We use cookies to improve your experience. By continuing to browse this site, you accept our cookie policy.×
Skip main navigation
Aging Health
Bioelectronics in Medicine
Biomarkers in Medicine
Breast Cancer Management
CNS Oncology
Colorectal Cancer
Concussion
Epigenomics
Future Cardiology
Future Medicine AI
Future Microbiology
Future Neurology
Future Oncology
Future Rare Diseases
Future Virology
Hepatic Oncology
HIV Therapy
Immunotherapy
International Journal of Endocrine Oncology
International Journal of Hematologic Oncology
Journal of 3D Printing in Medicine
Lung Cancer Management
Melanoma Management
Nanomedicine
Neurodegenerative Disease Management
Pain Management
Pediatric Health
Personalized Medicine
Pharmacogenomics
Regenerative Medicine

Parasitic infections in travelers and immigrants: part II helminths and ectoparasites

    Francesca F Norman

    Tropical Medicine & Clinical Parasitology, Infectious Diseases Department, Ramon y Cajal Hospital, Ctra. De Colmenar Km 9.1, 28034 Madrid, Spain

    ,
    Begoña Monge-Maillo

    Tropical Medicine & Clinical Parasitology, Infectious Diseases Department, Ramon y Cajal Hospital, Ctra. De Colmenar Km 9.1, 28034 Madrid, Spain

    ,
    Ángela Martínez-Pérez

    Tropical Medicine & Clinical Parasitology, Infectious Diseases Department, Ramon y Cajal Hospital, Ctra. De Colmenar Km 9.1, 28034 Madrid, Spain

    ,
    Jose A Perez-Molina

    Tropical Medicine & Clinical Parasitology, Infectious Diseases Department, Ramon y Cajal Hospital, Ctra. De Colmenar Km 9.1, 28034 Madrid, Spain

    &
    Rogelio López-Vélez

    *Author for correspondence:

    E-mail Address: rogelio.lopezvelez@salud.madrid.org

    Tropical Medicine & Clinical Parasitology, Infectious Diseases Department, Ramon y Cajal Hospital, Ctra. De Colmenar Km 9.1, 28034 Madrid, Spain

    Published Online:https://doi.org/10.2217/fmb.14.106

    ABSTRACT 

    Travel and migration contribute to the emergence of certain parasites which may be imported into nonendemic areas. Noncontrolled importation of food products and animals may also contribute to the diagnosis of infections caused by helminths in nonendemic countries. Some helminth infections such as strongyloidiasis may be life-threatening, especially in immunocompromised patients, and outcome depends on correct diagnosis and treatment. Other helminth infections are neglected tropical diseases associated with chronic disease and/or disability. Major challenges concern the development of improved diagnostic techniques, safer and more effective drug therapies and identification of markers of response to treatment. The study of these imported infections in travelers and immigrants may provide opportunities for research which may not be readily available in resource-poor endemic countries. Updated reviews and guidelines are necessary as new data become available. The second part of this review focuses on infections in travelers and immigrants caused by helminths and ectoparasites.

    Papers of special note have been highlighted as: • of interest; •• of considerable interest

    References

    • 1 UNTWO. Tourism Highlights (2012 Edition). World Tourism Organization. http://dtxtq4w60xqpw.cloudfront.net/sites/all/files/pdf/unwto_highlights13_en_hr_0.pdf.
    • 2 World Migration Report 2013 http://publications.iom.int/bookstore/free/WMR2013_EN.pdf.
    • 3 Utzinger J, Becker SL, Knopp S et al. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med. Wkly 142, w13727 (2012).
    • 4 Monge-Maillo B, Jimenez BC, Perez-Molina JA et al. Imported infectious diseases in mobile populations, Spain. Emerg. Infect. Dis. 15, 1745–1752 (2009).
    • 5 Norman FF, Perez de Ayala A, Perez-Molina JA, Monge-Maillo B, Zamarron P, Lopez-Velez R. Neglected tropical diseases outside the tropics. PLoS Negl. Trop. Dis. 4, e762 (2010).
    • 6 Zamarron Fuertes P, Perez-Ayala A, Perez Molina JA et al. Clinical and epidemiological characteristics of imported infectious diseases in Spanish travelers. J. Travel Med. 17, 303–309 (2010).
    • 7 Harvey K, Esposito DH, Han P et al. Centers for Disease Control and Prevention (CDC): Surveillance for travel-related disease ‐‐ GeoSentinel Surveillance System, United States, 1997–2011. MMWR Surveill. Summ. 62, 1–23 (2013).
    • 8 Monge-Maillo B, Norman FF, Perez-Molina JA, Navarro M, Diaz-Menendez M, Lopez-Velez R. Travelers visiting friends and relatives (VFR) and imported infectious disease: travelers, immigrants or both? A comparative analysis. Travel Med. Infect. Dis. 12, 88–94 (2014).
    • 9 Leder K, Tong S, Weld L et al. GeoSentinel Surveillance Network: illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin. Infect. Dis. 43, 1185–1193 (2006).
    • 10 Norman FF, Monge-Maillo B, Martínez-Pérez A, Perez-Molina JA, López-Vélez R. Parasitic infections in travelers and immigrants: part I Protozoa. Future Microbiol. 10(1), 69–86 (2014).
    • 11 WHO. Deworming for health and development. Report of the third global meeting of the partners for parasite control. http://whqlibdoc.who.int/hq/2005/who_cds_cpe_pvc_2005.14.pdf.
    • 12 Boggild AK, Yohanna S, Keystone JS, Kain KC. Prospective analysis of parasitic infections in Canadian travelers and immigrants. J. Travel Med. 13, 138–144 (2006).
    • 13 McCarthy AE, Weld LH, Barnett ED et al. GeoSentinel Surveillance Network: Spectrum of illness in international migrants seen at GeoSentinel clinics in 1997–2009, part 2: migrants resettled internationally and evaluated for specific health concerns. Clin. Infect. Dis. 56, 925–933 (2013).
    • 14 ten Hove RJ, van Esbroeck M, Vervoort T, van den Ende J, van Lieshout L, Verweij JJ. Molecular diagnostics of intestinal parasites in returning travellers. Eur. J. Clin. Microbiol. Infect. Dis. 28, 1045–1053 (2009).
    • 15 Schar F, Trostdorf U, Giardina F et al. Strongyloides stercoralis: Global Distribution and Risk Factors. PLoS Negl. Trop. Dis. 7, e2288 (2013).
    • 16 Verweij JJ, Canales M, Polman K et al. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg. 103, 342–346 (2009).
    • 17 Treatment Guidelines. Drugs for Parasitic Infections. The Medical Letter, Inc., Rochelle, New York (2013). http://gorgas.dom.uab.edu/syllabus/2014/03_Parasites/RxParasitesMedicalLetter2013.pdf.•• Recommendations for the treatment of the main parasitic diseases
    • 18 Adegnika AA, Zinsou JF, Issifou S et al. Efficacy of single versus repeated dose albendazole to treat Ascaris lumbricoides, Trichuris trichiura and hookworm infection: A randomized controlled assessor-blinded clinical trial. Antimicrob. Agents Chemother. 58, 2535–40 (2014).
    • 19 Lipner EM, Law MA, Barnett E et al. GeoSentinel Surveillance Network: Filariasis in travelers presenting to the GeoSentinel Surveillance Network. PLoS Negl. Trop. Dis. 1, e88 (2007).
    • 20 Taylor MJ, Hoerauf A, Bockarie M. Lymphatic filariasis and onchocerciasis. Lancet 376, 1175–1185 (2010).
    • 21 Debrah AY, Mand S, Marfo-Debrekyei Y et al. Reduction in levels of plasma vascular endothelial growth factor-A and improvement in hydrocele patients by targeting endosymbiotic Wolbachia sp. in Wuchereria bancrofti with doxycycline. Am. J. Trop. Med. Hyg. 80, 956–963 (2009).
    • 22 Genchi C, Kramer LH, Sassera D, Bandi C. Wolbachia and its implications for the immunopathology of filariasis. Endocr. Metab. Immune Disord. Drug Targets. 12, 53–56 (2012).
    • 23 Hoerauf A, Pfarr K, Mand S, Debrah AY, Specht S. Filariasis in Africa ‐‐ treatment challenges and prospects. Clin Microbiol Infect. 17, 977–985 (2011).
    • 24 Burbelo PD, Leahy HP, Iadarola MJ, Nutman TB. A four-antigen mixture for rapid assessment of Onchocerca volvulus infection. PLoS Negl. Trop. Dis. 3, e438 (2009).
    • 25 Geary TG, Mackenzie CD. Progress and challenges in the discovery of macrofilaricidal drugs. Expert Rev. Anti Infect. Ther. 9, 681–695 (2011).
    • 26 Antinori S, Schifanella L, Million M et al. Imported Loa loa filariasis: three cases and a review of cases reported in non-endemic countries in the past 25 years. Int. J. Infect. Dis. 16, e649–e662 (2012).
    • 27 Diaz-Menendez M, Norman F, Monge-Maillo B, Perez-Molina JA, Lopez-Velez R. Filariasis in clinical practice. Enferm. Infecc. Microbiol Clin. 29, 27–37 (2011).
    • 28 Jimenez M, Gonzalez LM, Carranza C et al. Detection and discrimination of Loa loa, Mansonella perstans and Wuchereria bancrofti by PCR-RFLP and nested-PCR of ribosomal DNA ITS1 region. Exp. Parasitol. 127, 282–286 (2011).
    • 29 Budke CM, Carabin H, Ndimubanzi PC et al. A systematic review of the literature on cystic echinococcosis frequency worldwide and its associated clinical manifestations. Am. J. Trop. Med. Hyg. 88, 1011–1027 (2013).
    • 30 Diaz-Menendez M, Perez-Molina JA, Norman FF et al. Management and outcome of cardiac and endovascular cystic echinococcosis. PLoS Negl. Trop. Dis. 6, e1437 (2012).
    • 31 WHO Informal Working Group on Echinococcosis. Guidelines for treatment of cystic and alveolar echinococcosis in humans. Bull. World Health Organ. 74, 231–242 (1996).
    • 32 Ito A, Nakao M, Wandra T. Human Taeniasis and cysticercosis in Asia. Lancet 362, 1918–1920 (2003).
    • 33 Zammarchi L, Strohmeyer M, Bartalesi F et al. for COHEMI Project Study Group. Epidemiology and management of cysticercosis and Taenia solium taeniasis in Europe, systematic review 1990–2011. PLoS ONE 8, e69537 (2013).• Comprehensive review of Taenia solium infection in Europe
    • 34 Bruno E, Bartoloni A, Zammarchi L et al. for COHEMI Project Study Group. Epilepsy and neurocysticercosis in Latin America: a systematic review and meta-analysis. PLoS Negl. Trop. Dis. 7, e2480 (2013).
    • 35 Gabriel S, Blocher J, Dorny P et al. Added value of antigen ELISA in the diagnosis of neurocysticercosis in resource poor settings. PLoS Negl. Trop. Dis. 6, e1851 (2012).
    • 36 Leder K, Torresi J, Libman MD et al. for GeoSentinel Surveillance Network. GeoSentinel surveillance of illness in returned travelers, 2007–2011. Ann. Intern. Med. 158, 456–468 (2013).
    • 37 Clerinx J, Van Gompel A. Schistosomiasis in travellers and migrants. Travel Med. Infect. Dis. 9, 6–24 (2011).
    • 38 Leshem E, Meltzer E, Marva E, Schwartz E. Travel-related schistosomiasis acquired in Laos. Emerg. Infect. Dis. 15, 1823–1826 (2009).
    • 39 Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA. Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl. Trop. Dis. 5, e1396 (2011).
    • 40 Cnops L, Soentjens P, Clerinx J, Van Esbroeck M. A Schistosoma haematobium-specific real-time PCR for diagnosis of urogenital schistosomiasis in serum samples of international travelers and migrants. PLoS Negl. Trop. Dis. 7, e2413 (2013).
    • 41 Van Gool T, Vetter H, Vervoort T, Doenhoff MJ, Wetsteyn J, Overbosch D. Serodiagnosis of imported schistosomiasis by a combination of a commercial indirect hemagglutination test with Schistosoma mansoni adult worm antigens and an enzyme-linked immunosorbent assay with S. mansoni egg antigens. J. Clin. Microbiol. 40, 3432–3437 (2002).
    • 42 Logan S, Armstrong M, Moore E et al. Acute schistosomiasis in travelers: 14 years’ experience at the Hospital for Tropical Diseases, London. Am. J. Trop. Med. Hyg. 88, 1032–1034 (2013).
    • 43 Olliaro PL, Vaillant MT, Belizario VJ et al. A multicentre randomized controlled trial of the efficacy and safety of single-dose praziquantel at 40 mg/kg vs. 60 mg/kg for treating intestinal schistosomiasis in the Philippines, Mauritania, Tanzania and Brazil. PLoS Negl. Trop. Dis. 5, e1165 (2011).
    • 44 Gryseels B, Mbaye A, De Vlas SJ et al. Are poor responses to praziquantel for the treatment of Schistosoma mansoni infections in Senegal due to resistance? An overview of the evidence. Trop. Med. Int. Health 6, 864–873 (2001).
    • 45 Helleberg M, Thybo S. High rate of failure in treatment of imported schistosomiasis. J. Travel Med. 17, 94–99 (2010).
    • 46 Li HJ, Wang W, Qu GL et al. Effect of the in vivo activity of dihydroartemisinin against Schistosoma mansoni infection in mice. Parasitol. Res. 110, 1727–1732 (2012).
    • 47 Perez del Villar L, Burguillo FJ, Lopez-Aban J, Muro A. Systematic review and meta-analysis of artemisinin based therapies for the treatment and prevention of schistosomiasis. PLoS ONE 7, e45867 (2012).
    • 48 Furst T, Duthaler U, Sripa B, Utzinger J, Keiser J. Trematode infections: liver and lung flukes. Infect. Dis. Clin. North Am. 26, 399–419 (2012).
    • 49 Lopez-Velez R, Dominguez-Castellano A, Garron C. Successful treatment of human fascioliasis with triclabendazole. Eur. J. Clin. Microbiol. Infect. Dis. 18, 525–526 (1999).
    • 50 Jensenius M, Flaegstad T, Stenstad T et al. Fascioliasis imported to Norway. Scand. J. Infect. Dis. 37, 534–537 (2005).
    • 51 Intapan PM, Khotsri P, Kanpittaya J, Chotmongkol V, Sawanyawisuth K, Maleewong W. Immunoblot diagnostic test for neurognathostomiasis. Am. J. Trop. Med. Hyg. 83, 927–929 (2010).
    • 52 Janwan P, Intapan PM, Yamasaki H et al. Application of recombinant Gnathostoma spinigerum matrix metalloproteinase-like protein for serodiagnosis of human gnathostomiasis by immunoblotting. Am. J. Trop. Med. Hyg 89, 63–67 (2013).
    • 53 Gottstein B, Pozio E, Nockler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin. Microbiol. Rev. 22, 127–145 (2009).• Comprehensive review of Trichinella sp. infections.
    • 54 Turrientes MC, Perez de Ayala A, Norman F et al. Visceral larva migrans in immigrants from latin america. Emerg. Infect. Dis. 17, 1263–1265 (2011).
    • 55 Lederman ER, Weld LH, Elyazar IR et al. for GeoSentinel Surveillance Network. Dermatologic conditions of the ill returned traveler: an analysis from the GeoSentinel Surveillance Network. Int. J. Infect. Dis. 12, 593–602 (2008).• Informative article on cutaneous illness in returning travelers.
    • 56 Ansart S, Perez L, Jaureguiberry S, Danis M, Bricaire F, Caumes E. Spectrum of dermatoses in 165 travelers returning from the tropics with skin diseases. Am. J. Trop. Med. Hyg. 76, 184–186 (2007).
    • 57 Hannam P, Khairnar K, Downey J, Powis J, Ralevski F, Pillai DR. Cutaneous myiasis in traveler returning from Ethiopia. Emerg. Infect. Dis. 17, 2385–2386 (2011).
    • 58 Puente S, Otranto D, Panadero R et al. First diagnosis of an imported human myiasis caused by Hypoderma sinense (Diptera: Oestridae), detected in a European traveler returning from India. J. Travel Med. 17, 419–423 (2010).
    • 59 Davis RF, Johnston GA, Sladden MJ. Recognition and management of common ectoparasitic diseases in travelers. Am. J. Clin. Dermatol. 10, 1–8 (2009).
    • 60 Shimose L, Munoz-Price LS. Diagnosis, prevention, and treatment of scabies. Curr. Infect. Dis. Rep. 15, 426–431 (2013).
    • 61 Goldust M, Rezaee E, Raghifar R, Hemayat S. Treatment of scabies: the topical ivermectin vs. permethrin 2.5% cream. Ann. Parasitol. 59, 79–84 (2013).