Travel-associated gonorrhoea in four Nordic countries, 2008 to 2013

Travel may be associated with a higher risk of gonorrhoea and infection by antibiotic-resistant strains. The objective of this study was to estimate the risk for gonorrhoea among travellers from four Nordic European countries using surveillance data and to identify at-risk travellers to help target interventions. We retrieved gonorrhoea surveillance data from Denmark, Finland, Norway and Sweden and tourism denominator data from the Statistical Office of the European Union. A travel-associated case of gonorrhoea was defined as one for which the reported country of infection differed from the reporting country. During 2008−2013, the four countries reported 3,224 travel-associated gonorrhoea cases, of which 53% were among individuals below 35 years of age. The overall risk associated with travel abroad was 2.4 cases per million nights abroad. The highest risk was observed with travel to Asia (9.4). Cases more likely to be reported as travel-associated were: males, heterosexuals of both sexes, people older than 65 years, and foreign-born individuals. More effective interventions targeting young adults and other at-risk groups are needed. The use of travel-planning websites and social media should be explored further.

Travel may be associated with a higher risk of gonorrhoea and infection by antibiotic-resistant strains. The objective of this study was to estimate the risk for gonorrhoea among travellers from four Nordic European countries using surveillance data and to identify at-risk travellers to help target interventions. We retrieved gonorrhoea surveillance data from Denmark, Finland, Norway and Sweden and tourism denominator data from the Statistical Office of the European Union. A travel-associated case of gonorrhoea was defined as one for which the reported country of infection differed from the reporting country. During 2008−2013, the four countries reported 3,224 travel-associated gonorrhoea cases, of which 53% were among individuals below 35 years of age. The overall risk associated with travel abroad was 2.4 cases per million nights abroad. The highest risk was observed with travel to Asia (9.4). Cases more likely to be reported as travelassociated were: males, heterosexuals of both sexes, people older than 65 years, and foreign-born individuals. More effective interventions targeting young adults and other at-risk groups are needed. The use of travel-planning websites and social media should be explored further.

Background
Gonorrhoea is a common sexually transmitted infection (STI). Although gonorrhoea can be asymptomatic, particularly in women and in pharyngeal and rectal infections, it is a major cause of urethritis in both men and women. In women, infection can lead to pelvic inflammatory disease, which may cause infertility [1].
The World Health Organization estimates that in 2012 there were over 78 million cases of gonorrhoea globally [2]. In 2013, 52,995 cases of gonorrhoea were reported in European Union (EU)/European Economic Area (EEA) countries (16.9 cases per 100,000 population) [3]. Of these, 2,701 (5.1%) were reported by Denmark, Finland, Norway and Sweden. Notification rate was close to the EU/EEA average in Denmark, Norway and Sweden (10-15 cases per 100,000 population) but lower in Finland (4.9). In these countries, most cases were reported among [25][26][27][28][29][30][31][32][33][34] year olds (960 cases; 36%) and among young adults aged 15-24 (908 cases; 34%). Men accounted for 75% of cases (2,012 cases) and 39% (1,050 cases) were reported among men who have sex with men (MSM). The number of reported cases has increased by 61% since 2009. MSM are a key at-risk group for infection and accounted for 43% of gonorrhoea cases in the EU/EEA in 2013 [3]. The risk of transmission of gonorrhoea can be reduced by consistent and correct condom use during sex [4]. Apart from primary prevention and partner notification, effective treatment is the only option for control of gonorrhoea in the absence of an effective vaccine. European and national treatment guidelines are available [5]. An increasing number of Neisseria gonorrhoeae strains have been reported with reduced susceptibility to antimicrobials used for treatment [6].
The relation between travel and infectious diseases is of public health concern for two main reasons. First, travel can facilitate the international spread of diseases. Second, travel may be associated with an additional disease burden due to both different risk and exposure in the destination country compared with the country of origin. Such specific risk may justify targeted preventive measures such as vaccination, prophylaxis [7], or in the case of STIs, the provision of advice before departure and testing upon return.
The historical role of travellers in spreading STIs is well documented [8]. Travel is also a known risk factor for STIs for a number of reasons, including changes in sexual behaviour when travelling [8]. Thus, travel has been shown to remove social taboos and to increase the likelihood of casual sexual relationships [9]. Travel is also associated with low condom use and sex may be the main objective of the journey (sex tourism) [9]. Travellers might also have sex with populations with higher prevalence of STIs, such as sex workers, or they might be visiting countries with a high prevalence of STI and therefore increase their risk of infection [9]. In addition, the emergence of antibiotic-resistant strains of gonorrhoea has been linked to countries in southeast Asia and Japan, and therefore travellers might import such strains to Europe [10]. Similarly, the prevalence of strains resistant to antimicrobials might be higher in further countries/regions outside Europe and lead to importation of resistant strains [9].
Estimating the real risk of travel-associated STIs is challenging. Data, particularly from Europe, are limited, notably because of reporting biases, incompleteness of STI surveillance data [8] and difficulties in obtaining sound data on travel patterns [11]. Yet, with an increasing number of travellers, it is important to better document, prevent and control travel-associated STI. Indeed, over the past 20 years, global tourist departures have doubled to reach half a billion in 2013, and Europe accounts for half of them [12]. The objective of this study is to estimate the risk for gonorrhoea among travellers from four Nordic countries using surveillance and tourism denominator data and to identify at-risk travellers to help target interventions.

Gonorrhoea data
The , which support a pooled analysis. A travel-associated case of gonorrhoea was defined as one for which the reported probable country of infection differed from the reporting country. A foreign-born case was defined as a case with a country of birth different from the reporting country.

Tourism data
Tourism denominator data for 2008−2013 were obtained from the Statistical Office of the EU (Eurostat) [15]. We used the total number of nights spent by destination country. This included all tourism nights spent by EU/ EEA residents aged 15 years or over, in a collective accommodation establishment or in private tourism accommodation for personal or professional purposes.
In most countries, this information is collected through household surveys. Number of nights by sex and age was only available for Denmark. Since tourism nights were not available for all country-region combinations for all years, we calculated the mean of tourism nights for the available years over the study period. To obtain a denominator for the entire study period (6 years), the mean number of tourism nights was then multiplied by six.

Analysis
Travel-associated cases of gonorrhoea were compared with non-travel-associated cases for main characteristics. Risk for travel-associated gonorrhoea was

Transmission
Of the 2,858 (88.6%) travel-associated cases with known probable route of transmission, 2,196 (76.8%) were reported as heterosexual transmission, 652 (22.8%) were due to sex between men, and 10 (0.3%) were through other routes of transmission (

Risk by country of residence, sex, age and destination
During 2008−2013, residents from Denmark, Finland, Norway and Sweden spent ca 1,320 million nights abroad ( Table 2).
The most visited regions were the EU (59.8% of all nights spent), Asia (12.5%) and North America (7.1%). The overall risk for travel-associated gonorrhoea was 2.4 cases per million nights spent in outbound destinations ( Table 2). The highest risk was found in Swedish travellers (3.1 cases per million nights) followed by Norwegian, Finnish and Danish travellers with 2.5, 2.2, and 1.2 cases per million nights, respectively. In Denmark, where tourism data were available by sex and age group, a higher risk for travel-associated gonorrhoea was observed in males compared with females (1.9 vs 0.3 cases per million nights, respectively) and among persons aged below 45 years, peaking at 2.2 cases per million nights for people aged 25-34 years (Table 3).
Of the 3,224 travel-associated cases, 2,793 (86.6%) had acquired their infection either in Asia or Europe (Table 3). From December to July, Asia was the top destination for travel-associated gonorrhoea (53.4% of all travel-associated cases) peaking in January when Asia accounted for 60.6% of all travel-associated cases. From August to November, the top destination was Europe (48.6%) although the proportion of cases who had travelled to Asia remained substantial (36.5%).
Monthly distributions of cases associated with travel to Africa, the Americas or Oceania did not show any obvious seasonal pattern. The highest risk was associated with travel to Asia with 9.4 cases per million nights. Travel to Africa and Central and South America was associated with a risk of ca 3 cases per million nights. Almost a third of all travel-associated cases were associated with a stay in Thailand, and the three destinations with the highest numbers of cases (Thailand, the Philippines and Spain) accounted for nearly half of all cases (Table 4).  Table 5).

Most cases with a probable country of infection in
The proportion of travel-associated cases with a probable infection in Thailand decreased from ca 40% in

Multivariable analysis
When adjusting for potential confounders, males were nearly three times more likely to have acquired their infection abroad compared with females (OR: 2.96, 95% CI: 2.62-3.34) ( Table 6).

Principal findings
Surveillance data from four Nordic countries suggested that at least 25% of gonorrhoea infections were related to travel, a proportion that slightly decreased over the study period. Half of these cases had a travel history in Asia, a continent that accounted for fewer than 15% of the nights spent abroad by the residents of these countries. Most of the travel-associated cases were observed among persons below 35 years of age. The Danish cases for which denominator information was available suggested that the highest risk for travelassociated gonorrhoea was among the 25-34 year-olds.
Danish data also showed that the risk for travel-associated gonorrhoea in men is six times higher compared with women. This is consistent with the finding that younger people and men are more likely to report having a new sex partner while travelling [16]; younger people are also more likely to have a higher number of sex partners in general [17], which is a risk factor for having a new sex partner while overseas [16].
Although the reported number of cases of gonorrhoea decreased with age, the proportion of cases of gonorrhoea which were travel-related increased with age, with a peak of 59% among those aged 65 years or over; almost all of these cases were reported among heterosexual men. Very few cases of travel-related gonorrhoea were diagnosed among people aged 65 years and above and therefore older persons are at lower risk of acquiring gonorrhoea per million bed nights.
During the study period, the number of gonorrhoea and travel-associated gonorrhoea cases increased in all four countries, but the proportion of travel-associated cases decreased most recently in 2012−2013. Overall, this rise in reported cases has been mainly due to increasing numbers of cases among MSM, regardless of travel status [3], which is partly linked to continuing high-risk behaviour in this subpopulation [18], partly to increased testing and use of more sensitive tests such nucleic acid amplification tests [19]. The larger increase among locally acquired cases compared with travel-associated cases is likely to reflect the larger proportion of MSM among locally acquired cases. The increasing number of travel-associated cases with MSM transmission over the study period cannot be explained solely by improved data completeness for transmission status, but should be considered in the context of increasing reports of cases among MSM overall during this time period [3].
A disproportionate number of cases were associated with travel to Thailand and the Philippines. Although some of these cases are likely to be acquired through contact with sex workers, many travellers, particularly backpackers, often find sexual partners among other travellers. The risk of new partner acquisition and overall risk of unsafe sex among backpackers in Thailand has been found to be associated with male gender and longer trip length [20]. Backpackers are also less likely to use condoms when having sex with travel partners compared than with commercial sex workers [21]. Thailand is reported to be the foreign country where the largest number of Swedish males contract HIV and many Swedish men have sex with commercial sex workers while on holiday there, leading to risk of transmission of STI also from the local population [22].
South-east Asian countries are reported to have high levels of multidrug-resistant N. gonorrhoeae [23]. Information on the laboratory test used to confirm gonorrhoea is not available within the European surveillance system. This makes it difficult to know how often culture and subsequent susceptibility testing were performed among travel-associated cases. Considering the current concerns on antimicrobial-resistant gonorrhoea in Europe and globally [24], monitoring susceptibility of strains acquired during travel is important.
Over half of gonorrhoea infections acquired in the top European destinations were in MSM. This reflects the high prevalence of MSM having sex abroad, reported to be 25% in the previous 12 months from the European Men-Who-Have-Sex-With-Men Internet Survey (EMIS), and the low proportion of condom use during anal intercourse while abroad [25]. The top destinations for sex abroad reported in EMIS were also Spain and Germany, as in our study. Barcelona and Berlin are both extremely popular sex tourism hotspots in Europe for MSM.
Foreign-born cases were more likely to be travel-associated compared with natives. Approximately 40% of travel-associated foreign-born cases travelled to their country of birth, probably visiting friends or relatives (VFR). VFR travellers are a well-identified risk group for travel-associated illness although the definition may mask a more complex reality [26].

Strengths and weaknesses of the study
The study is based on a relatively homogeneous population in the Nordic European countries. A substantial proportion of Nordic residents travel abroad and this makes the Nordic population very suitable for estimating risk of travel-associated conditions. The surveillance systems for STIs in these countries have been stable during this time, with good case ascertainment and availability of diagnostics. Unfortunately it was not possible to incorporate analysis of Euro-GASP data due to the low completeness of the relevant variables. Improving the completeness of these variables in Euro-GASP should be a priority to allow for better monitoring of the resistance patterns of strains imported into Europe.
The travel behaviour across the included countries is also rather similar: residents of Nordic countries tend to travel to warmer countries during the darkest and coldest months of the year. Travel tourism data were collected mostly via household survey, a method which is prone to memory bias. However, the number of nights spent by destination was fairly stable over the study period suggesting that these data were reliable. Our decision to average the number of nights spent for the study period may have masked annual variations, especially for destinations with fewer nights spent, such as Africa or Oceania. For such destinations the estimated risk may be less accurate.
Unfortunately, tourism data were not available by age group and sex for Finland, Norway and Sweden, limiting enhanced analysis of the data. In Denmark where tourism data were available by age group, there was little variation over 2012−2013. Information on the purpose of travel was not available for cases. Therefore, we were not able to differentiate leisure tourism from business travel or family visits.

Comparison with other studies
The data presented in this paper are consistent with data reported by Steffen et al. who estimated a risk of travel-associated gonorrhoea of 0.06% per month of stay in developing countries [27]. Our findings indicate the highest risk was associated with travel to Asia with 9.4 cases/million nights, which would correspond to an incidence rate of 0.03% per month.
The high proportion of travel-associated cases in older age groups has previously been reported in Sweden where more than 50% of gonorrhoea cases aged 35 years or over were infected abroad during 2007−2011, compared with 20% to 25% for persons below 35 years of age [28]. The Swedish study found that women and MSM were more frequently infected in Sweden than heterosexually infected men. A recent systematic review of casual sex and foreign travel found that people engaging in casual sex while abroad are more likely to be young and males [29].

Possible explanations and implications for clinicians and policymakers
The results presented here highlight the role of young adults below 35 years of age in the epidemiology of gonorrhoea, including travel-associated gonorrhoea.
International guidelines recommend specifically addressing STI during pre-travel consultations [7] but a recent systematic review underlined the low level of evidence on the impact of standard STI pre-travel advice on sexual behaviour [30]. The same review also found that motivational pre-travel STI interventions (described as 'a directive, client-centred counselling style for eliciting behaviour change by helping clients to explore and resolve ambivalence' [31]) were not superior to standard STI travel advice [30]. One cohort study identified in this review, however, did find that recall of reading STI information appeared to be related to more consistent condom use [30]. Since a large proportion of travellers do not seek advice in pretravel consultations [32], other channels of information such as social media including dating apps could be explored. Young adults could be targeted with safe-sex messages related to travel when visiting STI or youth clinics: persons with a history of multiple sex partners and/or an STI are at risk of travel-associated casual sex [29]. The role of social media in targeting prevention messages needs to be considered and further investigated: research suggests that social media plays an increasing role as information sources for travellers [33,34]. Apart from social media, online resources are extensively used by all age groups for travel planning [34]. Targeted online prevention messages could be considered at peak travel periods together with research on their effectiveness.
Apart from the safe-sex message, young adults should be educated to know that a large proportion of gonorrhoea cases are asymptomatic and hence, after risky behaviour, testing is important irrespective of symptoms.
Finally, these data indicate that older males have a higher likelihood of having been infected abroad when presenting with a gonorrhoea infection. This should be taken in consideration by clinicians when treating these patients. Although they represent a lesser burden when compared with younger age groups, this population should not be forgotten by public health interventions.