Travel and Sexually Transmitted Infections

Authors


Brian J. Ward, Montreal General Hospital, 1650 Cedar Avenue, Room D7-153, Montreal, Quebec, Canada H3G 1A4. E-mail: brian.ward@mcgill.ca

Abstract

Increasing population mobility and increasing frequency and variety of sexually transmitted infections (STI) are closely linked around the globe. Although all mobile populations are at increased risk for acquiring STIs, international travelers are the focus of this review. Several aspects of travel such as opportunity, isolation, and the desire for unique experiences all enhance the likelihood of casual sexual experiences while abroad. The situational loss of inhibition of travel can be markedly enhanced by alcohol and drugs. Several of the most important elements of the complex interaction between travel and STIs are discussed.

The History of Sex and Travel

Sex and travel have a long and occasionally inglorious shared history. From the Huns and Vikings to the current day, unscrupulous military and paramilitary commanders have used sex to motivate men to march across deserts, row open boats across oceans, and face all manner of other perils.1 Old sailors’ ballads make it clear that the promise of exotic sex in distant lands contributed to the willingness of young men to sign up for the navy or to serve on whaling vessels.2 When Captain Cook’s crew discovered that Tahitian women would trade sex for iron nails, guards had to be posted to prevent the boats from being dismantled, plank by rapturous plank.3 The less humorous consequence of this 17th century meeting of cultures is the subject of this review. Within months of their arrival in Tahiti, half of Cook’s crew had venereal diseases leading him to write that “we will be forever damned by the fact that we brought these diseases to these islands.” Since Cook’s time, there has been a remarkable democratization of travel: exotic itineraries are now accessible to a large majority of those living in the developed world including both genders and the extremes of age. Sex is still sex, however, and many will still do remarkably silly things in its pursuit. As a result, the population at risk of acquiring “exotic” sexually transmitted infections (STI) is steadily increasing. The purpose of the current review is to provide travel medicine practitioners with an up-to-date understanding of the complex relationship between sex and travel.

STIs—Global Overview

In the past 20 to 30 years, there has been a remarkable growth in population mobility both within and across national boundaries. The World Travel Organization estimates that ∼700 million people crossed international borders in 2002 for work, study, or pleasure and that traffic in 2003 to 2004 exceeded 1 billion such trips.4 All mobile populations including business travelers, expatriates, soldiers, and tourists are at increased risk for acquiring STIs.5–8 The anonymity of travel, the sense of isolation brought on by unfamiliar surroundings, and the desire for unique experiences all encourage travelers to shed social and sexual inhibitions. The risk of acquiring an STI may be enhanced in mobile populations by poor understanding of the global epidemiology of these infections9 and the means available to mitigate risk. Rates of STIs may also be elevated among migrant and marginalized populations (eg, refugees, internally displaced, street youth), and these populations may be overrepresented among commercial sex workers (CSW) in many countries.6,9–14 Many of the risk factors for disease acquisition in these vulnerable populations are distinct, however, and will not be addressed in this review.

STIs are among the most common notifiable infections worldwide, and rates are particularly high in many developing countries. In 1990, the WHO estimated the global burden of curable STIs at >250 million cases [syphilis, gonorrhea (GC), chlamydia, and trichomoniasis].15 Estimates rose to 333 and 340 million new cases of these infections in 1995 and 1999.8 The 1999 estimate includes 151 million cases in South/Southeast Asia, 38 million in Latin America, and 69 million in Africa.16,17 In many developing world countries, these increasing numbers have been fueled by the economic and societal disruption of the human immunodeficiency virus (HIV) pandemic. In sub-Saharan Africa in particular, there has been an explosive growth in the number of children who have lost one or both parents (∼14–20 million in 2000).18 In the mid-1990s, >40,000 street children were thought to live in Nairobi alone where many had been driven to trade sex for food to survive.19,20 Although HIV, syphilis, and GC are usually in the STI spotlight, more than 20 different infectious agents can be acquired and/or spread by various types of sexual contact9,21 (eg, vaginal sex, anal sex, oral–genital/oral–anal contact; Table 1). Although the prevalence rates for many of these infectious agents still vary widely by geographic region [eg, human lymphotropic virus (HTLV)-1, chancroid], changes in migration, immigration, and travel patterns during the past 50 years have ensured that almost any STI can be acquired anywhere in the world. As a result, the risk of acquiring a given STI in any particular setting is best considered in quantitative rather than qualitative terms.

Table 1.  Sexually transmitted infections
  1. Note that any “list” of diseases transmissible by sexual activity is somewhat arbitrary. The actual agents and risks are determined by what types of sexual activities are under consideration. HAV = hepatitis A virus; HBV = hepatitis B virus; HCV = hepatitis C virus; HSV = herpes simplex virus; HIV = human immunodeficiency virus; HTLV = human lymphotropic virus; NGU = nongonococcal urethritis; LGV = lymphogranuloma venereum.

Viral diseases
 Hepatitis viruses (HAV, HBV, HCV)
 HIV-1/2
 HSV-I and HSV-II
 HTLV-1
 Human papillomavirus
 Cytomegalovirus
 Epstein–Barr virus
 Moluscum contagiosum
Bacterial diseases
 Calymmatobacterium granulmatosis   (Granuloma inguinale, donovanosis)
 Chlamydia trachomatis (NGU)
 C trachomatis L1-3 (LGV)
 Gardnerella vaginalis (bacterial vaginosis)
 Haemophilus ducreyi (chancroid)
 Neisseria gonorrheae (gonorrhea)
 Treponema palidum (syphilis)
Fungal diseases
 Histoplasma capsulatum (histoplamosis)
Parasitic diseases
 Entamoeba histolytica
 Trichimonas vaginalis
Ectoparasitic diseases
 Phthirus pubis (lice)
 Sarcoptes scabiei (scabies)

STI Prevalence “Gradients” Between the Developed and Developing Worlds

Although STIs can be encountered anywhere, many are hyperendemic in developing world countries.9 Prevalence data for most developing world countries are derived largely from ad hoc surveys. Such surveys provide useful estimates but must be interpreted with caution because they may not be representative of the total population22 (Table 2). On the other hand, surveys that focus on CSW may actually be a good reflection of risk to travelers since individuals in this group are the most likely to engage in sex acts with foreigners. For example, prevalence rates for chlamydia infection in antenatal and family planning clinics range from 1.9% to 12.2% in Latin America, 6% to 13% in African countries, and 5.7% to 26% in South/Southeast Asia.9 These rates overlap with those reported in many developed countries (2.7%–8%). Estimated prevalence rates for GC range from 5.7% to 17% in sub-Saharan Africa and 0.1% to 3.5% in Asia and Western Pacific countries.9 Although the number of reported GC cases actually increased in some European countries during the 1990s, the overall incidence of GC urethritis in the developed world remains quite low (2.5–125 per 100,000).9 In most developed countries, syphilis incidence rates remained well below 5 per 100,000 through the 1990s. In contrast, there have been striking increases in the reported rates of new syphilis cases during this period in Eastern Europe and the independent states of the former Soviet Union (120–170 per 100,000). The reported seroprevalence of syphilis is generally higher in developing world countries ranging from 3.5% to 8% in South/Southeast Asia and the Western Pacific, 5% to 6% in Latin America, and 2.5% to 17% in sub-Saharan Africa.9 Not surprisingly, surveys of CSW in the developing world reveal much higher rates of STIs: 13% to 32% for chlamydia, 11% to 45% for GC, and 5% to 55% for syphilis.9,32,33 The rates for any curable STI among CSW vary from 5% to 65% in Africa, 20.9% in Brazil, and 0% to 13.6% in Southeast Asia.32,33 When prevalence rates for the major noncurable viral infections that can be sexually transmitted are included (Table 3), it is obvious that there is no such thing as a “safe” sexual encounter with a CSW [eg, HIV,5 hepatitis B virus (HBV),48 hepatitis C virus (HCV),49,50 HTLV-I51]. It is certainly worth noting that the presence of one of more STIs can increase the risk of HIV transmission by a factor of 3 to 10 or more.9

Table 2.  Examples of STI prevalence rates in healthy populations in the developing world (% of clinic visits)
CountryNSource of subjectsGCSyphilisChlamydiaTrichomonasChancroidGarnerellaHIVHBVHSV-IIGenital warts
  • STI = sexually transmitted infections; GC = gonorrhea; HIV = human immunodeficiency virus; HBV = hepatitis B virus; HSV = herpes simplex virus.

  • *

    Literature review.

  • Population-based study.

Nigeria (2003)23230Antenatal1.31.77.43.9
Zimbabwe (1984)24175Prenatal/STI17.85.925.517.813.7
Ethiopia (1997)251,907Family planning  and others56 to 6635 to 3961 to 6419 to 20
South Africa  (1996)26lit rev*Various clinics85 to 151620 to 4938 to 4038 to 41
Central African  Republic (1999)27481Antenatal3.16.76.29.92912.2
Thailand (1998)281,021Antenatal0.20.55.73 to 7
India (2002)291,981Various clinics1.85.3
Mongolia (1997)30popVarious1.40.31.6<0.001
Brazil (2003)3113,986Antenatal and  various43
Table 3.  Examples of STI prevalence rates in CSWs in the developing world (% of clinic visits)
CountryNSource of subjectsGCSyphilisChlamydiaTrichomonasChancroidGardnerellaHIVHBVHPVHCV
  • CSW = commercial sex workers; STI = sexually transmitted infections; GC = gonorrhea; HIV = human immunodeficiency virus; HBV = hepatitis B virus; HSV = herpes simplex virus.

  • *

    Clinical evidence of cervicitis (either GC or chlamydia).

Senegal (1998)34374Female CSW24.929.446
South Africa (1998)35145Female CSW14.342.116.341.37150.3
China van den Hoek 01)36966Female CSW24.9*29.424.946
Indonesia (1997-2003)37–391,340Female CSW10 to 607 to 309 to 184 to 80.537.7
Bangladesh (1998)40286Female CSW28*57.128*0
Indonesia (2003)41296Male CSW4 to 1343.62.4 to 3.8
Venezuela (2003)42212Female CSW2 to 4013.8
Brazil (1997)43Female CSW1.610.9
Peru (1993)44966Female CSW0.359.80.7
Uruguay (2003)45200Male CSW 21.550.56.5
DRC (2001)461,144Female CSW34.16.6
Argentina (2006)47625Female CSW45.73.214.44.3

Emerging Drug Resistance Among STIs

In addition to the higher prevalence rates of STIs in the developing world, a steadily increasing proportion of the infections acquired abroad are resistant to standard antibiotics.52 Beta lactamase–producing strains of Neisseria gonorrheae (NG) are prevalent in Africa, the Caribbean, and Asia.53–57 Several studies from Africa and Southeast Asia show that penicillin-resistant N gonorrheae (PRNG) can occur in ≥50% of isolates.58–60 In Canada, the rate of PRNG was only 8.7% in 1992, but the isolation of resistant organisms has increased substantially since then (15%–22%).61 Similar findings have been reported for antibiotic-resistant NG in many other countries of the industrialized world.61–65 Low-level, chromosomally mediated tetracycline resistance is also common among NG isolates in developing world settings,66 and spectinomycin resistance has begun to appear in some industrialized regions as well.61,67,68 Fluoroquinolone-resistant NG, which first appeared in 1992 is most prevalent in the Far East but now occurs around the world including Europe, the United States, and Canada.69 Antibiotic resistance in Haemophilus ducreyi, the causative agent of chancroid, continues to spread globally:57 resistance to trimethoprim/sulphonamide combination drugs is now widespread in Southeast Asia (eg, Thailand, Vietnam, Laos, Cambodia).52,70 Some believe that implementation of antiretroviral programs in the developing world will lead to the development of highly resistant HIV strains.71–73

Sexual Behavior of Travelers

The sexual attitudes and behaviors of developed world travelers have been extensively studied in the past 10 to 15 years5,58,59,74–83 and have been recently reviewed.84 Rates of reported casual sexual experiences (CSE) during travel vary between 5 and 51% (summarized in tabular form by Matteelli and Carosi81). Virtually all these studies have been conducted using questionnaires, and no study achieved a 100% response rate (some as low as 30%85). As a result, the reported figures, high as they may appear, are likely to be underestimates. In an “intention-to-have-sex” study of young Australian males traveling to Thailand, only 34% reported a definite intention not to have sex.76 As many as 47.5% of unmarried UK residents on vacation in Spain reported a CSE during a 2-week holiday.83 The rate of new partner acquisition during this 2-week period was roughly 12-fold higher than rates observed in the UK. A study of medical students reported that 32% had CSE while on holiday with a mean of three new partners.86

Although early studies demonstrated that men were far more likely than women to have CSE while traveling,85 more recent studies suggest that male and female travelers are quite similar in their willingness to acquire new partners while abroad.80,82,86–90 However, both quantitative and qualitative behavioral differences persist between the sexes (eg, number of partners, willingness to pay for sex, consistent condom use, and partner choice).83 For example, young women tend to choose fellow travelers or expatriates as new sexual partners, while older female travelers and men of all ages tend to seek out local partners.91,92 While logical to some extent, the young women’s strategy may not fully mitigate the risk since STI prevalence rates in expatriate communities are likely to be intermediate between those of the home and the local indigenous populations.93,94 As a second example of differences between the sexes, men tend to seek out “unencumbered” sex with CSW during travel while women are more likely to become romantically involved and assist their sex partners to emigrate.95

Factors that increase the chances that a given individual will engage in sex while traveling include youth, male sex, traveling alone or with a same-sex group, a history of casual sex or multiple partners at home, repeated visits to the same region, previous STIs, and higher social status.91,96,97 As with other high-risk behaviors, there is also considerable evidence that alcohol and drugs contribute to CSE in both men and women.12,83,87,91,97–102 Even without actually ingesting intoxicants, travel itself seems to be sufficiently intoxicating to encourage CSE in many people. This syndrome of sun, stimulants, and sex has been described as “situational disinhibition.”103,104

Travelers Who May Be at Particular Risk for Acquiring STIs

Expatriates

Long-term overseas workers or expatriates are more likely than other types of travelers to engage in sexual activity while abroad. Among 1,080 US Peace Corps volunteers, 60% had at least one CSE (40% of these contacts were with local residents) and only 33% used condoms.105 Among Belgian men working in Central Africa, 51 and 31% reported extramarital sex with a local woman and with a CSW, respectively.93 In a study of 1,968 Dutch expatriates working in sub-Saharan Africa, 31% of males and 13% of females had casual sex with African partners; regular condom use was reported by less than 25% of the participants.106 A more recent survey of 634 male and 230 female Dutch expatriates revealed that differences between the sexes are narrowing.107 In this study 41% of men and 31% of women had either casual or regular sex with local residents. Of the men who had CSE, 59% had paid for sex at least once. These figures help to explain why expatriates tend to have STI prevalence “profiles” that are intermediate between those of their countries of origin and their host countries.93,94,96,107

VFR Travelers

Travelers returning to their countries of origin to visit family and relatives (so-called VFR travelers) are at high risk for acquiring a number of travel-related illnesses.108,109 Although few studies exist that specifically address this issue, VFR travelers are likely to be at particularly high risk for acquiring STIs. Factors that may influence this risk include the choice of setting to solicit sex,46,110 more intimate contact with the local population and a willingness to use substandard, locally purchased condoms.111 A recent study of 756 UK residents of African origin found that 43% of the men and 46% of the women had visited their country of origin in the preceding 5 years. New sexual partners were reported by 40% of the men and 21% of the women.80 A similar study in 408 VFR travelers from the Netherlands returning to either Surinam or the Antilles revealed that 47% of the men and 11% of the women acquired a new sexual partner while overseas.112

Military Personnel and Seamen

Seamen and military personnel are reported to have high rates of sexual contact with overseas nationals during postings ranging from 45% to 56%.113–120 Among 1,744 US Navy and Marine corps personnel deployed abroad for 6 months, 49% reported having had sexual contact and 70% of these reported having had multiple partners.121 In a Dutch study of 2,289 UN peacekeepers in Cambodia between 1992 and 1993, 45% reported CSE with local partners including CSWs. UK troops posted in the tropics report similar rates of CSE with local partners (56.5%) with only 30% reporting consistent condom use.113 In a “spot check” of 1,028 US male military personnel in 2002, 7.4% reported either a current or recent (3 month) STI.114 As additional evidence of the equalization of risk between the sexes, a recent survey of 105 US female military recruits suggested that 66% of them were at risk for the acquisition of STIs.118,122

Men Who Have Sex With Men

Male homosexual travelers are less well studied than their heterosexual peers. However, the available data suggest that men who have sex with men (MSM) are at least as likely to engage in CSE while traveling as heterosexual men.89,97,123–126 In a Norwegian study, homosexual/bisexual travelers were twice as likely to have paid for sex while overseas as heterosexuals (64% vs 32%, respectively).97 A UK survey of 395 MSM travelers in 1995 revealed that 48% reported at least one CSE while abroad.124 The internationalization of STI risk in MSM was recently made very clear with the virtual simultaneous outbreaks of syphilis and lymphogranuloma venereum (LGV) in both Europe and the United States.126

Condom Use

Limited and/or inconsistent condom use in travelers appears to be independent of country of origin, travel “style” (eg, business, back-packer), and country of destination.86,88,89,91,97,98,105,106,123,127–129 Overall, at least 33% to 50% of travelers do not consistently use condoms. Although many travelers carry condoms, they often “forget” to use them in the heat of the moment.98,130 Even when condoms are used by travelers, there may be greater risks of failure due to poor quality of locally purchased products,111 improper storage (ie, the bottom of the knapsack for 2 months at 40°C), improper application, or anal sex.115,131,132

The Profile of the Traveler Who Will Have Sex Overseas

It should be obvious from the above that there is no single “profile” of the traveler likely to have CSE while traveling.91,96 With few exceptions, questions related to anticipated or actual sexual activity are appropriate for almost every pretravel interview and every post-travel review of systems. In this context, it is worth pointing out that the peak in new sexual partner acquisition in the teenage years is followed by a “second peak” among men and women 35 to 55 years of age (the “just-divorced” group).133 Finally, an ever-greater number of elderly individuals are traveling to exotic locations,134 and STIs among the elderly are easily overlooked.135 Based upon their studies in Dutch travelers, de Graaf and colleagues divide travelers into four groups, with regard to CSE overseas:92

  • 1The “unprepared” (who are surprised when sex happens).
  • 2The “fanatical” (who must have sex to have a successful vacation).
  • 3The “unaffected” (who feel that sex abroad is the same as sex at home).
  • 4The “slightly accessible” (who feel that sex abroad is different and come prepared).

Sexual Tourism

Although high levels of sexual activity have been documented in a wide range of travelers, “sexual tourism” is defined as travel expressly for the purpose of engaging in sexual activity.5,136 Such travel is highly risky with respect to STIs, and prevention/harm reduction measures should be encouraged (eg, consistent condom use, reduction in the number of partners). In many instances, sexual tourism is exploitative and illegal (eg, seeking sex with a minor) and should be strongly discouraged (reviewed in Marrazzo137). As noted above, the prevalence rates for STIs among CSW throughout the world can be very high (Table 3). However, relative risk gradients exist even in environments of overall elevated risk: street CSW generally have higher rates of STIs than their “higher class” competitors working in bars and hotels.46,110 However, in 2006, there is probably no community in the world so isolated that its CSW can be considered to be even “relatively safe.” Risk mitigation strategies used by sexual tourists (eg, seeking virgins or ever-younger CSW, insisting upon health certificates) are routinely thwarted. Some of these behaviors can also place travelers in serious jeopardy regarding both local and international laws.

Sexual Tourism by Another Name

The subtlety of sexual predation in the developing world must be explained to travelers. Many people in developing countries engage in sexual acts simply to survive: sex for a sandwich can be a fair trade in the eyes of a street child.19,20,137 In many settings, the fact that a traveler is not paying money for sex does not mean that he/she is not buying sex. Effective “currencies” in many regions of the developing world include food, gifts, and even hope (ie, the chance to emigrate). The commercial nature of such transactions is often not appreciated or acknowledged by the Western traveler. Although legitimate “barmaids” and “pool boys” certainly exist in resort areas and lasting relationships are occasionally forged in such environments, both male and female travelers more often delude themselves or rationalize their behavior by falling “in love.”130 As noted above, more female than male travelers follow through with their vacation trysts by longer term commitments such as assistance to emigrate.95

Risk of Acquiring an STI During International Travel

The risk of acquiring one or more STIs while traveling depends entirely on the behavior of the traveler. There is no such thing as the “standardized sexual act.” As a result, accurate estimates for rates of STI transmission per exposure are very hard to generate. However, the following general rules apply to all situations:

  • • Most STIs are more readily transmitted from males to females than the reverse.
  • • Individuals with obvious lesions (eg, sores, ulcers, vesicles) are more likely to transmit the agents that caused the lesions as well as copathogens (eg, HIV, HBV) than individuals without any evident genital pathology.
  • • Decisions about sexual partners and/or sex activities made under the influence of alcohol or drugs will increase the risk of acquiring STIs.
  • • Sex acts that result in bleeding or that occur during menses significantly enhance the risk of transmitting and/or acquiring sexually transmitted, blood-borne viruses (eg, HIV, hepatitis B and C viruses).

Because so many factors can influence risk, there have been relatively few attempts to quantify the risk of transmitting any given STI by individual sex acts. However, the risk of acquiring HIV, HBV, or HCV from a percutaneous injury are relatively well defined (0.5%, 4%–30%, and 3%–10%, respectively).138 The risks following a single, unprotected, heterosexual, and consensual sex act are thought to be much lower: ∼.001% for HIV139 and 0%–0.6% for HCV.140 The presence of genital lesions can dramatically increase the risk of acquiring HIV and possibly other sexually transmitted viruses. A study of Kenyan men who acquired chancroid from HIV+ CSW suggested a 43% risk of HIV transmission following a single CSE.141 The efficiency of purely sexual HBV transmission is currently unknown but is likely to be at least as high as HCV.142 The transmission of gonorrhea and chlamydia is highly efficient during both hetero- and homosexual sex. A single episode of vaginal intercourse incurs a 20 and 50% risk of acquiring gonorrhea in uninfected men and women, respectively.143 The transmission efficiencies for open syphilis and chancroid lesions are probably at least as high. Chlamydia trachomatis is transmitted heterosexually with only slightly lower efficiency (0.8%–8% per episode).144 In a large study of Swiss travelers, Steffen estimated that hepatitis B, GC, and syphilis were acquired at rates of 4, 3, and ∼1 per 1,000 traveler months, respectively.85 Reported rates of hepatitis B acquisition by unvaccinated, long-term travelers have been as high as 4%–7% per year.145,146

The Consequences of Acquiring an STI While Traveling

Acquisition of one or more STI can result in both short-term problems (eg, genital ulcers, urethritis, cervicitis) and long-term or chronic complications (eg, infertility and ectopic pregnancy, pelvic inflammatory disease, liver disease secondary to hepatitis B or C, cervical dysplasia secondary to human papillomavirus (HPV), immunodeficiency due to HIV). Several of these chronic infections can significantly shorten life [eg, cancer, liver cirrhosis, acquired immunodeficiency syndrome (AIDS)]. Both short- and long-term consequences of acquiring any particular STI while traveling can vary substantially. Infections that manifest while traveling can expose travelers to products that are not used in the developed world (eg, chloramphenicol, serum-based HBV vaccines) and to suboptimal medical practices and environments (eg, unsterilized needles/instruments). Some drugs and products such as hepatitis B immune globulin (HBIG) and antiretrovirals may not be readily available in some areas of the world or may be of unpredictable or unacceptably low potency. Infections that only manifest upon return of the traveler can also be problematic. Several of the STIs that can be acquired while traveling remain rare in North America and may go undiagnosed or be treated inappropriately by physicians who are unfamiliar with them (eg, chancroid, LGV). Finally, travelers who bring one or more STIs “home” to prior partners must also consider the emotional price including lost trust, broken relationships, and divorce.

Public Health Implications of STIs Acquired While Traveling

The potential impact of travel on STIs has significant public health implications in both departure and destination countries: the introduction of a new or more resistant organism can occur on either the outbound or the return voyage. Travelers who have CSEs overseas may also be more likely to engage in CSE back in their home country and vice versa. As a result, there are both small and large public health issues with CSE among travelers. At the “micro” level in the departure country, transmission of rare and/or resistant STIs to the nontraveling partner(s) must always be considered by treating physicians when confronted by a confusing clinical presentation. At the “macro” level, the potential to introduce exotic and/or resistant STIs into departure countries is very real.7,62,63,147,148 Because so many people are currently traveling, the risk-taking behavior of individuals can “add up” to epidemic spread rather quickly. For example, it has been estimated that >500,000 Australians have at least one CSE in the Philippines or Thailand every year.75 Tourism and travel by truck and airline were major factors in the spread of HIV across Africa and then around the globe.79 A recent survey among 1,325 male travelers in Hong Kong revealed that 453 (34.2%) had had at least one sexual contact with a CSW in the preceding 6-month period.149 The proportion of subjects presenting to some STI clinics with foreign sexual contact as their only risk factor can be impressive (10%–50%).58,123,128,150 In 1993, Rowbottom estimated that at least 44% of GC cases in Victoria, Australia, had been acquired abroad.75 Many of these imported STIs exhibit unusual or broad-spectrum antibiotic resistance.58

General Comments Regarding the Prevention and Treatment of STIs

The treatment of STIs has recently been reviewed in both the general population151–153 and specifically in travelers.33,78 Of course, the only way to reduce the risk of STIs to zero is abstinence or monogamous sex with a stable, uninfected partner. The following general statements apply to all STIs:

  • • Condoms reduce the risk of most, but not all, STIs.
  • • Prevention of STIs is preferred over treatment.
  • • Partner notification is essential to prevent STI spread.
  • • Prompt diagnosis and therapy can reduce both complications and spread.
  • • Therapy should be guided by cultures and sensitivity tests when possible.
  • • The presence of one STI should trigger a search for others.
  • • Global resistance patterns should be considered when choosing antimicrobials.

Despite several new therapeutic strategies,153 it is also worth pointing out that the treatment options for some of the most serious STIs remain very limited (eg, HBV, HCV). HIV can be controlled in most people for prolonged periods but at enormous financial and personal cost. For general treatment recommendations of the most common STIs, see Table 4. These recommendations have been abstracted largely from the Public Health Agency of Canada151 and CDC guidelines.152 The reader is encouraged to visit these sites to obtain more complete information.

Table 4.  Overview of STI screening, diagnosis, and treatments
Clinical presentation and RegimenAppropriate investigations and follow-up
  • This table is designed as a quick reference and is not meant to replace more comprehensive guidelines (eg, Health Canada,151 CDC152). STI = sexually transmitted infections; NAAT = nucleic acid amplification test; IDU = intravenous drug use; RFLP = restriction fragment length polymorphism; PEP = postexposure prophylaxis; HIV = human immunodeficiency virus; LGV = lymphogranuloma venereum; GC = gonorrhea; HAV = hepatitis A virus; HBV = hepatitis B virus; HCV = hepatitis C virus; CSE = casual sex experience; TPPA =Treponema pallidum particle agglutination; WBC = white blood cell count; ELISA = enzyme-linked immunosorbent assay; RPR = rapid plasmin reagin; VDRL = venereal diseases research laboratory.

  • *

    Treat until lesions have healed completely. An aminoglycoside can be added to regimens above if no improvement seen in first week of therapy (eg, gentamicin 1mg/kg IV every 8 hours—monitor levels).

Asymptomatic but at risk (ie, CSE  while traveling where STI status of contact(s) is not known)Culture or NAAT for Neisseria gonorrheae from all points of sexual contact (culture  only for rectal and pharyngeal specimens) and/or urine for NAAT
 NAAT or culture for Chlamydia trachomatis (urethral, cervical), culture for rectal and  pharyngeal specimens (if the only point of sexual contact), and/or urine for NAAT
 Serology for syphilis to include a nontreponemal test (eg, RPR, VDRL) or  treponemal-specific ELISA (or both)
 Advise or consider HIV testing
 HBV serology and offer HBV vaccination if not immune
 Consider wet mount and/or culture for Trichimonas vaginalis
 Consider HAV serology especially in the case of oral–anal contact and not vaccinated
 Consider HCV serology especially in the case of IDU history
Genital ulcer(s) (syphilis, HSV-II,  HSV-I, chancroid, LGV, granuloma inguinale (donovanosis))Darkfield microscopy or Immunofluorescence for Treponema pallidum (if available)
 Serology for syphilis to include a nontreponemal test (eg, RPR, VDRL) or  treponemal-specific ELISA (or both)
 GC culture or NAAT (where available) or antigen test for HSV
 Consider serology for HSV (if lesions not present or suitable for above tests)
 Culture or NAAT for C trachomatis (which if positive can be sent for DNA sequencing  or RFLP to confirm LGV)
 Culture or NAAT (where available) for Haemophilus ducreyi (alert laboratory, not  widely available)
 Advise or consider HIV testing
Purulent urethritis/cervicitis  (N gonorrheae, C trachomatis, rarely HSVI/II)Gram stain of discharge (looking for >5 WBCs per oil immersion field and GC)
 Urethral or cervical swab: culture or NAAT for C trachomatis and N gonorrheae (latter  requires special culture medium)
 Consider urine specimen for NAAT
Sexual assaultCulture or NAAT for C trachomatis and N gonorrheae from all partially or fully  penetrated orifices (culture only for rectal and pharyngeal specimens)
 Cultures should be repeated 1 to 2 weeks postexposure in the absence of prophylaxis
 Urine for NAAT for C trachomatis and N gonorrheae should also be collected
 Wet mount and/or culture for T vaginalis
 A nontreponemal (eg, RPR, VDRL) and a treponemal test (eg, TPPA) for syphilis (repeat  at 12 and 24 weeks after exposure, and possibly at 2 to 4 weeks postassault if high risk)
 If patient known to be immune to HBV, no testing is required; if not, serum sample  for baseline antibodies to hepatitis B surface antigen
 Baseline HIV antibody (repeat HIV serology at 6, 12, and 24 weeks)
 Baseline HCV antibody is optional (consider HCV risk of perpetrator, and associated  trauma during the assault—if performed should be repeated at 12 and 24 weeks)
 Consider or advise PEP for bacterial STIs, HBV, and HIV (below)
Choice of antimicrobial therapy for selected STIs (preferred regimens listed first, followed by alternates)
Clinical presentationRegimen
Chancroid (H ducreyi)Azithromycin 1 g PO × 1 or ceftriaxone 250 mg IM × 1 or ciprofloxacin 500 mg  PO BID × 3 days or erythromycin base 500 mg PO TID × 7 days
Bacterial Vaginosis (Gardnerella vaginalis)Metronidazole 500 mg BID × 7 days or metronidazole gel (0.75%) per vagina QD × 5  days or clindamycin cream (2%) per vagina QHS × 7 days
Granuloma inguinale  (Calymmatobacterium granulomatis)Doxycycline 100 mg PO BID × 21 days (at least)* or trimethoprim-sulfamethoxazole  DS (800/160 mg) PO BID for 21 days (at least) or ciprofloxacin 750 mg PO BID for 21 days (at least) or erythromycin base 500 mg PO QID for 21 days (at least) or azithromycin 1 g PO once per week for 3 weeks (at least)
HSV-II (first episode)Acyclovir 400 mg PO TID × 7 to 10 days or acyclovir 200 mg PO five times/day × 7 to 10 days or famciclovir 250 mg PO TID × 7 to 10 days or valacyclovir 1 g PO BID × 7 to 10 days
HSV-II (recurrent)Acyclovir 400 mg PO TID × 5 days or acyclovir 200 mg PO five times/day × 5 days or  acyclovir 800 mg PO BID × 5 days or famciclovir 125 mg PO BID × 5 days or valacyclovir 500 mg PO BID × 5 days or valacyclovir 1 g PO QD × 7 to 10 days
Human papillomavirusImiquimod cream (5%) applied to warts QHS 3 × per week for up to 16 weeks
 Podofilox (0.5% solution or gel) applied QHS to warts × 3 days then 4 days “rest” for up to four cycles
LGV (C trachomatis L1-3)Doxycycline 100 mg PO BID × 21 days or erythromycin base 500 mg PO QID for  21 days or azithromycin 1g PO once per week for 21 days
Neisseria gonorheaeCefixime 400 mg PO × 1 or ceftriaxone 125 mg IM × 1 or ciprofloxacin 500 mg  PO × 1 or ofloxacin 400 mg PO BID × 7 days or levofloxacin 250 mg PO QD × 7 days or doxycycline 100 mg PO BID × 7 days or spectinomycin 2 g IM × 1 or gentamicin 240 mg IM × 1 or kanamycin 2 g IM × 1
C trachomatis or Nongonococcal  urethritis or Mucopurulent cervicitisAzithromycin 1 g PO × 1 or doxycycline 100 mg PO BID × 7 days or erythromycin  base 500 mg PO QID × 7 days or erythromycin ethylsusuccinate 800 mg PO QID × 7 days or ofloxacin 300 mg PO BID × 7 days or levofloxacin 500 mg PO QD × 7 days
Sexual assaultCeftriaxone 125 mg IM × 1 and metronidazole 2 g PO × 1 and azithromycin 1 g  PO × 1 plus antiretrovirals (triple therapy such as Combivir + efavirenz), HBV vaccination (if unvaccinated)
Syphilis (T pallidum) (primary)Benzathine penicillin G 2.4 million units IM × 1 or doxycycline 100 mg PO BID × 14 days or tetracycline 500 mg PO QID × 14 days or azithromycin 2 g PO × 1 (caution as efficacy may only be 70%) or ceftriaxone 1 g QD × 8 to 10 days
T vaginalisMetronidazole 2 g PO × 1

Prevention of STIs

Health care professionals who see international travelers should make advice about STIs and avoidance strategies a routine part of the pretravel visit. Among the microbial risks of travel, the STIs are probably second only to malaria in terms of their potential for serious morbidity and mortality. Safer sex and harm reduction counseling should be emphasized. Barrier contraceptive devices, specifically male and female condoms, provide the best alternative to abstinence by preventing direct contact with infective genital lesions. Although male and female condoms are likely to have similar efficacy for many STIs when used appropriately, almost all of the available data come from studies of male condom use. Condoms made from latex provide a more effective barrier than “natural” condoms made from animal membranes. In experimental models, the latter are not impervious to viruses such as hepatitis B, hepatitis C, and HIV.152 In the event that a latex condom is not available, natural condoms do provide some degree of protection against a range of pathogens and are certainly better than nothing. If possible, latex condoms should be purchased in a developed world country since the quality of condoms produced in many regions of the world is inconsistent.111 Only water-base lubricants should be used with condoms since oil-based products (eg, petroleum jelly, mineral oil, massage oil) can significantly weaken latex condoms and lead to breakage.152 High-quality polyurethane condoms are available in most developed world countries for travelers with latex allergies.154

The reported efficacy of latex condoms against STIs ranges from 40% to 70%,155 but the contraceptive literature suggests that consistent and correct use can reduce the risk of heterosexual HIV transmission by 80%. They are generally more effective against viral pathogens spread by semen, vaginal secretions, and blood than bacterial agents associated with lesions around the genitalia. The most serious limitation of condoms is their inability to spontaneously migrate from pocket to penis (see above). The most common factors involved in condom breakage include inappropriate application, repeated or prolonged use, and anal intercourse. Although not as widely available as standard male condoms, the so-called female condom can also be a relatively effective barrier against STIs.156,157 Spermicides, such as nonoxynol-9, interfere with sperm viability, and early studies suggested a protective effect against a range of sexually transmitted viruses and bacteria.158 However, a recent Cochrane Database review suggests that nonoxynol-9 has no protective effect against a range of pathogens.159,160 In fact, with too frequent vaginal use or use in anal receptive intercourse, nonoxynol-9 can disrupt epithelial integrity and lead to increased transmission of HIV and other STIs.159,160

Screening for STIs is appropriate for many travelers who report CSE while abroad.161,162 Such screening should be guided by the nature of the sexual contact and current or past symptoms and could include an examination of the genitals, a cervical/urethral/anal/pharyngeal swab and/or urine testing as well as serologic tests for syphilis, HIV, and possibly HBV and HCV (Table 4).

The “Morning-After” STI Pill

Although it may be tempting to “arm” travelers likely to engage in high-risk sexual activities while abroad (eg, by stated intention or past behavior) with a morning-after course of antibiotic therapy, this practice is not recommended. Ready access to antibiotics could lead to a false sense of security and increased exposure to STIs not targeted by the therapy provided (eg, HIV, HCV, HPV). Such behavioral effects have recently been documented among CSW.163

Postexposure Prophylaxis for Sexual Assault Victims

The management of sexual assault victims has recently been reviewed.164–166 Women traveling for prolonged periods of time in developing world countries should be counseled with regards to risk mitigation strategies in the event of sexual assault. In all such long-term travelers (male and female), verification of hepatitis B vaccination status should be routine. Unvaccinated travelers who have been assaulted should begin active immunization as well as HBIG if a trustworthy product can be found locally. Individuals with incomplete immunization schedules must be reviewed on a case-by-case basis (ie, complete or reinitiate active immunization with or without HBIG). Although postexposure prophylaxis (PEP) for HIV using three drugs would be appropriate in many circumstances, these combinations are expensive (eg, ∼US$1,500 for 28 days of 3TC+AZT plus efavirenz) and would not be appropriate to prescribe for all travelers. However, such an expenditure might be reasonable for groups living or working overseas for prolonged periods (eg, semester abroad, large international projects). Many institutions in the developing world (eg, embassies, private schools, industries) have access to appropriate HIV PEP drugs. An alternate and lower cost strategy for individual travelers might be the purchase of a “starter kit” with 3 to 5 days of PEP drugs (US$160–$260). In some countries with high rates of sexual assault and limited availability of antiretrovirals (eg, South Africa), specific insurance policies can be purchased to ensure access to HIV PEP. It is logical to offer broad prophylaxis for other STIs if it is unsure whether or not the victim of assault will return, if the assailant has a known STI, if prophylaxis is requested or if the assault victim has signs and symptoms of an STI (see Table 4). However, the efficacy of prophylaxis following sexual assault has not been studied. Unintended pregnancy may also result from sexual assault, and the emergency contraceptive pill may also be considered in these circumstances. Treatment should be taken as soon as possible (0–72 hours for maximum efficacy) but may be of benefit up to 120 hours after exposure.167

Special Traveling Groups

Pregnant and Lactating Women

Pregnancy is also one of the major risks of CSE in any setting. Although few data are available, pregnancy does not appear to be a major risk factor for the acquisition or evolution of most STIs, although treatment can be complicated by the presence of the fetus.

Children

As a general rule, most children who travel do so with their parents and are relatively unlikely to be at high risk for the sexually transmitted disease. However, it is worth noting that developing world children are common targets of the sex trade. Tens, if not hundreds or thousands, of street children work in the sex trade in many cities of the developing world.19,20,137

Adolescents and Young Adults

Adolescents and young adults are at particularly high risk for acquiring and spreading STIs. Peak acquisition of new sexual partners occurs in all cultures during the teen and early adult years.133

Immunocompromised Hosts

A recent survey of 133 HIV+ Canadian travelers (93% male) suggest these individuals are as likely as their noninfected peers to engage in casual sex while overseas (23%) and are just as unlikely to use condoms consistently (only 58%).125 Not only do STIs facilitate the transmission of HIV but also the diagnosis of these infections, their clinical presentation, and treatment can all be influenced by HIV (reviewed by Dallabetta166). HIV+ subjects are more likely to have asymptomatic primary syphilis and to progress rapidly to neurologic and ophthalmologic complications.168 GC is more severe and more likely to disseminate in HIV+ subjects.166 Pelvic inflammatory disease of all etiologies is more common and severe,169,170 and molluscum contagiosum can be profuse in HIV/AIDS patients.171 With the exception of neurosyphilis that can be difficult to treat, STIs in HIV+ subjects can generally be expected to respond to standard therapy.150,151,166,171 It is worth noting that HIV testing is increasingly demanded of immigrants and refugees in many countries.172,173 There has been a parallel worldwide increase in mandatory HIV testing for long-term, nonresident visas (eg, expatriates, students, missionaries).

The Mature or Elderly Traveler

Sexual activity with all its attendant pleasures and risks, is a central part of a healthy life at all ages.134,135,174 As noted above, the rapid acquisition of new sexual partners is not restricted to the teenage years: a second peak between the ages of 45 to 55 has been described even among nontravelers (the restless and the divorced).133 It is important not to make assumptions about the actual or intended sexual activity of either male or female travelers at any age.

Barriers to the Promotion of Sexual Health in Travelers

Several obstacles to the promotion of sexual health in travelers have recently been discussed by Abdullah and colleagues8 These include traveler diversity, the ambivalence of both the travel industry and destination governments to a frank discussion of the risks of sexual encounters while abroad and a lack of support for travel counseling and preventative services in many departure countries. As noted above, there is often a pervasive and even willful denial of both sexual risk and responsibility among developed world travelers. In this context, a forced discussion of sexual behaviors and responsibility can be intrusive and unwanted. Furthermore, as pointed out by Sanford,175 the role of the travel advisor is not to be a killjoy but to help each traveler find a reasonable balance between risk acceptance and appropriate risk avoidance or mitigation.

Advocacy for Sexual Health in Travelers

The rapidity with which international travel has expanded in recent years has provided unprecedented potential for the development of global sexual networks. Holiday, business, and VFR travelers each present particular challenges to travel medicine practitioners. At the current time, travel health messages reach only a tiny proportion of the traveling community (certainly <20%).176 Innovative approaches are needed to gain access to these diverse groups of travelers and to encourage the travel industry and both departure and destination governments to accept responsibility for ensuring that sexual health issues receive the attention that they deserve.

Conclusions

Individuals who acquire new sexual partners while traveling, especially those who pay for sex or have multiple CSEs overseas, are at risk for a wide range of STIs. Although the behaviors of some travelers put them at higher risk of contracting STIs, there is no single profile of the “at-risk” traveler. Barrier contraceptives can provide some degree of protection against many STIs, but 100% protection cannot be achieved even with meticulous use. Only HBV and HPV genotypes can currently be prevented by vaccination, although vaccines for chlamydia species and HSV-II (among others) are in development.177 Although drug resistance is more commonly encountered in STIs acquired overseas, all the bacterial STIs can be treated successfully at the current time if appropriate antimicrobials are chosen. A series of evidence-based recommendations for managing travelers and STIs are presented in Table 5.178

Table 5.  Evidence-based* recommendations for managing travelers and STIs
  • CSW = commercial sex workers; STI = sexually transmitted infections; CSE = casual sex experience.

  • *

    Strength of Recommendation scored as A Good evidence to support a recommendation for use. B Moderate evidence to support a recommendation for use. C Poor evidence to support a recommendation for or against use. D Moderate evidence to support a recommendation against use. E Good evidence to support a recommendation against use.Quality of Evidence scored as   I Evidence from at least one properly randomized, controlled trial.  II Evidence from at least one well-designed clinical trial without randomization, from cohort or case-controlled analytic studies, preferably from more than one centre, from multiple time series, or dramatic results in uncontrolled experiments. III Evidence from opinions of respected authorities on the basis of clinical experience, descriptive studies, or reports of expert committees.178

Evidence-based recommendations related to behaviors
Evidence-based recommendations related to behaviors
 Alcohol and drugs contribute to unhealthy decisions regarding sex and condom use (AII)
 Solo travel and same-sex groups increase the risk of CSEs (AII)
 Male travelers are more likely to have CSE and to buy sex than females (AII)
 Sexual contact with a CSW is always a high-risk behavior (AII)
 Men and women with multiple sexual partners at home or a history of STIs are more likely to have CSE while traveling (AII)
 Sexual tourism is highly risky with respect to STIs (EIII)
 Sexual tourism with minors is illegal (EIII)
Evidence-based recommendations related to prophylaxis
 A discussion of STI risk and prevention should be part of pretravel counseling (AII)
 Hepatitis B vaccination should be offered to all travelers who may have CSE (AI)
 Hepatitis A vaccination should be offered to those who anticipate oral–anal contact (AI)
 Condoms reduce the risk of most, but not all, STIs (AII)
 Spermicides should not be used without a condom (AII)
 Condoms should be used for all casual sexual encounters (male AI, female AII)
 Use condoms manufactured in the developed world and stored appropriately (AI)
 Natural condoms do not protect against viral STIs and should not be used if reliable latex or polyurethane condoms   are available (DI)
 Reuse of condoms and use for anal intercourse will increase the risk of breakage (AII)
 Oil-based lubricants should not be used with latex condoms (EI)
Evidence-based recommendations related to treatment and screening
 Travelers who have had CSEs overseas should be assessed for STIs by a reliable clinic abroad or upon their return to   Canada (AIII)
 Obtain sensitivity testing for all bacterial STIs acquired while traveling (AIII)
 Follow national/international guidelines for the empiric treatment of STIs while waiting for culture results (AI)
 Consider all the possible STIs to which a traveler may have been exposed during CSEs and screen appropriately (AIII)

Declaration of Interests

The authors state that they have no conflicts of interest.

Ancillary