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Am. J. Trop. Med. Hyg., 94(4), 2016, pp. 757–766
doi:10.4269/ajtmh.15-0731
Copyright © 2016 by The American Society of Tropical Medicine and Hygiene
Spectrum of Imported Infectious Diseases: A Comparative Prevalence Study of 16,817 German
Travelers and 977 Immigrants from the Tropics and Subtropics
Karl-Heinz Herbinger,* Martin Alberer, Nicole Berens-Riha, Mirjam Schunk, Gisela Bretzel, Frank von Sonnenburg,
Hans Dieter Nothdurft, Thomas Löscher, and Marcus Beissner
Department of Infectious Diseases and Tropical Medicine (DITM), Medical Center of the University of Munich, Munich, Germany
Abstract. The aim of this study was to assess the spectrum of imported infectious diseases (IDs) among patients consulting the University of Munich, Germany, between 1999 and 2014 after being in the sub-/tropics. The analysis investigated complete data sets of 16,817 diseased German travelers (2,318 business travelers, 4,029 all-inclusive travelers,
and 10,470 backpackers) returning from Latin America (3,225), Africa (4,865), or Asia (8,727), and 977 diseased immigrants, originating from the same regions (112, 654 and 211 respectively). The most frequent symptoms assessed were
diarrhea (38%), fever (29%), and skin disorder (22%). The most frequent IDs detected were intestinal infections with species of Blastocystis (900), Giardia (730), Campylobacter (556), Shigella (209), and Salmonella (183). Also frequently
observed were cutaneous larva migrans (379), dengue (257), and malaria (160). The number of IDs with significantly
elevated proportions was higher among backpackers (18) and immigrants (17), especially among those from Africa
(18) and Asia (17), whereas it was lower for business travelers (5), all-inclusive travelers (1), and those from Latin
America (5). This study demonstrates a large spectrum of imported IDs among returning German travelers and immigrants, which varies greatly based not only on travel destination and origin of immigrants, but also on type of travel.
INTRODUCTION
large samples of more than 7,600 migrants and 82,800 travelers, with data collected from more than 40 sites on six continents, although none of these studies compared imported IDs
among travelers and immigrants with a sample size as large
as this study.9–14 EuroTravNet is a European network that
has collected data from more than 15 European sites and published studies with sample sizes of up to more than 900 migrants
and 32,000 travelers.15–17 As multicenter studies, these networks analyzed data of a highly heterogeneous international
population, and consequently the comparability between the
different study groups, such as type of travel or immigrants,
was limited. Furthermore, the data presented in these studies
were highly descriptive.
In these studies it was shown that a greater proportion of
immigrants who had been visiting friends and relatives (VFRs),
had serious, potentially preventable travel-related illnesses
when compared with tourists. They also showed that migrant
patients have acute illnesses or chronic conditions related to
exposure in their country of origin.9,10 Several studies have
shown that the most prevalent symptoms among travelers and
immigrants were diarrhea, fever, and skin disorders.6,11,18–20 In
some studies that compared travelers with immigrants whose
purpose of travel was VFR, the risk of acute diarrhea was
higher among travelers, whereas the risk for malaria and viral
hepatitis was higher among VFRs.21
The findings mentioned above were considered when
patients consulted the Department of Infectious Diseases
and Tropical Medicine (DITM) of the University of Munich,
Germany. The results of these consultations showing the spectrum of imported IDs were published recently.22–27 The aim
of the present cross-sectional study was to evaluate differences in the spectrum of imported IDs 1) between German
travelers returning from the sub-/tropics and immigrants originating from the sub-/tropics; 2) between different sub-/tropical
travel destinations and origins of immigrants, respectively,
divided into Latin America, Africa, and Asia; and 3) between
the different types of German travelers, differentiated into
business travelers, all-inclusive travelers, and backpackers.
The study was performed using the data from a large number of patients who consulted the University of Munich,
The number of international travels worldwide has increased
from 25 million in 1950 to 626 million in 1999, and to
1,133 million in 2014. In addition to the traditional favorite
destinations of Europe and North America, many new destinations have emerged, especially in subtropical and tropical countries.1 In 2014, about 18.2 million individuals traveled
from Germany to destinations outside of Europe. Out of them,
1.5 million traveled to Latin America, 2.8 million to Africa,
and 7.8 million to Asia.2
Beside the growth of international travelers, the global
number of immigrants (including migrant workers and forcibly displaced persons) is constantly increasing. The global
number of international migrant workers was 179 million in
1999 and 232 million in 2014.3 According to United Nations
High Commissioner of Refugees, in 1999, 37 million individuals were forcibly displaced, whereas this number increased
to approximately 60 million in 2014. Among them, it is estimated that 19.5 million are refugees and another 1.8 million
are asylum seekers. In 2013, Germany became the country
hosting the highest absolute number of asylum seekers, with
over 173,000 new asylum applications registered in 2014.4
The increasing number of international travelers and immigrants has, and continues, to lead to new health challenges,
especially in terms of infectious diseases (IDs).5 Growing mobility means there is an increased potential of travelers acquiring
IDs and importing these “exotic” diseases to their home countries, especially those traveling to sub-/tropical regions.6 As
IDs are becoming a more prominent global issue,7 a broader
differential diagnostic thinking is paramount for assessing
returning travelers.8
In recent years, various publications have shown that international travelers and immigrants enlarge the spectrum of imported
IDs. Studies performed by GeoSentinel Surveillance analyzed
*Address correspondence to Karl-Heinz Herbinger, Department of
Infectious Diseases and Tropical Medicine (DITM), Medical Center
of the University of Munich, Leopoldstraße 5, Munich 80802, Germany.
E-mail: herbinger@lrz.uni-muenchen.de
757
758
HERBINGER AND OTHERS
Germany, between 1999 and 2014 after being in the sub-/
tropics. All 17,794 patients were diagnosed and treated at
a single study site. Consequently, all patients were subject of
the same standardized process, allowing for maximal comparability of the data between the study groups.
MATERIALS AND METHODS
Database. A database from the DITM has been collecting
data on sociodemographics (sex, age, origin, and profession),
travel (duration of travel, destination, and type of travel), clinical history and symptoms, diagnostics, and—if applicable—
diagnosis of individuals consulting its outpatient department
for treatment or medical checkup. From January 1999 through
December 2014, the database registered 38,059 individuals
with complete data sets. Out of them, 22,588 (59.35%) individuals had symptoms after traveling to the sub-/tropics
(Latin America, Africa, or Asia), 7,514 (19.74%) individuals
did not have symptoms and had not recently traveled to the
sub-/tropics, 4,810 (12.64%) individuals had symptoms but
had not recently traveled to the sub-/tropics, and 3,147
(8.27%) individuals did not have symptoms after traveling
in the sub-/tropics. The symptoms presented here are those
from patients’ first consultation at DITM after being in the
sub-/tropics.
Study design. In this study, all patients consulted the
DITM, at which time the data of the independent variables
(exposure as sociodemographics and travel) and dependent
variables (outcomes as symptoms, diagnostics, and diagnosis)
were assessed simultaneously: transversal study or crosssectional study. The independent variables were not influenced
by the study design: noninterventional or observant study.
The results of the study were presented in terms of prevalences of imported IDs among different study groups: prevalence study.
Study groups of German travelers. Of the 22,588 patients
returning from traveling in the sub-/tropics, 19,581 (86.69%)
were of German origin (defined as born in Germany). Among
them, 2,318 (11.84%) were business travelers (defined as such
who were primarily on travel because of business or related
issues), 4,029 (20.58%) were all-inclusive travelers (defined as
such whose travel was not organized by themselves including
package holiday), and 10,470 (53.47%) were backpackers
(including low-budget and adventure travelers). The remaining
2,764 (14.12%) patients comprised a miscellaneous group of
students, scientists, missionaries, volunteers, and other persons
with activities during travel not being clearly defined. Of these
2,318 business travelers (BU), 388 (16.74%) had traveled to
Latin America (BU-LA), 848 (36.58%) to Africa (BU-AF),
and 1,082 (46.68%) to Asia (BU-AS). Of the 4,029 allinclusive travelers (AL), 799 (19.33%) had traveled to Latin
America (AL-LA), 1,567 (38.89%) to Africa (AL-AF), and
1,683 (41.77%) to Asia (AL-AS). Of the 10,470 backpackers
(BA), 2,058 (19.66%) had traveled to Latin America (BA-LA),
2,450 (23.40%) to Africa (BA-AF), and 5,962 (56.94%) to Asia
(BA-AS). These nine groups (BU-LA, BU-AF, BU-AS,
AL-LA, AL-AF, AL-AS, BA-LA, BA-AF, and BA-AS)
were defined as study groups, comprising altogether 16,817
diseased German travelers returning from the sub-/tropics
(Table 1).
Study groups of immigrants. The term “immigrant” in this
study refers to persons VFRs and forcibly displaced persons
(including asylum seekers) of non-German origin (defined as
born outside of Germany) and their family members. Of the
22,588 patients returning from the sub-/tropics, 3,007 (13.31%)
patients were diseased immigrants, including 842 (3.73%)
patients of African origin, 830 (3.67%) of West-European
origin, 511 (2.26%) of East-European origin, 421 (1.86%) of
Asian origin, and 233 (1.03%) of Latin American origin, 146
(0.65%) from United States or Canada, and 24 (0.11%) from
Oceania. Of the 233 patients of Latin American (LA) origin,
112 (48.07%) had traveled from Latin America as immigrants
to Germany (IM-LA), while of the 842 patients of African
(AF) origin, 654 (77.67%) had traveled from Africa as immigrants to Germany (IM-AF), and of the 421 patients of Asian
(AS) origin, 211 (50.12%) had traveled from Asia as immigrants to Germany (IM-AS). These three groups (IM-LA,
IM-AF, and IM-AS) comprised altogether 977 diseased immigrants originating from the sub-/tropics (Table 1).
Study population and IDs. The study population comprised
17,794 patients: 16,817 diseased German travelers returning
from the sub-/tropics (divided into nine study groups) and 977
diseased immigrants originating from the sub-/tropics (divided
into three study groups). The study identified 36 imported
IDs which had a sample size of > 10 cases: eight viral, eight
bacterial, nine protozoal, seven helminthic, and four ectoparasitic IDs. These 36 IDs comprised 4,198 laboratory-confirmed
cases with complete data sets. Only exact laboratory-confirmed
IDs were considered in this study. Clinically suspected or probable cases were not included.
Data analysis. The database of the DITM was the source
of all data analyzed in this study. The descriptive analysis was
performed by Excel Worksheet (Microsoft, Redmond, WA).
The aim of this study was to evaluate associations between
the 12 different study groups (independent variable) and the
risk for any imported ID (dependent variable). Bivariate
approximative test (χ2 test) and exact test (Fisher’s test)
were conducted using EpiInfo, version 3.3.2 (Centers for
Disease Control and Prevention, Atlanta, GA) and Stata software, version 9.0 (Stata Corporation, College Station, TX) for
comparing the proportion of any variables in a certain study
group with the overall proportion of the same variable: comparative prevalence study. Significant differences were defined
as P < 0.05. Ethical considerations. Ethical clearance for the study protocol was provided by the Ethical Committee of the Medical Faculty at the University of Munich, Germany. Clinical and laboratory data were used only from patients who provided written informed consent, or in the case of minors, had a general written informed consent from the legal caretakers. RESULTS Sociodemographic data. Data from 17,794 patients fulfilled the inclusion criteria and were therefore included in this study (study population). Of them, 9,114 (51.2%) were female, whereas this proportion differed significantly in 12 study groups. The proportion of females was significantly higher among all-inclusive travelers (AL-LA: 57.3%, P < 0.01; AL-AF: 58.5%, P < 0.01; AL-AS: 56.5%, P < 0.01), among IM-LA (68.8%, P < 0.01), and among BA-AS (53.6%, P < 0.01). The age range was 4 months to 91 years, with a median of 35.0 years, and an interquartile range (IQR) of 27.7–46.9 years. In all three regions, the study groups with the highest median Travel data Duration: median (days) Interquartile range Symptoms Diarrhea % P value Fever % P value Skin disorders % P value Nausea % P value Arthralgia % P value Viral IDs (8) Dengue fever % P value Mononucleosis % P value HIV infection % P value Cytomegalovirus infection % P value Sample size Proportion (%) Origin (place of birth) Sample size Proportion (%) Type of travel/immigrant Study groups: 12 Sample size Proportion (%) % Demographic data Sex: female % P value Age: median (years) Interquartile range Destination/home region 14 14; 21 268 34.40 0.02* 197 25.29 0.042* 184 23.62 0.29 141 18.10 0.91 103 13.22 0.21 AL-LA 9 1.16 0.49 0 0 0.18† 0 0 0.64† 1 0.13 1.00† 138 35.57 0.26 102 26.29 0.33 86 22.16 0.97 65 16.75 0.53 42 10.82 0.054 BU-LA 7 1.80 0.55 2 0.52 0.30† 1 0.26 0.48† 4 1.03 < 0.01†* 174 44.85 0.01* 36.00 29.05; 46.72 21 7; 90 446 57.25 < 0.01* 36.32 28.57; 49.56 BU BU-LA 388 2.18 100 813 39.50 0.25 447 21.72 < 0.01* 563 27.36 < 0.01* 336 16.33 0.04* 222 10.79 0.13 BA-LA 32 1.55 0.65 5 0.24 0.73 1 0.05 0.25† 3 0.15 1.00† 28 17; 49 1,072 52.09 0.40 31.48 25.84; 41.11 3,337 18.75 Germany 3,225 18.12 AL BA AL-LA BA-LA 779 2,058 4.38 11.57 100 100 LA 34 30.36 0.08 21 18.75 0.02* 33 29.46 0.06 19 16.96 0.79 21 18.75 0.02* IM-LA 2 1.79 0.68† 1 0.89 0.27† 1 0.89 0.17† 1 0.89 0.15† NA 77 68.75 < 0.01* 34.58 27.18; 43.03 LA 112 0.63 IM IM-LA 112 0.63 100 317 37.38 0.56 258 30.42 0.20 136 16.04 < 0.01* 132 15.57 0.06 93 10.97 0.43 BU-AF 3 0.35 < 0.01* 1 0.12 0.73† 2 0.24 0.65† 0 0 0.63† 21 10; 120 334 39.39 < 0.01* 38.54 31.03; 48.59 BU BU-AF 848 4.77 100 683 43.59 < 0.01* 421 26.87 0.13 309 19.72 0.02* 315 20.10 0.02* 165 10.53 0.10 AL-AF 2 0.13 < 0.01* 2 0.13 0.32† 2 0.13 1.00† 4 0.26 0.28† 14 10; 15 916 58.46 < 0.01* 40.07 30.39; 55.34 924 37.71 0.49 814 33.22 < 0.01* 498 20.33 0.02* 456 18.61 0.36 272 11.10 0.24 BA-AF 4 0.16 < 0.01* 9 0.37 0.38 1 0.04 0.11† 2 0.08 0.57† 21 14; 28 1,276 52.08 0.36 35.09 27.63; 47.33 5,519 31.02 Germany 4,865 27.34 AL BA AL-AF BA-AF 1,567 2,450 8.81 13.77 100 100 AF 103 15.75 < 0.01* 299 45.72 < 0.01* 96 14.68 < 0.01* 84 12.84 < 0.01* 108 16.51 < 0.01* IM-AF 3 0.46 0.03* 0 0 0.26† 10 1.53 < 0.01†* 0 0 1.00† NA 213 32.57 < 0.01* 37.00 29.49; 43.62 AF 654 3.68 IM IM-AF 654 3.68 100 484 44.73 < 0.01* 313 28.93 0.75 179 16.54 < 0.01* 197 18.21 0.82 147 13.59 0.06 BU-AS 19 1.76 0.38 5 0.46 0.23† 3 0.28 0.43† 4 0.37 0.07† 18.5 7; 60 373 34.47 < 0.01* 39.75 32.19; 49.51 BU BU-AS 1,082 6.08 100 577 34.28 < 0.01* 494 29.35 0.41 426 25.31 < 0.01* 282 16.76 0.18 219 13.01 0.11 AL-AS 33 1.96 0.06 1 0.06 0.09† 1 0.06 0.36† 2 0.12 1.00† 14 14; 21 951 56.51 < 0.01* 42.78 31.23; 56.33 2,436 40.86 < 0.01* 1,624 27.24 < 0.01* 1,373 23.03 0.03* 1,148 19.26 < 0.01* 670 11.24 0.09 BA-AS 136 2.28 < 0.01* 24 0.40 0.03* 8 0.13 0.43 5 0.08 0.12 25 21; 35 3,195 53.59 < 0.01* 32.02 26.44; 42.46 8,938 50.23 Germany 8,727 49.04 AL BA AL-AS BA-AS 1,683 5,962 9.46 33.51 100 100 AS 45 21.33 < 0.01* 81 38.39 < 0.01* 49 23.22 0.69 19 9.00 < 0.01* 40 18.96 < 0.01* IM-AS 7 3.32 0.02* 0 0 1.00† 0 0 1.00† 0 0 1.00† NA 87 41.23 < 0.01* 38.92 29.08; 47.01 AS 211 1.19 IM IM-AS 211 1.19 100 (continued) 6,822 38.34 NA 5,071 28.50 NA 3,932 22.10 NA 3,194 17.95 NA 2,102 11.81 NA ALL 257 1.44 NA 50 0.28 NA 30 0.17 NA 26 0.15 NA 21 14; 30 9,114 51.22 NA 35.00 27.70; 46.94 17,794 100 All 17,794 100 All All 17,794 100 100 All TABLE 1 Spectrum of imported IDs among diseased German travelers (business travelers, all-inclusive travelers, and backpackers) after returning from the sub-/tropics, and among diseased immigrants originally from these regions IMPORTED INFECTIOUS DISEASES AMONG TRAVELERS AND IMMIGRANTS 759 Herpes simplex % P value Chronic hepatitis C % P value Chikungunya % P value Herpes zoster % P value Bacterial IDs (8) Campylobacter spp. infection % P value Shigellosis % P value Salmonellosis % P value Rickettsiosis % P value Typhoid fever % P value Paratyphoid fever % P value Syphilis % P value Tuberculosis % P value Protozoal IDs (9) Blastocystis hominis infection % P value Giardiasis % P value Malaria % P value Entamoeba spp. infection % P value Destination/home region 0 0 1.00† 0 0 1.00† 2 0.26 0.19† 0 0 1.00† AL-LA 11 1.41 < 0.01* 7 0.90 0.46 11 1.41 0.28 0 0 0.03†* 0 0 1.00† 0 0 1.00† 0 0 1.00† 0 0 1.00† AL-LA 22 2.82 < 0.01* 18 2.18 < 0.01* 3 0.39 0.12 2 0.26 0.11 0 0 1.00† 1 0.26 0.33† 1 0.26 0.33† 1 0.26 0.30† BU-LA 4 1.03 0.02* 3 0.77 0.63† 1 0.26 0.20† 0 0 0.27† 0 0 1.00† 0 0 1.00† 0 0 1.00† 0 0 1.00† BU-LA 18 4.64 0.70 5 0.88 < 0.01* 2 0.52 0.59† 3 0.77 0.76† LA 4.47 0.20 81 3.60 0.69 2 0.10 < 0.01* 14 0.68 0.78 2 0.10 1.00† 2 0.10 1.00† 1 0.05 0.71† 1 0.05 1.00† BA-LA 44 2.14 < 0.01* 23 1.12 0.79 10 0.49 < 0.01* 0 0 < 0.01* 0 0 0.24† 0 0 0.63† 0 0 0.63† 0 0 0.63† BA-LA 92 5.36 0.88 2 1.61 0.33† 0 0 0.63 0 0 1.00† 0 0 1.00† 0 0 1.00† 2 1.79 < 0.01†* 0 0 1.00† IM-LA 1 0.89 0.27† 1 0.89 1.00† 0 0 0.63† 0 0 1.00† 0 0 1.00† 0 0 1.00† 0 0 1.00† 1 0.89 0.07† IM-LA 6 6.84 0.02* 22 1.88 0.02* 20 2.36 < 0.01* 10 1.18 0.12 0 0 1.00† 0 0 1.00† 1 0.12 0.59† 2 0.24 0.18† BU-AF 21 2.48 0.31 14 1.65 0.19 8 0.94 0.80 4 0.47 1.00† 0 0 1.00† 0 0 1.00† 1 0.12 0.42† 0 0 1.00† BU-AF 58 4.59 0.38 31 1.87 < 0.01* 8 0.51 0.09 6 0.38 0.09 4 0.26 0.08† 0 0 0.40† 2 0.13 0.67† 2 0.13 0.65† AL-AF 22 1.40 < 0.01* 16 1.02 0.55 17 1.08 0.82 18 1.15 < 0.01* 0 0 0.64† 0 0 0.61† 0 0 0.61† 0 0 0.61† AL-AF 72 TABLE 1 Continued AF 4.20 0.04* 77 2.71 < 0.01* 38 1.55 < 0.01* 14 0.57 0.32 0 0 0.10† 1 0.04 0.50† 1 0.04 0.50† 2 0.08 1.00† BA-AF 62 2.53 0.08 29 1.18 0.96 24 0.98 0.80 60 2.45 < 0.01* 2 0.08 1.00† 0 0 0.38† 1 0.04 1.00† 0 0 0.38† BA-AF 103 4.89 0.84 17 2.22 0.048* 68 10.40 < 0.01* 9 1.38 0.048* 2 0.31 0.15† 3 0.46 0.03†* 0 0 1.00† 0 0 1.00† IM-AF 5 0.76 < 0.01* 5 0.76 0.32 3 0.46 0.14 1 0.15 0.38† 1 0.15 0.43† 0 0 1.00† 4 0.61 < 0.01†* 4 0.61 < 0.01† IM-AF 32 4.44 0.34 41 2.86 0.59 2 0.18 0.01* 11 1.02 0.25 1 0.09 1.00† 0 0 0.62† 2 0.18 0.30† 3 0.28 0.07† BU-AS 37 3.42 0.57 17 1.57 0.21 16 1.48 0.13 1 0.09 0.054 1 0.09 0.61† 1 0.09 0.50† 2 0.18 0.14† 0 0 1.00† BU-AS 48 4.34 0.16 40 2.24 < 0.01* 0 0 < 0.01* 11 0.65 0.70 3 0.18 0.42† 1 0.06 1.00† 3 0.18 0.24† 2 0.12 0.66† AL-AS 47 2.79 0.41 12 0.71 0.06 18 1.07 0.86 0 0 < 0.01* 1 0.06 1.00† 0 0 0.62† 1 0.06 1.00† 0 0 0.62† AL-AS 73 AS 6.17 < 0.01* 392 6.10 < 0.01* 13 0.22 < 0.01* 50 0.8 ... 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