Pre-travel Health Care Utilization Among Travelers Who Visit Friends and Relatives

In the past 30 years, many immigrants to higher-income regions of North America have originated from lower-income countries in Asia, Latin America, the Caribbean, and subSaharan Africa. According to the United Nations, 244 million international migrants, including 20 million refugees, were living abroad in 2015.1 In the United States in 2013, 13% of the population (40 million) was foreign-born.2 These immigrants and their children often return to their countries of origin to visit friends and relatives (VFRs).3 One study reported that 23% (2.1 million) of 9.1 million international travelers were VFRs.4 Minnesota is experiencing rapid growth of its foreignborn population; from 1990-2015, the number of Asian and African residents tripled, and the number of Hispanic residents quadrupled.5 According to the Minnesota State Demographic Center, the nonwhite population is estimated to grow from 14% in 2005 to 25% in 2035.6 Therefore, the rate of international VFR travel is likely to increase. Compared with tourist travelers, VFRs have higher travelassociated health risks.7,8 VFRs have a higher incidence of travel-related infections such as typhoid fever, tuberculosis, and hepatitis A, and they are 8 times more likely to receive a diagnosis of malaria.3 In a 2011 study of 772 Quebecois travelers, VFRs accounted for 53% of malaria cases, 57% of hepatitis A cases, and 94% of typhoid cases.9 The Centers for Disease Control and Prevention (CDC) list several reasons underlying the increased prevalence of travel-related illnesses in VFRs, including lack of awareness of risk, low rate of http://ijtmgh.com Int J Travel Med Glob Health. 2017 June;5(2):53-59 doi 10.15171/ijtmgh.2017.11


Introduction
In the past 30 years, many immigrants to higher-income regions of North America have originated from lower-income countries in Asia, Latin America, the Caribbean, and sub-Saharan Africa.According to the United Nations, 244 million international migrants, including 20 million refugees, were living abroad in 2015. 1 In the United States in 2013, 13% of the population (40 million) was foreign-born. 2These immigrants and their children often return to their countries of origin to visit friends and relatives (VFRs). 3One study reported that 23% (2.1 million) of 9.1 million international travelers were VFRs. 4 Minnesota is experiencing rapid growth of its foreignborn population; from 1990-2015, the number of Asian and African residents tripled, and the number of Hispanic residents quadrupled. 5According to the Minnesota State Demographic Center, the nonwhite population is estimated to grow from 14% in 2005 to 25% in 2035. 6Therefore, the rate of international VFR travel is likely to increase.
Compared with tourist travelers, VFRs have higher travelassociated health risks. 7,8VFRs have a higher incidence of travel-related infections such as typhoid fever, tuberculosis, and hepatitis A, and they are 8 times more likely to receive a diagnosis of malaria. 3In a 2011 study of 772 Quebecois travelers, VFRs accounted for 53% of malaria cases, 57% of hepatitis A cases, and 94% of typhoid cases. 9The Centers for Disease Control and Prevention (CDC) list several reasons underlying the increased prevalence of travel-related illnesses in VFRs, including lack of awareness of risk, low rate of

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International air travel has increased during the recent century, and the number of pregnant women who travel internationally by air is on the rise.Most pregnant women are able to fly safely, but general considerations must be taken into account.Prior to traveling, pregnant women should be assessed for gestational age, fetus and placenta status, blood group and Rh status by laboratory evaluation or with diagnostic ultrasound imaging.The Center for Disease Control and Prevention (CDC) recommends that pregnant women travelers carry a copy of their medical records with them on their trip. 1 The latest recommendation of the ACOG indicates that occasional travel by air during pregnancy is safe.Specifically, occasional air travel by women with a singleton pregnancy can be done until 36 weeks gestation.Women with an uncomplicated multiple pregnancy are allowed to fly up to the end of the 32nd week.As emergencies usually happen in the first and third trimesters, the safest time to travel is probably the middle of the pregnancy, between 14-18 weeks. 2,3lmost all women with a normal pregnancy can travel without limitation up to 28 weeks, but there are few contraindications for air travel, including obstetric complications, severe anemia (Hb<7.5 g/dL), recent hemorrhage, sickle cell anemia, acute otitis media and sinusitis, uncontrolled cardiac or respiratory disease, and a post-operative condition as with recent gastrointestinal surgery. 3lthough air travel is safe, there are specific risks during pregnancy.The incidences of miscarriage and preterm birth are greater among flight attendants than the general population.Exposure to cosmic radiation is not hazardous to the fetus for the occasional pregnant air traveler.One other concern is venous thromboembolism for which flight duration is a key factor.Air travel of more than 4 hours at a time may increase the risk of venous thromboembolism, but this is a weak risk factor.Immobility during long flights can lead to such a condition. 4,5here are some general suggestions for the pregnant traveler to minimize the risk of an adverse outcome related to air travel during pregnancy.Before planning to travel, women should check the airline's policy about air travel during pregnancy.The traveler's seat belt should be closed during a flight, and unnecessary traffic should be avoided.Because of the necessity of take occasional walks, pregnant women should have an aisle seat to facilitate movement.Women should drink plenty of fluids to avoid dehydration.][3] pre-travel health care utilization, and financial and cultural barriers. 3While abroad, VFRs tend to stay with family members and may quickly re-adopt local lifestyle practicesfor example, they may live in crowded conditions, sleep without window screens, and consume untreated water and uncooked food. 7iven these high travel-related health risks, VFRs may benefit from pre-travel consultation.However, only approximately 31.4% of VFRs (compared with 60.9% of tourist travelers) seek pre-travel advice. 8Furthermore, information on pre-travel assessment of VFRs is limited.This study aimed to characterize VFRs and non-VFRs who sought pre-travel consultation at a local travel clinic and describe the VFRs' travel patterns and adherence to pre-travel recommendations.For those VFRs who sought pre-travel health care, this study compared adherence with recommended vaccines between VFRs and non-VFRs.This study aimed to assess these measures, as past studies on VFRs suggested this population may be at higher risk of travel-related infection due to longer durations of stay and lower adherence with pre-travel medical advice. 10

Pre-travel Health Care
A retrospective cohort study of all patients (VFRs and non-VFRs) who received pre-travel health care at the Mayo Clinic Travel and Tropical Medicine Clinic (TTMC) from January 1, 2012, through December 31, 2013 was conducted.The Mayo TTMC is the largest travel clinic serving residents of Olmsted County, Minnesota.Consultations there include an assessment of the following four primary topics: vaccines, malaria, diarrhea, and safety.Based on the patient's travel itinerary and medical and immunization history, the travel medicine provider assesses the risk for vaccine-preventable illness, mosquito-transmitted illnesses (particularly malaria), traveler's diarrhea, and environmental and safety hazards.Counseling is provided regarding risks and benefits of recommended routines and travel-related vaccines, rabies post-exposure prevention after animal bites, mosquito avoidance measures, malaria chemoprophylaxis, food and water precautions, and self-management of traveler's diarrhea with an antidiarrheal and antibiotic.Recommendations for vaccines and preventive travel-related medications (e.g., malaria chemoprophylaxis and an antibiotic for self-treatment of traveler's diarrhea) are provided in accordance with CDC guidelines. 11

Data Collection and Measures
All children and adults who sought pre-travel consultation at the Mayo TTMC from January 1, 2012 through December 31, 2013 met the inclusion criteria for this study.The pretravel consultation at the Mayo TTMC is standardized, and all patients seeking pre-travel consultation are provided a questionnaire that asks about the purpose of travel.Visiting friends and relatives is listed as one of the reasons for travel on the questionnaire.Those who selected "Visiting Friends and Relatives" were included in the VFR cohort.VFRs were defined as immigrants and refugees who returned to their countries of origin to visit their friends and relatives. 3Patients were excluded if they did not have a Minnesota Research Authorization, which authorized the review of medical records for study purposes.
The following data was abstracted from the electronic health records of all TTMC patients: demographics (age, gender, race/ethnicity, VFR status, and insurance type); travel characteristics (time from travel clinic visit to date of departure, destination, and duration of travel); immunizations; and anti-malarial and antibiotic prescriptions.Place of travel was categorized into 5 groups: (1) Africa, (2) Asia,( 3) Latin America, Europe, the Caribbean, or Australia, (4) Middle East, and (5) missing data or unknown.These categories were not mutually exclusive, because travelers could list multiple countries.Dates were obtained by reviewing pre-travel consultation clinical notes, which are based on the patient's responses to the standardized questionnaire provided prior to the appointment.During the pre-travel consultation, the health care provider elicits and documents any additional travel-related information as needed.
Recommendations for and completion of travel-related vaccines (hepatitis A, hepatitis B, Japanese encephalitis, rabies, typhoid, and yellow fever) and routine vaccines (human papillomavirus, influenza, measles-mumps-rubella [MMR], meningococcus, pneumococcus, polio, tetanus-diphtheriapertussis, and zoster) were recorded in the immunization module within the electronic medical record as administered, declined, or deferred (with rationale for deferral).Vaccine recommendations were based on the patient's travel itinerary and medical and immunization history, following current CDC guidelines. 11t the Mayo TTMC, serologic testing is often performed when travelers report a potential history of vaccination or infection for hepatitis A, hepatitis B, MMR, or varicella, especially if the traveler is deemed to be at high risk of acquiring any of these infections during travel.If serologic testing is negative (i.e., no serologic evidence of immunity), then patients are advised to undergo vaccination; if serologic testing is positive (i.e., serologic evidence of immunity is present), patients are considered to have completed the specific vaccination recommendations.
Vaccine completion was defined as receipt (with documentation) or confirmed positive serology of the recommended vaccine (influenza, MMR, meningococcus, pneumococcus, polio, typhoid, varicella, zoster, yellow fever) or completion of the entire multi-dose series (hepatitis A, hepatitis B, human papillomavirus, Japanese encephalitis, and rabies).If the vaccine series was only partially completed, it was categorized as a partial or incomplete vaccination.For children, polio vaccine completion was defined as completion of the series; for adults, polio vaccination was considered complete with receipt of one booster injection, when indicated.If a patient refused a recommended vaccine or did not have adequate time to complete a recommended vaccine series, it was considered an incomplete vaccine.Only vaccines that were recommended on the basis of the traveler's specific itinerary or risks (as determined by the health care provider) were included in the analysis of completed vaccines.

Data Analysis and Modeling
All data analyzed during this study is included in this published article.Demographic and travel data were categorized and summarized as frequencies and percentages.Completed vaccinations were summarized by number and percentage.The χ 2 test was used to assess differences in demographics, travel characteristics, vaccinations, and antimalarial and antibiotic prescriptions between VFRs and non-VFRs.Multivariable analysis with logistic regression was used to adjust for factors that were significant with univariate analysis.Results of the logistic regression models are presented as odds ratios (OR) and 95% confidence intervals (CIs).Statistical significance was defined as P ≤ 0.05.All analyses were performed using SAS version 9.4 (SAS Institute Inc.).
VFRs were less likely to complete the recommended tetanus, polio, and rabies vaccinations (Table 3).Although the difference was not significant for the MMR vaccine, VFRs were more likely to complete it when recommended.After adjusting for age, sex, insurance type, and duration of travel, VFRs remained less likely to complete tetanus and polio vaccines and more likely to complete MMR vaccines, but these associations were not statistically significant.However, VFRs remained significantly less likely to complete the rabies vaccinations (OR, 0.31 [95% CI, 0.13-0.77]),even after adjusting for age, sex, insurance type, and duration of travel.Travelers departing more than four weeks after their pre-travel clinic visit had higher odds of completing the rabies vaccine series than those seen fewer than four weeks before The most common reasons stated for incomplete vaccinations included a perceived low risk of illness (n = 10), insufficient time before departure (n = 23), fear of adverse effects (n = 5), uncertainty regarding vaccination history (n = 3), and preference to defer vaccination (n = 4).Given the low numbers of documented reasons, no statistical comparisons between VFRs and non-VFRs could be made.

Discussion
This study identified several important demographic, travel, and vaccination differences between VFR and non-VFR travelers.Compared with non-VFRs, more VFRs at the travel clinic were young, nonwhite, used interpreters, traveled to Africa and Asia, and traveled for longer durations.Both traveler groups had low vaccine completion rates for hepatitis A, hepatitis B, Japanese encephalitis, and rabies.VFRs were significantly less likely to complete rabies vaccinations than non-VFRs.
The findings highlight several features of VFRs that should prompt changes in pre-travel counseling.Because the study included many younger travelers (age 0-20 years), pediatric patients may be an important subgroup that merits more intensive pre-travel counseling.Although this study did not examine incidence of travel-associated infection in pediatric travelers, others have documented a high rate of traveler's diarrhea in the pediatric population.In a 1991 study of 446 young Swiss travelers, 12 traveler's diarrhea occurred in 90 of 250 travelers (36.0%) aged 15 to 20 years.Therefore, children and their parents may require more intensive pre-travel counseling to ensure proper rehydration during bouts of traveler's diarrhea.
In addition, VFRs tend to have longer periods of travel.In the current study, 183 (46.6%)VFRs planned to travel for at least four weeks.Long-term travel has been associated with increased risk of chronic diarrhea, giardiasis, malaria, schistosomiasis, and leishmaniasis. 13VFRs also sought pretravel consultation closer to their departure date than non-VFRs, possibly because of last-minute travel plans for family emergencies.This short timeframe can limit the feasibility of completing vaccine series. 11Given these last-minute, longterm travel patterns, primary care providers may want to take a moment during a general medical examination to remind VFRs to seek pre-travel counseling early in the course of travel planning.
Vaccination rates for several preventable illnesses (hepatitis A, hepatitis B, Japanese encephalitis, and rabies) were low for both groups in the current study.These low rates are particularly worrisome for VFRs who often travel to and stay longer in regions in which they have a higher risk of acquiring these illnesses.For example, 61.1% of viral hepatitis cases among VFRs returning from sub-Saharan Africa were caused by hepatitis B. 14 VFRs also tend to have closer contact with local residents.In a study of African immigrants living in London, 40.0% of men and 21.0% of women had a new sexual partner upon returning to Africa, where the prevalence of human immunodeficiency virus and hepatitis B is higher. 15he low rate of rabies vaccination (12.3%) among VFRs in this study has a considerable number of potential implications on travelers' health, because rabies has a near-100% fatality rate for patients bitten by a rabid animal. 16accination series may not be completed for several reasons.A multi-dose vaccine may require up to three clinic visits; therefore, travelers may not have sufficient time before departure.Among VFRs, 92/390 (23.6%) were seen less than 1 week before departure, and 190/390 (48.7%) were seen between 1 and 4 weeks before departure.The costs associated with multiple clinic visits also may serve as a disincentive for vaccine completion.In addition, prospective travelers may not fully understand the health implications of travel-related infections and the potential benefits of immunizations.
Some studies have shown that VFRs who seek pre-travel care are treated differently than non-VFRs.Among pediatric travelers in Boston, VFRs were less likely than non-VFRs to be prescribed atovaquone-proguanil and antidiarrheal medication.In addition, among those who indicated English as their primary language, non-VFRs were more likely to receive typhoid and yellow fever vaccine than VFRs. 17No significant differences were observed between VFRs and non-VFRs for antimalarial prescriptions, but a greater percentage of VFRs were prescribed antidiarrheal medications.This may be because more VFRs planned travel to Africa, Asia, and the Middle East, where antidiarrheal precautions are more strongly recommended. 18 limitation of the current study is the small number of VFRs; it was not possible to include VFRs who did not seek pre-travel care at the TTMC.It is possible that the VFRs included in this study were a relatively more motivated and health-literate subgroup; therefore, the differences in pretravel vaccinations between VFRs and non-VFRs may have been underestimated.Some travelers will not seek pre-travel consultation unless there is a requirement to enter a country, such as proof of yellow fever or meningococcal vaccination.This study has a lack data on whether prescriptions were filled and whether travelers adhered to antimalarial prophylaxis.This study was conducted at a single clinic, which limits the generalizability of the findings.
Nonetheless, the findings of this study highlight some disparities in pre-travel care for VFRs and highlight several opportunities to improve pre-travel education and vaccinations.Further research exploring specific reasons for incompletion of recommended vaccines will pinpoint changes to be made in practice and improve pre-travel health care.The potential impact of language barriers in adherence to travel recommendations also needs to be elucidated.

Conclusion
VFRs visiting the Mayo TTMC were more commonly younger travelers planning to visit African and Asian countries.They also had longer travel durations and lower rates of vaccine completion than non-VFRs.VFRs may be at higher risk of being affected by certain infectious diseases associated with travel.Travel clinics have the opportunity to provide focused pre-travel counseling and improved vaccinations for VFR travelers.

Table 1 .
Traveler Characteristics (N=2073) Places of travel were not mutually exclusive.χ 2 comparisons of the proportion visiting and not visiting friends and relatives were compared for each place of travel.
a VFRs were defined as immigrants and refugees who were returning to their countries of origin to visit friends and relatives.b Percentages were calculated using the following denominators: VFR, n = 390; non-VFR, n = 1676.c departure (OR, 2.61 [95% CI, 1.38-4.93]).

Table 2 .
Comparison of Pre-travel Vaccination Rates Among VFR and Non-VFR Travelers

Received Vaccine or Had Positive Serology, No. (%) a Vaccine Recommended, No. Received Vaccine or Had Positive Serology, No. (%) a Routine Vaccines
Only those who were recommended to have each vaccine were included in the comparisons.All patients who completed a vaccine series or had positive serology testing were included.
a c Polio vaccine refers to the injectable polio virus vaccine.d Typhoid vaccine includes both oral and injectable forms.

Table 3 .
Associations Between Patient Characteristics and Completion of Specific Recommended Vaccinations Adjusted for VFR, age, sex, insurance, and duration of travel b For rabies, the odds ratio was adjusted for VFR, age, sex, insurance, duration of travel, and time from travel clinic visit to date of departure. a