DÄ internationalArchive46/2008Eosinophilia in Returning Travelers and Migrants

Review article

Eosinophilia in Returning Travelers and Migrants

Dtsch Arztebl Int 2008; 105(46): 801-7. DOI: 10.3238/arztebl.2008.0801

Ehrhardt, S; Burchard, G D

Introduction: Eosinophilia in travelers returning from tropical countries is often caused by helminths. The high eosinophil counts arise particularly from tissue migration of invasive larvae.
Methods: Review of literature selected by means of a Medline search using the MeSH terms "eosinophilia" and "helminth."
Results: The patient's geographic and alimentary history may suggest infection with particular parasitic worms. A targeted diagnostic approach is suggested. The physician should concentrate on the principal signs and be guided by the geographic and alimentary history. Elaborate diagnostic measures are seldom indicated.
Discussion: Although eosinophilia alone has low positive predictive value for a worm infection, it points clearly to helminthosis if the patient has recently returned from the tropics and the eosinophilia is new.
Dtsch Arztebl Int 2008; 105(46): 801–7
DOI: 10.3238/arztebl.2008.0801
Key words: eosinophilia, helminth infection, foreign travel, migration, differential diagnosis
LNSLNS Eosinophilia has a wide variety of causes, including allergic illnesses, skin diseases, malignant conditions or even medication use (1). Nonparasitic causes should therefore also be considered when attempting to establish the cause of eosinophilia (1). New-onset eosinophilia following a visit to the tropics, however, is most likely due to a worm infection (helminthosis). Up to 5% of asymptomatic travelers returning from the tropics have eosinophilia requiring diagnostic clarification and between 14% and 48% of these travelers with eosinophilia are suffering from a parasitosis requiring treatment (26). Screening of immigrants with eosinophilia has shown that helminths are present in up to 77% of cases depending on the country of origin (7, 8). On the other hand, the sensitivity and specificity of eosinophilia for diagnosing helminthosis are low and the positive predictive value was only about 10% in some studies (4).

In medical practice, an increased percentage of eosinophilic granulocytes in the differential blood count is often erroneously referred to as "eosinophilia." In fact, the decisive factor is the number of eosinophilic granulocytes per µL blood. Healthy persons have on average fewer than 450 eosinophils per µL blood. Depending on the time of day, this value can vary by as much as 40% depending on the cortisol level (9). The patient's age, physical training condition as well as environmental factors (especially allergen exposure) also influence the eosinophil count in peripheral blood. The degree of eosinophilia can be categorized as follows:

- Mild eosinophilia: up to 1500/µL
- Moderate to severe eosinophilia >1500/µL (according to [10], modified).

Another helpful laboratory parameter is total IgE. An increase in the IgE concentration occurs in various worm diseases. Mutual pathophysiological relationships, but only a low correlation exist between IgE and eosinophilia (11).

No guidelines are yet available for diagnostic evaluation of eosinophilia in the primary care setting. Physicians frequently contact institutes of tropical medicine for advice. In the following, the authors recommend structured screening programs guided by the geographic history and cardinal symptoms. These programs are based on epidemiological data on imported diseases (1220), especially surveillance data from the GeoSentinel Network (2123). An economical procedure and the lowest possible stress for the patient were also among the goals in developing these programs. The authors propose screening programs for "generalists" and not for specialists assumed to possess detailed knowledge of the routes of transmission and clinical presentations, even of very rare tropical infectious diseases. In doubtful cases a physician specializing in tropical medicine has to be consulted who possesses specialized knowledge of the prevalences and clinical manifestations of rare tropical diseases.

The most important helminthoses—including clinical signs, diagnosis, and treatment—are summarized in the e-table (gif ppt).

Systematic search for evidence
The diagnosis and treatment of tropical diseases should be evidence based. Unfortunately, no sufficiently controlled studies are available on many topics of tropical medicine. Many of the studies that are available were performed in developing countries and their results cannot be extrapolated to Germany. Moreover, many parasitic diseases are rarely imported into industrialized countries, with the result that there are no adequate case numbers. It is therefore difficult to state methods with which to interpret and assess the level of evidence. The Cochrane Collaboration studies are also of limited assistance because for the reasons outlined above they cover only small partial areas of tropical medicine and most of the topics addressed focus on developing countries. It is therefore not surprising that there are hardly any international guidelines. Germany also lacks guidelines for the diagnostic evaluation of eosinophilia in travelers returning from the tropics and migrants. This article is a reflection of expert opinion and was produced on the basis of an informal consensus. The authors performed a review of literature selected by means of a Medline search using the MeSH terms "eosinophilia" and "helminth" for the period 1983 to 2008.

Diagnostic strategies
Since helminth infections can result in serious health impairment and eosinophilia can also point to the presence of various malignant diseases, rapid and efficient diagnostic clarification is essential. Whereas in most cases the treatment of worm diseases is easy, cost effective and safe, an unstructured investigation of eosinophilia is often time consuming, cost intensive and burdensome for the patient. If test results are negative but there is a continued suspicion of helminthosis, an expert in tropical medicine should be consulted.

History
The geographic history is especially important. Some helminths have worldwide prevalence, while others are found only in circumscribed geographic areas. Loa loa (figure 1 jpg ppt), for example, is found only in Central and West Africa. Ascaris, on the other hand, has a worldwide distribution. Travelers returning from schistosomiasis-endemic regions, for example, must be questioned specifically about contact with natural fresh waters. An alimentary history can also provide useful information regarding the type of worm infection. Liver flukes, for example, are usually transmitted by the consumption of aquatic plants such as watercress, lung flukes by fresh water crabs and the herring worm by raw sea fish (table 1 gif ppt).

Laboratory diagnostics
Besides quantifying eosinophilia in the differential blood count, primary importance attaches to direct identification of pathogens and immune diagnostics. Most desirable is the direct detection of adult worms, larvae in the blood or worm eggs in feces because this is an unequivocal result and requires no interpretation, as for instance in immune diagnostic procedures. For infections with adult worms or with worm larvae which are localized in the tissue, however, direct detection is often not possible. It is then necessary to resort to antibody diagnosis. It should be noted that cross reactions are common within the three groups of tapeworms (cestodes), roundworms (nematodes), and flukes (trematodes). In migrants and travelers who frequently sojourn in tropical regions, the possibility of a serological scar should be considered. Molecular biological techniques, especially the polymerase chain reaction (PCR), will in future simplify the diagnosis of tropical diseases and improve specificity. For example, a PCR for the detection of schistosomiasis is currently being developed.

Asymptomatic eosinophilia
New-onset asymptomatic eosinophilia following a journey to the tropics should first prompt the physician to rule out the presence of parasitic diseases even if the patient has an allergic predisposition. Table 2 (gif ppt) presents a structured screening program for this purpose. First it is recommended to analyze the stool three times for worm eggs on three consecutive days. If the stool analyses are negative, tests should be performed for Strongyloides stercoralis. This worm has a worldwide distribution in warm countries (e1). The larvae usually hatch while still in the intestine, which is why the eggs are not detectable in the normal stool tests (figure 2 jpg ppt). It is important to exclude Strongyloidiasis because internal and external autoinfection can lead to chronic, persisting disease. It is also possible for a potentially life-threatening hyperinfection syndrome to develop in immunosuppressed persons. A search should also be made for antibodies against schistosomes if the patient has spent time in a schistosomiasis-endemic region (box 1 gif ppt) and the stool samples have tested negative.

Severe eosinophilia (>1500/µL blood) often cannot be sufficiently explained by the detection of worm eggs in the stool. Additional antibody tests for a cestode (tapeworm), a trematode (fluke), and a nematode (roundworm) should thus always be performed. Because of the cross reactions within these groups, a positive antibody test should then be the starting point for further investigations appropriate to the geographic and alimentary history. Chest radiography in two planes is useful in excluding eosinophilic pulmonary infiltrates that can develop during the larval migration of various helminths (frequently: Ascaris, hookworm, or Strongyloides). Upper abdominal imaging (sonography or CT; figure 3 jpg ppt) can reveal hepatic lesions that substantiate the suspicion of an infection with liver flukes. Electrocardiography should also rule out nonspecific endomyocardial damage that can develop due to eosinophil degranulation products. If no evidence of the origin of the eosinophilia is found, clarification by a specialist is required.

Fever
The geographic history is particularly important in patients with eosinophilia and fever (box 1 and table 3 gif ppt). The commonest cause of fever in travelers returning from schistosomiasis-endemic regions and who present with eosinophilia is Katayama syndrome (e2, e3). About 14 to 90 days after initial contact with schistosomes, this acute form of schistosomiasis produces clinical symptoms comprising nocturnal fever, cough, myalgia, headache and abdominal pain developing as a reaction to the maturing worms. In this infectious phase, therefore, usually no eggs are yet excreted in the urine (bladder schistosomiasis) or stools (intestinal schistosomiasis). Antibody diagnosis may initially also give negative results. In such cases the patient should be re-examined after about four weeks and in severe courses a shorter interval is recommended. If eggs are then found, the schistosome species can be identified from the egg morphology, allowing targeted treatment.

In patients who have not visited a schistosomiasis-endemic region, an infection with Fasciola spp. (liver fluke) may be a possible cause of eosinophilia with subfebrile temperatures (e4). These patients are found to have intrahepatic space occupying lesions in imaging studies and also test positive for antibodies. The patient's further management should then be entrusted to a specialist.

Cutaneous swellings
Periorbital edema in patients with a relevant history—for example following consumption of insufficiently cooked pork or wild boar meat—(table 1) is typical of trichinosis (e5). Blood filtration for trichina larvae should then be performed; a suitable serological screening test is also available (table 4 gif ppt).

If urticaria is present, however, a Katayama syndrome should be considered the prime candidate. Alternating subcutaneous swellings occur in gnathostomiasis (e6) and also in loiasis (Calabar swelling). Patients originally from Central and West Africa can therefore immediately be tested for Loa loa (e7). The latest data from the GeoSentinel Surveillance Network show that filaria - such as Loa loa - can also be transmitted during short trips to endemic regions (22).

Abdominal pain
Abdominal pain associated with eosinophilia suggests the presence of acute disease (table 5 gif ppt). Persons infected with liver flukes (such as Fasciola) experience permanent or intermittent pain. Abdominal pain and elevated laboratory values for transaminases may be a sign of toxocariasis (e8). Anisakiasis (caused mainly by the herring worm Anisakis spp. and the codworm Pseudoterranova spp.) may be associated with acute disease symptoms such as acute abdomen or chronic gastroenteritis with recurrent abdominal pain (e9). These diseases, however, are reported less from the tropics than from Holland, Japan, and the American coastal regions. These worms are transmitted by the consumption of raw or insufficiently heated fish (table 1). A sonographic examination should always be performed if there is eosinophilia and abdominal pain, for example in order to identify any liver lesions. Rare causes such as Ascaris lumbricoides that has migrated into the bile duct can also be detected by ultrasonography.

Elevated transaminase concentrations
Toxocariasis can lead to increased transaminase concentrations (box 2 gif ppt). Infections with Toxocara canis are common worldwide but only rarely become symptomatic.

Diarrhea
Diarrhea frequently occurs after a period spent in the tropics, but helminths are only rarely the cause of acute traveler's diarrhea (e10). If the diarrhea is associated with eosinophilia, the usual screening procedure must be extended. Besides the obligatory screening for Strongyloidiasis, the early stage of trichinosis should also be considered (box 3 gif ppt).

Pulmonary infiltrates
Worm larvae that pass through the lung cause transient pulmonary infiltrates (e11, e12). If this suspicion is present, a stool test should be arranged for about 4 to 6 weeks after the presumed date of infection (table 6 gif ppt). Echinococcosis may manifest in the form of pulmonary, possibly septated cysts on chest radiograph or thoracic CT, and the diagnosis can be substantiated by an antibody test (e13). Imported infections with lung flukes (Paragonimus) have only been described in migrants in a small number of individual cases. The worm cyst with pericystic infiltration appears in the radiograph as an extensive opacity and on CT as an annular structure. The diagnosis is confirmed by the detection of eggs in sputum and stools and by specific antibodies in the serum (e14). Immigrants from South and South East Asia with asthmatic complaints, pulmonary infiltrates, and pronounced eosinophilia in very rare cases have "tropical pulmonary eosinophilia," a special variant of lymphatic filariasis. These patients should be referred to a specialist (e15).

The authors thank Prof. Dr. Dr. Büttner of the Bernard Nocht Institute for Tropical Medicine, Hamburg, for his critical review of the manuscript and for supplying the illustrations.

Conflict of interest statement
The authors declare that no conflict of interest exists according to the guidelines of the International Committee of Medical Journal Editors.

Manuscript received on 29 January 2008, revised version accepted on
30 June 2008.

Translated from the original German by mt-g.


Corresponding author
Prof. Dr. med. Gerd D. Burchard
Sektion Infektiologie und Bernhard-Nocht-Klinik für
Tropenmedizin, I. Medizinische Klinik,
Universitätsklinikum Hamburg-Eppendorf
Martinistr. 52
20246 Hamburg, Germany
gerd.burchard@bni-hamburg.de
1.
Rothenberg ME: Eosinophilia. N Engl J Med. 1998; 338: 1592–600. MEDLINE
2.
Whitty CJM, Mabey DC, Armstrong M, Wright SG, Chiodini PL: Presentation and outcome of 1107 cases of schistosomiasis from Africa diagnosed in a non-endemic country. Trans R Soc Trop Med Hyg 2000; 94: 531–4. MEDLINE
3.
Harries AD, Fryatt R, Walker J, Chiodini PL, Bryceson AD: Schistosomiasis in expatriates returning to Britain from the tropics. Lancet 1986; 11: 86–8. MEDLINE
4.
Libman MD, MacLean JD, Gyorkos TW: Screening for schistosomiasis, filariasis, and strongyloidiasis among expatriates returning from the tropics. Clin Infect Dis 1993; 17: 353–9. MEDLINE
5.
Weller PF: Eosinophilia in travellers. Med Clin North Am 1992; 76: 1413–32. MEDLINE
6.
Harries AD, Myers B, Bhattacharrya D: Eosinophilia in Caucasians returning from the tropics. Trans R Soc Trop Med Hyg 1986; 80: 327–8. MEDLINE
7.
Pardo J, Carranza C, Muro A et al.: Helminth-related eosinophilia in African immigrants, Gran Canaria. Emerg Infect Dis 2006; 12: 1587–9. MEDLINE
8.
Seybold LM, Christiansen D, Barnett ED: Diagnostic evaluation of newly arrived asymptomatic refugees with eosinophilia. Clin Inf Dis 2006; 42: 363–7. MEDLINE
9.
Nutman TB: Evaluation and differential diagnosis of marked, persistent eosinophilia. Immunol Allergy Clin North Am 2007; 27: 529–49. MEDLINE
10.
Brigden ML: A practical workup for eosinophilia. Postgrad Med 1999; 105: 193–210. MEDLINE
11.
Löscher T: Fortschritte in der Immundiagnostik und Chemotherapie der Wurminfektionen. Internist 1983; 24: 610–18.
12.
Wolfe MS: Eosinophilia in the returning traveller. Med Clin North Am 1999; 83: 1019–32. MEDLINE
13.
Whetham J, Day JN, Armstrong M, Chiodini PL, Whitty CJM: Investigation of tropical eosinophilia; assessing a strategy based on geographical area. J Infect 2003; 46: 180–5. MEDLINE
14.
Ansart S, Perez L, Vergely O, Danis M, Bricaire F, Caumes E: Illnesses in travelers returning from the tropics: a prospective study of 622 patients. J Travel Med 2005; 12: 312–8. MEDLINE
15.
Boggild AK, Yohanna S, Keystone JS, Kain KC: Prospective analysis of parasitic infections in Canadian travelers and immigrants. J Travel Med 2006; 13: 138–44. MEDLINE
16.
O'Brien DP, Leder K, Matchett E, Brown GV, Torresi J: Illness in returned travelers and immigrants/refugees: the 6-year experience of two Australian infectious diseases units. J Travel Med 2006; 13: 138–44. MEDLINE
17.
Toovey S, Moerman F, van Gompel A: Special infectious disease risks of expatriates and long-term travelers in tropical countries. Part II: Infections other than malaria. J Travel Med 2007; 14: 50–60. MEDLINE
18.
Löscher T, Saathoff E: Eosinophilia during intestinal infection. Best Pract Res Clin Gastroenterol 2008; 22: 511–36. MEDLINE
19.
Meltzer E, Percik R, Shatzkes J, Sidi Y, Schwartz E: Eosinophilia among returning travelers. A practical approach. Am J Trop Med Hyg 2008; 78: 702–709. MEDLINE
20.
Jelinek T: European Network on Imported Infectious Disease Surveillance. Imported schistosomiasis in Europe: preliminary data for 2007 from TropNetEurop. Euro Surveill 2008 Feb 14;13. pii: 8038. MEDLINE
21.
Freedman DO, Weld LH, Kozarsky PE, Fisk T, Robins R, von Sonnenburg F, Keystone JS, Pandey P, Cetron MS: GeoSentinel Surveillance Network. Spectrum of disease and relation to place of exposure among ill returned travelers. N Engl J Med 2006; 354: 119–30. MEDLINE
22.
Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J: GeoSentinel Surveillance Network. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 2006; 43: 1185–93. MEDLINE
23.
Lipner EM, Law MA, Barnett E et al. for the GeoSentinel Surveillance Network: Filariasis in Travelers Presenting to the GeoSentinel Surveillance Network. PLoS Negl Trop Dis 2007; 1: e88. MEDLINE
e1.
Greiner K, Bettencourt J, Semolic C. Strongyloidiasis: a review and update by case example. Clin Lab Sci 2008; 21: 82–8. MEDLINE
e2.
Gryseels B, Polman K, Clerinx J, Kestens L: Human schistosomiasis. Lancet. 2006; 368: 1106–18. MEDLINE
e3.
Ross AG, Vickers D, Olds GR, Shah SM, McManus DP: Katayama syndrome. Lancet Infect Dis 2007; 7: 218–24. MEDLINE
e4.
Garcia HH, Moro PL, Schantz PM: Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Curr Opin Infect Dis 2007; 20: 489–94. MEDLINE
e5.
Pozio E, Gomez Morales MA, Dupouy-Camet J: Clinical aspects, diagnosis and treatment of trichinellosis. Expert Rev Anti Infect Ther 2003; 1: 471–82. MEDLINE
e6.
Clément-Rigolet MC, Danis M, Caumes E: La gnathostomose, une maladie exotique de plus en plus souvent importée dans les pays occidentaux. Presse Med 2004; 33: 1527–32. MEDLINE
e7.
Boussinesq M: Loiasis. Ann Trop Med Parasitol 2006; 100: 715–31. MEDLINE
e8.
Despommier D: Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 2003; 16: 265–72. MEDLINE
e9.
Seitz HM: Die Anisakidose (Heringswurmkrankheit). Dtsch Arztebl 1990; 87(41): A 3116–20.
e10.
Genta RM: Diarrhea in helminthic infections. Clin Infect Dis 1993;16 Suppl 2: S122–9. MEDLINE
e11.
Chitkara RK, Krishna G: Parasitic pulmonary eosinophilia. Semin Respir Crit Care Med 2006; 27: 171–84. MEDLINE
e12.
Vijayan VK: How to diagnose and manage common parasitic pneumonias. Curr Opin Pulm Med 2007; 13: 218–24. MEDLINE
e13.
Gottstein B, Reichen J: Hydatid lung disease (echinococcosis/hydatidosis).Clin Chest Med 2002; 23: 397–408. MEDLINE
e14.
Kagawa F: Pulmonary paragonimiasis. Semin Respir Infect 1997; 12: 149–58. MEDLINE
e15.
Vijayan VK:Tropical pulmonary eosinophilia: pathogenesis, diagnosis and management.Curr Opin Pulm Med 2007; 13: 428–33. MEDLINE
e16.
Bethony J, Brooker S, Albonico M et al.: Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006; 367: 1521–32. MEDLINE
e17.
Reddy M, Gill SS, Kalkar SR, Wu W, Anderson PJ, Rochon PA: Oral drug therapy for multiple neglected tropical diseases: a systematic review. JAMA 2007; 298: 1911–24. MEDLINE
e18.
Craig P, Ito A: Intestinal cestodes. Curr Opin Infect Dis 2007; 20: 524–32. MEDLINE
e19.
Keiser J, Utzinger J: Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 2008; 299: 1937–48. MEDLINE
e20.
Bruckner DA: Helminthic food-borne infections. Clin Lab Med 1999; 19: 639–60. MEDLINE
e21.
Fried B, Graczyk TK, Tamang L: Food-borne intestinal trematodiases in humans. Parasitol Res 2004; 93: 159–70. MEDLINE
e22.
Macpherson CN, Gottstein B, Geerts S: Parasitic food-borne and water-borne zoonoses. Rev Sci Tech 2000; 19: 240–58. MEDLINE
e23.
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J: Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 2006; 6: 411–25. MEDLINE
Bernhard-Nocht-Institut für Tropenmedizin, Hamburg: Dr. med. Ehrhardt
Sektion Infektiologie und Bernhard-Nocht-Klinik für Tropenmedizin,
I. Medizinische Klinik, Universitätsklinikum Hamburg-Eppendorf, Hamburg: Prof. Dr. med. Burchard
1. Rothenberg ME: Eosinophilia. N Engl J Med. 1998; 338: 1592–600. MEDLINE
2. Whitty CJM, Mabey DC, Armstrong M, Wright SG, Chiodini PL: Presentation and outcome of 1107 cases of schistosomiasis from Africa diagnosed in a non-endemic country. Trans R Soc Trop Med Hyg 2000; 94: 531–4. MEDLINE
3. Harries AD, Fryatt R, Walker J, Chiodini PL, Bryceson AD: Schistosomiasis in expatriates returning to Britain from the tropics. Lancet 1986; 11: 86–8. MEDLINE
4. Libman MD, MacLean JD, Gyorkos TW: Screening for schistosomiasis, filariasis, and strongyloidiasis among expatriates returning from the tropics. Clin Infect Dis 1993; 17: 353–9. MEDLINE
5. Weller PF: Eosinophilia in travellers. Med Clin North Am 1992; 76: 1413–32. MEDLINE
6. Harries AD, Myers B, Bhattacharrya D: Eosinophilia in Caucasians returning from the tropics. Trans R Soc Trop Med Hyg 1986; 80: 327–8. MEDLINE
7. Pardo J, Carranza C, Muro A et al.: Helminth-related eosinophilia in African immigrants, Gran Canaria. Emerg Infect Dis 2006; 12: 1587–9. MEDLINE
8. Seybold LM, Christiansen D, Barnett ED: Diagnostic evaluation of newly arrived asymptomatic refugees with eosinophilia. Clin Inf Dis 2006; 42: 363–7. MEDLINE
9. Nutman TB: Evaluation and differential diagnosis of marked, persistent eosinophilia. Immunol Allergy Clin North Am 2007; 27: 529–49. MEDLINE
10. Brigden ML: A practical workup for eosinophilia. Postgrad Med 1999; 105: 193–210. MEDLINE
11. Löscher T: Fortschritte in der Immundiagnostik und Chemotherapie der Wurminfektionen. Internist 1983; 24: 610–18.
12. Wolfe MS: Eosinophilia in the returning traveller. Med Clin North Am 1999; 83: 1019–32. MEDLINE
13. Whetham J, Day JN, Armstrong M, Chiodini PL, Whitty CJM: Investigation of tropical eosinophilia; assessing a strategy based on geographical area. J Infect 2003; 46: 180–5. MEDLINE
14. Ansart S, Perez L, Vergely O, Danis M, Bricaire F, Caumes E: Illnesses in travelers returning from the tropics: a prospective study of 622 patients. J Travel Med 2005; 12: 312–8. MEDLINE
15. Boggild AK, Yohanna S, Keystone JS, Kain KC: Prospective analysis of parasitic infections in Canadian travelers and immigrants. J Travel Med 2006; 13: 138–44. MEDLINE
16. O'Brien DP, Leder K, Matchett E, Brown GV, Torresi J: Illness in returned travelers and immigrants/refugees: the 6-year experience of two Australian infectious diseases units. J Travel Med 2006; 13: 138–44. MEDLINE
17. Toovey S, Moerman F, van Gompel A: Special infectious disease risks of expatriates and long-term travelers in tropical countries. Part II: Infections other than malaria. J Travel Med 2007; 14: 50–60. MEDLINE
18. Löscher T, Saathoff E: Eosinophilia during intestinal infection. Best Pract Res Clin Gastroenterol 2008; 22: 511–36. MEDLINE
19. Meltzer E, Percik R, Shatzkes J, Sidi Y, Schwartz E: Eosinophilia among returning travelers. A practical approach. Am J Trop Med Hyg 2008; 78: 702–709. MEDLINE
20. Jelinek T: European Network on Imported Infectious Disease Surveillance. Imported schistosomiasis in Europe: preliminary data for 2007 from TropNetEurop. Euro Surveill 2008 Feb 14;13. pii: 8038. MEDLINE
21. Freedman DO, Weld LH, Kozarsky PE, Fisk T, Robins R, von Sonnenburg F, Keystone JS, Pandey P, Cetron MS: GeoSentinel Surveillance Network. Spectrum of disease and relation to place of exposure among ill returned travelers. N Engl J Med 2006; 354: 119–30. MEDLINE
22. Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J: GeoSentinel Surveillance Network. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 2006; 43: 1185–93. MEDLINE
23. Lipner EM, Law MA, Barnett E et al. for the GeoSentinel Surveillance Network: Filariasis in Travelers Presenting to the GeoSentinel Surveillance Network. PLoS Negl Trop Dis 2007; 1: e88. MEDLINE
e1. Greiner K, Bettencourt J, Semolic C. Strongyloidiasis: a review and update by case example. Clin Lab Sci 2008; 21: 82–8. MEDLINE
e2. Gryseels B, Polman K, Clerinx J, Kestens L: Human schistosomiasis. Lancet. 2006; 368: 1106–18. MEDLINE
e3. Ross AG, Vickers D, Olds GR, Shah SM, McManus DP: Katayama syndrome. Lancet Infect Dis 2007; 7: 218–24. MEDLINE
e4. Garcia HH, Moro PL, Schantz PM: Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Curr Opin Infect Dis 2007; 20: 489–94. MEDLINE
e5. Pozio E, Gomez Morales MA, Dupouy-Camet J: Clinical aspects, diagnosis and treatment of trichinellosis. Expert Rev Anti Infect Ther 2003; 1: 471–82. MEDLINE
e6. Clément-Rigolet MC, Danis M, Caumes E: La gnathostomose, une maladie exotique de plus en plus souvent importée dans les pays occidentaux. Presse Med 2004; 33: 1527–32. MEDLINE
e7. Boussinesq M: Loiasis. Ann Trop Med Parasitol 2006; 100: 715–31. MEDLINE
e8. Despommier D: Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 2003; 16: 265–72. MEDLINE
e9. Seitz HM: Die Anisakidose (Heringswurmkrankheit). Dtsch Arztebl 1990; 87(41): A 3116–20.
e10. Genta RM: Diarrhea in helminthic infections. Clin Infect Dis 1993;16 Suppl 2: S122–9. MEDLINE
e11. Chitkara RK, Krishna G: Parasitic pulmonary eosinophilia. Semin Respir Crit Care Med 2006; 27: 171–84. MEDLINE
e12. Vijayan VK: How to diagnose and manage common parasitic pneumonias. Curr Opin Pulm Med 2007; 13: 218–24. MEDLINE
e13. Gottstein B, Reichen J: Hydatid lung disease (echinococcosis/hydatidosis).Clin Chest Med 2002; 23: 397–408. MEDLINE
e14. Kagawa F: Pulmonary paragonimiasis. Semin Respir Infect 1997; 12: 149–58. MEDLINE
e15. Vijayan VK:Tropical pulmonary eosinophilia: pathogenesis, diagnosis and management.Curr Opin Pulm Med 2007; 13: 428–33. MEDLINE
e16. Bethony J, Brooker S, Albonico M et al.: Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006; 367: 1521–32. MEDLINE
e17. Reddy M, Gill SS, Kalkar SR, Wu W, Anderson PJ, Rochon PA: Oral drug therapy for multiple neglected tropical diseases: a systematic review. JAMA 2007; 298: 1911–24. MEDLINE
e18. Craig P, Ito A: Intestinal cestodes. Curr Opin Infect Dis 2007; 20: 524–32. MEDLINE
e19. Keiser J, Utzinger J: Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 2008; 299: 1937–48. MEDLINE
e20. Bruckner DA: Helminthic food-borne infections. Clin Lab Med 1999; 19: 639–60. MEDLINE
e21. Fried B, Graczyk TK, Tamang L: Food-borne intestinal trematodiases in humans. Parasitol Res 2004; 93: 159–70. MEDLINE
e22. Macpherson CN, Gottstein B, Geerts S: Parasitic food-borne and water-borne zoonoses. Rev Sci Tech 2000; 19: 240–58. MEDLINE
e23. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J: Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 2006; 6: 411–25. MEDLINE