Impact of Traveling to Visit Friends and Relatives on Chronic Disease Management

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1 95 ORIGINAL ARTICLE Impact of Traveling to Visit Friends and Relatives on Chronic Disease Management Holly E. Gurgle, PharmD, BCACP, David J. Roesel, MD, MPH, DTM&H, Tiffany N. Erickson, PharmD, BCACP, and Emily Beth Devine, PhD, MBA, PharmD College of Pharmacy, University of Utah, Salt Lake City, UT, USA; Department of Medicine, Harborview Medical Center, UW Medicine, Seattle, WA, USA; Department of Pharmacy, Harborview Medical Center, UW Medicine, Seattle, WA, USA; School of Pharmacy, University of Washington, Seattle, WA, USA DOI: /jtm Background. Travelers visiting friends and relatives (VFR) are known to be at high risk of acquiring infectious diseases during travel. However, little is known about the impact of VFR travel on chronic diseases. Methods. This was a nonrandomized, retrospective observational study. Patients were adult VFR travelers who received care from an internal medical clinic serving immigrants and refugees. The primary objective was to determine the impact of VFR travel on markers of chronic disease management including: blood pressure, glycosylated hemoglobin, body mass index, serum creatinine, and anticoagulation. Results. Of the 110 VFR travelers in our study, N = 48 traveled to Africa and N = 62 traveled to Asia for a mean duration of 59 (range ) days. Of the 433 counseling points discussed at pre-travel visits, 71% were infectious disease prevention, 16% chronic disease related, and 13% travel safety. A total of 63 patients (57%) reported one or more health problems while traveling. Of these, 35 patients (32%) experienced a problem related to a chronic condition. In comparison, 24 (22%) patients experienced an acute infection. Sixty percent of patients were nonadherent to medications during travel. An average increase in diastolic blood pressure of 3.6 mmhg among patients with hypertension was the only statistically significant change in a chronic disease marker when values before and after travel were compared. Subgroup analysis revealed that travel to Africa and nonadherence to medications were also associated with worsening blood pressure control, and patients traveling to Africa experienced a decrease in body mass index. Conclusions. This study identified a high proportion of problems related to chronic conditions experienced during VFR travel, while pre-travel appointments tended to focus on infectious disease prevention. A greater emphasis on medication adherence and chronic disease management during VFR travel is also needed during pre-travel preparations. International tourist arrivals were estimated to reach 1 billion for the first time in 2012, with nearly half of all traveler arrivals in emerging economies. 1 In 2011, 46% of individuals traveling internationally by air from the United States were visiting friends and relatives (VFR) travelers. 2 Although the definition of VFR travelers varies throughout the literature, this term generally refers to immigrants currently residing in high-income countries returning to their homelands for a temporary visit, particularly when there is a gradient of epidemiologic risk between home and destination. 3 Corresponding Author: Holly E. Gurgle, PharmD, BCACP, College of Pharmacy, University of Utah, 30 South 2000 East, Room 267, Salt Lake City, UT 84112, USA. holly.gurgle@pharm.utah.edu VFR travelers are generally considered to have higher travel-related health risks than tourists and business travelers. They typically have longer durations of travel, have more intimate contact with the host population, and travel to regions of the world with higher prevalence of communicable disease. They generally live and share meals with local hosts, with potentially greater exposure to unsafe food, water, and vector-borne diseases. VFR travelers have been consistently found to experience an increased burden of travel-related infectious diseases including malaria, viral hepatitis, typhoid fever, and sexually transmitted infections relative to tourists and business travelers Unfortunately, VFR travelers may underestimate their travel-associated health risks and may be less likely to seek pre-travel health advice or be appropriately vaccinated prior to travel. 4 7,9, International Society of Travel Medicine, Journal of Travel Medicine 2013; Volume 20 (Issue 2):

2 96 Gurgle et al. While the available literature demonstrates that VFR travelers have increased risk of travel-related infectious diseases relative to other travelers, little is known about the impact of VFR travel on chronic disease. Pretravel health consultations often emphasize diarrhea prevention and treatment, vaccine-preventable diseases, and malaria prophylaxis. 8,11 20 However, epidemiologic evidence suggests that travelers are far more likely to die from the same illnesses, complications, and acute events as they would at home, with cardiovascular disease accounting for the greatest proportion of all deaths during travel. One study of US travelers found that 49% of all deaths were due to cardiovascular events, much more than deaths due to accidents and infectious causes combined. 21 Others have described unique challenges to chronic disease management associated with travel However, it is unclear if management of chronic medical conditions might also be impacted by VFR travel. It is anticipated that VFR travelers may experience poorer control of cardiovascular risk factors such as blood pressure, blood glucose, and lipid profile during their trips. In addition, serum levels of drugs with a narrow therapeutic window, such as warfarin, may be inadequately monitored, leading to increased risk of complications. The purpose of this study was to conduct a retrospective review to investigate the impact of VFR travel on health with a particular focus on markers of chronic disease management: hemoglobin A1c, low density lipoprotein (LDL), systolic blood pressure (SBP), diastolic blood pressure (DBP), body mass index (BMI), serum creatinine (SCr), and international normalized ratio (INR). Methods This investigation was approved by the Institutional Review Board of the University of Washington. All subjects in the study receive primary care services at a clinic serving adult, first-generation immigrants and refugees residing in King County, Washington. The clinic is associated with an academic medical center and visits were conducted by attending physician, medicine resident, physician s assistant, or clinical pharmacist. All patient visits were conducted face-to-face with the assistance of a professional interpreter owing to the limited English proficiency of the study patient population. Travel health services are routinely offered in the clinic and two of the attending physicians have specific training in travel medicine. A retrospective chart review was performed on patients engaged in VFR travel between January 1, 2003 and December 31, Candidates for the study were identified by searching the electronic medical record for clinic notes in which travel was identified as the primary reason for the visit. Additional candidates were identified by reviewing the clinic s pharmacy dispensing records for patients who received the drug doxycycline. This strategy was chosen because virtually all of the clinic s patients who travel to malaria-endemic regions use doxycycline for malaria prophylaxis, as it represents the most affordable choice for those with limited incomes traveling for prolonged time periods in chloroquine-resistant areas. Inclusion criteria for the study included age 18, travel 21 days to a low-income country, documentation of a travel health counseling visit within the 6-month time period before the beginning of travel, and at least one additional visit within 6 months of return from travel. For patients who had more than one episode of travel, only the most recent travel encounter was included. Additionally, patients needed to have one or more of the following medical conditions at baseline in order to be included: diabetes, hyperlipidemia, hypertension, obesity, renal insufficiency, or a condition requiring chronic anticoagulation. Study patients records were reviewed to determine all chronic medical conditions at baseline, topics covered during the pre-travel visit, and any self-reported health problems or nonadherence to medications that occurred during travel. For the purposes of this investigation, medication nonadherence is defined as a patient stopping or running out of one or more medications during the travel period. In addition, the following markers of chronic disease management were compared before and after travel using a two-sided paired t-test: hemoglobin A1c, LDL, SBP, DBP, BMI, SCr, and INR. A linear regression analysis was performed to identify predictors of medication nonadherence, including the following covariates: patient age, the number of medications, travel destination, duration of travel, and whether the patient received counseling on how to obtain medications to cover the duration of travel. A second linear regression was performed to identify factors associated with having a problem related to chronic conditions during travel, including the following covariates: patient age, travel destination, duration of travel, number of medications, documented nonadherence to medications, and whether or not the patient received counseling on chronic disease management during the pre-travel visit. Results A total of 110 patients were included in our analysis (Figure 1). Patient demographics are summarized in Table 1. All patients traveled either to Asia (N = 62) or Africa (N = 48), and the median duration of travel was 59 days (range ). Languages spoken are summarized in Table 1 and are representative of both country of origin and travel destinations in Asia and Africa. Key elements of pre-travel preparations are described in Table 2. A total of 433 travel-related counseling points were documented in the medical record, averaging 4 counseling points per patient. Of these, 71% (N = 309) of all travel topics discussed were related to infectious disease prevention. Chronic disease and safety-related counseling topics comprised 16% (N = 69) and 13% (N = 55) of total health topics discussed at pre-travel

3 Visit Friends and Relatives Travel 97 Table 1 Patient demographics Median (range) Age 65 (34 86) Year of immigration 1995 ( ) Percent Figure 1 Identification of patients for inclusion in investigation. visits, respectively. Table 2 further describes the percent of patients that received at least one piece of travel counseling advice in specific topic areas including: infectious disease, chronic disease, and safety. Sixty-three patients (57%) reported one or more health problems while traveling; 10 of these patients were sick enough that they sought care from a health care provider while abroad. Thirty-five patients (32% of travelers) experienced a health problem related to one or more chronic conditions diagnosed prior to travel (Table 3). Thirty patients had a problem related to one chronic condition and five patients experienced problems related to two chronic conditions. The most commonly identified health problems were related to diabetes management, worsening of reflux or other chronic gastrointestinal complaints, difficulties with blood pressure control, exacerbation of mental health issues, and worsening of chronic pain complaints. Two patients required inpatient admission after return to the United States, one patient presented with a congestive heart failure exacerbation and the other with new-onset atrial fibrillation in the setting of a hypertensive crisis. Both patients had been nonadherent to antihypertensive medications during travel. By contrast, 34 patients (31%) reported a health problem that was new and not related to a chronic condition diagnosed prior to travel. Of these, 24 (22%) patients experienced an infection; most commonly, respiratory tract infections and skin and soft tissue infections. There were no reported hospitalizations in this group. A linear regression model using age of patient, duration of travel, travel destination, number of medications before travel, documented nonadherence to medications, and whether chronic disease management was discussed as part of pre-travel counseling found that the number of medications taken before travel was associated with increased likelihood of a health problem related to a chronic condition. Patients were categorized as taking a small (0 3), moderate (4 6), large (7 10), or very large (>10) number of medications. For each increase in category, the odds of experiencing a health problem related to a chronic medical condition increased by 4.13-fold. Female 67.3% Primary language Cambodian (Khmer) 25% Vietnamese 23% Somali 16% Tigrinia 12% Other 10% Amharic 9% Cantonese 5% Chronic conditions Hypertension 77% Dyslipidemia 76% Diabetes 36% Renal insufficiency 12% Overweight 70% Obesity 17% Chronic anticoagulation 3% Additional baseline chronic conditions Reflux/dyspepsia 33% Chronic pain/neuropathy 31% Depression/anxiety 26% Coronary disease/heart failure 17% Osteoporosis 15% Asthma/chronic obstructive pulmonary 13% disease Allergic rhinitis 12% Nondiarrheal gastrointestinal disorders 11% Post-traumatic stress disorder 10% Headache/migraine 10% Anemia 9% Cancer 8% Arthritis 8% Thyroid disorder 7% Benign prostatic hypertrophy/urinary 7% incontinence Gout 6% Glaucoma/cataracts 5% Chronic skin conditions 5% Chronic hepatitis 5% The primary language generally reflects the country of birth. The chronic conditions listed are those preselected as comprising the inclusion criteria. The reported percentages reflect the percent of total patients (N = 110) with a particular condition. Many patients had more than one chronic condition. A comparison of markers of chronic disease management before and after travel is described in Table 4. It did not reveal any statistically significant changes, except for an average increase in DBP of 3.6 mmhg among patients with hypertension (p = 0.01). Subgroup analysis revealed that travel to Africa and reported nonadherence to medications were associated with worsening blood pressure control. Patients traveling to Africa experienced an increase in both SBP (131.8 ± 16 vs ± 17.7, 95% CI [ 12.87, 0.34]) and DBP (70.6 ± 10.4 vs 74.9 ± 8.7, 95% CI [ 8.28, 0.39])

4 98 Gurgle et al. Table 2 Details of the pre-travel health visits Table 3 Self-reported health problems during travel Median (range) Number (%) Description of visits Number of pre-travel visits 1 (1 4) Duration of pre-travel visit(s) (minutes) 30 (5 100) Days between pre-travel visit and travel 7 (1 120) Days between travel and post-travel visit 23 (1 129) Percent (N = 110) Immunizations prescribed Patients provided 1 vaccine(s) 84% Routine vaccine 63% Travel vaccine 37% Travel topics discussed Infectious disease 78% Malaria prevention 61% Water safety 58% Food safety 56% Diarrhea prevention 46% Swimming 11% Walking barefoot 7% Chronic disease 44% Purchase of medications 40% Chronic disease safety 33% Safety 26% General safety 20% Caution around animals 16% Deep vein thrombosis prevention 17% Travel insurance 5% Routine adult immunizations refer to those immunizations recommended by the Centers for Disease Control and Prevention for all adults living in the United States. Travel-specific immunizations are vaccines given to protect against illnesses related to travel, specifically such as typhoid, meningococcal, and yellow fever. Listed percentages are the percent of total (N = 110) patients that received one or more counseling points related to each possible travel topic during their pre-travel visit. when values before and after travel were compared. Travel to Asia was not associated with worsening of blood pressure. Patients traveling to Africa also experienced a decrease in BMI (29.1 ± 2.8 vs 28.6 ± 3.3, 95% CI [0.04, 0.80]). Patients who were nonadherent to medications during travel, not surprisingly, also had an increase in both SBP (130.0 ± 16.3 vs ± 17.8, 95% CI [ 9.86, 0.56]) and DBP (69.2 ± 9.7 vs 73.2 ± 10.0, 95% CI [ 6.45, 1.72]). On average, patients included in this study took the same amount of chronic medications before and after travel, 7 ± 4 medications. Sixty percent of patients reported nonadherence to one or more prescribed medications during travel. Patients either chose not to take their medication(s) during travel or failed to bring an adequate supply for their entire trip. A linear regression analysis found that duration of travel increased the risk of medication nonadherence. For each additional month of travel, the odds of being nonadherent increased 1.44 times compared to one less month (p = 0.045; 95% CI: 1.01, 2.06). Problem not associated with chronic condition 34 (31%) Infection 24 (22%) Respiratory infection 11 (10%) Skin and soft tissue infection 6 (6%) Diarrheal infection 5 (5%) Urinary tract infection 2 (2%) Accident/injury 6 (6%) Other 4 (4%) Problem associated with chronic condition, 35 (32%) Endocrine 8 (7%) Gastrointestinal 7 (6%) Pain 7 (6%) Mental health 6 (6%) Cardiovascular 6 (6%) Pulmonary 3 (3%) Renal 2 (2%) Headaches/migraines 2 (2%) Additional problems Medication nonadherence 66 (60%) Lost medications 3 (3%) Of the 63 patients who reported health problems while traveling, 6 reported both a problem associated with a chronic condition and a problem not associated with a chronic condition. Of the 35 patients who reported health problems associated with a chronic condition, 30 patients reported a problem related to one condition, and 5 patients reported problems related to two chronic conditions. Discussion Little is known about the impact of travel on chronic disease management, especially among VFR travelers. This small study is an attempt to fill this important gap in knowledge. We found that nearly one-third of VFR travelers in our study population experienced health problems while traveling in Africa or Asia that were related to one or more chronic medical conditions. This rate exceeded that of travelers who reported an acute health problem related to an infectious disease. The two patients in our study requiring hospitalization after travel were admitted as a result of cardiovascular issues, and none required admission for an infectious illness. Although we found a low rate of travelers diarrhea in our cohort (N = 5 or 4.5%), these rates were comparable to other reports of acute diarrhea in long-term or immigrant VFR travelers. 4,8 Furthermore, we found very high rates of medication nonadherence during VFR travel, particularly with travel of longer duration. We also found that the likelihood of a health problem while traveling corresponded to the number of chronic medications the traveler was taking. These findings are important because we also found that the focus of pre-travel counseling in our clinic conformed to the traditional emphasis on vaccine-preventable illnesses, malaria prophylaxis, and advice on safe food and water. Prior studies have shown that the leading cause of death among travelers is cardiovascular disease, so the worsening of blood pressure control found among our African travelers is concerning. 21,29 These

5 Visit Friends and Relatives Travel 99 Table 4 Chronic disease markers before and after travel Before After p Value 95% CI Body mass index (N = 76) 28.3 ± ± ( 0.406, 0.09) Systolic blood pressure (N = 84) ± ± ( 1.29, 5.62) Diastolic blood pressure (N = 84) 68.1 ± ± ( 6.63, 0.88) International normalized ratio (N = 3) 3.0 ± ± ( 3.60, 2.87) Low density lipoprotein (N = 58) ± ± ( 11.96, 5.60) Serum creatinine (N = 12) 1.77 ± ± ( 0.18, 0.10) Hemoglobin A1c (N = 33) 7.55 ± ± ( 0.24, 0.68) results suggest that for VFR travelers on numerous medications or traveling for extended trips, it may be important for the pre-travel visit to include strategies for chronic disease management and medication adherence during travel. Following this recommendation is likely to be challenging. In our study, the pre-travel visit occurred a median of only 7 days prior to departure, with a median visit length of only 30 minutes, compelling the provider to prioritize the focus of the visit. Prior studies have shown that VFR travelers tend to underestimate their risk and rarely seek care from specialized travel clinics. Therefore, the onus of providing this advice falls on primary care providers, who already have many competing priorities and increasingly constrained time to spend with patients. 4 7,9,10 Additionally, a specific barrier we have found in our clinic (in Washington State) to medication adherence is that those receiving Medicare, Medicaid, or hospital-sponsored charity care are usually limited to only a 30-day supply of medications, and many cannot afford to pay for additional supplies of medications out of pocket if their travels extend beyond this period. There are several limitations to this study including our limited patient population and retrospective study design. Owing to the fact that ours is a primary care clinic, not a travel clinic, along with limitations to our electronic medical record system, it is not possible to easily identify all patients who are traveling. A small number were identified because travel counseling was explicitly identified as the reason for the visit. For the majority, they were identified by screening the records of patients who were given a prescription of doxycycline as a proxy for travel, but this may have missed those who did not inform their physician that they were traveling, traveled to nonmalarious areas, declined this medication, or received it from an outside pharmacy. In addition, the clinic records may underestimate the number of patients who ran out of medications or experienced problems while traveling, because this was not always asked about in post-travel visits or may not have been reported by the patient. Markers of chronic disease related to cardiovascular risk were prioritized in this investigation. However, the large number of health problems related to mental health conditions and high rate of respiratory infections potentially related to chronic respiratory conditions also warrant further study on the impact of VFR travel on other chronic conditions. Finally, although the mean time of follow-up from end of travel to being seen in clinic was 23 days, some patients were not seen until 4 months after they returned, which may have reduced the patient s recollection of health problems or the impact of travel on the variables measured. Our study did not identify any statistically significant change in objective markers of chronic disease management, with the exception of a small worsening of DBP. The small sample size and retrospective nature of this study may have limited its ability to capture these changes. In addition, although some patients may have had worsening of chronic disease management due to issues related to medication nonadherence, others may have had improvements due to more positive changes in lifestyle. Our patients routinely report increased exercise, improvements in diet, and decreased stress levels while in their home countries during VFR travel. Our investigation was not able to capture these factors, with the exception of the important finding that travelers to Africa did have a small decrease in BMI after they returned. This decrease in BMI did not seem to correlate with diarrhea or other acute infections and we postulate that it is related to changes in activity level and diet during travel. Conclusion This small, retrospective study revealed that a high proportion of low-income immigrants from Asia and Africa who returned home to visit friends and relatives experienced health problems related to chronic disease, while their pre-travel clinic appointments tended to focus on ways to minimize infectious disease risk. These findings have important implications for the travel medicine community as well as primary care providers caring for immigrants and refugees. Identifying VFR travelers prior to their trips and discussing strategies with them to maintain medication adherence and chronic disease management while traveling should be given greater emphasis.

6 100 Gurgle et al. Acknowledgments This study was conducted while Dr Gurgle was a PGY1 Pharmacy Practice Resident at UW Medicine in Seattle, WA. Declaration of Interests The authors state that they have no conflicts of interest. References 1. UNWTO World Tourism Barometer. World Tourism Organization. Volume 10. January Available at: (Accessed 2012 Feb 1). 2. US Department of Commerce Profile of U.S. Resident Traveler Visiting Overseas Destinations Reported From: Survey of International Air Travelers. Office of Travel and Tourism Industries, US Department of Commerce. Available at: (Accessed 2012 Aug 7). 3. Barnett ED, MacPherson DW, Stauffer WM, et al. The visiting friends or relatives traveler in the 21st century: time for a new definition. J Travel Med 2010; 17: Leder K, Tong S, Weld L, et al.; GeoSentinel Surveillance Network. Illness in travelers visiting friends and relatives: A review of the GeoSentinel Surveillance Network. Clin Infect Dis 2006; 43: Angell SY, Cetron MS. Health disparities among travelers visiting friends and relatives abroad. Ann Intern Med 2005; 142: McCarthy M. Should visits to relatives carry a health warning? Lancet 2001; 357: Angell SY, Behrens RH. Risk assessment and disease prevention in travelers visiting friends and relatives. Infect Dis Clin North Am 2005; 19: Chen LH, Wilson ME, Davis X, et al. Illness in long-term travelers visiting GeoSentinel clinics. Emerg Infect Dis 2009; 15: Boggild AK, Castelli F, Gautret P, et al. Vaccine preventable diseases in returned international travelers: Results from the GeoSentinel Surveillance Network. Vaccine 2010; 28: Bui YG, Trepanier S, Milord F, et al. Cases of malaria, hepatitis A, and typhoid fever among VFRs, Quebec (Canada). J Travel Med 2011; 18: Baggett HC, Graham S, Kozarsky PE, et al. Pretravel health preparation among US residents traveling to India to VFRs: importance of ethnicity in defining VFRs. J Travel Med 2009; 16: Greenwood Z, Black J, Weld L, et al. Gastrointestinal infection among international travelers globally. J Travel Med 2008; 15: Steffen R, Sack RB. Epidemiology. In: Ericsson CD, DuPont HL, Steffen R, eds. Travelers diarrhea. Hamilton, ON: BC Decker, 2003: Pavli A, Maltezou HC. Malaria and travelers visiting friends and relatives. Travel Med Infect Dis 2010; 8: Pavli A, Katerelos P, Pierroutsakos IN, Maltezou HC. Pretravel counseling in Greece for travelers visiting friends and relatives. Travel Med Infect Dis 2009; 7: Behrens RH, Stauffer WM, Barnett ED, et al. Travel case scenarios as a demonstration of risk assessment of VFR travelers: introduction to criteria and evidencebased definition and framework. J Travel Med 2010; 17: Becaner N, Stauffer B, Boulware DR, et al. Travel medicine considerations for North American immigrants visiting friends and relatives. JAMA 2004; 291: Cossar JH, Reid D, Fallon RJ, et al. A cumulative review of studies on travelers, their experiences of illness and the implications of these findings. J Infect 1990; 21: Han P, Yanni E, Jentes ES, et al. Health challenges of young travelers visiting friends and relatives compared with those traveling for other purposes. Pediatr Infect Dis J 2012; 31: Hagmann S, Benavides V, Neugebauer R, Purswani M. Travel health care for immigrant children visiting friends and relatives abroad: retrospective analysis of a hospitalbased travel health service in a US urban underserved area. J Travel Med 2009; 16: Hargarten SW, Baker TD, Guptill K. Overseas fatalities of United States citizen travelers: an analysis of deaths related to international travel. Ann Emerg Med 1991; 20: Driessen SO, Cobelens FG, Ligthelm RJ. Travel-related morbidity in travelers with insulin-dependent diabetes mellitus. J Travel Med 1999; 6: Rimoldi SF, Sartori C, Seiler C, et al. Highaltitude exposure in patients with cardiovascular disease: risk assessment and practical recommendations. Prog Cardiovasc Dis 2010; 52: Ringwald J, Strobel J, Eckstein R. Travel and oral anticoagulation. J Travel Med 2009; 16: Smith D, Toff W, Joy M, et al. Fitness to fly for passengers with cardiovascular disease. Heart 2010; 96: Tzani P, Pisi G, Aiello M, et al. Flying with respiratory disease. Respiration 2010; 80: DeHart R. Health issues of air travel. Annu Rev Public Health 2003; 24: Ringwald J, Schifferdecker C, Raemsch C, et al. Travelers thrombosis a state of practice in Germany. J Travel Med 2011; 18: Leggat PA, Wilks J. Overseas visitor deaths in Australia, 2001 to J Travel Med 2009; 16:

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