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Am. J. Trop. Med. Hyg., 72(6), 2005, pp. 825-830
Copyright © 2005 by The American Society of Tropical Medicine and Hygiene

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IMPORTED GIARDIASIS: IMPACT OF INTERNATIONAL TRAVEL, IMMIGRATION, AND ADOPTION

KARL EKDAHL AND YVONNE ANDERSSON
Department of Epidemiology, Swedish Institute for Infectious Disease Control (SMI), Solna, Sweden; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden


ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
From the Swedish national database, regarding notified Giardia cases, we could for the period 1997–2003 identify 3,697 cases of travel-associated giardiasis, 4,151 cases in newly arrived immigrants and refugees, and 455 cases in internationally adopted children. These were compared with data sets on the number of international travelers, immigrants/refugees, and adopted children. The overall risk of being notified with giardiasis in returning travelers was 5.3 of 100,000, with the highest incidences in travelers from the Indian Subcontinent (628 of 100,000), East Africa (358 of 100,000), and West Africa (169 of 100,000). A large proportion of the travel-related cases were seen in persons with family roots in the country of infection—a risk group deserving special attention. The overall risk in immigrants and refugees was 1,180/100,000 with the highest risk in persons from Afghanistan (3,800 of 100,000) and Iraq (2,990 of 100,000). The incidence was highest among internationally adopted children (8,110 of 100,000), with geographical risks not entirely correlating to those in travelers and immigrants.


INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Giardia lamblia (syn. G. intestinalis, G. duodenalis) is a waterborne protozoan parasite and a common cause of intestinal disease in all parts of the world.1,2 Common recognized routes of transmission are contaminated drinking water and food, recreational exposure to contaminated surface water, person-to-person contact (especially in daycare centers).1,37 Waterborne outbreaks are not uncommon.6 Although recognized in all parts of the world, the incidence of giardiasis is considerably more common in developing countries, and specifically under circumstances with poor sanitary conditions, such as settings with civil unrest and many displaced persons.8

Between, 25% and 50% of travelers to developing countries in the tropics and subtropics experience diarrhea.9 Although bacteria are dominating in acute travelers’ diarrhea, protozoa are the most common pathogens in chronic diarrhea.10,11 The risk of contracting travel-associated intestinal parasites has been associated with long duration of stay, hygiene, and socioeconomic development of the host country.12 Waterborne outbreaks of Giardia have also been noted in tourist resort hotels.13

With increasing international travel and large contingents of refugees and immigrants from highly endemic countries, the epidemiology of giardiasis in many Western countries has been changing in the recent years. In this paper, we describe the impact of immigration and international travel on the epidemiology of giardiasis in Sweden 1997–2003 and give detailed relative risk estimates of giardiasis in persons coming from different regions of the world.


PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Notification data on giardiasis. We used notification data from all cases of giardiasis 1997–2003. Giardiasis is a notifiable disease in Sweden according to the Communicable Disease Act, and notifications are made to the Swedish Institute for Infectious Disease Control (SMI), both by the clinician having seen the patient (clinical notification) and the microbiologist having diagnosed the pathogen (laboratory notification). Besides data on name, age, sex, and date of notification, the clinical notifications also contain information on presumed country of infection, reason for sampling (e.g., clinical disease, or health check of asylum seeker/adopted children), and other epidemiologic information of importance. All information in the database is derived from the notifications. The information regarding "country of infection" is thus based on the best judgment of the notifying clinician from the overall patient history and knowledge of the characteristics of the pathogen in question, and not derived from any specified time intervals.

At the SMI, the different notifications on the same patient and episode of disease are merged into case files using the unique personal identification number issued to all Swedish residents, and used in all contacts with the health care. In newly arrived immigrants and refugees, the issue process takes a few weeks. Based on notified country of infection completeness of the personal identification number, reason for sampling, and other information in the notification, the data set was divided in a) domestic cases (infected in Sweden), b) returning travelers, c) immigrants, d) internationally adopted children, and e) unknowns (notifications lacking data on country of infection. These data were also used to identify persons among the returning travelers with family roots in the country of infection, having visited friends and relatives, so-called VFRs.14

Denominator data on travel patterns. As denominator in risk calculations of travel-related giardiasis, we used data, for the same years (1997–2003), from an extensive database on domestic and international travel of Swedish residents, the Swedish Tourist and Travel Database (TDB) (http://www.resursab.se).15 The TDB is based on monthly interviews with 2,000 randomly selected Swedish residents. Detailed questions are asked on recent overnight travel. Because the number of travelers to some countries is too small to draw any specific conclusions from it, and many persons travel to several countries in a region, data on travel destination is often given as region, rather as single country. From the TDB we retrieved case-based (but anonymous) data on all respondents (N = 16,255) having traveled overnight to a country/region outside Sweden. Using the demographic distribution of respondents in the dataset and the demographic distribution of Swedish residents, the total number of travelers could be extrapolated. In the analysis, we used both the actual number of respondents and the estimated total number of travelers.

Denominator data on immigrants and international adoptions. We obtained information on the yearly number of immigrants from different countries from the Swedish Migration Board (http://www.migrationsverket.se/english.jsp). This group includes visiting students, asylum seekers, convention refugees, and persons with residence permits due to family ties or by cause of labor-market. The Swedish National Board for Intercountry Adoptions (http://www.nia.se) provided data on the yearly number of international adoptions, by country.

Statistical methods. The crude risk of being notified with giardiasis per 100,000 travelers (per sex, age group and destination) with 95% confidence intervals (95% CI) for the estimates was calculated from the notifications and the extrapolated number of travelers. To adjust for confounding and detect possible effect modification, we also calculated odds ratios (OR) of being notified with giardiasis in a logistic regression model. Crude risk estimates (with 95% CI) of giardiasis, per 100,000 immigrants and per 1,000 adopted children and country of origin, were calculated using notification data and the above denominators. All analyses were done using the Stata 6.0 software (Stata Corporation, College Station, TX).

Ethical considerations. Collection and use of notification data is regulated by the Swedish Communicable disease act, and the notification reports contain full personal identification. The TDB contains anonymous data records only. The study was approved by the Medical Ethics Committee of the Karolinska Institute, Stockholm, Sweden.


RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In the study period, 11,590 patients were notified with giardiasis. Of these notified patients, 3,697 (32%) were travel related, 4,151 (36%) diagnosed in newly arrived immigrants and refugees, 455 (4%) diagnosed in internationally adopted children, and 1,708 (15%) were domestic cases (infected in Sweden). Altogether 1,441 (13%) notifications lacked information enough to be grouped (Table 1Go).


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TABLE 1
Notified cases of giardiasis 1997–2003 per category of infection
 
Giardiasis in returning travelers. Data on country of infection was available for 3,571 (97%) of the 3,697 travel-related cases. These patients were compared with 16,255 respondents with overnight travel outside Sweden in 1997–2003 from the TDB database. The TDB respondents corresponded to almost 68 million travel episodes (Table 2Go).


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TABLE 2
Estimated number of travelers, respondents in the TDB (controls), and notified cases of travel-associated giardiasis 1997–2003, with an unadjusted risk estimate (per 100,000) and multivariate odds ratio from a logistic regression model adjusted for the risk factors age, sex, month of travel, and travel destination
 
The overall risk of travel-associated giardiasis was 5.3 per 100,000 travelers. Most cases had been traveling to India (N = 499), Thailand (N = 282), Turkey (N = 264), Spain (N = 137), Pakistan (N = 106), Brazil (N = 89), Egypt (N = 82), Kenya (N = 78), and Nepal (N = 65). The highest unadjusted risks (per 100,000 travelers) for returning with giardiasis were noted in travelers from the Indian Subcontinent, East Africa, West Africa, South America, and Central America (Table 1Go and Figure 1Go). Adjusting for age, sex, and month in the logistic regression model only slightly changed the rank between the regions (Table 1Go).



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    FIGURE 1. Map showing Giardia risk per 100,000 returning travelers from different regions of the world.

 
Altogether, 855 of the 3,571 (24%) travel-associated cases were seen in VFRs. This proportion was highest in the Arab countries and Iran, where 86% of the travel-associated Giardia infections were seen in travelers belonging to this group (Table 2Go). Within the Eastern Mediterranean region, 84 of 90 cases (90%) from former Yugoslavia, but 0 of 64 cases from Greece and Cyprus were VFRs. Other countries with a high proportion of VFR cases were Iran (7 of 7; 100%), Lebanon (45 of 47; 96%), Syria (54 of 59; 92%), Somalia (21 of 24; 88%), Eritrea (53 of 63; 84%), Bangladesh (49 of 63; 63%), Pakistan (79 of 106; 75%), and Chile (10 of 14; 71%). Conversely, in some countries with a high Giardia incidence in the returning travelers relatively few had family roots in the country of infection; Kenya (11 of 78; 14%), Egypt (8 of 82; 10%), India (30 of 499; 6%), Thailand (16 of 282; 6%), Brazil (4 of 89; 4%), and Spain (3 of 137; 2%).

The highest risk was seen in the youngest age group (OR 22; 95% CI 16–31), with a decreasing risk with higher age. This age pattern was the same in all regions under study. In the crude risk estimate there was no significant gender difference, but after adjusting for destination, age and month, men were at a slightly higher risk (OR 1.13; 95% CI 1.01–1.27) (Table 2Go). A higher proportion of the children than the adults belonged to the VFR group (Table 2Go).

Giardiasis in refugees and other immigrants. Country of presumed infection was stated in 3,221 (78%) of the 4,151 Giardia notifications in immigrants. Most of the immigrant cases were presumably infected in the Middle East, former Yugoslavia, Afghanistan, Iran, and the Horn of Africa (Table 3Go). The highest risk of giardiasis was seen in persons from Afghanistan and Pakistan, many of the later being Afghan refugees, having stayed in refugee camps in Pakistan before arriving to Sweden. The risk in immigrants was in the magnitude 10 to 20 times higher than in the returning travelers, and the prevalence in immigrants from most regions between 1,000 and 2,000 per 100,000.


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TABLE 3
Notified cases of giardiasis in newly arrived immigrants, number of immigrants, and risk per 100,000 immigrants 1997–2003, per country (the list includes the 12 countries with most Giardia cases)
 
Giardiasis in adopted children. According to official statistics, 5,661 internationally adopted children below the age of 10 years were granted residence permit between 1997 and 2003. In the same period giardiasis was notified in 455 children with notifications stating international adoption (8% of all adopted children). The number and risk per 100,000 children is given Table 4Go. For more than half of the countries, the Giardia prevalence was exceeding 10,000 per 100,000 children, being as high as 50,000 per 100,000 children.


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TABLE 4
Notified cases of giardiasis in adopted children, number of adopted children, and risk per 100,000 children 1997–2003, per country (the list includes countries with more than one Giardia case)
 

DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
With a large proportion Giardia cases in the developed world being imported, public health measures against the disease need to have focus on travelers and immigrants.16 However, comparable data on the risk of contracting giardiasis in different parts of the world have so far largely been lacking. In this study we report data on risk factors based on more than 8,000 notified cases of Giardia infection in returning travelers, immigrants and adopted children. The strength of our study is that all regions were assessed with the same methodology, and the risk estimates should thus be reasonably comparable. Because all data are denominator based, the main conclusions should also be valid for other Western countries.

Methodological issues. The travel data from the TDB have previously been evaluated and found to be quite accurate.15 However, bias in the travel risk calculations may have been introduced in several other steps of the investigation. First, patients coming from distant destinations in tropical countries are likely more inclined to consult a doctor for gastrointestinal symptoms than persons returning from neighboring Nordic countries. The doctor may also be more inclined to pursue the investigation with stool samples for microscopy in a patient arriving from endemic countries in the developing world. The relative risk of getting infected in a tropical country, or a country with a presumed high Giardia incidence (such as Russia), may therefore be exaggerated in the study. Second, because giardiasis often has an insidious onset, it may be hard to determine the exact time and place of infection.1,17 In studies of travelers’ diarrhea in Nepal, giardiasis was more often diagnosed in patients with more than 2 weeks disease duration than with less than 2 weeks duration.18 Third, the study does not take into account various length of stay in different regions. Travelers who stay out for longer periods are more likely to get infected, but on the other hand they are also more likely to have been diagnosed and treated while abroad. However, with these limitations in mind, we believe that our data give a more comprehensive view of comparative risks in different regions of the world than most previous studies.

Regional risks. The risks of coming to Sweden with giardiasis varied immensely between different regions, in all three groups under study. The risk in returning traveler was several thousand times higher in the Indian Subcontinent, the Arab countries/Iran and East Africa compared with the Nordic countries. These same regions were also associated with the highest risks in the newly arrived immigrants, while in the adopted children the highest risk was noted for Morocco, Eastern European countries, and Ecuador. The very different risk profiles in the adopted children on the one hand and travelers and immigrants on the other hand suggest that orphanages are independent epidemiologic units with risks that do not necessarily correlate with the risks in the general populations.

In the travelers there were large and unexplained differences within Africa. The risk in East Africa was 3 times higher than in West Africa, 6 times higher than in Central Africa, 9 times higher than in Southern Africa, and 27 times higher than in North Africa. East Africa and India are recognized high-risk areas for travel-associated diarrhea of various etiology, but the large risk differences within Africa have to our knowledge not previously been described.19,20 The very high risk on the Indian Subcontinent was consistent with our immigrant data, as well as data from a study of diarrhea in returning Austrian travelers, in which 36% of all patients with parasitic infections had spent their vacation in India.21

In Europe, the highest risk by far was in Russia and the former OSS. Many Western tourists travel to St. Petersburg, a city with long-standing problems with giardiasis in the water system.2224 Almost 8,000 Giardia cases are annually notified from this city (http://www.epinorth.org). However, the very high risk in adopted children also from Ukraine, Belarus, Latvia, Bulgaria, and Romania suggest a widely spread Giardia problem in large areas of the former Soviet Union and Eastern Europe.

A large proportion of the notified cases were infected in countries outside the normal tourist routes, from which many Western countries have received large numbers of refugees and asylum seekers in the past decades. Our data clearly suggest that these persons are now increasingly often returning, with their families, to their native home countries for holidays, where they are at high risk for infection. VFRs is thus a group of travelers deserving special attention, especially as they are less inclined to get pretravel advice than other travelers.14 Vague gastrointestinal complaints in persons, especially children, originating from these countries should therefore always be investigated for giardiasis.

In comparable countries, the calculated risk for being notified with giardiasis was 3–30 times higher in immigrant/refugees than in tourists and about 2–5 times higher in adopted children than in immigrants/refugees. Because the 3 different groups were tested differently after arrival to Sweden, all comparisons between the groups should be made with caution. Returning tourists are seldom tested unless they have gastrointestinal complaints, and even then a Giardia infection may be mistaken for a noninfectious disorder, while adopted children are most often thoroughly examined after arrival to Sweden

The incidence of notified giardiasis in immigrants/refugees from East Africa in our study (1–2%) was lower than the 13 to 14% noted among African refugees coming to the United States or Sweden.25,26 However, these studies measured the incidence in persons being tested for giardiasis, whereas we were measuring the proportion of persons being diagnosed of all refugees/immigrants arriving to Sweden. Thus, our data suggest an under-diagnosis both in recently arrived refugees and in other immigrants.

A recent study on infectious diseases in internationally adopted children to the United States, identified the same high-risk countries as we did, but the incidences was higher than in our study (overall risk 8.1%).27 Virtually all internationally adopted children are thoroughly health checked, but also in this group, fecal microscopy may be neglected. We may also have failed to properly identify all the adopted children in our surveillance material.

Age and gender. In all regions, the highest risk was seen in the youngest children, with a decreasing risk with increasing age. This is in contrast with the findings in a UK case-control study of sporadic endemic giardiasis, in which cases were most frequent in the 30–39-year age group.7 In the United States, the peak incidence is seen in children aged 0–5 years, closely followed by persons aged 31–40 years.28 Nonimmune Swedish-borne children, returning to the home countries of their parents, and staying under less than adequate hygienic conditions, may partly explain the very high relative risk seen in the youngest children. The higher risk seen in males was (although statistically significant) of such a low magnitude that the practical importance could be neglected.

Conclusions. Our risk data for imported Giardia infection from different regions of the world could be used as basis for pretravel advice and posttravel/immigration health controls. Effective means of protection against giardiasis exist and include good hand hygiene, avoiding ingestion of surface water, and preferably drinking only bottled water, or, when bottled water is not available, disinfecting/filtrating the drinking water.29,30 Such advice should focus on persons traveling in areas with less than optimal hygienic conditions. Special attention, before and after travel, should be given to parents of young children and to VFRs. All newly arrived immigrants from highly endemic countries should be health-checked, including microscopy on fecal specimen, and regardless if they have gastrointestinal complaints.


Received October 30, 2004. Accepted for publication December 6, 2004.

Financial support: This work was supported by the Swedish Institute for Infectious Disease Control (SMI).

Authors’ addresses: Karl Ekdahl and Yvonne Andersson, Department of Epidemiology, Swedish Institute for Infectious Disease Control (SMI), SE-171 82 Solna, Sweden.


REFERENCES
 TOP
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 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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