were visited, including Bahir Dar, Gonder, Debark, Laibela, and Turmi. The index case was diagnosed by one of the authors (I.P), when presenting as an outpatient with skin lesions consistent with tungiasis .In response to direct questioning, the patient mentioned that other members of the travel group were also affected by similar skin lesions. Over the following days, emails were sent to the members of the travel group, accompanied by photographs of tungiasis skin lesions. Travelers reporting being affected by similar lesions were categorized as cases of tungiasis, contacted by email and/or phone, and interviewed using a structured questionnaire by either of the authors. The structured questionnaire included queries regarding demographic, epidemiological, and clinical features. Travel group members unaffected by skin lesions were asked to answer a limited set of questions, regarding the level of similarity between their travel path and possible risk factors for tungiasis as opposed to their affected counterparts. Data of completed questionnaires was analyzed using Excel software.
Results The travel group included 18 people, two of whom were tour guides (one was from Israel, and the other Ethiopian). Data were available for 17 members of the group (16 travelers, and the Israeli guide). Overall, 9 of the available group members were categorized as cases of tungiasis (attack rate of 53%). Patients’ characteristics are presented in Table 1. Most of the patients were men (67%). All cases were older than 60 years old, with a mean age of 64.7 (2.2) years. Six of 9 cases were married couples. All cases have reported sharing the exact same travel route, accommodations and transportation as the other, non-affected, group members. No pigs were seen during the trip, but domestic dogs were seen, reportedly, by 3 travelers. Accommodation was reported by all travelers to
221 Table 1 Summary of demographic and clinical findings, tungiasis outbreak, Ethiopia. Parameter
Result
Comments
Sex (M/F) Mean age (range)
6/3 64.7 (61e68 years) Walking barefoot No Z 7, Yes Z 2 Outside accommodations Wearing open sandals No Z 1, Yes Z 8 Felt insect bite None Time from trip onset Earliest e 7 days, to lesion recognition Latest e 12 days post end of trip No. of skin lesions 1e3 (1) (median) Site of lesions Foot Z 7, 5 e on soles, Hand Z 2 5 e on/around fingers Local pain/itch No Z 6, Yes Z 3 Itch was very mild Local erythema/ No Z 5, Yes Z 4 discharge Applied ointment 5 Mupirocin, iodine Needle exploration All (self) Saw eggs inside No Z 5, Yes Z 4 lesions Surgical exploration None Lesions healed All completely? Time to lesions 4 dayse5 weeks complete (week) healing (median)
take place only in rooms with a concrete floor. Only 2 of 9 cases reported episodes of walking barefoot outside hotels, but the skin lesions were already noticed on those occasions. However, all travelers were asked to take off their sneakers while entering churches (mostly in Lalibela). The floor in these churches was either covered with grass or carpets. Most patients (89%) wore open sandals during prolonged periods of their journey. Unaffected travelers were reported by patients to use open and closed footwear of similar nature. Notably, one of the affected spouses was discordant regarding footwear, and another patient used only closed shoes throughout the trip. All 8 non-affected travelers reported sharing the exact travel route with their affected members. Only one member of the latter group wore closed shoes throughout the trip, while 7 of them used open shoes or sandals at various time points. Interestingly, an insect bite was not felt by any patient. Skin lesions were first recognized by patients from as early as 7 days from journey outset, up to 12 days after the journey ended. The median number of skin lesions was one. Most lesions were located on foot (7 of 9 travelers). The hands were affected in only 2 travelers: one of them also had lesion on his right big toe and denied walking barefoot during the journey, while the other had a single hand lesion and reported episodic barefoot walking. The foot lesions
222 were either located on soles or on and around toes. Sensations of pain or mild itch in the location of skin lesion were reported by a minority of patients. Either local erythema or discharge from the skin lesions were noticed by 4 of the patients. None of the patients sought medical diagnosis for the skin lesions while traveling. As described in the Methods, the index case was diagnosed in a clinic setting by an infectious disease specialist, while only one of the other patients attended his family physician, only after the diagnosis was known. All patients conducted self manipulation of the local lesions with a needle, and 4 of them noticed eggs while doing that. Surgical exploration was not needed in any patient. The skin lesions were treated locally by an antibacterial ointment in most patients. Complete healing of the lesions was reported in all patients, occurring from 4 days up to 5 weeks from their appearance.
Discussion To the best of our knowledge, this report describes the largest outbreak of tungiasis in travelers in the literature. The small number of reported tungiasis cases, and complete absence of outbreak reports, is believed to result from travelers’ avoidance of visiting poor areas on their route.11,12 The current outbreak occurred in Ethiopia where large parts of the country are economically deprived. In the face of continuously increasing demand for exotic and less traveled destinations, it might be expected that a growing number of travelers will be exposed to low resource environments. This, in turn, will probably result in increased exposure to neglected pathogens, such as T. penetrans. As a result of this outbreak there are important implications for the field of travel medicine. Awareness of tungiasis should be raised among travel practitioners and family physicians, who may encounter returning travelers. Pre-travel recommendations should include minimization of exposure by avoiding, as much as possible, walking barefoot or with open footwear. Travelers should be instructed to avoid self manipulation of lesions, and to seek appropriate medical advice in case they develop skin lesions compatible with tungiasis. This will help to avoid the danger of superimposed infection.4 Increased knowledge among medical personnel regarding the diagnosis, natural history, and appropriate management would also prevent unnecessary investigations and inappropriate treatments. We recently encountered a highly illustrative case, in which an associate infectious disease physician returned from a trip in Ethiopia with a skin lesion on the big toe, which necessitated a diagnostic biopsy for suspicion of malignant melanoma, only to find out that it was in fact tungiasis, promptly diagnosed by the pathologist (personal communication). Travelers returning with tungiasis may serve as “Trojan horses” due to the potential of spreading the parasite’s eggs; these eggs, in turn, can develop into mature parasites, and infest bystanders. Such a mechanism was strongly considered in a case of an Italian lifeguard, who developed tungiasis despite never visiting an endemic country. The sources in the latter case were probably African street vendors coming from the sub-Saharan region, and walking barefoot on the beach.13
M. Grupper, I. Potasman Several features of this outbreak exemplify the difficulty of determining the exact place where the exposure to the parasite took place. Interestingly, the skin lesions were first noticed by patients at highly variable time points. Moreover, the event of parasite penetration into the skin was unnoticed by all patients. This is consistent with current knowledge regarding the considerable difference between individuals in the perception of parasite penetration. Natives are much more likely to report the sensation of penetration than “newcomers”. It has been suggested that the perception of the particular pain and itching associated with the entrance of the parasite to the epidermis, depends on the experience of the individual with previous exposures.8,9 Thus, we could not state whether all cases were exposed simultaneously or on separate occasions. The current study has certain limitations. Only the index case was diagnosed by physically attending a physician; others were self diagnosed using reference photographs of tungiasis skin lesions. In spite of this, we feel confident with the diagnosis in all cases. Considering that all cases participated in the same trip, the typical location of the skin lesions, and the disease trajectory, there does not appear to be other matching diagnosis. In addition, tungiasis is diagnosed clinically,4 thus permitting a visual diagnosis. Recall bias cannot be ruled out in the current study considering its retrospective nature. Nevertheless, the short time frame from the trip end to the time of diagnosis and conduction of the study (14e21 days in all cases), is reassuring in that context. In summary, this reported outbreak of tungiasis should alert everyone involved in the field of travel medicine. As the disease course is usually benign in travelers, increased awareness to this entity may result in increased diagnosis in cases once overlooked.
Conflict of interest We declare that we have no conflict of interest. We declare that we have no financial disclosure.
References 1. Lefebvre M, Capito C, Durant C, Hervier B, Grossi O. Tungiasis: a poorly documented tropical dermatosis. Med Mal Infect 2011; 41:465e8. 2. Field V, Gautret P, Schlagenhauf P, Caumes E, Jensenius M, Gkrania-Klotsas E. EuroTravNet network. Travel and migration associated infectious diseases morbidity in Europe, 2008. BMC Infect Dis 2010;10:330. 3. Ugbomoiko US, Ariza L, Heukelbach J. Pigs are the most important animal reservoir for Tunga penetrans (jigger flea) in rural Nigeria. Trop Doct 2008;38:226e7. 4. Franck S, Feldmeier H, Heukelbach J. Tungiasis: more than an exotic nuisance. Travel Med Infect Dis 2003;1:159e66. 5. Heukelbach J, de Oliveira FA, Hesse G, Feldmeier H. Tungiasis: a neglected health problem of poor communities. Trop Med Int Health 2001;6:267e72. 6. Pilger D, Schwalfenberg S, Heukelbach J, Witt L, Mehlhorn H, Mencke N, et al. Investigations on the biology, epidemiology, pathology, and control of Tunga penetrans in Brazil: VII. The importance of animal reservoirs for human infestation. Parasitol Res 2008;102:875e80.
Outbreak of tungiasis 7. Kehr JD, Heukelbach J, Mehlhorn H, Feldmeier H. Morbidity assessment in sand flea disease (tungiasis). Parasitol Res 2007; 100:413e21. 8. Feldmeier H, Eisele M, Van Marck E, Mehlhorn H, Ribeiro R, Heukelbach J. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: IV. Clinical and histopathology. Parasitol Res 2004; 94:275e82. 9. Eisele M, Heukelbach J, Van Marck E, Mehlhorn H, Meckes O, Franck S, 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;90:87e99.
223 10. Heukelbach J, Wilcke T, Eisele M, Felmeier H. Ectopic localization of tungiasis. Am J Trop Med Hyg 2002;67:214e6. 11. Caumes E, Carrie `re J, Guermonprez G, Bricaire F, Danis M, Gentilini M. Dermatoses associated with travel to tropical countries: a prospective study of the diagnosis and management of 269 patients presenting to a tropical disease unit. Clin Infect Dis 1995;20:542e8. 12. Herbinger KH, Siess C, Nothdurft HD, von Sonnenburg F, Loscher T. Skin disorders among travellers returning from tropical and non-tropical countries consulting a travel medicine clinic. Trop Med Int Health 2011;16:1457e64. 13. Veraldi S, Carrera C, Schianchi R. Tungiasis has reached Europe. Dermatology 2000;201:382.