Abstract

Background

Hookworm‐related cutaneous larva migrans (CLM) and tungiasis are commonly diagnosed in travelers returning from endemic areas, but reliable data on disease occurrence do not exist. To describe the occurrence of CLM and tungiasis in international travelers, a cross‐sectional study was done.

Method

We conducted an airport survey in European travelers exiting northeast Brazil. Questionnaires were distributed at the departure gate of the international airport of Fortaleza (Ceará State) while passengers were waiting to board their plane. The questionnaire included questions on personal characteristics, pretravel health advice, acquired parasitic skin diseases during their stay in Brazil, and clinical characteristics of the infestation. To help identify CLM and tungiasis, photographs of the typical appearances of the infestations were presented.

Results

Data from 372 tourists (aged 16–76 y, median = 40 y) were available for analysis; 45% had obtained pretravel health advice, usually from travel clinics (46.2%) and Internet sites (39.6%). Only 14% of those who obtained advice had been informed about CLM as a travel health risk and 22% about tungiasis. During their stay in Brazil, 12 (3.2%) tourists had experienced tungiasis and 3 (0.8%) CLM. In all cases, lesions were confined to the feet. The three travelers with CLM complained of irritability; itching was present in two cases. Pain (58.3%) and itching (50%) were the most common symptoms in travelers with tungiasis. The length of stay was a clear predictor for tungiasis, with a 20 times higher occurrence in travelers who had stayed for more than 4 weeks in Brazil.

Conclusions

Tungiasis and CLM are not rare in international tourists departing from Brazil, and pretravel counseling is insufficient. Pretravel health advice should include information on the risk of acquiring tungiasis and CLM and how to prevent an infestation. Airport surveys using questionnaires can be used to obtain incidence data on both parasitic infestations.

People from moderate climates traveling to tropical regions are exposed to a series of health hazards, including the risk of acquiring infectious and particularly parasitic diseases. 1,2

Tungiasis, a parasitic skin disease, is endemic in Latin America, in several Caribbean countries, and in sub‐Saharan Africa. 3 It is caused by the permanent penetration of the female jigger flea Tunga penetrans into the epidermis.

Tungiasis is unequally distributed in the affected countries, and prevalence may be as high as 50% in risk areas. 4 Jigger fleas are also regularly seen in returning travelers. 5–7 Recently, tungiasis was diagnosed in a group of refugees from Tanzania arriving in Australia. 8

Hookworm‐related cutaneous larva migrans (CLM) is ubiquitous in the subtropics and tropics. CLM occurs after infestation with larvae of animal nematodes, such as Ancylostoma braziliense. These nematodes usually parasitize dogs and cats, but larvae may also penetrate into the epidermis of humans. 9 CLM is one of the most common imported parasitic infestation diagnosed in travel clinics. 2,6,7,10–14

Reliable data on the frequency of parasitic skin diseases in travelers are not at hand because only a small proportion of those infested present at specialized clinics and occurrence is not registered in national infectious disease databases.

CLM and tungiasis are highly endemic in resource‐poor communities in northeast Brazil, irrespective of whether they are located on the coast or in the rural areas. 15–17 For example, prevalence of CLM and tungiasis may reach 3 and 54%, respectively, in an urban slum in Fortaleza, a capital city in northeast Brazil. 17,18

In case reports, returning travelers from Brazil have also been described to be infested. 5,19 There were around 5 million incoming travelers in 2004, most of them from European countries. 20 In northeast Brazil, tourists spend most of their time at beaches, but excursions to the rural hinterland become more and more popular.

To assess whether European travelers are at risk to acquire tungiasis or CLM, to describe disease‐related behavior, and to identify factors associated with an infestation, we conducted a cross‐sectional study at an airport. This is the first airport survey focusing on parasitic skin diseases.

Methods

The study was conducted at the International Airport “Pinto Martins” in Fortaleza, the capital of Ceará State (northeast Brazil). The state is a popular tourist destination, mainly for Europeans. The coast of Ceará is known for its beautiful beaches and a sunny climate, with about 360 days of sunshine per year.

The survey was done in December 2004, the peak tourist season. In this period, prevalence of tungiasis is highest but lowest for CLM in affected communities in northeast Brazil. 17,18

During a period of 2 weeks, all passengers boarding on intercontinental flights to European destinations were eligible for the study. Pretested, structured and anonymous questionnaires were distributed by trained personnel at the international departure gate of the airport while passengers were waiting to board their plane.

Travelers were only asked to participate if they were ≥16 years of age, fully understood the language of the questionnaire, and were of non‐Brazilian nationality, living permanently in a European country. The questionnaires were available in English, Portuguese, German, Italian, Spanish, French, and Dutch.

We tested the questionnaires in a pilot study and adapted them afterward. Questions asked concerned personal characteristics (age, sex, nationality, country of residence, length of stay); pretravel health advice (source and type of information obtained) and, if experienced, on the clinical characteristics of CLM and tungiasis; and what the traveler did after becoming infested (localization of lesions, symptoms and signs, therapy). In addition, we asked about the places visited and about risk behavior when being on the beach, such as the use of towels and footwear.

To help identify CLM and tungiasis, we presented photographs of the appearance of both parasitic infestations. In the pilot study, we had observed that travelers were able to recognize CLM and tungiasis based on such images and that they did not mistake one disease for the other. Members of the research team were present to respond to questions.

Data were entered into a database, checked for entry errors, and analyzed using the Epi Info software package (version 6.04d; CDC, Atlanta, GA, USA). Relative frequencies were compared using the chi‐square test and the Fisher’s exact test.

The study was approved by the Brazilian airport authority (INFRAERO) and the Federal Police of the airport. We obtained oral consent from the participants. The travelers participated in the survey on a voluntary basis. All data were kept confidential.

Results

In total, 372 (82.7%) of 450 questionnaires were returned and included in the data analysis. A total of 78 travelers refused to participate in the study. The characteristics of the respondents are detailed in Table 1. The majority were male. Almost two thirds resided in Portugal, The Netherlands, or Italy (Table 1).

Table 1

Characteristics of 372 international travelers exiting northeast Brazil, 2004

Characteristics 
Age (y), median (interquartile range) 40 (31–50) 
Sex, n (%)* 
 Female 89 (24.8) 
 Male 270 (75.2) 
Nationality, n (%) 
 Portuguese 103 (27.7) 
 Dutch 74 (19.9) 
 Italian 63 (16.9) 
 German 50 (13.4) 
 Austrian 17 (4.6) 
 Spanish 10 (2.7) 
 Norwegian 10 (2.7) 
 British 10 (2.7) 
 Other 37 (9.9) 
Length of stay in Brazil (d), median (interquartile range) 14 (8–21) 
Characteristics 
Age (y), median (interquartile range) 40 (31–50) 
Sex, n (%)* 
 Female 89 (24.8) 
 Male 270 (75.2) 
Nationality, n (%) 
 Portuguese 103 (27.7) 
 Dutch 74 (19.9) 
 Italian 63 (16.9) 
 German 50 (13.4) 
 Austrian 17 (4.6) 
 Spanish 10 (2.7) 
 Norwegian 10 (2.7) 
 British 10 (2.7) 
 Other 37 (9.9) 
Length of stay in Brazil (d), median (interquartile range) 14 (8–21) 
*

Information on sex was not provided in all cases.

In decreasing order: Swiss, French, Belgian, Polish, Danish, Swedish, Slovenian, Croatian.

Less than half of the respondents had obtained any type of pretravel health advice (Table 2). The most common sources of information were travel clinics and travel‐related Internet sites. However, only 14% of those who obtained advice had been informed about the risk of acquiring CLM and 22% about tungiasis (Table 2). About one fifth of the respondents had heard about CLM or tungiasis when leaving Brazil.

Table 2

Pretravel advice and knowledge on parasitic skin diseases of international travelers exiting northeast Brazil, 2004 (n = 372)

 n (%) 
Pretravel health advice 169 (45.4) 
Sources of advice* 
 Travel clinic 78 (46.2) 
 Internet sites 67 (39.6) 
 Friends 10 (5.9) 
 General practitioner 9 (5.3) 
 Travel magazines or travel guides 6 (3.6) 
 Travel agency 5 (3.0) 
 Other sources 9 (5.3) 
Health information on* 
 Cutaneous larva migrans 23 (13.6) 
 Tungiasis 37 (21.9) 
Knowledge of 
 Cutaneous larva migrans 60 (16.1) 
 Tungiasis 79 (21.2) 
 n (%) 
Pretravel health advice 169 (45.4) 
Sources of advice* 
 Travel clinic 78 (46.2) 
 Internet sites 67 (39.6) 
 Friends 10 (5.9) 
 General practitioner 9 (5.3) 
 Travel magazines or travel guides 6 (3.6) 
 Travel agency 5 (3.0) 
 Other sources 9 (5.3) 
Health information on* 
 Cutaneous larva migrans 23 (13.6) 
 Tungiasis 37 (21.9) 
Knowledge of 
 Cutaneous larva migrans 60 (16.1) 
 Tungiasis 79 (21.2) 
*

Of those who obtained pretravel health advice.

Among the respondents, 12 (3.2%) were infested with tungiasis during their stay in Brazil and 3 (0.8%) acquired CLM (Table 3). In all cases of tungiasis and CLM, lesions were confined to the feet. Symptoms and signs are summarized in Table 3. Interestingly, 15% of travelers who had stayed for 4 weeks or more in Brazil were infested with T penetrans during their stay.

Table 3

Infestation during stay in Brazil and clinicoepidemiological characteristics of international travelers exiting northeast Brazil, 2004

 n (%) 
Tungiasis 
 Infested during stay 12 (3.2) 
 Body part affected 
  Foot 12 (100) 
 Symptoms and signs 
  Pain 7 (58.3) 
  Itching 6 (50) 
  Erythema 4 (33.3) 
  Irritability 1 (8.3) 
  Sleep disturbances 1 (8.3) 
 Treatment 
  Embedded flea was taken out by a nonmedical local with a needle 8 (66.7) 
  Embedded flea was taken out by the traveler 3 (25) 
  Thiabendazole ointment 1 (8.3) 
Cutaneous larva migrans 
 Infested during stay 3 (0.8) 
 Body part affected 
  Foot 3 (100) 
 Symptoms and signs 
  Irritability 3 (100) 
  Itching 2 (66.7) 
  Erythema 2 (66.7) 
  Pain 1 (33.3) 
  Sleep disturbances 1 (33.3) 
 Treatment 
  Topical thiabendazole ointment 3 (100) 
 n (%) 
Tungiasis 
 Infested during stay 12 (3.2) 
 Body part affected 
  Foot 12 (100) 
 Symptoms and signs 
  Pain 7 (58.3) 
  Itching 6 (50) 
  Erythema 4 (33.3) 
  Irritability 1 (8.3) 
  Sleep disturbances 1 (8.3) 
 Treatment 
  Embedded flea was taken out by a nonmedical local with a needle 8 (66.7) 
  Embedded flea was taken out by the traveler 3 (25) 
  Thiabendazole ointment 1 (8.3) 
Cutaneous larva migrans 
 Infested during stay 3 (0.8) 
 Body part affected 
  Foot 3 (100) 
 Symptoms and signs 
  Irritability 3 (100) 
  Itching 2 (66.7) 
  Erythema 2 (66.7) 
  Pain 1 (33.3) 
  Sleep disturbances 1 (33.3) 
 Treatment 
  Topical thiabendazole ointment 3 (100) 

Most travelers with tungiasis asked local nonmedical people to take out the embedded flea or took it out by themselves (Table 3). All travelers with CLM treated themselves with topical thiabendazole ointment (available over the counter in Brazil). None of the travelers planned to counsel a travel clinic after returning to their country of residence concerning the infestation experienced in Brazil.

Factors associated with the risk of acquiring CLM or tungiasis are depicted in Table 4. Apparently, due to the small number of travelers with CLM, no significant associations could be revealed. However, CLM only occurred in travelers who had visited beaches. One infested traveler stated having walked barefooted on the beach, and the other two always used thongs or sandals. The condition seemed also to be more common in travelers who had stayed longer in Brazil (Table 4).

Table 4

Risk factors associated with the presence of CLM or tungiasis in international travelers exiting northeast Brazil, 2004

 N n (%) Infested OR (95% CI) p Value 
CLM 
 Length of stay in Brazil > 4 wk* 
  Yes 57 2 (3.5) 10.84 (0.74–312.74) =0.07 
  No 299 1 (0.3)   
 Visited beaches 
  Yes 349 3 (0.9) Undefined =1.0 
  No 23 0 (0)   
 Time of the day spent on the beach 
  Morning (until 12 pm) 259 2 (0.8) 0.68 (0.05–19.65) =0.6 
  Afternoon (12 pm to 6 pm) 292 3 (1.0) Undefined =1.0 
  Night (after 6 pm) 34 2 (6.3) 19.56 (1.32–571.36) =0.03 
 Always sat on a chair on the beach* 
  Yes 153 3 (2.0) Undefined =0.1 
  No 164 0 (0)   
 Always sat or lay down on humid sand* 
  Yes 26 0 (0) 0.0 (0.0–29.1) =1.0 
  No 316 3 (0.9)   
 Always wore shoes or slippers on the beach* 
  Yes 63 2 (3.2) 9.31 (0.64–268.33) =0.09 
  No 285 1 (0.4)   
Tungiasis 
 Length of stay in Brazil > 4 wk* 
  Yes 60 9 (15) 25.85 (4.94–181.25) <0.0001 
  No 295 2 (0.7)   
 Visited beaches 
  Yes 347 10 (2.9) 0.65 (0.08–14.48) =0.5 
  No 23 1 (4.3)   
 Time of the day spent on the beach 
  Morning (until 12 pm) 258 8 (3.1) 1.39 (0.26–9.82) =1.0 
  Afternoon (12 pm to 6 pm) 289 6 (2.1) 0.29 (0.07–1.27) =0.07 
  Night (after 6 pm) 31 2 (6.5) 2.66 (0.00–14.7) =0.2 
 Always sat on a chair on the beach* 
  Yes 149 1 (0.7) 0.22 (0.01–1.96) =0.2 
  No 165 5 (3.0)   
 Always sat or lay on humid sand* 
  Yes 26 0 (0) 0.0 (0.0–10.04) =1.0 
  No 313 7 (2.2)   
 Always wore shoes or slippers on the beach* 
  Yes 59 2 (3.4) 1.23 (0.0–6.56) =0.7 
  No 288 8 (2.8)   
 N n (%) Infested OR (95% CI) p Value 
CLM 
 Length of stay in Brazil > 4 wk* 
  Yes 57 2 (3.5) 10.84 (0.74–312.74) =0.07 
  No 299 1 (0.3)   
 Visited beaches 
  Yes 349 3 (0.9) Undefined =1.0 
  No 23 0 (0)   
 Time of the day spent on the beach 
  Morning (until 12 pm) 259 2 (0.8) 0.68 (0.05–19.65) =0.6 
  Afternoon (12 pm to 6 pm) 292 3 (1.0) Undefined =1.0 
  Night (after 6 pm) 34 2 (6.3) 19.56 (1.32–571.36) =0.03 
 Always sat on a chair on the beach* 
  Yes 153 3 (2.0) Undefined =0.1 
  No 164 0 (0)   
 Always sat or lay down on humid sand* 
  Yes 26 0 (0) 0.0 (0.0–29.1) =1.0 
  No 316 3 (0.9)   
 Always wore shoes or slippers on the beach* 
  Yes 63 2 (3.2) 9.31 (0.64–268.33) =0.09 
  No 285 1 (0.4)   
Tungiasis 
 Length of stay in Brazil > 4 wk* 
  Yes 60 9 (15) 25.85 (4.94–181.25) <0.0001 
  No 295 2 (0.7)   
 Visited beaches 
  Yes 347 10 (2.9) 0.65 (0.08–14.48) =0.5 
  No 23 1 (4.3)   
 Time of the day spent on the beach 
  Morning (until 12 pm) 258 8 (3.1) 1.39 (0.26–9.82) =1.0 
  Afternoon (12 pm to 6 pm) 289 6 (2.1) 0.29 (0.07–1.27) =0.07 
  Night (after 6 pm) 31 2 (6.5) 2.66 (0.00–14.7) =0.2 
 Always sat on a chair on the beach* 
  Yes 149 1 (0.7) 0.22 (0.01–1.96) =0.2 
  No 165 5 (3.0)   
 Always sat or lay on humid sand* 
  Yes 26 0 (0) 0.0 (0.0–10.04) =1.0 
  No 313 7 (2.2)   
 Always wore shoes or slippers on the beach* 
  Yes 59 2 (3.4) 1.23 (0.0–6.56) =0.7 
  No 288 8 (2.8)   

CLM = cutaneous larva migran.

*

Data were not available in all cases.

Fisher’s exact test.

The length of stay was a clear predictor for tungiasis: the prevalence of the infestation was more than 20 times higher in travelers who had stayed for more than 4 weeks in Brazil (Table 4). One tourist had stayed for 60 days in Brazil and experienced both CLM and tungiasis.

Discussion

Our study shows that a considerable number of travelers acquired tungiasis (3.2%) but less than 1% had acquired CLM during an average stay of 2 weeks in northeast Brazil. Infestation with tungiasis was strongly correlated with the length of stay. Our data do not allow us to conclude if this is mainly due to a riskier behavior of long‐term travelers or due to the different places visited.

Airport studies have frequently been used to obtain data on knowledge and risk perception regarding infectious diseases. 21–26 In general, similar to our data, these studies demonstrated that knowledge on health risks and modes of transmission of infectious agents is rather poor. To our knowledge, this is the first airport study describing the occurrence of parasitic skin diseases in returning travelers and the associated risk factors for infestation.

However, airport surveys clearly have a limited value to assess disease occurrence. Many parasitic diseases have a relatively long incubation period or do not show characteristic symptoms and signs. Consequently, they are not diagnosed during travel. On the other hand, acute diseases and incidents, such as travelers’ diarrhea, bee bites, and injuries, can be studied at travel destinations and can give more accurate estimations of occurrence than studies based on travel clinic data in the country of origin. 27–29 In contrast to other parasitic diseases, tungiasis and CLM are easily diagnosed, even by nonmedical personnel, and have an incubation period of only a few days. 30 Thus, airport studies are an interesting approach to obtain data on disease occurrence of both infestations in travelers and to identify the associated risk factors.

However, it is possible that patients with CLM did not present any symptoms yet and that we missed a significant number of infested individuals. This may partly explain the relatively low rate of CLM found in this study.

Usually, more patients with CLM than with tungiasis are seen at travel clinics. For example, among 269 patients with skin diseases presenting at a specialized clinic in Paris, 25% had CLM, but only 6% had tungiasis. 6 This ratio was similar in three Italian dermatology units. 7 It can be speculated that individuals with tungiasis less frequently consult specialized institutions after returning than those with CLM, as tungiasis is self‐limiting (≤3 wk) and treatment (extraction of the flea) can be done by the patient himself or herself or by an experienced local. In contrast, CLM progresses for weeks or even months and usually needs medical treatment. 10

However, all three individuals infested with CLM in our study treated themselves with topical thiabendazole while traveling in Brazil, a drug that is available over the counter in Brazil, in contrast to most European countries. The fact that the travelers treated their infestation during their stay further indicates that only a small fraction of those infested eventually consult a specialized institution at their home country. Not a single traveler stated that he or she intended to visit a travel clinic after return.

In our study, CLM only occurred in travelers who had visited beaches, but due to the small number of cases, it is difficult to conclude on any risk factors. A study on risk factors for CLM identified walking barefooted to and on the beach as risks in a group of 126 Canadian tourists to Barbados. 31 Another Canadian study found that CLM was acquired mainly on beach destinations (such as Jamaica, Barbados, Brazil, Thailand, and Mexico) and that CLM occurred more commonly in tourists compared to business travelers. 14 A recent study from France also found a correlation between tourism and CLM. 32 This is not a surprise, as tourists usually visit beaches more often than business travelers.

Using thongs protects sufficiently against CLM, as the feet do not come into contact with animal feces containing infective hookworm larvae. Thus, tourists should be advised to use thongs when walking to and on the beach, avoid beaches where dogs and cats stroll around, use a sun chair, and lie on areas on the beach where the sand has been humidified by the tide. 33

A long stay in northeast Brazil was a risk factor for acquiring tungiasis. This may not only be due to the increasing risk of exposure with time but also due to the different behavior. A long‐term traveler may more often visit resource‐poor endemic communities and in addition show a different risk‐related behavior compared to a short‐term tourist who has booked a holiday in a hotel complex. In addition, the data suggest that tungiasis is usually not acquired on beaches in northeast Brazil.

In our study, all tungiasis lesions occurred at the feet. In fact, a review of case reports on tungiasis in travelers has shown that lesions on other sites are very rare in this group. 5 This is in contrast to inhabitants of endemic areas, where ectopic localizations are common. 34 Similarly, several studies have shown that CLM lesions in travelers are mostly located at the feet, buttocks, and thighs—areas that come into contact with sand while on the beach. 6,10,31,35–37 In northeast Brazil, locals and tourists usually do not lie down on sand on the beach but sit on chairs. Correspondingly, travelers were only infested on the feet in this study.

The majority of tourists were not adequately informed about health hazards before traveling to Brazil. Pretravel health advice usually included information on hygiene, food safety, and immunizations but rarely included information on prevention of parasitic skin diseases. Considering the relatively high occurrence of parasitic infestations in travelers, there is a clear need to extend pretravel health advice and to include tungiasis and CLM.

This lack of appropriate travel information has been described previously. For example, in Manu National Park in Peru, where cutaneous leishmaniasis is endemic, the vast majority of tourists had received health advice prior to traveling, but only a very small fraction of them had ever heard about the disease. 38 Information leaflets were distributed in the area and received a very good acceptance. About 93% of travelers stated having read the leaflet on cutaneous leishmaniasis.

It may be true that the tourist industry and local authorities often prefer not to mention potential health hazards too extensively because they fear economic losses. 38 However, we suggest distributing travel health information, adapted to the local situation (such as on tungiasis and CLM) when tourists enter the endemic area.

Although the response rate in our study was relatively high (83%), our study is prone to selection bias. Due to practical reasons, we only included travelers ≥16 years of age, but children are known to be more vulnerable for acquiring parasitic skin diseases, such as tungiasis and CLM. 4,30 Participation bias may also have played a role, as tourists having experienced an infestation may be less reluctant to complete a questionnaire.

In addition, the cross‐sectional design does not take into account the seasonal dynamics of both diseases. In Brazil, population‐based studies have shown that CLM and tungiasis have a considerable seasonal variation, with lowest incidence of CLM in the dry season, when occurrence of tungiasis peaks. 17,18 Thus, in the rainy season, when incidence of CLM in endemic communities is 15 times higher compared to the dry season, the number of tourists experiencing CLM can be expected to be higher, whereas the opposite may be observed with tungiasis. This study was done in December, the end of the dry season. In the rainy season, the incidence of CLM in tourists may be considerably higher.

We conclude that airport studies are a feasible approach to investigate occurrence and risk factors of tungiasis and CLM. Both infestations occur in international tourists departing from Brazil, and health education avoiding exposure should be implemented. Pretravel health advice should include information on risk of tungiasis and CLM and how to prevent the infestations.

We thank the airport authority of Fortaleza International Airport “Pinto Martins” for collaboration. This study was funded by the “Deutsche Akademie für Flug und Reisemedizin,” Germany.

Declaration of interests

The authors state that they have no conflicts of interest.

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