Travel Medicine and Infectious Disease (2014) 12, 757e763
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Chronic illnesses in travelers to developing countries*,** Shmuel Stienlauf a,b,e,*, Bianca Streltsin c,e, Eyal Meltzer a,b,e, Eran Kopel b, Eyal Leshem a,b,e, Gad Segal d,e, Shaye Kivity b,e, Eli Schwartz a,b,e a
The Center of Geographic Medicine, The Chaim Sheba Medical Center, Tel Hashomer 52621, Israel The Department of Internal Medicine “C”, Sheba Medical Center, Tel Hashomer 52621, Israel c The Arrow Project, Sheba Medical Center, Tel Hashomer 52621, Israel d Department of Internal Medicine “T”, Sheba Medical Center, Tel Hashomer 52621, Israel e Tel Aviv University, the Sackler School of Medicine, Tel-Aviv 69978, Israel b
Received 28 February 2014; received in revised form 5 October 2014; accepted 7 October 2014
Available online 16 October 2014
KEYWORDS Travel; Chronic disease; Chronic use of prescription drugs; Israel; Developing countries
Summary Background: Data regarding travelers with chronic illnesses (TCI) traveling to developing countries is limited. Methods: A retrospective cohort study of travelers. We analyzed demographics, travel destinations, travel dates and duration, as well as the medical history (chronic illnesses, chronic medications, and allergies) of the travelers. Results: Of 16,681 travelers evaluated, 3046 (18%) were TCI, of who, 2221 (13%) were taking chronic medications. The percentage of TCI ranged from 4% in the first decade of life to 65% in the 8th decade. The highest number of TCI (1085) was among the 20e30 years age group. The median age (IQR) of TCI was 39.0 (23.1e58.2), compared to 24.2 (22.0e32.1) years, of healthy travelers (p < 0.001). The major pre-existing medical conditions among TCI were endocrine/metabolic (38%), cardiovascular (26%) and pulmonary illnesses (16%).
*
This work was performed in partial fulfillment of the M.D. thesis requirements of the Sackler Faculty of Medicine, Tel Aviv University of the 2nd author. ** Meetings at which the paper has been presented: 1. Annual Meeting of the Israel Society for Parasitology, Protozoology and Tropical Diseases, Ramat Gan, Israel, December 14e15, 2010 (Oral Presentation, session 4). 2. The 9th Asia Pacific Travel Health Conference, Singapore, May 2e5, 2012 (Oral Presentation, abstract FC01-2). 3. 11th Congress of the European Federation of Internal Medicine and the XXXIII National Congress of the Spanish Society of Internal Medicine, Madrid, Spain, 24the27th October 2012 (Poster and short oral presentation abstract V-090). * Corresponding author. The Department of Internal Medicine “C”, Sheba Medical Center, Tel Hashomer 52621, Israel. Tel.: þ972 52 6666131; fax: þ972 3 5535953. E-mail addresses: [email protected] (S. Stienlauf), [email protected] (B. Streltsin), [email protected] (E. Meltzer), eran. [email protected] (E. Kopel), [email protected] (E. Leshem), [email protected] (G. Segal), [email protected] (S. Kivity), [email protected] (E. Schwartz). http://dx.doi.org/10.1016/j.tmaid.2014.10.004 1477-8939/ª 2014 Elsevier Ltd. All rights reserved.
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S. Stienlauf et al. Within age groups, no difference was found in itinerary and other travel characteristics. However, 20e30 years old TCI, who were using chronic medications had significantly shorter travel duration (P < 0.001). Conclusions: TCI form a significant proportion of travelers among all age groups and travel destinations. Chronic illnesses appear to have little impact on travel itinerary and characteristics, but chronic medication use is associated with shorter travel duration to developing countries. ª 2014 Elsevier Ltd. All rights reserved.
1. Introduction Over the past six decades, tourism has shown continued expansion and diversification. In spite of occasional slumps, international tourist arrivals have shown virtually uninterrupted growth, from 25 million in 1950 to 940 million in 2010 [1]. The average annual growth in tourist arrivals between the years 2001e2010, was 3.4%. The number of tourists traveling to developing countries had grown from 70 million in 1990 to 260 million in 2010, concomitant with a growth in the proportion of tourism to developing countries from 16% to 27% [1]. The diversity of travelers to the developing countries is increasing. We found, in a large cohort of Israeli travelers, that backpackers e young adults in their 20’s-30’s traveling for recreation, composed only 43% of travelers and travelers older than 60 years of age composed 5% of our cohort of travelers [2], many of them are at risk for developing drug interaction with medications prescribed for travel related illnesses [3]. As the population of travelers diversifies, the number of travelers with chronic illness (TCI) is expected to rise. However, the characteristics of TCI to developing countries are not well studied.
2. Methods A retrospective cohort study of all travelers that attended the pre-travel clinic at the Chaim Sheba medical center between 1/1/2005 and 31/12/2007. Travelers to developed countries, and travelers who consulted our clinic more than once during the study period, were excluded from analysis. The Chaim Sheba Medical Center human subjects’ research review board approved this study.
2.1. Data analysis The data collected included date of visit, demographics (date of birth, gender and country of birth), travel destinations, purpose of travel, expected date of travel and the planned duration of travel (in days). The traveler was also asked to record the existence and type of chronic illnesses, chronic use of medications and drug allergies. Age (expressed in years) and the interval between the clinic visit and the travel date (expressed in days) were calculated. Travelers in whom date of travel and destination were not recorded were excluded. Geographic destinations were grouped according to the classification of the United Nation Statistics Division [4].
Travelers were asked to select one of the following purposes for their trip: leisure/tourism, business, governmental or non-governmental organization worker, research/education, returning to region of origin of self or family to visit friends and relatives (VFR). 2.1.1. Chronic illness Chronic illnesses were grouped according to the following groups: cardiovascular, endocrine and metabolic, ottolaryngeal, Gastrointestinal, genitourinary, hematologic, immunological, musculoskeletal, neurological, rheumatologic, cancer, ophthalmological, psychiatric, pulmonary and dermatological disorders. We defined as immunosuppressed travelers who suffered from malignant diseases, who were receiving antineoplastic therapy, currently or within 2 years prior to travel, travelers after bone marrow or solid organ transplantation, travelers infected with HIV, travelers who underwent splenectomy, and travelers suffering from common variable immunodeficiency disease (CVID).
2.2. Statistical analysis The c2-test was used for analysis of nonparametric data. Proportions and 95% confidence intervals were calculated for variables with binomial distribution. Confidence interval for proportions in binomial distributions was calculated as previously described [5]. Continuous data were described as median with interquartile range (IQR). The ManneWhitney test was used for the analysis of the difference between medians of the travel planned duration among TCI and healthy travelers. The linear regression model was used in order to analyze correlation between parameters All p values calculations were 2-tailed and were considered statistically significant if their value was 0.05. Data were maintained using Microsoft Access (Microsoft, Redmond, WA, USA). Statistical analysis was conducted by IBM SPSS Statistics version 19(Chicago, Illinois, USA).
3. Results Between 1/1/2005 and 31/12/2007, 19,410 travelers consulted our pre-travel clinic, 16,681 of which were included in the study (Fig. 1). The age distribution was three months to 87 years old. As shown in Fig. 1, travelers with chronic illness (TCI) constituted 18% of all cases, and travelers who reported using chronic medication constituted 13% of all cases. The proportion of TCI was stable during all the years of the study.
Chronic illnesses in travelers
Fig. 1 Screening, exclusion and characteristics of Israeli travelers to developing countries.
Fig. 2 shows the age distribution of TCI and healthy travelers. The percentage of TCI increased with age, from 4% in the first decade of life to 65% in the 8th decade. The percentage of TCI taking chronic medications also increase with age from 2% (out of all travelers) in the first decade of life to 61% in the 8th decade. TCI and TCI taking chronic medications composed 12% (1085) and 6% (512), respectively, of the 20e30 years old age group, making it the numerically largest group among TCI.
759 Table 1 summarizes the demographic and travel characteristics of our travelers. TCI were significantly older than healthy travelers. Travel for business accounted for a significantly larger proportion of TCI compared with healthy travelers. A significantly larger proportion of TCI (compared to healthy travelers) traveled to sub-Saharan Africa. In order to control for the effect of age on those parameters (Table 2) we compared the travel characteristics between TCI and healthy travelers according to age group by decade. Within the age groups (i.e. 20e30, 30e40, 40e50, 50e60 and above 60 years of age) no difference was found in the distributions of travel destinations, distributions of gender and the planned duration of travel between TCI and healthy travelers (Table 2). Reasons for travel were similar in TCI and healthy travelers up to age of 50 years. However, TCI travelers that were older than 50 years of age were less likely to travel on business or on mission than their healthy counterparts, 11% versus 19% respectively (Table 2, P < 0.04). A sub analysis of TCI who were taking chronic medications revealed that female travelers composed 56% of the travelers who used chronic medications versus 51% of the healthy travelers (p < 0.02). The planned duration of travel was nearly identical for most age groups of TCI on medications and healthy travelers, with the sole exception of young travelers (20e30 years of age, the largest travelers group). In contrast to other age groups, the planned duration of travel was shorter by a month in the chronic medications users [median 60(30e150) days vs. 90(30e180) days (p < 0.001). This difference remained significant even when only leisure travelers were considered.
3.1. Illnesses Among 3046 TCI there were 322 different diagnoses, with a mean of 1.4 0.8 diagnoses per TCI (median number of diagnoses per person-1, minimum-1, maximum-8). Table 3 summarizes the distribution of illnesses among our travelers. Asthma and seasonal allergies were the most common diseases among travelers younger than 40 years old (3.3% and 1.5% of all travelers in that age group respectively). Hypercholesterolemia (14.2%) and hypertension (14%) were the commonest illness in travelers older than 40 (Table 4). Immunosuppressed travelers comprised 0.74% of travelers (124 travelers: active malignancy in 94, organ and bone marrow transplantations in 12, post-splenectomy in 15and HIV in 2 travelers). Pregnancy was reported by only 25 travelers (0.31% of all female travelers). Glucose-6-phosphate dehydrogenase deficiency was reported by 204 (1.2% of all travelers).
3.2. Chronic use of medications
Fig. 2 Age distribution of healthy travelers and travelers with chronic illnesses.
Oral Contraceptives were the commonest chronic drug reported by our travelers (929 travelers of 6118 female travelers between the ages 16e44, 15.1%). The 2221 travelers, who were on chronic medications other than oral contraceptive, took 353 different medications, an average of 1.9 1.3 medication per traveler (median-1, range
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S. Stienlauf et al.
Table 1
Demographics and travel characteristics. Travelers with chronic illness
Gender Age (years) Interval between consult and departure (days) Travel purpose% (n)
Continents% (n)
a b c d
P P P P
value value value value
% Male (n) (95% CI) Median (IQR) Median (IQR)
50.5 (1538) (48.7e52.3) 39.0 (23.1e58.2)b 28 (16e38)
52.8 (7202)a (52e53.7) 24.2 (22.0e32.1)b 28 (15e39)
Tourism/leisure Business Mission Asia Latin America Sub-Saharan Africa Oceania
90.9 (2718)c 6.7 (199)c 2.4 (72)c 59.7 (1817)d 27.8 (848)d 12.9 (392)d 2.7 (82)d
91.3 (11,887)c 5.6 (730)c 3.1 (400)c 61.0 (8321)d 29.6 (4042)d 10.3 (1399)d 4.2 (571)d
Z 0.021 gender distribution between TCI and healthy travelers. < 0.001 median age distributions between TCI and healthy travelers. Z 0.016 travel purpose distributions between TCI and healthy travelers. < 0.001 travel destinations distributions between TCI and healthy travelers.
(1e9)). Table 5 summarizes the distribution of common medication groups in our travelers. In the group of travelers taking respiratory medications, the chronic use of medications for asthma control was reported by 175 travelers (6% of TCI, 1.05% of all travelers). Acid suppressive therapy was taken by 146 travelers (5% of TCI, 0.9% of all travelers). Among travelers who were using medications to control diabetes, insulin was used by 26% (39 out of 151). Diuretic use was reported by 80 travelers (3% of TCI, 0.5% of all travelers). Immunosuppressive medications were used by 39 travelers (1% of TCI, 0.2% of all travelers).
4. Discussion Travelers to developing countries are commonly perceived to be healthy young backpackers. We have shown that in Table 2
Healthy travelers
a
fact, TCI constituted 18.3% of all travelers to developing countries during the study period. Even among the 20e30 years old typical of backpackers age group, TCI constituted 12.5% of travelers. These young adult travelers reported mainly asthma and seasonal allergies whereas in travelers older than 40 years, endocrine and metabolic diseases, (mainly hypercholesterolemia and hypothyroidism-7.4% of all travelers), and cardiovascular diseases (mainly hypertension-5.1% of all travelers), were the most frequent chronic conditions. The existing medical literature regarding TCI is very limited. In addition to the magnitude of this issue, our study also underscores the scope of medical conditions affecting travelers and the many problems medical practitioners need to address during the pre-travel consultation.
Demographics and travel characteristics of travelers in different age groups.
% Travel destination (n)a Age group Traveler % Of age Travel duration (days) Asia (years) group groupa Sub-Saharan Latin (n) median(IQR) Africa America
% Travel purpose (n)a
20e30
98(1057) 97(7592) 97(8652) 80(176) 78(1221) 78(1394) 72(174) 77(757) 76(934) 86(510)b 77(661)b 81(1171) 92(534)c 88(369)c 90(900)
30e40
40e50
50e60
>60
a b c
TCI Healthy All TCI Healthy All TCI Healthy All TCI Healthy All TCI Healthy All
12(1085) 88(7898) 62(8986) 12(222) 88(1590) 12(1811) 20(245) 80(1008) 9(1254) 41(611) 59(874) 10(1485) 58(590) 42(435) 7(1019)
90(30e180) 90(30e180) 90(30e180) 22(14e35) 22(14e40) 22(14e40) 15(10e21) 15(11e21) 15(10e21) 17(14e23) 17(14e21) 17(14e22) 18(15e22) 19(15e24) 19(15e23)
59(635) 60(4759) 60(5394) 69(152) 71(1130) 71(1283) 62(153) 65(651) 64(803) 62(393) 62(547) 64(944) 54(319) 51(222) 53(537)
3(31) 3(260) 37(3282) 17(37) 17(275) 12(212) 30(70) 27(268) 9(111) 21(109) 21(186) 16(243) 19(111) 18(77) 29(290)
39(418) 36(2863) 3(293) 14(30) 12(183) 17(311) 9(22) 9(88) 27(339) 16(99) 16(144) 20(294) 27(157) 31(134) 18(187)
Tourism/ Business Mission leisure
% of age group for TCI/healthy travelers, for all travelers % of all travelers. P value < 0.001, distribution of purpose of travel between TCI vs. healthy travelers age >50. P value < 0.04, distribution of purpose of travel between TCI vs. healthy travelers age >60.
1(7) 1(87) 1(094) 5(10) 7(108) 7(119) 6(14) 6(62) 6(75) 3(18)b 7(61)b 5(79) 3(15)c 5(23)c 4(038)
1(13) 2(142) 2(155) 15(33) 15(229) 15(263) 22(53) 17(167) 18(219) 11(64)b 16(134)b 14(200) 5(31)c 7(28)c 6(057)
% Males (n)
46(501) 49(3892) 49(4393) 58(129) 62(983) 61(1112) 56(136) 52(528) 53(664) 51(310) 56(486) 54(796) 53(309) 54(237) 54(546)
Chronic illnesses in travelers
761
Table 3 Frequent chronic illness among travelers to the developing countries. % Of travelers (n) Chronic illness groups Endocrine & metabolic Cardiovascular Pulmonary Allergic & immunologic Gastrointestinal Hematology Psychiatric Neurology Musculoskeletal Rheumatology Oncology Frequent illnesses Hypercholesterolemia Hypertension Asthma Hypothyroidism Seasonal allergies Diabetes mellitus Osteoporosis Depression Anemia Gastro-esophageal reflux Migraine headaches Ischemic heart disease
7.4% 5.1% 3.0% 1.9% 1.9% 1.2% 1.0% 1.0% 0.8% 0.6% 0.6%
(1236) (850) (507) (321) (316) (194) (162) (161) (127) (102) (94)
3.5% 3.4% 3.0% 1.6% 1.4% 1.2% 0.7% 0.7% 0.7% 0.6% 0.5% 0.5%
(587) (571) (496) (262) (240) (196) (124) (120) (115) (93) (87) (86)
The travelers in our study formed a heterogeneous group regarding age, travel destination, purpose and duration. We performed subgroup analyses to compare the demographics and travel characteristics of TCI and healthy travelers. We found that although TCI differed as a group in travel characteristics from healthy travelers, sub-analysis by age groups eliminated all such differences. It would appear that age, rather than the mere presence of underlying medical conditions, is a major factor in the reason for travel, choice of destination and travel duration. Surprisingly, we found that use of chronic medications did have a significant impact on travel duration. The Table 4 The most common chronic illnesses in different age groups. Age group (years)
Commonest diseases
% Of travelers in age group (n)
0e20
Asthma Seasonal allergies ADHD Asthma Seasonal allergies Hypothyroidism Hypercholesterolemia Hypertension Hypothyroidism Hypertension Hypercholesterolemia Diabetes mellitus
1.6% 1.4% 0.9% 3.5% 1.5% 0.8% 10.8% 9.5% 3.8% 26.3% 23.6% 7.4%
20e40
40e60
60e80
(13) (11) (7) (415) (176) (98) (302) (265) (107) (273) (245) (77)
Table 5 Frequent chronic medications used by travelers to developing countries. Medications
% Of travelers (n)
Cardiovascular agents Anti-hyperlipidemic agents Hormones Coagulation modifiers Respiratory agents Anti-diabetic agents Psychotherapeutic agents Nutritional products Gastrointestinal agents Metabolic agents
3.5% 3.4% 2.3% 2.1% 1.7% 0.9% 1.1% 1.0% 1.1% 0.9%
(586) (565) (389) (348) (287) (151) (185) (166) (186) (144)
median travel duration of young travelers in the typical “backpacker” 20e30 years age group who were using chronic medications, was 1 month shorter than in their healthy counterparts. In contrast, such a difference was not found in the older age groups, in whom no difference in travel duration existed between healthy travelers and even among TCI on medication. This probably reflects the fact the in the older age groups the duration of travel is anyhow short, probably due to work related or familial obligations, regardless of health problems. It is not self-evident why travel is curtailed in young travelers who take medications. In the majority of these cases, the medical condition for which medications were used (i.e. mild, well controlled asthma or hypothyroidism) was not an objective barrier to extended travel. It is possible that chronic medication use may be associated with perceived ill health, the subjective assessment of being at risk, or due to technical issue of lack of medications supply during a long trip, all may lead to a shorter travel duration These questions need to be addressed in prospective studies. TCI did not appear to be more scrupulous in preparing for travel, as we did not find any difference in the time interval between pre-travel consultation and planned travel date. We found only three previous studies that addressed the subject of chronic illness and its effects on travel. In a study conducted in a single US travel clinic between 1984 and 1989, 27% of 2445 Americans travelers to developing countries, were TCI [6]. In another, multi-center study of American travelers, between 2009e2011, 59% of 13,235 travelers were TCI [7]. The third study, performed in France during 2009 [8], found that TCI composed 11% of 3442 travelers. Thus, the rate of TCI among travelers attending pre-travel clinics appears to differ from country to country. However, the distribution of chronic illnesses, except for the higher rate of seasonal allergies in the American travelers, was similar in all the studies. In contrast to our study neither of those studies had dealt with the epidemiology and travel characteristics of TCI. Preparations for travel to developing countries may include the administration of live attenuated (Yellow fever vaccine, MMR vaccine) vaccines, and the prescription of medications for malaria prophylaxis, travelers’ diarrhea and high altitude illness. About 1.5% of the study population
762 were immunosuppressed and pregnant travelers with possible contraindications against live attenuated vaccines. The choice of malaria prophylaxis can pose problems in several groups of travelers. Mefloquine and atovaquone/ proguanil, are both labeled by the FDA as pregnancy category C drugs [9,10], while doxycycline is category D e which makes malaria prophylaxis contraindicated in pregnant travelers. For travelers with neuro-psychiatric disorders mefloquine is contraindicated. In our series, 0.15% of travelers were pregnant, whereas 1.5% self-reported neuropsychiatric disorders. Travel to developing countries can impact TCI in two ways e travel can adversely affect the control of chronic illnesses or raise the traveler’s risk of acquiring travel related conditions (such as: travelers’ diarrhea, enteric fever, malaria, high altitude sickness etc.). Few studies address the impact of the travel on the chronic medical condition among travelers to developing countries. Studies on asthma and insulin dependent diabetes mellitus (IDDM) have shown a worsening of both pretravel conditions [11e13]. On the other hand, a caseecontrol study in travelers with inflammatory bowel diseases (IBD) did not find an increased risk of gastrointestinal morbidity in these patients [14]. The impact of chronic illness on travel related diseases was even more neglected. A recent Dutch study found that HIV patients with CD4 count bellow 500, and Insulin treated diabetic patients had a higher risk of acquiring travel related infections. Surprisingly, in this study recent cancer chemotherapy and usage of anti-tumor necrosis factor (TNF) agents was not associated with an increased risk of infections [15]. Patients who chronically use gastric acid lowering therapy (proton pump inhibitors, H2 antagonists etc.) are at increased risk for developing gastrointestinal infections [16,17]. Although there is no such study showing a similar higher risk in travelers (1% of our travelers), the International Society of Travel Medicine (ISTM) recommends a daily use of prophylaxis against travelers’ diarrhea in travelers who use stomach acid lowering [18,19] therapy traveling to Sub-Saharan Africa, South East Asia and Latin America [20]. Travel to, low to middle income countries [18,19], can lead to difficulties in controlling chronic illness in TCI, many of whom receive chronic medications. Travelers may encounter logistical problems, especially during longer trips, acquiring and maintaining medications (e.g. supplies, refrigeration, stability of medication in extreme temperature etc.). Whether chronic illness actually affects travel planning has hardly been addressed in the literature. A single study has shown that among diabetic travelers, 15% of travelers changed travel destination and duration because of insulin usage [11]. Our study suggests that the existence of chronic illness does not have a significant impact on travel planning. However, chronic use of medications seems to have an impact on travel duration in the younger group age.
5. Conclusions TCI accounted for nearly one fifth of Israeli travelers to developing countries who presented at our clinic. TCI were a significant population even among younger travelers.
S. Stienlauf et al. The implications of chronic illness and chronic medication use on travel to developing countries are not well studied. Our study, which to best of our knowledge, is the first large scale study to address the issue, suggests that chronic medication use, rather than the existence of chronic illnesses, does impact travel itinerary and characteristics. Further studies are needed to elucidate the possible roles of subjective health perception and objective disabilities in curtailing travel for TCI. Also, the outcome of this population while traveling to developing countries requires further study.
Conflict of interest None.
Acknowledgments No funding source was available for this study.
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Chronic illnesses in travelers to developing countries*,** Shmuel Stienlauf a,b,e,*, Bianca Streltsin c,e, Eyal Meltzer a,b,e, Eran Kopel b, Eyal Leshem a,b,e, Gad Segal d,e, Shaye Kivity b,e, Eli Schwartz a,b,e a
The Center of Geographic Medicine, The Chaim Sheba Medical Center, Tel Hashomer 52621, Israel The Department of Internal Medicine “C”, Sheba Medical Center, Tel Hashomer 52621, Israel c The Arrow Project, Sheba Medical Center, Tel Hashomer 52621, Israel d Department of Internal Medicine “T”, Sheba Medical Center, Tel Hashomer 52621, Israel e Tel Aviv University, the Sackler School of Medicine, Tel-Aviv 69978, Israel b
Received 28 February 2014; received in revised form 5 October 2014; accepted 7 October 2014
Available online 16 October 2014
KEYWORDS Travel; Chronic disease; Chronic use of prescription drugs; Israel; Developing countries
Summary Background: Data regarding travelers with chronic illnesses (TCI) traveling to developing countries is limited. Methods: A retrospective cohort study of travelers. We analyzed demographics, travel destinations, travel dates and duration, as well as the medical history (chronic illnesses, chronic medications, and allergies) of the travelers. Results: Of 16,681 travelers evaluated, 3046 (18%) were TCI, of who, 2221 (13%) were taking chronic medications. The percentage of TCI ranged from 4% in the first decade of life to 65% in the 8th decade. The highest number of TCI (1085) was among the 20e30 years age group. The median age (IQR) of TCI was 39.0 (23.1e58.2), compared to 24.2 (22.0e32.1) years, of healthy travelers (p < 0.001). The major pre-existing medical conditions among TCI were endocrine/metabolic (38%), cardiovascular (26%) and pulmonary illnesses (16%).
*
This work was performed in partial fulfillment of the M.D. thesis requirements of the Sackler Faculty of Medicine, Tel Aviv University of the 2nd author. ** Meetings at which the paper has been presented: 1. Annual Meeting of the Israel Society for Parasitology, Protozoology and Tropical Diseases, Ramat Gan, Israel, December 14e15, 2010 (Oral Presentation, session 4). 2. The 9th Asia Pacific Travel Health Conference, Singapore, May 2e5, 2012 (Oral Presentation, abstract FC01-2). 3. 11th Congress of the European Federation of Internal Medicine and the XXXIII National Congress of the Spanish Society of Internal Medicine, Madrid, Spain, 24the27th October 2012 (Poster and short oral presentation abstract V-090). * Corresponding author. The Department of Internal Medicine “C”, Sheba Medical Center, Tel Hashomer 52621, Israel. Tel.: þ972 52 6666131; fax: þ972 3 5535953. E-mail addresses: [email protected] (S. Stienlauf), [email protected] (B. Streltsin), [email protected] (E. Meltzer), eran. [email protected] (E. Kopel), [email protected] (E. Leshem), [email protected] (G. Segal), [email protected] (S. Kivity), [email protected] (E. Schwartz). http://dx.doi.org/10.1016/j.tmaid.2014.10.004 1477-8939/ª 2014 Elsevier Ltd. All rights reserved.
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S. Stienlauf et al. Within age groups, no difference was found in itinerary and other travel characteristics. However, 20e30 years old TCI, who were using chronic medications had significantly shorter travel duration (P < 0.001). Conclusions: TCI form a significant proportion of travelers among all age groups and travel destinations. Chronic illnesses appear to have little impact on travel itinerary and characteristics, but chronic medication use is associated with shorter travel duration to developing countries. ª 2014 Elsevier Ltd. All rights reserved.
1. Introduction Over the past six decades, tourism has shown continued expansion and diversification. In spite of occasional slumps, international tourist arrivals have shown virtually uninterrupted growth, from 25 million in 1950 to 940 million in 2010 [1]. The average annual growth in tourist arrivals between the years 2001e2010, was 3.4%. The number of tourists traveling to developing countries had grown from 70 million in 1990 to 260 million in 2010, concomitant with a growth in the proportion of tourism to developing countries from 16% to 27% [1]. The diversity of travelers to the developing countries is increasing. We found, in a large cohort of Israeli travelers, that backpackers e young adults in their 20’s-30’s traveling for recreation, composed only 43% of travelers and travelers older than 60 years of age composed 5% of our cohort of travelers [2], many of them are at risk for developing drug interaction with medications prescribed for travel related illnesses [3]. As the population of travelers diversifies, the number of travelers with chronic illness (TCI) is expected to rise. However, the characteristics of TCI to developing countries are not well studied.
2. Methods A retrospective cohort study of all travelers that attended the pre-travel clinic at the Chaim Sheba medical center between 1/1/2005 and 31/12/2007. Travelers to developed countries, and travelers who consulted our clinic more than once during the study period, were excluded from analysis. The Chaim Sheba Medical Center human subjects’ research review board approved this study.
2.1. Data analysis The data collected included date of visit, demographics (date of birth, gender and country of birth), travel destinations, purpose of travel, expected date of travel and the planned duration of travel (in days). The traveler was also asked to record the existence and type of chronic illnesses, chronic use of medications and drug allergies. Age (expressed in years) and the interval between the clinic visit and the travel date (expressed in days) were calculated. Travelers in whom date of travel and destination were not recorded were excluded. Geographic destinations were grouped according to the classification of the United Nation Statistics Division [4].
Travelers were asked to select one of the following purposes for their trip: leisure/tourism, business, governmental or non-governmental organization worker, research/education, returning to region of origin of self or family to visit friends and relatives (VFR). 2.1.1. Chronic illness Chronic illnesses were grouped according to the following groups: cardiovascular, endocrine and metabolic, ottolaryngeal, Gastrointestinal, genitourinary, hematologic, immunological, musculoskeletal, neurological, rheumatologic, cancer, ophthalmological, psychiatric, pulmonary and dermatological disorders. We defined as immunosuppressed travelers who suffered from malignant diseases, who were receiving antineoplastic therapy, currently or within 2 years prior to travel, travelers after bone marrow or solid organ transplantation, travelers infected with HIV, travelers who underwent splenectomy, and travelers suffering from common variable immunodeficiency disease (CVID).
2.2. Statistical analysis The c2-test was used for analysis of nonparametric data. Proportions and 95% confidence intervals were calculated for variables with binomial distribution. Confidence interval for proportions in binomial distributions was calculated as previously described [5]. Continuous data were described as median with interquartile range (IQR). The ManneWhitney test was used for the analysis of the difference between medians of the travel planned duration among TCI and healthy travelers. The linear regression model was used in order to analyze correlation between parameters All p values calculations were 2-tailed and were considered statistically significant if their value was 0.05. Data were maintained using Microsoft Access (Microsoft, Redmond, WA, USA). Statistical analysis was conducted by IBM SPSS Statistics version 19(Chicago, Illinois, USA).
3. Results Between 1/1/2005 and 31/12/2007, 19,410 travelers consulted our pre-travel clinic, 16,681 of which were included in the study (Fig. 1). The age distribution was three months to 87 years old. As shown in Fig. 1, travelers with chronic illness (TCI) constituted 18% of all cases, and travelers who reported using chronic medication constituted 13% of all cases. The proportion of TCI was stable during all the years of the study.
Chronic illnesses in travelers
Fig. 1 Screening, exclusion and characteristics of Israeli travelers to developing countries.
Fig. 2 shows the age distribution of TCI and healthy travelers. The percentage of TCI increased with age, from 4% in the first decade of life to 65% in the 8th decade. The percentage of TCI taking chronic medications also increase with age from 2% (out of all travelers) in the first decade of life to 61% in the 8th decade. TCI and TCI taking chronic medications composed 12% (1085) and 6% (512), respectively, of the 20e30 years old age group, making it the numerically largest group among TCI.
759 Table 1 summarizes the demographic and travel characteristics of our travelers. TCI were significantly older than healthy travelers. Travel for business accounted for a significantly larger proportion of TCI compared with healthy travelers. A significantly larger proportion of TCI (compared to healthy travelers) traveled to sub-Saharan Africa. In order to control for the effect of age on those parameters (Table 2) we compared the travel characteristics between TCI and healthy travelers according to age group by decade. Within the age groups (i.e. 20e30, 30e40, 40e50, 50e60 and above 60 years of age) no difference was found in the distributions of travel destinations, distributions of gender and the planned duration of travel between TCI and healthy travelers (Table 2). Reasons for travel were similar in TCI and healthy travelers up to age of 50 years. However, TCI travelers that were older than 50 years of age were less likely to travel on business or on mission than their healthy counterparts, 11% versus 19% respectively (Table 2, P < 0.04). A sub analysis of TCI who were taking chronic medications revealed that female travelers composed 56% of the travelers who used chronic medications versus 51% of the healthy travelers (p < 0.02). The planned duration of travel was nearly identical for most age groups of TCI on medications and healthy travelers, with the sole exception of young travelers (20e30 years of age, the largest travelers group). In contrast to other age groups, the planned duration of travel was shorter by a month in the chronic medications users [median 60(30e150) days vs. 90(30e180) days (p < 0.001). This difference remained significant even when only leisure travelers were considered.
3.1. Illnesses Among 3046 TCI there were 322 different diagnoses, with a mean of 1.4 0.8 diagnoses per TCI (median number of diagnoses per person-1, minimum-1, maximum-8). Table 3 summarizes the distribution of illnesses among our travelers. Asthma and seasonal allergies were the most common diseases among travelers younger than 40 years old (3.3% and 1.5% of all travelers in that age group respectively). Hypercholesterolemia (14.2%) and hypertension (14%) were the commonest illness in travelers older than 40 (Table 4). Immunosuppressed travelers comprised 0.74% of travelers (124 travelers: active malignancy in 94, organ and bone marrow transplantations in 12, post-splenectomy in 15and HIV in 2 travelers). Pregnancy was reported by only 25 travelers (0.31% of all female travelers). Glucose-6-phosphate dehydrogenase deficiency was reported by 204 (1.2% of all travelers).
3.2. Chronic use of medications
Fig. 2 Age distribution of healthy travelers and travelers with chronic illnesses.
Oral Contraceptives were the commonest chronic drug reported by our travelers (929 travelers of 6118 female travelers between the ages 16e44, 15.1%). The 2221 travelers, who were on chronic medications other than oral contraceptive, took 353 different medications, an average of 1.9 1.3 medication per traveler (median-1, range
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Table 1
Demographics and travel characteristics. Travelers with chronic illness
Gender Age (years) Interval between consult and departure (days) Travel purpose% (n)
Continents% (n)
a b c d
P P P P
value value value value
% Male (n) (95% CI) Median (IQR) Median (IQR)
50.5 (1538) (48.7e52.3) 39.0 (23.1e58.2)b 28 (16e38)
52.8 (7202)a (52e53.7) 24.2 (22.0e32.1)b 28 (15e39)
Tourism/leisure Business Mission Asia Latin America Sub-Saharan Africa Oceania
90.9 (2718)c 6.7 (199)c 2.4 (72)c 59.7 (1817)d 27.8 (848)d 12.9 (392)d 2.7 (82)d
91.3 (11,887)c 5.6 (730)c 3.1 (400)c 61.0 (8321)d 29.6 (4042)d 10.3 (1399)d 4.2 (571)d
Z 0.021 gender distribution between TCI and healthy travelers. < 0.001 median age distributions between TCI and healthy travelers. Z 0.016 travel purpose distributions between TCI and healthy travelers. < 0.001 travel destinations distributions between TCI and healthy travelers.
(1e9)). Table 5 summarizes the distribution of common medication groups in our travelers. In the group of travelers taking respiratory medications, the chronic use of medications for asthma control was reported by 175 travelers (6% of TCI, 1.05% of all travelers). Acid suppressive therapy was taken by 146 travelers (5% of TCI, 0.9% of all travelers). Among travelers who were using medications to control diabetes, insulin was used by 26% (39 out of 151). Diuretic use was reported by 80 travelers (3% of TCI, 0.5% of all travelers). Immunosuppressive medications were used by 39 travelers (1% of TCI, 0.2% of all travelers).
4. Discussion Travelers to developing countries are commonly perceived to be healthy young backpackers. We have shown that in Table 2
Healthy travelers
a
fact, TCI constituted 18.3% of all travelers to developing countries during the study period. Even among the 20e30 years old typical of backpackers age group, TCI constituted 12.5% of travelers. These young adult travelers reported mainly asthma and seasonal allergies whereas in travelers older than 40 years, endocrine and metabolic diseases, (mainly hypercholesterolemia and hypothyroidism-7.4% of all travelers), and cardiovascular diseases (mainly hypertension-5.1% of all travelers), were the most frequent chronic conditions. The existing medical literature regarding TCI is very limited. In addition to the magnitude of this issue, our study also underscores the scope of medical conditions affecting travelers and the many problems medical practitioners need to address during the pre-travel consultation.
Demographics and travel characteristics of travelers in different age groups.
% Travel destination (n)a Age group Traveler % Of age Travel duration (days) Asia (years) group groupa Sub-Saharan Latin (n) median(IQR) Africa America
% Travel purpose (n)a
20e30
98(1057) 97(7592) 97(8652) 80(176) 78(1221) 78(1394) 72(174) 77(757) 76(934) 86(510)b 77(661)b 81(1171) 92(534)c 88(369)c 90(900)
30e40
40e50
50e60
>60
a b c
TCI Healthy All TCI Healthy All TCI Healthy All TCI Healthy All TCI Healthy All
12(1085) 88(7898) 62(8986) 12(222) 88(1590) 12(1811) 20(245) 80(1008) 9(1254) 41(611) 59(874) 10(1485) 58(590) 42(435) 7(1019)
90(30e180) 90(30e180) 90(30e180) 22(14e35) 22(14e40) 22(14e40) 15(10e21) 15(11e21) 15(10e21) 17(14e23) 17(14e21) 17(14e22) 18(15e22) 19(15e24) 19(15e23)
59(635) 60(4759) 60(5394) 69(152) 71(1130) 71(1283) 62(153) 65(651) 64(803) 62(393) 62(547) 64(944) 54(319) 51(222) 53(537)
3(31) 3(260) 37(3282) 17(37) 17(275) 12(212) 30(70) 27(268) 9(111) 21(109) 21(186) 16(243) 19(111) 18(77) 29(290)
39(418) 36(2863) 3(293) 14(30) 12(183) 17(311) 9(22) 9(88) 27(339) 16(99) 16(144) 20(294) 27(157) 31(134) 18(187)
Tourism/ Business Mission leisure
% of age group for TCI/healthy travelers, for all travelers % of all travelers. P value < 0.001, distribution of purpose of travel between TCI vs. healthy travelers age >50. P value < 0.04, distribution of purpose of travel between TCI vs. healthy travelers age >60.
1(7) 1(87) 1(094) 5(10) 7(108) 7(119) 6(14) 6(62) 6(75) 3(18)b 7(61)b 5(79) 3(15)c 5(23)c 4(038)
1(13) 2(142) 2(155) 15(33) 15(229) 15(263) 22(53) 17(167) 18(219) 11(64)b 16(134)b 14(200) 5(31)c 7(28)c 6(057)
% Males (n)
46(501) 49(3892) 49(4393) 58(129) 62(983) 61(1112) 56(136) 52(528) 53(664) 51(310) 56(486) 54(796) 53(309) 54(237) 54(546)
Chronic illnesses in travelers
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Table 3 Frequent chronic illness among travelers to the developing countries. % Of travelers (n) Chronic illness groups Endocrine & metabolic Cardiovascular Pulmonary Allergic & immunologic Gastrointestinal Hematology Psychiatric Neurology Musculoskeletal Rheumatology Oncology Frequent illnesses Hypercholesterolemia Hypertension Asthma Hypothyroidism Seasonal allergies Diabetes mellitus Osteoporosis Depression Anemia Gastro-esophageal reflux Migraine headaches Ischemic heart disease
7.4% 5.1% 3.0% 1.9% 1.9% 1.2% 1.0% 1.0% 0.8% 0.6% 0.6%
(1236) (850) (507) (321) (316) (194) (162) (161) (127) (102) (94)
3.5% 3.4% 3.0% 1.6% 1.4% 1.2% 0.7% 0.7% 0.7% 0.6% 0.5% 0.5%
(587) (571) (496) (262) (240) (196) (124) (120) (115) (93) (87) (86)
The travelers in our study formed a heterogeneous group regarding age, travel destination, purpose and duration. We performed subgroup analyses to compare the demographics and travel characteristics of TCI and healthy travelers. We found that although TCI differed as a group in travel characteristics from healthy travelers, sub-analysis by age groups eliminated all such differences. It would appear that age, rather than the mere presence of underlying medical conditions, is a major factor in the reason for travel, choice of destination and travel duration. Surprisingly, we found that use of chronic medications did have a significant impact on travel duration. The Table 4 The most common chronic illnesses in different age groups. Age group (years)
Commonest diseases
% Of travelers in age group (n)
0e20
Asthma Seasonal allergies ADHD Asthma Seasonal allergies Hypothyroidism Hypercholesterolemia Hypertension Hypothyroidism Hypertension Hypercholesterolemia Diabetes mellitus
1.6% 1.4% 0.9% 3.5% 1.5% 0.8% 10.8% 9.5% 3.8% 26.3% 23.6% 7.4%
20e40
40e60
60e80
(13) (11) (7) (415) (176) (98) (302) (265) (107) (273) (245) (77)
Table 5 Frequent chronic medications used by travelers to developing countries. Medications
% Of travelers (n)
Cardiovascular agents Anti-hyperlipidemic agents Hormones Coagulation modifiers Respiratory agents Anti-diabetic agents Psychotherapeutic agents Nutritional products Gastrointestinal agents Metabolic agents
3.5% 3.4% 2.3% 2.1% 1.7% 0.9% 1.1% 1.0% 1.1% 0.9%
(586) (565) (389) (348) (287) (151) (185) (166) (186) (144)
median travel duration of young travelers in the typical “backpacker” 20e30 years age group who were using chronic medications, was 1 month shorter than in their healthy counterparts. In contrast, such a difference was not found in the older age groups, in whom no difference in travel duration existed between healthy travelers and even among TCI on medication. This probably reflects the fact the in the older age groups the duration of travel is anyhow short, probably due to work related or familial obligations, regardless of health problems. It is not self-evident why travel is curtailed in young travelers who take medications. In the majority of these cases, the medical condition for which medications were used (i.e. mild, well controlled asthma or hypothyroidism) was not an objective barrier to extended travel. It is possible that chronic medication use may be associated with perceived ill health, the subjective assessment of being at risk, or due to technical issue of lack of medications supply during a long trip, all may lead to a shorter travel duration These questions need to be addressed in prospective studies. TCI did not appear to be more scrupulous in preparing for travel, as we did not find any difference in the time interval between pre-travel consultation and planned travel date. We found only three previous studies that addressed the subject of chronic illness and its effects on travel. In a study conducted in a single US travel clinic between 1984 and 1989, 27% of 2445 Americans travelers to developing countries, were TCI [6]. In another, multi-center study of American travelers, between 2009e2011, 59% of 13,235 travelers were TCI [7]. The third study, performed in France during 2009 [8], found that TCI composed 11% of 3442 travelers. Thus, the rate of TCI among travelers attending pre-travel clinics appears to differ from country to country. However, the distribution of chronic illnesses, except for the higher rate of seasonal allergies in the American travelers, was similar in all the studies. In contrast to our study neither of those studies had dealt with the epidemiology and travel characteristics of TCI. Preparations for travel to developing countries may include the administration of live attenuated (Yellow fever vaccine, MMR vaccine) vaccines, and the prescription of medications for malaria prophylaxis, travelers’ diarrhea and high altitude illness. About 1.5% of the study population
762 were immunosuppressed and pregnant travelers with possible contraindications against live attenuated vaccines. The choice of malaria prophylaxis can pose problems in several groups of travelers. Mefloquine and atovaquone/ proguanil, are both labeled by the FDA as pregnancy category C drugs [9,10], while doxycycline is category D e which makes malaria prophylaxis contraindicated in pregnant travelers. For travelers with neuro-psychiatric disorders mefloquine is contraindicated. In our series, 0.15% of travelers were pregnant, whereas 1.5% self-reported neuropsychiatric disorders. Travel to developing countries can impact TCI in two ways e travel can adversely affect the control of chronic illnesses or raise the traveler’s risk of acquiring travel related conditions (such as: travelers’ diarrhea, enteric fever, malaria, high altitude sickness etc.). Few studies address the impact of the travel on the chronic medical condition among travelers to developing countries. Studies on asthma and insulin dependent diabetes mellitus (IDDM) have shown a worsening of both pretravel conditions [11e13]. On the other hand, a caseecontrol study in travelers with inflammatory bowel diseases (IBD) did not find an increased risk of gastrointestinal morbidity in these patients [14]. The impact of chronic illness on travel related diseases was even more neglected. A recent Dutch study found that HIV patients with CD4 count bellow 500, and Insulin treated diabetic patients had a higher risk of acquiring travel related infections. Surprisingly, in this study recent cancer chemotherapy and usage of anti-tumor necrosis factor (TNF) agents was not associated with an increased risk of infections [15]. Patients who chronically use gastric acid lowering therapy (proton pump inhibitors, H2 antagonists etc.) are at increased risk for developing gastrointestinal infections [16,17]. Although there is no such study showing a similar higher risk in travelers (1% of our travelers), the International Society of Travel Medicine (ISTM) recommends a daily use of prophylaxis against travelers’ diarrhea in travelers who use stomach acid lowering [18,19] therapy traveling to Sub-Saharan Africa, South East Asia and Latin America [20]. Travel to, low to middle income countries [18,19], can lead to difficulties in controlling chronic illness in TCI, many of whom receive chronic medications. Travelers may encounter logistical problems, especially during longer trips, acquiring and maintaining medications (e.g. supplies, refrigeration, stability of medication in extreme temperature etc.). Whether chronic illness actually affects travel planning has hardly been addressed in the literature. A single study has shown that among diabetic travelers, 15% of travelers changed travel destination and duration because of insulin usage [11]. Our study suggests that the existence of chronic illness does not have a significant impact on travel planning. However, chronic use of medications seems to have an impact on travel duration in the younger group age.
5. Conclusions TCI accounted for nearly one fifth of Israeli travelers to developing countries who presented at our clinic. TCI were a significant population even among younger travelers.
S. Stienlauf et al. The implications of chronic illness and chronic medication use on travel to developing countries are not well studied. Our study, which to best of our knowledge, is the first large scale study to address the issue, suggests that chronic medication use, rather than the existence of chronic illnesses, does impact travel itinerary and characteristics. Further studies are needed to elucidate the possible roles of subjective health perception and objective disabilities in curtailing travel for TCI. Also, the outcome of this population while traveling to developing countries requires further study.
Conflict of interest None.
Acknowledgments No funding source was available for this study.
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