Abstract

Objectives

Data are lacking on the spectrum of sexually transmitted diseases (STDs) diagnosed in returning travelers.

Study Design

All consecutive travelers consulting our tropical unit between November 1, 2002 and October 31, 2003 were included if they presented within 1 month after their return from the tropics, with mucocutaneous signs suggesting STDs.

Results

Forty‐nine patients (12 women and 37 men; median age 36.4 y, 35 heterosexuals) were included. Four patients had traveled with their usual sexual partner and 45 patients had casual sex while abroad (31 with locals and 14 with other tourists). The main diagnoses were gonococcal urethritis (n= 18), herpes simplex virus 2 infection (n= 12), urethritis of undetermined origin (n= 9),Chlamydia trachomatis infection (n= 4), primary syphilis (n= 4), and primary human immunodeficiency virus infection (n= 2).

Conclusions

These results illustrate the broad spectrum of STDs contracted by travelers to the tropics. They suggest the need to also inform travelers of the risks of STD and to promote the use of condoms in case of casual sex while abroad.

Travel is a major factor contributing to the spread of sexually transmitted infections (STIs), as it removes many of the social taboos that normally restrict sexual behavior. It has been reported that between 5% and 51% of short‐term travelers engage in casual sex abroad, and the rate is even higher among long‐term travelers. 1 A recent cohort study of Belgian and Dutch travelers showed that 4.7% had sexual contact with a new partner during travel and that this contact was usually unexpected, 2 whereas a cohort study of Finns traveling worldwide in the 1980s showed that 39% engaged in at‐risk sexual behavior 3 and a Swiss cohort of travelers in the 1990s found that 51% engaged in casual sex abroad. 4

It is estimated that between 24% and 75% of travelers use condoms when having casual sex abroad. 5–8 Such behavior clearly places travelers at risk of STI. However, previous studies have focused more specifically on the prevention of STI and on at‐risk behavior in travelers. 1–8 To the best of our knowledge, specific evaluation of STIs diagnosed among returning travelers has not been performed so far. The spectrum of STIs contracted in this setting is thus unknown. We decided therefore to evaluate the spectrum of STIs diagnosed among travelers consulting our unit after their return from the tropics.

Materials and Methods

All consecutive adult patients consulting our tropical diseases unit in Paris, France, from November 1, 2002 to October 31, 2003, were prospectively included in the study if they presented with mucocutaneous signs suggestive of STIs that had occurred during travel or less than 1 month after their return from a tropical country. Mucocutaneous signs indicative of STIs were genital discharge, genital ulcer, inguinal bubo, buccal ulcer, and STI‐related exanthema. Exanthema was attributed to STIs [ie, primary human immunodeficiency virus (HIV) infection or secondary syphilis] according to the results of lab tests. Patients with recurrent genital or oral lesions, chronic herpes simplex virus (HSV) infection, or hepatitis were excluded.

The following epidemiological data were recorded: age, gender, country of birth, country of residence, HIV serostatus, travel history (destination and duration), reason for travel [expatriation, tourism, business travel, and immigrants returning from visiting friends and relatives (VFR) in their country of origin], sexual orientation, number of casual sexual partners during the trip, and condom use. Travel destinations were classified according to the tropical region visited, that is, America (including the Caribbean), Asia, Africa, and Oceania.

The time between return and presentation to our unit and between return and symptom onset were recorded in each case. Final diagnoses were made by the two clinicians who examined the patients (S. A. and E. C.). Diagnoses were established by detection [direct exam, culture, and polymerase chain reaction (PCR)] of a microorganism in genital swabs (Treponema pallidum,Neisseria gonorrhoeae,Haemophilus ducreyi,Chlamydia trachomatis, HSV, and Candida spp.) or by serologic testing for an infectious agent (T pallidum, HIV) compatible with the clinical manifestations. If no specific pathogen was identified, the diagnosis was based on clinical grounds. The following signs were recorded: general health impairment, fever, genital lesions, inguinal bubo, and mouth and skin lesions. Laboratory tests included blood cell counts, urinalysis, serologic tests for C trachomatis, syphilis, viral hepatitis (hepatitis B virus and hepatitis C virus) and HIV, and PCR for C trachomatis(in male urine and female genital swabs).

The relative frequency of the diagnoses and their association with gender was analyzed with SPSS software version 9.0 (Statistical Software Inc., Los Angeles, CA, USA). The statistical significance of differences in dichotomous variables was determined by using chi‐square tests with the Fischer’s two‐tailed exact text. The alpha risk was set at 5% (two tailed).

Results

Fifty‐nine patients presented with mucocutaneous signs presumed to be related to STIs during the study period. Of these 59 patients, 10 women were excluded because their vaginal discharge was linked to candidiasis, a disease considered as not sexually transmitted. Therefore, 49 patients with STIs were included whose demographic and behavioral characteristics are summarized inTable 1. Five travelers, all immigrants, were aware that they had chronic HIV infection. Fifteen patients (30.6%) traveled alone. Of the remaining 34 patients, 4 (11.8%) traveled with their usual sexual partner, 21 with a friend (61.8%), 5 with a group (14.7%), and 4 with a colleague (11.8%). The following regions were visited: Africa (n= 30, 61.2%), Asia (n= 14, 28.6%), South America (n= 3, 6.1%), Mauritius (n= 1, 2%), and Oceania (n= 1, 2%). The median duration of travel was 14.3 days (2–45 d). The travel lasted more than 4 weeks in 19% of travelers.

Table 1

Demographic and behavioral characteristics of 49 travelers consulting with sexually transmitted diseases

 N= 49 
Median age (range), y 36.4 (18–49) 
Male 37 (sex ratio = 3.08) 
Median number of sexual partners abroad (range) 2.3 (1–4) 
Origin of sexual partners 
 Locals 31 (63.3) 
 Others tourists 14 (28.6) 
 Usual sexual partner 4 (8.1) 
Homosexual men 10 (16.9) 
Heterosexuals 35 (76.3) 
Bisexual men 4 (6.8) 
Tourists 26 (53) 
Immigrants visiting friends and relatives 15 (30.6) 
Business 4 (8.2) 
Expatriate 4 (8.2) 
Vacationing 41 (83.7) 
Business 8 (16.3) 
 N= 49 
Median age (range), y 36.4 (18–49) 
Male 37 (sex ratio = 3.08) 
Median number of sexual partners abroad (range) 2.3 (1–4) 
Origin of sexual partners 
 Locals 31 (63.3) 
 Others tourists 14 (28.6) 
 Usual sexual partner 4 (8.1) 
Homosexual men 10 (16.9) 
Heterosexuals 35 (76.3) 
Bisexual men 4 (6.8) 
Tourists 26 (53) 
Immigrants visiting friends and relatives 15 (30.6) 
Business 4 (8.2) 
Expatriate 4 (8.2) 
Vacationing 41 (83.7) 
Business 8 (16.3) 

Values are given as n(%) unless otherwise stated.

During the trip, 32 patients had one sexual partner and the other 17 patients (34.7%) had at least two partners. Thirty‐one patients (63.3%) had casual sex abroad with locals, 14 (28.6%) with other tourists, and 4 (8.1%) with their usual sexual partner (Figure 1). Among the 45 patients who had casual sex abroad, 18 patients (40%) reported irregular condom use and 27 (60%) never used condoms. Finally, none of the patients used condoms systematically.

Figure 1

Diagnosis of sexually transmitted diseases among 49 travelers, according to casual sex abroad.

Figure 1

Diagnosis of sexually transmitted diseases among 49 travelers, according to casual sex abroad.

The median interval between return and presentation to our unit was 13.6 days (1–39 d). Symptoms started during travel in 20 patients (40.8%). In the remaining 29 patients, the median interval between return and symptom onset was 9.1 days (1–25 d). Among the 20 patients who developed symptoms during the trip, only 5 (25%) had consulted a doctor in the country of travel.

Various STIs were diagnosed (Table 2). The leading STI was genital gonorrhea (18 patients), which was only observed in men (p< 0.001). The men were infected in Asia in 7 patients (38.8%) and Africa in 11 patients (61.1%). Four of the 18 isolates of N gonorrhoeae exhibited decreased susceptibility to fluoroquinolones (resistant to nalidixic acid and sensitive or intermediate‐resistant to ciprofloxacin); these patients had all visited Asia (Thailand in two patients and Cambodia in two patients).

Table 2

Sexually transmitted diseases diagnosed in 12 women and 37 men consulting after their return from the tropics

 Women Men 
Gonococcal urethritis (n= 18) 18 
Genital or oral herpes (n= 12) 
Undetermined urethritis (n= 9) 
Primary syphilis (n= 4) 
Chlamydia urethritis (n= 4) 
Primary human immunodeficiency virus infection (n= 2) 
Total 12 37 
 Women Men 
Gonococcal urethritis (n= 18) 18 
Genital or oral herpes (n= 12) 
Undetermined urethritis (n= 9) 
Primary syphilis (n= 4) 
Chlamydia urethritis (n= 4) 
Primary human immunodeficiency virus infection (n= 2) 
Total 12 37 

Primary HSV2 infection was the second most prevalent STI (n= 12). The infection was oral in two women and genital in four women and six men. We diagnosed four patients with primary syphilis, all involving male homosexuals, who presented with genital chancre in three patients and oral chancre in one patient. Two of these patients were known to be infected by HIV.Chlamydia trachomatis urethritis was diagnosed by PCR in three women with cervicovaginitis and in one man with nongonococcal urethritis. This latter patient was the sexual partner of one of the three infected women. The cause of urethritis was undetermined in nine travelers who had received antibiotics before consulting our unit or who refused additional tests. Two patients with febrile rash related to primary HIV infection were diagnosed, a man returning from Cambodia and a woman returning from the Democratic Republic of Congo.

Among the 14 homosexual men, 7 (50%) were diagnosed with gonorrhea, 4 (28.6%) with primary syphilis, and 3 (28.6%) with HSV2 infection. Among the five patients with known HIV infection, two contracted syphilis, one genital HSV2 infection, and 2 gonococcal urethritis. Four patients who traveled with their usual sexual partner consulted for oral (n= 1) or genital HSV2 infection (n= 2) or undetermined urethritis (n= 1).

Discussion

There are several possible weaknesses with our study. First, we did not assess reasons for referral, that is, self‐referral due to their recent travel or medical referral by general practitioners (GPs) or other doctors. In a similar study, however, performed over a 6‐month period in the same unit, two thirds of our patients were referred to us by their GP. 9 Second, our travelers probably do not reflect the population as a whole of travelers returning from the tropics with STIs as the majority probably consults their GP first. Finally, we only focused on the presenting population of travelers with sexually transmitted diseases (STDs), that is, those with clinical signs, whereas many STIs are primarily asymptomatic.

The place occupied by STIs in the spectrum of health care problems occurring in travelers has changed over the years. In the 1980s, STIs were one of the leading health care problems during travel or after return, genital discharge (urethritis and vaginitis) and genital ulcer being the most frequent identified infection. 10,11 Conversely, in prospective studies performed in the late 1990s, STIs no longer appeared to be a leading health impairment among travelers. 12,13 It is worth noting, however, that these latter studies were done before the widespread resurgence of STIs in the early 2000s.

Despite these apparent trends, STIs probably remain a common cause of health impairment among travelers returning from the tropics. In a cohort of 622 consecutive French travelers with health impairments in 2003 to 2004, STIs were the sixth reason for seeking medical advice (3.7%) after return. 9 Similarly, Hawkes and colleagues 14 reported that 5.7% of 731 returning travelers seen at the Hospital for Tropical Diseases in London had contracted an STI during their most recent travel experience. The overall incidence of STIs in a Swiss study has been estimated as 1.6% among those VFR and 0.3% in conventional travelers. 15 The proportionate morbidity for travel‐related STI and HIV infection was estimated to be 8 of 1,000 and 2 of 1,000, respectively, among 17,353 patients, recruited in 30 tropical disease centers worldwide. The authors themselves, however, considered these rates to be underestimated, 16 suggesting that people with STIs self‐recognized risk experience and consulted elsewhere than in tropical disease units.

Unsurprisingly, 45 of 49 patients (91.8%) had casual sex while abroad, with locals or other tourists. But the reasons behind why our travelers with STIs had casual travel sex and did not adhere to existing travel health/STD prevention efforts were not assessed. Factors associated with casual sex abroad have been investigated in three large cohort studies of Europeans traveling worldwide and two on‐site studies performed in traveling destinations. 2,5–8 Combined, these studies demonstrated the main factors associated with having casual travel sex being male, traveling alone, alcohol or drugs use, having had casual sex contacts in home country, expectation of a new sexual partner during travel, and, possibly, being VFR travelers.

The main STIs diagnosed in our cohort were urethritis (mainly due to N gonorrhoeae) and primary HSV2 infection. The only results that may be comparable are from a very differently designed British study of 386 travelers, of whom 61 had an STI presumably contracted during travel. Here, nonspecific urethritis (31.1%), primary human papilloma virus (32.8%),Trichomonas vaginalis(6.5%),N gonorrhoeae(8.2%), and HSV infections (6.5%) were the leading STIs. 7 The spectrum of STIs diagnosed in our cohort of 49 travelers and this subgroup of 61 British patients with an STI and a history of travel looks thus quite different. However, the link between the travel and the STI is probably better established in our study than in the British study (mean of 9 d compared to 3 mo between travel and consultation). 7 In addition, our results agree better with those found in large epidemiological studies of travelers in which genital discharge and genital ulcer were the most frequent diagnoses. 10

Neisseria gonorrhoeae is the major STI threat in travelers. In a study performed in the 1980s, gonorrhea was the fourth identified infection in short‐term visitors to developing countries. 10 In addition,N gonorrhoeae resistance to antibiotics is increasing. 17 In our study, 4 (18%) of the 22 isolates showed diminished sensitivity to quinolones. All four patients had visited Asia. Likewise, most quinolone‐resistant gonococci identified in Australia between 1991 and 1995 were isolated from travelers returning from the Philippines or other Asian destinations. 18 The prevalence of fluoroquinolone resistance among N gonorrhoeae isolates in Asia in 2001 was reported to be 86.9% in China, 64% in Japan, and 54.3% in the Philippines. 17 This resistance has now spread beyond Asia, reaching a prevalence of 13% in 2002 in France and 19.7% in 2001 in Hawaii. 19

HSV2 infection was the second cause of STI in our cohort. This result agrees with those found in on‐site studies and one large epidemiological study of travelers where genital ulcer was a frequent diagnoses. 10,11 Of note, our results point to the fact that genital herpes is the leading cause of genital ulcer in travelers as it is the case in the general population. It is worth noting that two female travelers had only oral HSV2 infection acquired after unprotected orogenital intercourse but either no or protected vaginal intercourse.

The four patients with primary syphilis were diagnosed in male homosexuals. Considering the resurgence of syphilis in many developed countries among men who have sex with men, the sometimes confusing clinical presentation, and the common implication of oral sex for transmission, diagnosis should be systematically suspected in patients returning from abroad with oral or genital lesion and a history of casual sex.

Primary HIV infection was diagnosed in 4% of our travelers with STDs. Both presented with febrile exanthema but had no genital lesions. In a recent study concerning 62 travelers returning from abroad with febrile exanthema, primary HIV infection was diagnosed in 3% of the travelers. 20 This diagnosis must therefore be ruled out in every traveler presenting with febrile exanthema with a history of casual sex abroad. Indeed, in a cohort of Belgian expatriates studied between 1985 and 1987, risk factors for HIV seroconversion were sexual contact with local women (OR = 14.7), sexual contact with prostitutes (OR = 10.8), and injections by unqualified staff (OR = 13.5). 21 Similarly, our two patients with primary HIV infection had had sexual intercourse with locals.

In conclusion, this study shows a broad spectrum of STIs diagnosed among travelers returning from the tropics, ranging from urethritis to severe infections such as HIV. Given the high frequency of STIs, preventive advice should target identified subgroups of travelers, and use of condoms should be systematically advised to protect travelers and their partners, and to try and stem the worldwide spread of STIs.

We thank Michel Janier for helpful reviewing.

Declaration of interests

The authors state that they have no conflicts of interest.

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