International Travel Patterns and Travel Risks of Patients Diagnosed With Cancer

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1 71 ORIGINAL ARTICLE International Travel Patterns and Travel Risks of Patients Diagnosed With Cancer Tarek Mikati, MD, Ying Taur, MD, MPH, Susan K. Seo, MD, and Monika K. Shah, MD Infectious Disease Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, Weill Cornell Medical College, New York, NY, USA DOI: /jtm See the Editorial by Camille Kotton, pp of this issue. Background. Immunocompromised travelers living with cancer can be at increased risk of travel-related illnesses. Their international travel patterns and associated risks remain largely unknown. Methods. This was a retrospective cohort study of all patients diagnosed with cancer who presented for pre-travel health advice between January 1, 2003 and June 30, Demographics, travel patterns, and infectious diseases exposure risks of immunocompromised travelers were characterized and compared with those of immunocompetent travelers. Reported travel-related illnesses were assessed in both groups. Results. A total of 149 travelers were included in this study. Fifty-one percent had solid tumors, 32% had hematological malignancies, and 17% underwent stem cell transplantation. Seventy travelers (47%) were immunocompromised. Immunocompromised travelers had similar demographics, trip itineraries, and infectious diseases exposure risks to hepatitis A, malaria, typhoid fever, and yellow fever as immunocompetent travelers. Most of the reported travel-related illnesses were of minor nature. Conclusion. Travelers with cancer who have impaired immunity had similar infectious diseases exposure risks and travel patterns as travelers whose cancer is cured or in remission. Improved understanding of travel patterns and risks of patients with cancer may assist in providing more focused pre-travel health interventions to this complex subset of travelers. International travel has grown by 50% over the past decade as it has become more affordable and available. 1 In 2009, over 30 million US residents traveled overseas. 2 International travelers, especially those visiting tropical and sub-tropical locations, are at increased risk for acquiring infections that may lead to adverse health events during or upon return from travel. 3,4 Among immunocompromised travelers, the risk of acquiring travel-related infections may The preliminary findings of this study have been presented as a poster at the Infectious Diseases Society of America annual meeting in Vancouver, October Corresponding Author: Monika K. Shah, MD, Infectious Disease Service, Department of Medicine, Memorial Sloan- Kettering Cancer Center, Weill Cornell Medical College, 1275 York Avenue, Box 420, New York, NY 10065, USA. shahm@mskcc.org be higher owing to deficits in their immune system and their potential to have attenuated responses to vaccines. 5 Given the higher prevalence of people living with human immunodeficiency virus (HIV) infection, the increasing use of biological therapies with chronically immunosuppressive effects in patients with chronic inflammatory disorders, and the increased global burden of cancer, there are now potentially more immunocompromised people interested in international travel. 6 8 In the United States, as the prognosis of multiple cancer types has improved over the past few decades, 9 more persons living with cancer are enjoying a better quality of life which includes increased mobility and the ability to travel. In the past decade, other studies have evaluated international travel, exposure risks, and travel-related illnesses among specific groups of immunocompromised travelers, such as those infected with HIV and solid organ transplant (SOT) recipients However, international travel patterns and exposure risks among 2013 International Society of Travel Medicine, Journal of Travel Medicine 2013; Volume 20 (Issue 2): 71 77

2 72 Mikati et al. immunocompromised travelers diagnosed with cancer remain to be described. The purpose of this study was to describe and compare the international travel patterns, infectious diseases exposure risks, pre-travel interventions, and travel-related illnesses among both immunocompromised and immunocompetent patients with a history of cancer. Methods Study Characteristics This was a retrospective cohort study of all patients who obtained pre-travel counseling at the travel clinic at Memorial Sloan-Kettering Cancer Center (MSKCC), a tertiary care cancer center, between January 1, 2003 and June 30, Travelers who were diagnosed with cancer or underwent stem cell transplantation (SCT) were included in the study. Travelers with carcinoma in situ or nonmelanoma skin cancer were excluded. Demographic information, comprehensive cancer history, current medications, pertinent laboratory tests and radiological reports, and immunization history were obtained from the medical record. Information regarding detailed trip itinerary, departure date, length of stay, and purpose of travel, vaccinations, and malaria prophylaxis was obtained from the pre-travel encounter visit. The first follow-up visit with the oncologist after return from travel was reviewed to determine the presence of any reports of travel-related illness. Charts were also reviewed to determine if death within 1 year of a pre-travel health visit occurred, and if so, cause of death was extracted. Data Analysis Using the Centers for Disease Control and Prevention (CDC) travel guidelines, 15 travelers were classified as immunocompromised if their immune status was impaired at the time of the pre-travel visit. This immunocompromised group included travelers who had received radiation therapy and/or immunosuppressive chemotherapy within the past 3 months prior to the pre-travel visit or who had undergone SCT within the past 2 years prior to the pre-travel visit. Travelers with active leukemia or lymphoma, generalized metastatic solid malignancies, active graftversus-host disease (GVHD), history of splenectomy, and/or travelers who had received treatment in which immunosuppressive effects lasted more than 3 months as evidenced by laboratory abnormalities including a low absolute neutrophil count or T-cell repertoire, were also classified as immunocompromised. Travelers were classified as immunocompetent if their cancer was considered to be in remission or cure and were not on any immunosuppressive medications. This group also included travelers who underwent SCT more than 2 years prior to travel and with no active GVHD. The purpose of travel included three categories: tourism, business, and visiting friends and relatives (VFR). VFR travelers were defined as immigrants who are ethnically or racially distinct from their country of residence and return to their homeland country to visit friends and relatives. 16 Time from travel was defined as the time difference in days between the pre-travel health visit and the travel departure date. Infectious risks for exposure to hepatitis A, malaria, typhoid fever, and yellow fever were assessed. A travel destination was defined as at-risk for hepatitis A if the estimated prevalence of hepatitis A was high or intermediate, 17 at-risk for typhoid fever if the incidence of typhoid fever exceeded 100 of 100,000 persons, 18 and at-risk for yellow fever and malaria if the CDC recommended yellow fever vaccination and malaria prophylaxis for travelers frequenting that destination. Travel-related illness was defined as an illness whose onset was during or upon return from travel. The proportion of travelers who died within 1 year of their pre-travel health visit was also calculated in each group. The characteristics and travel patterns of the immunocompromised group of travelers were compared to those of the immunocompetent travelers. Continuous variables were described as medians and interquartile ranges (IR). The chi-square test was used to compare categorical variables and the Mann Whitney Wilcoxon test to compare continuous variables. A p value of 0.05 or less was considered statistically significant and all statistical tests used were two sided. The MSKCC Institutional Review Board granted approval for this study. Analyses were conducted using sas software, version 9.3 (SAS Institute Inc., Cary, NC). Results During the study period, 512 travelers presented to the travel clinic. One hundred and forty-nine travelers with a history of cancer or SCT were identified. The majority of excluded travelers were hospital employees (Figure 1). Traveler Characteristics and Exposure Risks The median age of travelers was 52 years (range 8 87) and gender was predominantly female (69%). There was no statistical difference in demographics between immunocompromised and immunocompetent groups (Table 1). The median duration of travel abroad was 15 days (range 4 131). The major travel destinations were Asia (42%), sub-saharan Africa (28%), and South and Central America (including Mexico) (19%). A higher proportion of immunocompetent travelers visited destinations at risk for yellow fever than immunocompromised travelers (22% vs 11%, p = 0.07). Immunocompromised travelers were as likely to visit destinations that were at risk for each of the three other studied infections as immunocompetent travelers (Table 1). The majority traveled for tourism (68%), followed by VFR (20%) and business (11%). When compared to tourist and business travelers, VFR

3 International Travel Patterns and Risks of Cancer Patients 73 Table 1 Selected characteristics of travelers with history of cancer or SCT by immune status Immunocompetent (N = 79) Immunocompromised (N = 70) No (%) No (%) p Male gender 22 (28) 24 (34) 0.40 Age, years Median (IR) 50 (25) 55 (22) 0.12 Foreign-born 21 (28) 24 (35) 0.38 Disease category 0.46 Solid tumors 44 (56) 32 (46) Hematological diseases 22 (28) 25 (36) SCT 13 (17) 13 (19) Time from cancer diagnosis/sct Months, median (IR) 48 (86) 23 (57) Reason for travel 0.59 Tourism 53 (67) 48 (69) Visiting friends/relatives 14 (18) 15 (21) Business 12 (15) 7 (10) Time from travel 14 days 18 (23) 13 (19) 0.60 >14 and 28 days 28 (36) 22 (32) >28 days 31 (40) 33 (49) Duration of travel Days, median (IR) 15 (15) 15 (9) 0.87 Infectious diseases risk at destination Hepatitis A 54 (68) 48 (69) 0.91 Malaria 40 (51) 37 (49) 0.67 Typhoid 23 (29) 22 (32) 0.66 Yellow fever 18 (22) 8 (11) 0.07 One year mortality after pre-travel visit 1 (2) 9 (16) SCT = stem cell transplantation; IR = interquartile range; No = number. Missing data: birth location (N = 5); time from cancer diagnosis (N = 1); time from travel (N = 4); trip duration (N = 2). travelers were more likely to be foreign-born (65% vs 22%, p < 0.001), younger (median 43 vs 53 years, p = 0.003), and have longer travel duration (median 18.5 vs 14.0 days, p = 0.02). VFR travelers were as likely to visit destinations at risk for each of the four studied infections as non-vfr travelers. Thirty-one travelers presented within 2 weeks of their departure date for pre-travel health interventions. Immunocompromised travelers were as likely to present within 2 weeks of travel as immunocompetent travelers (Table 1). Among the travelers who presented within 2 weeks of travel, 10 (32%) were both immunocompromised and traveling to areas at risk for infection. Cancer and SCT Characteristics Immunocompromised travelers were more likely to have a recent cancer diagnosis or SCT than immunocompetent travelers (23 vs 48 months, p = 0.001). Both groups had similar proportions of solid tumors, hematological conditions, and SCT (Table 2). The Figure 1 Flow diagram of subject selection criteria. most common reasons for being immunocompromised among travelers with solid malignancies were active/metastatic disease (N = 28) and chemotherapy within 3 months of the pre-travel visit (N = 25). As for travelers diagnosed with hematological malignancies, 20 patients were immunocompromised due to the disease itself and 13 patients were immunocompromised due to administration of chemotherapy within 3 months of the pre-travel visit. Among SCT patients, the shortest time after SCT that a patient presented for a pre-travel consultation was 15 weeks after autologous SCT and 13 months after allogeneic SCT. Pre-Travel Health Interventions Pre-travel health interventions were administered to decrease the risk of the four studied travel-related infections (Table 3). Twenty-six patients, among whom eight were immunocompromised, traveled to areas at risk for acquiring yellow fever infection. Yellow fever vaccine (YF-VAX) was safely administered to 15 of the 18 immunocompetent patients. Three immunocompetent travelers did not receive the yellow fever vaccine: two opted not to be vaccinated due to their history of hematological malignancies and one because he received yellow fever vaccine within the last 10 years. The remaining eight travelers who did not receive the vaccine were immunocompromised and were provided letters of exemption.

4 74 Mikati et al. Table 2 Cancer and SCT categories of travelers Immunocompetent Immunocompromised (N = 79) (N = 70) Cancer category No (%) No (%) Solid 44 (56) 32 (45) Breast CNS 3 0 Gastrointestinal 5 4 Genitourinary 5 2 Gynecologic 4 3 Head and neck 4 0 Thoracic 0 3 Hematological 22 (28) 25 (36) Leukemias 4 9 Lymphomas Others 0 4 SCT 13 (16) 13 (19) Allogeneic 8 6 Autologous 5 7 SCT = stem cell transplantation; CNS = central nervous system; No = number. All SCT patients had hematological malignancies and conditions prior to SCT and were all in remission at the time of the pre-travel visit. Table 3 Pre-travel interventions administered to travelers Total interventions Interventions adm to immunocompromised travelers (%) Hepatitis A Hepatitis A vaccine (38) (Havrix) Immunoglobulins (71) (Gammagard) Both 2 2 (100) Malaria Atovaquone/proguanil (43) Chloroquine or mefloquine 13 7 (54) Typhoid fever Typhoid Vi capsular (40) polysaccharide vaccine (Typhim Vi) Yellow fever Yellow fever vaccine (YF-Vax) 15 0 Adm = administered. No oral live attenuated typhoid vaccine was administered. Travel-Related Illnesses Five patients cancelled their international trip, the majority because of hospitalization. Among the 68 immunocompromised patients who traveled, 64 (94%) had an outpatient visit with their oncologist within 6 months of their return from travel. Nine immunocompromised (12.9%) travelers reported a travel-related illness among which seven required medical attention. Two immunocompromised travelers were hospitalized during their travel, the first because of a ruptured ovarian cyst and the second because of a respiratory infection. Two travelers sought medical care upon return from travel. The first was hospitalized for weakness and cancer progression, and the second visited the emergency room directly upon return because of leg cramps and chills. Other travel-related illnesses among immunocompromised travelers were diarrheal illnesses, sinusitis, amebiasis, salivary gland obstruction, and right meniscal knee tear. Among the immunocompetent travelers, 61 (80%) saw their oncologists within 6 months of return. Six (7.6%) reported a travel-related illness among whom four required medical attention. All illnesses were infectious in etiology: diarrhea (N = 2), respiratory infections (N = 2), and fever (N = 2). Immunocompromised travelers had significantly higher mortality at 1 year after their pre-travel visit compared to immunocompetent travelers (16.1% vs 1.5%, p = 0.005). All deaths were related to cancer in patients diagnosed with solid tumors. No deaths were secondary to a travel-related illness. Discussion This retrospective cohort study provides unique information about patients with a history of cancer or SCT who seek pre-travel health care prior to international travel. Immunocompromised travelers had similar demographic factors and travel-related variables when compared to the immunocompetent group. Both groups were as likely to be exposed to each of the major travel-related infections examined in this study, with the exception of yellow fever, although this difference was not statistically significant. Compared to other immunocompromised groups of travelers previously studied, the median age of immunocompromised cancer travelers was similar to SOT but higher than HIV-infected travelers The majority of the international trips taken by this cohort were of short duration, similar to other immunocompromised groups of travelers Nearly half of the travelers in this study were immunocompromised at the time of their pre-travel health visit, of which 84% were traveling to destinations at risk for at least one of the four studied travelrelated infections. Infections remain a major cause of morbidity and mortality among cancer patients because of their impaired immunity. 19,20 Patients with cancer are immunocompromised from the malignancy itself and from cancer treatment. However, the travelers in the immunocompromised group were not homogenous. The degree of immunosuppression varies greatly among individuals diagnosed with cancer and even in the same individual at different times. Patients receiving treatment for solid tumors typically have a milder degree and shorter duration of immunosuppression as compared to those with hematological malignancies. The introduction of novel treatments may extend immunosuppression even beyond 3 months. For example, complete recovery of the immune system may take up to a year in patients treated with lymphocyte-depleting agents thus increasing the risk

5 International Travel Patterns and Risks of Cancer Patients 75 of opportunistic infections and precluding the use of live vaccines. 21 In this cohort, one traveler received cladribine 13 months prior to the pre-travel visit and remained immunocompromised at that time owing to prolonged suppression of the neutrophil and lymphocyte count. In general, the CDC considers travelers to be immunocompromised for 3 months after their last chemotherapeutic treatment. 15 Because the duration of immunosuppression following cancer treatment can vary widely, having specific knowledge of the therapeutic strategies and duration of their associated immunosuppressive effects used in patients with cancer is required. This highlights how in addition to the guidelines, it is crucial to obtain a detailed treatment history in these patients that extends beyond when the last cancer treatment was given, taking into account the current net state of immunosuppression when counseling and administering prophylactic vaccines and medications to this group of travelers. VFR was the second most common reason for travel in this study. It is well known in the literature that VFR represents a disproportionately higher volume of international travel and VFR travelers are an established higher risk group less likely to seek pre-travel health advice and stay longer at risk areas. 2,16 They are also at increased risk of acquiring travel-related infections such as malaria and typhoid fever due to lack of compliance with preventive measures. 22,23 Pre-travel health counseling and preventive interventions to immunocompromised VFR travelers are highly important given that they are at double epidemiological risk of travel-related infections because of their impaired immune status and behavioral and environmental risk related to contact with the local population and adaptation of local habits. In this study, one in two travelers presented to the travel clinic within 4 weeks prior to departure. Obtaining pre-travel health advice 28 days or more prior to travel is recommended by the CDC to provide enough time for preventive measures to be effective at the start of travel. 15 An interval of 10 to 14 days is required for protective immune responses to develop in the majority of immunocompetent travelers for the three travel-related vaccines administered in this study In addition, administration of certain malaria prophylaxis medications such as mefloquine and chloroquine should commence 1 to 2 weeks prior to travel for efficacy and tolerability. 15 Presenting in a timely manner for pre-travel health interventions is even more important for immunocompromised travelers. The immunocompromised host is less responsive to vaccinations and protective levels of vaccines may also be of shorter duration. Studies of SOT recipients and patients infected with HIV have shown lower serological response to hepatitis A, typhoid fever, and yellow fever vaccines Studies are lacking to evaluate the response to travel-related vaccines in immunocompromised cancer patients and SCT recipients and thus specific guidelines regarding travel-related vaccine administration to these groups of travelers are absent. Even if optimal timing is not achieved, a pre-travel health encounter, even at the last minute, is likely to avoid a travel-related illness by advantage of pre-travel health counseling. Given that vaccination strategies may be less protective among immunocompromised travelers, pre-travel health counseling against travel-related infections by an experienced provider in travel medicine is of higher importance. In addition, cancer patients should be counseled for other travel-related illnesses because they are at increased risk for venous thromboembolic disease during long travel times because of their prothrombotic condition and are at higher risk of sunburn due to radiation, chemotherapy, and lymphedema. 31 Finally, a letter of exemption provided by a yellow fever vaccination center helps to facilitate the entry of travelers to countries that require yellow fever vaccination, in whom the vaccine is contraindicated. Thirteen percent of immunocompromised cancer travelers reported a traveled-related illness. This number was lower than those reported by other groups of immunocompromised travelers, which was around 18% Unlike our study, in which all participants were evaluated in the travel clinic, other studies of immunocompromised travelers had different inclusion criteria, where the percentage of travelers who sought pre-travel health advice and prophylaxis ranged from 5% to 65% The preventive measures provided during the pre-travel health visit and lower risk behavior among individuals who seek pre-travel health advice could also explain the lower overall incidence of illness. Also, the method in which posttravel illnesses were ascertained in our study likely resulted in underreporting, and is described below in study limitations. The difference in the mortality at 1 year after the pre-travel visit between both groups of travelers is attributed to advanced stage disease in the immunocompromised solid tumor subgroup. This is the largest observational study that examines travel patterns and infectious diseases exposure risks of patients diagnosed with cancer. The location of the travel health clinic in a tertiary cancer center facilitated an accurate determination of the immune status of all the travelers because of the easy access to extensive clinical information about the travelers cancer history by the travel medicine specialist. In addition, there was high follow-up among the immunocompromised group with their oncologist upon return from travel and all travelers had their vital status assessed 1 year post-travel such that a travel-related cause of death would not be missed. Several limitations of this study need to be addressed. Not all cancer patients at our center seek pre-travel health care at our travel clinic and the group of travelers that sought pre-travel health care was affected by the referring practices of their health care providers. In addition, the information available at the pre-travel

6 76 Mikati et al. visit may not reflect the underlying immune status of all the travelers with absolute accuracy at their time of departure. The number of travel-related illnesses in this study is likely to be underestimated for several reasons. In this retrospective review, follow-up visits to the center were primarily for ongoing oncologic care. In these visits, the presence or absence of travel-related illnesses was not consistently elicited. In addition, about 20% of the immunocompetent travelers did not have a followup visit, likely because immunocompetent patients with a history of cancer do not require as frequent follow-up with their oncologists as compared with immunocompromised patients. Also, given the very low risk of serious travel-related illnesses reported in the literature, an increased risk of serious travel-related illnesses among immunocompromised travelers with cancer is unlikely to be demonstrated in this small cohort. 15 In summary, travel patterns and infectious diseases risks did not significantly differ between those deemed immunocompromised and immunocompetent travelers. Although immunocompromised travelers experienced a higher number of travel-related illnesses compared with immunocompetent patients, many of the travel-related morbidities were minor in nature. Further prospective studies among cancer and SCT patients would be helpful to determine the rate of international travel, travelrelated vaccine effectiveness, and travel-related illnesses. With the increase in international travel and advances in cancer treatment accompanied by improvement in the quality of life of cancer patients, studies are needed to provide focused pre-travel health interventions to this complex group of travelers. Declaration of Interests The authors state that they have no conflicts of interest to declare. References 1. World Tourism Organization. World tourism barometer. Available at: wtb.html. (Accessed 2011 Oct 7). 2. International Trade Administration, Office of Travel and Tourism Industries, US Department of Commerce. United States resident travelers visiting overseas destinations: 2010 outbound. Available at: (Accessed 2011 Aug 24). 3. Steffen R, Rickenbach M, Wilhelm U, et al. Health problems after travel to developing countries. J Infect Dis 1987; 156: Hill DR. The burden of illness in international travelers. N Engl J Med 2006; 354: Mileno MD, Bia FJ. The compromised traveler. 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