Illness among US resident student travellers after return to the USA: a GeoSentinel analysis, 2007–17

Abstract

Background:

The number of US students studying abroad more than tripled during the past 20 years. As study abroad programmes’ destinations diversify, students increasingly travel to resource-limited countries, placing them at risk for infectious diseases. Data describing infections acquired by US students while travelling internationally are limited. We describe illnesses among students who returned from international travel and suggest how to prevent illness among these travellers.

Methods:

GeoSentinel is a global surveillance network of travel and tropical medicine providers that monitors travel-related morbidity. This study included the records of US resident student international travellers, 17–24 years old, who returned to the USA, had a confirmed travel-related illness at one of 15 US GeoSentinel sites during 2007–17 and had a documented exposure region. Records were analysed to describe demographic and travel characteristics and diagnoses.

Results:

The study included 432 students. The median age was 21 years; 69% were female. More than 70% had a pre-travel consultation with a healthcare provider. The most common exposure region was sub-Saharan Africa (112; 26%). Students were most commonly exposed in India (44; 11%), Ecuador (28; 7%), Ghana (25; 6%) and China (24; 6%). The median duration of travel abroad was 40 days (range: 1–469) and presented to a GeoSentinel site a median of 8 days (range: 0–181) after travel; 98% were outpatients. Of 581 confirmed diagnoses, the most common diagnosis category was gastrointestinal (45%). Acute diarrhoea was the most common gastrointestinal diagnosis (113 of 261; 43%). Thirty-one (7%) students had vector-borne diseases [14 (41%) malaria and 11 (32%) dengue]. Three had vaccine-preventable diseases (two typhoid; one hepatitis A); two had acute human immunodeficiency virus infection.

Conclusions:

Students experienced travel-related infections, despite the majority having a pre-travel consultation. US students should receive pre-travel advice, vaccinations and chemoprophylaxis to prevent gastrointestinal, vector-borne, sexually transmitted and vaccine-preventable infections.

Introduction

US universities encourage students to study internationally to increase cultural awareness and expand foreign language skills.^1–3 During the 2015–16 academic year, more than 325 000 US students (1.6% of all US students enrolled in higher education institutions⁴) studied abroad, an increase of 3.8% from 2014 to 20 15.⁵ The number of students studying abroad has more than tripled in the past 20 years. Most US students studying abroad are undergraduates, Caucasian and female. Most students travel to western Europe, but study abroad programme diversification has led to increasing numbers of students travelling to resource-limited countries (23% of students in 2015–16).⁵

Students might encounter health risks abroad. One examination of US study abroad students found that despite both self-reported confidence in their ability to engage in preventive behaviours and 60% receiving a pre-travel health consultation, 25% reported travel-related health problems.⁶ Most US undergraduates are 17–24 years old, and young adults might be subjected to stressors such as sleep deprivation,⁷ culture shock, navigation of a new language, loneliness⁸ and new relationships, which might contribute to experimentation and risky behaviours while travelling.⁹ Students have reported risky sexual behaviour^10–14 and excessive alcohol consumption^15–17 during international travel. Student travellers might also experience physical trauma from extreme sports or road traffic injuries.

Students travelling abroad are also at risk for infectious diseases. Few studies describe infectious diseases acquired while studying abroad; most articles are case reports^18–20 or small prospective observational studies.^13–22 Post-travel surveys directed at students are subjected to recall and response biases. Students who become ill might seek care at various domestic and international sites; only reportable conditions are systematically collected, and reportable diseases vary by state and country.²³

Using data from GeoSentinel, the global surveillance system that collects data on ill travellers, we aim to describe the spectrum of illness among US students who returned to the USA after international travel and presented for care.

Methods

Data Source

GeoSentinel is a global clinician-based sentinel surveillance system that monitors travel-related illness among international travellers, including students. Established in 1995 as a collaboration between the Centers for Disease Control and Prevention (CDC) and the International Society of Travel Medicine,^24,25 GeoSentinel currently consists of 70 specialized travel and tropical medicine clinical sites in 31 countries. These sites collect data on international travellers, including traveller demographics, trip details, region and country of exposure, clinical information and diagnoses; clinical treatment and outcomes are not routinely reported.²⁵ GeoSentinel’s data collection protocol has been reviewed by a human subjects advisor at CDC’s National Center for Emerging and Zoonotic Infectious Diseases and is classified as public health surveillance and not human subjects research. Additional ethics clearance was obtained by participating sites as required by their respective institutions.

Inclusion Criteria

Records of US residents, 17–24 years old, whose reason for travel was ‘student’, who returned ill to the USA after international travel, and who were given a confirmed diagnosis at the US GeoSentinel site during 2007–17, were included. Those with an unascertainable exposure country were excluded. Exposure countries were classified by income level using the World Bank classification scheme.²⁶ GeoSentinel diagnosis codes were classified based on physical exam systems (cardiovascular, dermatologic, head/eyes/ears/nose/throat, gastrointestinal, genitourinary, lymphatic, musculoskeletal, neurologic, pulmonary and psychiatric). Two additional classifications were developed for systemic febrile syndromes and other diagnoses. If applicable, diagnoses were further classified as vector-borne, sexually transmitted or vaccine-preventable infections.

Statistical Analysis

Data were managed using Microsoft Access (Redmond, Washington, USA). All analyses were descriptive and performed using SAS Version 9.4 (Cary, NC, USA).

Results

From 2007 to 2017, 432 students from 15 US GeoSentinel sites met the inclusion criteria. Eleven (73%) sites were affiliated with an undergraduate university; two sites contributed just over half (57%) of the records, both of which are affiliated with undergraduate universities with large study abroad programmes located in the Midwest and West, respectively.

The median age was 21 years; 69% were female. Almost all students (95%) were born in the USA. Among 383 records with information available, 70% of students received a pre-travel consultation with a healthcare provider. Students who did not have a pre-travel visit most commonly travelled to Central America (29 of 116; 25%), western Europe (19 of 116; 16%), and north-east Asia (15 of 116; 13%); students who had a pretravel visit most commonly travelled to sub-Saharan Africa (90 of 267; 34%), South America (66 of 267; 25%) and south central Asia (37 of 267; 14%).

The median length of travel abroad was 40 days [range: 1–469; interquartile range (IQR): 21–96]. Exposures occurred in 69 countries; 56 (81%) were classified by the World Bank as low- or middle-income countries (LMICs). The most common regions of exposure were sub-Saharan Africa (112; 26%), South America (82; 19%) and Central America (62; 14%) (Table 1). The top five exposure countries were India (44; 11%), Ecuador (28; 7%), Ghana (25; 6%), China (24; 6%) and Peru (19; 5%). The most common exposure countries among the 112 students with an exposure in sub-Saharan Africa included Ghana (25; 22%), Tanzania (12; 11%), Sierra Leone (11; 10%) and Uganda (10; 9%).

Table 1.

Regions and top countries of exposure among ill students reported to GeoSentinel, 2007–17 (n = 432)

Regions and top countries of exposurea	n (%)
Sub-Saharan Africa	112 (26)
Ghana	25 (22)
United Republic of Tanzania	12 (11)
Sierra Leone	11 (10)
Uganda	10 (9)
South America	82 (19)
Ecuador	28 (35)
Peru	19 (23)
Brazil	9 (11)
Chile	5 (6)
Central America	62 (14)
Costa Rica	15 (24)
Mexico	15 (24)
Guatemala	13 (21)
South Central Asia	54 (13)
India	44 (81)
Nepal	4 (7)
North-east Asia	32 (7)
China	24 (75)
Japan	4 (13)
South-east Asia	25 (6)
Thailand	10 (40)
Vietnam	7 (28)
Cambodia	5 (20)
Western Europe	24 (6)
France	5 (21)
Italy	5 (21)
UK	4 (17)
Spain	3 (13)
Middle East	15 (3)
Turkey	10 (67)
Israel	4 (27)
Caribbean	10 (2)
Dominican Republic	4 (40)
Cuba	3 (30)
North Africa	8 (2)
Morocco	6 (75)
Egypt	1 (13)
Eastern Europe	5 (1)
Croatia	1 (20)
Czech Republic	1 (20)
Montenegro	1 (20)
Romania	1 (20)
Oceania	3 (1)
Fiji	2 (67)
French Polynesia	1 (33)

^aNumbers of students in each country may not add up to the total in each region because 46 records had a region of exposure listed but no country of exposure.

The median duration between the end of travel to presentation to the US GeoSentinel site was 8 days (range: 0–181; IQR: 2–29). Ninety-eight percent of students were seen as outpatients. Students returned from travel with various infectious, non-infectious and symptom-based diagnoses (Table 2). Of 581 confirmed diagnoses, the gastrointestinal system (261; 45%) was most commonly involved; acute diarrhoea was the most common gastrointestinal diagnosis (113 of 261; 43%). There were six regions where acute diarrhoea was the most common diagnosis (Table 3). Dermatologic diagnoses were also commonly reported (101; 17%), most frequently insect bite(s) (26 of 101; 26%). Nine travellers (9%) with a dermatologic diagnosis had animal bites or exposures, which were sustained in Brazil (one monkey bite and one monkey exposure; n = 2), Honduras (dog bite; n = 1), India (dog bites; n = 2), Indonesia (monkey bite; n = 1), Peru (‘other’ unspecified animal bites; n = 1), the Republic of Tanzania (cat bite; n = 1) and Thailand (monkey bite; n = 1). Five students received rabies post-exposure prophylaxis at a GeoSentinel site.

Table 2.

System-based top diagnoses among ill students reported to GeoSentinel, 2007–17 (n = 581)

System and diagnoses	n (%)
Gastrointestinal	261 (45)
Acute diarrhoea	113 (43)
Post-infectious irritable bowel syndrome	29 (11)
Campylobacteriosis	16(6)
Giardiasis	14 (5)
Acute abdominal pain	10 (4)
Dermatologic	101 (17)
Insect or other arthropod bite or sting	26 (26)
Rash, dermatitis-like	19 (19)
Skin and soft tissue infection (abscess, impetigo, cellulitis, etc.)	12 (12)
Scabies	9 (9)
Animal bite or exposurea	9 (9)
Systemic febrile syndromes	83 (14)
Fever of unknown origin (<3 weeks)	17 (20)
Malariab	14 (17)
Viral syndrome	13 (15)
Influenza-like illness	11 (13)
Denguec	11 (13)
Pulmonary	38 (7)
Upper respiratory tract infection	19 (50)
Acute bronchitis	9 (24)
Lobar pneumonia	3 (8)
Asthma	3 (8)
Cough	2 (5)
Head, eyes, ears, nose, throat	25 (4)
Acute sinusitis	6 (25)
Streptococcal pharyngitis	5 (21)
Tonsillitis	4 (17)
Other pharyngitis	3 (13)
Acute otitis media	2 (8)
Genitourinaryd	11 (2)
Schistosomiasise	3 (28)
Pyelonephritis	2 (19)
Abnormal urinalysis (hematuria or proteinuria)	2 (19)
Chlamydia	1 (9)
Herpes simplex (genital)	1 (9)
Syphilis	1 (9)
Musculoskeletal	8 (1)
Myalgia	4 (50)
Arthralgia	2 (25)
Joint dislocation	1 (13)
Non-septic arthritis	1 (13)
Neurologic	7 (1)
Headache	5 (71)
Neurocysticercosis	1 (14)
Seizure disorder	1 (14)
Lymphatic	3 (1)
Lymphedema	3 (100)
Psychiatric	3 (1)
Anxiety or panic attacks	2 (67)
Post-traumatic stress disorder	1 (33)
Other	41 (7)
Fatigue	7 (16)
Rabies post-exposure prophylaxis	5 (11)
Eosinophilia	3 (7)
Jet lag	3 (7)

^aThree monkey bites, three dog bites, one cat bite, one ‘other’ animal bite and one monkey exposure (unspecified type of exposure).

^bSix had an unknown species, five were P. vivax and three were P. falciparum.

^cAll dengue cases were uncomplicated.

^dOne additional case had vaginitis (9%).

^eTwo cases of Schistosoma mansoni, and one case of Schistosoma with species unknown.

Table 3.

Region of exposure with acute diarrhoea as the most frequent diagnosis, 2007–17

Region of exposure	Total number of diagnoses	Number of diagnoses of acute diarrhoea	%
Sub-Saharan Africa	172	30	17
South America	111	24	22
Central America	79	22	28
South Central Asia	65	12	18
North-east Asia	42	5	12
South-east Asia	29	6	21

Systemic febrile illnesses (83 of 581; 14%), including malaria (14 of 83; 17%) and dengue (11 of 83; 13%), were also reported. Plasmodium falciparum malaria was acquired in Ghana (n = 3); Plasmodium vivax was acquired in Brazil (n = 1), the Republic of Tanzania (n = 2), Senegal (n = 1) and South America with no country ascertainable (n = 1). Six students had malaria without a species identified. Thirteen (93%) students with malaria had a pre-travel visit; one student who neither had a pre-travel visit nor took malaria prophylaxis acquired P. falciparum in Ghana. Information on malaria prophylaxis was available for 9 of the 13 students with malaria who had a pretravel consultation; five (56%) did not take malaria prophylaxis. Students acquired dengue in Asia (Thailand or India; n = 5), sub-Saharan Africa (Ghana; n = 4) and Central America (Nicaragua; n = 2). Among students with dengue, eight of nine (89%) with information available had a pre-travel consultation. Seven percent (31 of 432) of students were diagnosed with a vector-borne disease [in addition to malaria and dengue, four students were diagnosed with cutaneous leishmaniasis (three with Leishmania braziliensis and one with species unknown), and one each with Zika and endemic typhus] (Table 4). Five students were diagnosed with a sexually transmitted infection [acute febrile human immunodeficiency virus (HIV) infection (n = 2), chlamydia (n = 1), genital herpes (n = 1) and syphilis (n = 1)]. Both acute HIV infections were acquired in sub-Saharan Africa; the one student for whom pre-travel consultation information was available did not attend a consultation. Three student travellers were diagnosed with a vaccine-preventable disease: two with typhoid fever (the one student for whom pretravel consultation information was available did not attend a consultation) and one with hepatitis A (this student had a pretravel consultation but vaccination status was not available).

Table 4.

Additional classification of diagnoses as vector-borne diseases, sexually transmitted and vaccine-preventable infections among students reported to GeoSentinel, 2007–17

Classification	N	n (%)
Vector-borne diseases	31
Malariaa		14 (45)
Dengue (uncomplicated)		11 (35)
Leishmaniasisb		4 (13)
Zika		1 (3)
Endemic typhus		1 (3)
Sexually transmitted infection	5
Acute HIV infectionc		2 (40)
Chlamydia		1 (20)
Genital herpes		1 (20)
Syphilis		1 (20)
Vaccine-preventable diseasesd	3
Typhoid		2 (67)
Hepatitis A		1 (33)

^aSix were an unknown species, five were P. vivax and three were P. falciparum.

^bThree were L. braziliensis and one was an unknown species.

^cNo further details regarding risk factors or mode of transmission were available.

^dNo information was available regarding vaccination status.

Discussion

In this study, the demographics of ill students studying abroad and seeking post-travel care at a US GeoSentinel site were consistent with previous study findings. Females more frequently sought post-travel care at a GeoSentinel site than males, possibly because, as previous studies have found, more females participate in study abroad programmes than males.⁵ Over 70% of the students in this analysis received pre-travel counselling, similar to a previous study showing 60% of students received pretravel counselling.⁶ In both studies, this percentage is higher than that reported by other travellers, such as individuals visiting friends and relatives, or tourists, where <50% attended a pre-travel consultation.²⁵ The percentage of students receiving a pre-travel consultation may reflect the pre-travel requirements of the universities that provided data for this study. Students studied abroad for a median of 41 days or about 7 weeks, consistent with national data in which 80% of US study abroad students in 2015–16 studied abroad for approximately one term, the equivalent of 8 weeks.⁵

Ill students who received pre-travel consultations travelled most frequently to high-risk destinations, such as sub-Saharan Africa. However, despite attending a pre-travel consultation, students still became ill with preventable diseases, such as malaria, hepatitis A and typhoid. The reasons for this finding are unknown but may be due to pre-travel preparation deficiencies or vaccine refusal leading to a lack of pre-travel vaccine coverage, or high out-of-pocket costs of vaccines and chemoprophylaxis.²⁷ Also, several students in the study returned with malaria. Most students with malaria did not take malaria prophylaxis, despite attending a pre-travel consultation; this behaviour may be related to non-engagement in prevention due to low perceived risk,^6,28 or may be due to possible cost constraints of filling a prescription or forgetting to take the medication as prescribed. Both study abroad programmes and healthcare providers should emphasize location-specific disease risks, particularly for diseases with a high prevalence in the destination or diseases with high morbidity or mortality, such as malaria. Universities may require students to attend a pre-travel consultation if they are travelling to LMICs; further studies are needed to delineate university practices and study abroad programme requirements.

Most of the destination countries in which students acquired an illness, including four of the top five exposure countries, were LMICs. The trend towards study abroad globalization may foster cultural sensitivity,²⁹ but students may have increased exposure to infectious diseases not endemic in their home countries. For example, students in this analysis acquired infectious diseases non-endemic in the USA, such as typhoid and malaria; both diseases cause a high burden in LMICs due to limited access to clean water,³⁰ or poor mosquito control and prevention measures.³¹ Between 43% and 79% of travellers to developing countries may become ill,³² and students must be aware of infectious diseases in the country in which they are travelling, particularly in LMICs. The number of students with illnesses acquired in LMICs in this analysis may also reflect a referral bias; students travelling to LMICs may be more likely to become ill and thus more likely to seek care.

The most frequently reported illnesses in this study were related to the gastrointestinal system, with acute diarrhoea representing the majority of cases. Acute diarrhoea affects 30–70% of travellers and is the most common travel-related illness³³ regardless of travel purpose. Given the number of students in this report who travelled to LMICs, it is not surprising that diarrhoeal illness was common. The most frequent diagnosis reported after travel to sub-Saharan Africa, Central America, South America and South Central, south-east, and north-east Asia was acute diarrhoea, which likely reflects the high prevalence of travellers’ diarrhoea in regions without adequate levels of safe water, sanitation and hygiene. Pre-travel counselling by a healthcare provider typically includes advice on hand hygiene, water purification, limitation to drinking sealed bottled beverages and avoidance of foods washed with water, raw or undercooked foods and ice.³⁴ Although 70% received pre-travel advice, diarrhoea was still the most common complaint, suggesting the need to integrate information on diarrhoeal management in addition to information on prevention during the pre-travel consultation.

Almost one in five students who returned ill after travelling abroad had a dermatologic diagnosis, most frequently an insect bite or sting. Eight percent of students acquired a vector-borne disease spread by mosquitoes, fleas or sand flies. Healthcare providers should advise students on how to avoid vector-borne diseases, emphasizing preventive measures such as behavioural modification, repellent use or prophylaxis use (such as for malaria) to avoid acquiring a potentially fatal disease.

Students should be advised on how to prevent or manage health-related issues related to jet lag, stress or high-risk activities (e.g. touching animals or engaging in unprotected sexual encounters that may result in unintended pregnancy or sexually transmitted infections) and when to seek clinical advice and care. Students should be informed of the risk of petting or contacting animals and be offered pre-travel rabies vaccination, if travelling to areas where rabies is enzootic and immediate access to appropriate medical care including biologics is limited. They should be aware that rabies post-exposure prophylaxis available if bitten or scratched by an animal but could be difficult to get in some settings.³⁵ Students should also get information on safe sex, be provided condoms and pre-exposure HIV prophylaxis should be discussed with high-risk students. Students should be directed to report any trauma, crimes or assaults to their study abroad programme and local authorities as appropriate.

Analyses using GeoSentinel data have several limitations. GeoSentinel data are not generalizable; over half of the records in this study were from two US GeoSentinel sites. GeoSentinel is an event-based surveillance system and is not population-based; therefore, we cannot derive rates or risk estimates. GeoSentinel may not adequately capture the following data: severe illness or death, because GeoSentinel records are from a single point in time during the patient’s illness; outcome data, which are not routinely reported; route of transmission; or risk factors for certain diseases (such as HIV). GeoSentinel also does not collect data on pre-travel vaccinations, antimalarial medications or what was discussed at the pre-travel consultation. Although GeoSentinel reporting includes infectious, non-infectious and symptom-based diagnoses, the latter two categories are not routinely or systematically collected, and no assumptions can be drawn from these data. Also, activities while abroad and behavioural risks, such as alcohol or drug use, are not collected. Diagnosis data depend upon the GeoSentinel site clinician following standardized diagnosis codes. Fianlly, this report does not include US students who were seen at an international GeoSentinel site during travel, since this information was biased. Thus, illnesses acquired during travel that resolved by the time of departure may not have been captured.

Students may acquire infectious diseases while studying abroad. Students should adhere to strict food and water precautions, use insect repellent to prevent vector-borne diseases, receive destination-specific immunizations and malaria prophylaxis and receive behavioral counselling on how to avoid sexually transmitted infections. Both universities and study abroad programmes should encourage a pre-travel consultation for all students studying abroad, regardless of destination. Additional prospective studies are needed to analyse the entire spectrum of illnesses acquired by students studying abroad. The use of smartphone applications to facilitate research data collection or schedule reminders should be considered in this population.³⁶ These studies should collect information on specific pre-travel preparations (including vaccines) and advice received or reasons for refusal, reasons for non-adherence to malaria chemoprophylaxis, risk behaviours during travel and both infectious and non-infectious conditions acquired while abroad.