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Occupational Medicine 2007 57(5):313-321; doi:10.1093/occmed/kqm044
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© The Author 2007. Published by Oxford University Press on behalf of the Society of Occupational Medicine. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Sexual health and HIV in travellers and expatriates

Elizabeth Hamlyn, Aneesa Peer and Philippa Easterbrook

Department of HIV/GUM, Kings College, London SE5 9RJ, UK

Correspondence to: Elizabeth Hamlyn, Caldecot Centre, Kings College Hospital, London SE5 9RS, UK. Tel: +44 787 066 5620; fax: +44 207 346 3486; e-mail: elizabeth.hamlyn{at}kingsch.nhs.uk


   Abstract
Top
 Abstract
Introduction
 Methods
 Conclusion
 Conflicts of interest
 References
 
Abstract Travellers engaging in sexual contact with a new partner abroad may be at high risk of acquiring a sexually transmitted infection. This review examines the impact of travel on sexual health and provides prevention, management and treatment recommendations to practising occupational health physicians.

Keywords      Expatriates; HIV; sexual health; travel


   Introduction
Top
 Abstract
 Introduction
Methods
 Conclusion
 Conflicts of interest
 References
 
Global travel is common among UK residents—approximately 68 million UK residents travelled abroad from May 2005 to May 2006 [1]. Although the majority of these travellers remain within the European Union, visits to regions outside Western Europe and North America increased by 15% to 12 million over this time period. Travel to areas where human immunodeficiency virus (HIV) and other sexually transmitted infections (STIs) are endemic is common, in particular to Sub Saharan Africa and India where visits increased by 19 and 15%, respectively in 2003 [1,2].

There is a well-established association between travel and the acquisition or transmission of STIs. Travellers themselves may be vectors for disease, and cause onward transmission of infection elsewhere. A delay in diagnosis is not uncommon, as many STIs may be asymptomatic or have a long incubation period, resulting in the potential infection of further sexual partners prior to diagnosis and treatment.

The risk of acquiring an STI abroad depends on their prevalence in the local population and the type of risk behaviours. STIs are among the most common notifiable infectious diseases worldwide, and rates of infection including HIV are endemic in many developing countries, particularly among specific core groups such as commercial sex workers [3]. The risk is reduced by avoiding unprotected or casual sexual intercourse and by use of condoms. The presence of an untreated STI, both ulcerative and non-ulcerative greatly enhances the risk of both HIV acquisition and transmission [4], and thus prompt STI diagnosis and treatment is paramount from both an individual and public health perspective.


   Methods
Top
 Abstract
 Introduction
 Methods
Conclusion
 Conflicts of interest
 References
 
We conducted an Athens Ovid search of the Medline, Cochrane, Embase and Psychoinfo databases using the key words ‘travel’, ‘STIs’, ‘sexual health’, ‘HIV’, ‘expatriate’, ‘tourist’ and ‘sex tourist’. The references of cited articles, and the following websites Health Protection Agency (http://www.hpa.org.uk), National Statistics (http://www.statistics.gov.uk) and World Health Organization (http://www.who.int), were also examined.

Levels of risk behaviour among travellers
A high proportion of travellers engage in casual sexual intercourse while abroad, and lack of condom use is common. In a survey of 386 genitourinary medicine (GUM) clinic attendees in London who had travelled abroad in the last 3 months, 12% of STI diagnoses were contracted abroad [5]. Twenty-five per cent reported that they had had sex with a new partner during their trip and of these two-thirds never or inconsistently used condoms. Similarly, in a study from Glasgow, 20, 31 and 42% of women, heterosexual men and homosexual men, respectively, had a new sexual partner while abroad. Half of the women and nearly two-thirds of heterosexual men were inconsistent users of condoms [6]. Travellers may have received little or no effective pre-travel advice on sexual behaviour and some are unaware of the risk of acquiring an infection abroad [7]. A questionnaire survey of female travellers to the Caribbean found that some women confused contraception with STI protection [8].

Risk factors shown to be associated with a higher risk of casual sex abroad are summarized in Table 1 and include younger age, male gender, having a large number of sexual partners at home, misuse of alcohol and drugs, single marital status and travelling alone or with friends [5, 9–12].


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  		Table 1. Factors associated with casual or unprotected sex abroad

 
A UK study of young people aged 18–34 years who had travelled abroad without a partner in the preceding 2 years found that 10% had a new sexual partner abroad, 75% used condoms on all occasions and 12% never used them. Patterns of condom use varied by sex; in men, condom use abroad with casual partners reflected patterns of use at home, whereas for women, patterns of condom use were influenced by their partners' backgrounds [9]. Despite the relatively high levels of condom use in this study, there are indications that travellers have misperceptions about the risk of sex with a new partner.

Groups at particular risk
Young people
Numerous studies have indicated that young people are more likely to engage in sexual activity abroad than at home. In a survey of 150 people in the departure lounges of Tenerife, 35% reported that they had had sex with someone other than their regular partner while on holiday, and this was greatest among those <25 years, of whom 50% had sex with a new partner. Overall, 65% did not use barrier contraception [13]. In a further study on the sexual behaviour of young (16–35 years) travellers in Ibiza, 56% reported having sex with at least one person on holiday, and with more than one partner in 26% of men and 14.5% of women. Overall, 38% did not always use condoms. Those having sex abroad were more likely to be of younger age, to have a higher number of sexual partners before their visit and to use illicit drugs (Table 1) [11]. The excessive use of alcohol and drugs has been consistently identified as an important contributory factor to reducing inhibitions and increasing risk-taking behaviour in young persons. A questionnaire survey of 534 US college students before and after the spring break vacation, found that a significant proportion of students went on holiday with the intention of experimenting sexually (42% males, 18% females) and 28% of males and 3% of females intended to have sex with a new partner. Following their vacation, a high proportion reported excessive drinking (86% men, 79% women), having sex (66% men, 63% women) and drug use (39% men, 27% women). Alcohol or drugs frequently influenced their decisions involving sex; 49% of men and 38% of women reported having sex as a direct result of drinking. Of concern, three-quarters reported that they rarely or never used a condom [14].

Young casual workers in bars and nightclubs abroad represent another high-risk group for acquiring an STI, but may be in a good position to deliver sexual health interventions to other young travellers. A case–control study of the sexual behaviour of 92 British bar and nightclub workers in Ibiza aged from 18 to 35 years compared to 868 young people visiting Ibiza on holiday during the same summer season found that casual workers were more likely to have multiple sexual partners (OR 2.8, 95% CI 1.4–5.6) and unprotected sex (OR 3.0, 95% CI 1.6–5.6) than holidaymakers [15].

Men who have sex with men
In a Brighton-based survey of the sexual behaviours of 391 men who have sex with men (MSM) who had travelled abroad, overall about half (47%) had sex with new partners on holiday. This was higher among those who were not in committed relationships (61%) or who travelled alone or with friends (63%), as well as those having a high number of new partners at home or being motivated by ‘gay social life’ in planning a holiday (Table 1) [12]. Nine per cent reported unprotected sex and this was associated with not taking condoms on holiday (40% non-takers versus 13% takers, P < 0.05), having higher sexual expectations (39% high versus 7% low, P < 0.0005) and being HIV positive (34% unsure/positive versus 8% negative, P < 0.001). Several other studies have also identified that unprotected sex is more common in HIV-positive men, which raises concerns about the potential for onward transmission [12,16,17].

There is also a link between substance misuse and an increase in unsafe sexual practises and risk of subsequent HIV acquisition among MSM. A study of 295 gay and bisexual men who attend dance parties in different US and international cities found unprotected anal intercourse to be associated with the use of crystal methamphetamines (OR 2.4, 95% CI 1.1–4.9), sildenafil (Viagra) (OR 3.8, 95% CI 2.0–7.3) and amyl nitrate (OR 2.2, 95% CI 1.3–4.0) as well as HIV positivity (OR 3.2, 95% CI 1.4–7.5) [17]. In a further study from South Florida, club drug use, ketamine and cocaine in particular was significantly associated with unprotected anal intercourse (P < 0.001) and this was highest among visitors (P = 0.03) [18].

Expatriates
It is reported that expatriates develop a sense of ‘invulnerability’, which increases with the number and duration of their overseas postings, raising concerns about the potential for substantial HIV and other sexually transmitted disease transmission within this group [19]. Twenty-three per cent of 864 returning Dutch expatriates reported unprotected sex with partners from highly prevalent HIV areas, although their HIV prevalence was lower compared with 1409 Belgian and 4564 male European expatriates returning from Africa, but higher than the general population in most European countries [20]. Factors associated with sex abroad were younger age, positive intention of having sex prior to departure, single status, men working in a commercial organization and feeling lonely or bored. Of the men who have had sex with local partners, 59% paid for sex. Consistent condom use was found in 69% of men and 64% of women who reported casual local partners, and was lower between casual expatriate partners [20]. In an in-depth interview with a sample of 55 expatriates who had been sexually active in HIV endemic areas, there were four types of motivation for having sex abroad—‘the unprepared’, where sex happened unexpectedly and the expatriates felt that they would not have behaved the same way if they had been at home; ‘the fanatical’, where sexual activity and a pre-occupation with sex were much greater than at home; ‘the unaffected’, where being abroad did not influence the decision to have sex or the circumstances surrounding it and ‘the slightly accessible’, who were characterized by the fact that being abroad did exert a certain influence on their sexual conduct, but sex never happened unexpectedly or took them by surprise [19]. Although their group status was not static, within these groups individuals shared common behavioural practices with regards to sexual relations before departure and abroad as well as their attitudes to condom use. Overall, such qualitative studies may improve understanding of the motivations to have sex abroad, enabling high-risk individuals to be targeted [19].

Health care professionals working abroad
Health care workers working abroad are not only exposed to the same risks as other expatriates in terms of sexual behaviour and STI acquisition but also face the additional risk of occupationally acquired HIV infection. Although the risk from a single occupational exposure is low, there is a cumulative risk of seroconversion with repeat incidents [21]. In a study of HIV exposures at a rural district hospital in southern Africa, where the majority of staff were junior doctors from Europe, the estimated risk of HIV exposure from a needlestick injury was 0.75 exposures per doctor per year [22]. In a further study of 99 Dutch medics working in HIV endemic areas, 61% reported percutaneous exposures during an average stay of 21 months [23]. Although post-exposure prophylaxis (PEP), is recommended for both occupational and non-occupational HIV exposures, medication costs, timely access, as well as ensuring adequate counselling and follow-up, raise difficulties [22]. In a survey of 22 medical schools, only eight provided or advised their students on PEP against HIV when they visited developing countries as part of their elective [24]. In a further study of medical students visiting high-risk countries, only 34% of students took a starter pack of zidovudine with them for PEP, 53% took latex gloves and 63% a medical kit [25]. Health care workers moving to work in high prevalence countries should purchase or arrange a supply of antiretroviral medication to take with them prior to travelling, usually in the form of a ‘starter pack’, to ensure its availability in the event of an exposure to the virus [22]. Health care workers also need to ensure that they are fully vaccinated against hepatitis B, and consider the risk of other blood-borne viruses such as hepatitis C.

Military personnel
Military personal are likely to be deployed to areas with a high prevalence of viral hepatitis and HIV, and studies have shown that both male and female personnel frequently engage in sexual contact with local people when overseas. A questionnaire survey of 1744 American military personnel deployed aboard ship for 6 months to South America, West Africa and Mediterranean found that 42% reported sexual contact with a prostitute, 10% did not consistently use condoms and 10% acquired an STI [26]. There is a three-fold increase in the hepatitis B core antibody seropositivity in US military personnel deployed to hepatitis endemic areas for greater than a year [27].

In a study of 520 recently HIV-infected military personnel, 5.4% were infected with a non-B subtype, and these were more likely to have had heterosexual than homosexual contacts (OR 10, 95% CI 2.3–43.4), to have had sex with a commercial sex worker (OR 4.9, 95% CI 2.0–11.5) and sexual contact overseas (OR 5.3, 95% CI 2.0–14.7). There was a broad diversity of strains reflecting the specific regions of deployment [28].

Sex tourists
Sexual tourism is defined as travel specifically for the purpose of engaging in sexual activity. Although illegal as an organized entity, it is a well-described phenomenon that occurs in many popular tourist destinations such as Thailand, Brazil, Kenya and the Dominican Republic [29–31]. Sex tourists are usually male, and an increasing number are homosexual; only10% are women and many are from affluent countries [29]. Men traditionally prefer Thailand and the Philippines while women, the Caribbean and Kenya [30]. In a study of German sex tourists, they were typically men in their mid to late thirties who stayed in their host country for 4–5 weeks and had an average of four female partners [29]. One-third had a history of a previous STI, and only 45% regularly used condoms. Some did not regard themselves as prostitute users and therefore formed relationships with the foreign women.

Although the majority of sex tourists carry condoms and use them consistently, female and non-white travellers have been shown to be exceptions [30] and a particularly close relationship between the foreigner and the local partner may further compromise condom use. One-third of 81 German women visiting the Kenyan coast had sex with local men, and 68% did not use condoms [29]. There is some controversy over viewing women as sex tourists, as many perceive the relationship as a ‘holiday romance’. Thirteen per cent of 240 women on tourist beaches in Jamaica and the Dominican Republic felt that their relationships with local men were ‘real love’ and these women in particular were found not to have used condoms [8].

Pre-travel advice
A lack of knowledge does not appear to be a major factor leading to unsafe sex abroad. In an intervention study of 3509 people attending a travel clinic, of whom 51% had sex abroad, there was no difference between those who received interventions such as brochures about consequences of sex tourism compared to travellers to Kenya who were contacted at the airport [32]. Similarly, an education and awareness intervention to arriving and departing passengers at Zurich airport showed that increasing education in travellers did not impact significantly on condom use [33]. The authors concluded that high-risk groups should be targeted separately. However, the diversity of the target groups is a barrier for sexual health promotion and different groups may need to be addressed separately.

Physicians assessing travellers prior to departure for vaccinations and other advice are in an ideal position to provide information on sexual health. For the substantial numbers of travellers who go abroad with the planned intention of having sex, directly asking them of their plans to do so may establish risk. As many sexual encounters abroad are unanticipated, travellers should be aware that unfamiliar or unusual surroundings might lead to a change in normal attitude or behaviour resulting in unplanned sexual activity. A pre-travel sexual health discussion, aimed at increasing awareness of STI and encouraging a reduction in risk-taking behaviour, should include a risk assessment, a discussion on condom use and protection against STI, contraceptive advice for female travellers, as well as advice on vaccinations and prevention of blood-borne viruses (Table 2).


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  		Table 2. Components of a pre-travel sexual health discussion

 
With the exception of abstinence, condom use is the most effective method of STI prevention. Longitudinal prospective studies of serodiscordant couples where only one partner is HIV positive have shown that consistent use of condoms is highly effective in preventing HIV transmission [34,35]. Travellers should be aware that condoms purchased abroad may be of inferior quality and humid or hot conditions may reduce their effectiveness. They should also not be used with oil-based lubricants or commonly used vaginal creams such as clotrimazole.

The need for effective contraception should be discussed with female travellers prior to departure. Long-term methods of contraception such as the progesterone implant or intrauterine device may be appropriate for those who are away for longer periods, although they should be inserted some time in advance of departure in order to establish unacceptable side-effects. Travellers should be reminded that non-barrier methods of contraception are not protective against STI. Those using the oral contraceptive pill should be advised that a gastrointestinal upset or the use of antibiotics may affect its absorption leading to a reduction in efficacy, and additional precautions will be necessary. Where long-term antibiotics are prescribed, such as doxycycline for malaria prophylaxis, precautions may be discontinued after 3 weeks as the bowel flora develops antibiotic resistance and is therefore unaffected.

World Health Organization estimates indicate that there are 40 million HIV-infected individuals worldwide, with a population prevalence of up to 25% in some African countries such as Botswana [36]. Travellers to or expatriates living in high-risk areas should be aware of the risk of HIV infection and of the existence and availability of PEP, in addition to the importance of vaccination against hepatitis A and B. Although hepatitis A is most commonly acquired through the faecal-oral route, it may be acquired sexually in those engaging in oro-anal sex as demonstrated by recent outbreaks in men who have sex with men [37]. Vaccination against hepatitis A is recommended for travellers likely to be exposed to contaminated food or water in developing countries, and for homosexual men and injecting drug users.

It is estimated that there are 350 million carriers of hepatitis B virus, with prevalence of 8–10% in many developing countries where most infection is acquired during childhood [38]. Travellers may be exposed to hepatitis B through sexual contact, through blood transfusion and contaminated equipment or through non-sterile needles from activities such as acupuncture, body piercing and tattoos. The WHO recommends that vaccination against hepatitis B should be part of routine childhood vaccination in all countries; however, there remains no consensus on whether to adopt a universal vaccination programme in the UK where the overall prevalence remains relatively low [39].

Vaccination against hepatitis B is not routinely offered prior to travel, yet a high proportion of travellers are at risk. In a telephone survey of 9000 European travellers, 75% had potential risk factors for contracting hepatitis B, but only 19% were vaccinated [40]. Travellers may be unaware of risk factors for acquiring the virus or of the availability of a vaccination. Standard hepatitis B vaccination involves vaccines given at 0, 1 and 6 months. Accelerated schedules may be given to confer rapid immunity and provide protection for last-minute travellers [41,42], and in this situation, a booster should be given at 1 year to ensure long-lasting protective immunity. Combined vaccine against hepatitis A and B is as efficacious as separate vaccinations with fewer injections [43].

Hepatitis C is primarily spread by the parenteral route and rates of sexual transmission appear to be low [44,45]. However, the presence of concomitant STIs such as lymphogranuloma venereum (LGV) and sexual practises causing mucosal damage are likely to facilitate transmission as demonstrated by a recent cluster of acute hepatitis C infection among MSM engaging in high-risk sexual intercourse in the Netherlands [46].

Assessment of the returned traveller
A sexual history is a key factor in the assessment of the returning traveller, and an STI screen should be offered to all those who have had new sexual partners abroad, regardless of whether symptoms are present. The incubation period of individual infections should be taken into account. Symptomatic individuals may be referred to a GUM clinic for diagnosis and treatment. Table 3 shows the infections that may be acquired overseas, which include blood-borne viruses, bacterial infections such as chlamydia, gonorrhoea and syphilis, protozoan infections such as trichomonas vaginalis and viral infections including herpes simplex. ‘Tropical’ genital infections include chancroid, donovanosis and LGV. It should be noted that outbreaks of LGV have recently been described among MSM in several European cities [47]. Between 1997 and 2003, there has been a 3-, 6- and 21-fold rise in syphilis diagnoses among women, heterosexual males and MSM, respectively, with 21% of heterosexual cases and 10% of cases in MSM being acquired abroad in a recent London outbreak [2].


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  		Table 3. STI that may be acquired abroad

 
Increasing proportions of STI acquired abroad are resistant to standard antibiotics. Patterns of gonococcal resistance vary according to region, with an increase to an overall prevalence of resistance to penicillin and ciprofloxacin of 11 and 14%, respectively, in the UK by the end of 2004. Between 2003 and 2004, there was a marked increase in multidrug resistant gonorrhoea diagnosed in the UK, from 7 to 13% of strains. Eleven per cent of gonococcal infections were likely to have been acquired abroad, an increase from 8% in the previous year and being infected with a multidrug resistant strain was significantly associated with having overseas sexual contact (P < 0.01) [48].

Antimicrobial resistance in other infections is of increasing global importance. Antibiotic resistance in Haemophilus ducreyi, the causative agent of chancroid, continues to spread across endemic regions [49]. Azithromycin resistance in the treatment of syphilis has been described in outbreaks among MSM in America [50]. Physicians diagnosing and prescribing treatment for STI acquired abroad should take resistance patterns in the likely area of acquisition into account and ensure adequate follow-up to ensure resolution of the infection.


   Conclusion
Top
 Abstract
 Introduction
 Methods
 Conclusion
Conflicts of interest
 References
 
Investigating the sexual health of travellers poses several challenges. Travellers are a heterogeneous population making targeted interventions difficult and STI may be diagnosed some time after travel so it may be difficult to link an infection with a risk exposure while travelling. Most studies on the sexual health of travellers have been cross-sectional and descriptive rather than prospective and analytical. Other limitations include the lack of comparison or control groups and the impact of recall bias as a result of retrospective data collection.

High proportions of travellers have sex while abroad and condom use is inconsistent. Establishing sexual expectations prior to going on holiday and identifying those at high risk of sexual contact abroad, such as young lone male travellers, those with a large number of partners at home or heavy use of alcohol and drugs, means that sexual health advice may be tailored to the individual and the traveller can then make informed decisions while away from home. A pre-travel sexual heath discussion can be integrated into any medical consultation with the departing traveller. An emphasis on the importance of condom use is important, as much sexual contact overseas is spontaneous and unpredictable. Ensuring adequate vaccination against hepatitis A and B, and discussing the use and availability of PEP against HIV, may protect travellers from blood-borne viruses. Those who have had a new sexual partner while travelling may benefit from screening tests for STI on their return even if they are asymptomatic.


   Conflicts of interest
Top
 Abstract
 Introduction
 Methods
 Conclusion
 Conflicts of interest
References
 
None declared.


   References
Top
 Abstract
 Introduction
 Methods
 Conclusion
 Conflicts of interest
 References
 

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