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BioMed Research International
Volume 2015, Article ID 573904, 15 pages
http://dx.doi.org/10.1155/2015/573904
Research Article

Surveillance of Food- and Smear-Transmitted Pathogens in European Soldiers with Diarrhea on Deployment in the Tropics: Experience from the European Union Training Mission (EUTM) Mali

1Department of Tropical Medicine at the Bernhard Nocht Institute, German Armed Forces Hospital of Hamburg, 20359 Hamburg, Germany
2Institute for Medical Microbiology, Virology and Hygiene, University Medicine Rostock, 18057 Rostock, Germany
3Sub-Department VI.2, Department A, Military Medical Command, 56070 Koblenz, Germany
4Department II (Veterinary Medicine), Central Institute of the German Armed Forces Medical Service Kiel-Kronshagen, 24119 Kiel-Kronshagen, Germany
5Deployment Health Surveillance Capability/NATO MilMed COE, 80637 Munich, Germany
6Department of Infectious Disease Epidemiology, Bernhard Nocht Institute for Tropical Medicine Hamburg, 20359 Hamburg, Germany

Received 2 December 2014; Revised 5 June 2015; Accepted 8 June 2015

Academic Editor: Pierre Colin

Copyright © 2015 Hagen Frickmann et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. R. Kasper, A. G. Lescano, C. Lucas et al., “Diarrhea outbreak during U.S. military training in El Salvador,” PLoS ONE, vol. 7, no. 7, Article ID e40404, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. S. O. Brockmann, C. Dreweck, C. Wagner-Wiening et al., “Serological and epidemiological analysis of an outbreak of gastroenteritis among military recruits in Germany caused by Cryptosporidium parvum,” Infection, vol. 36, no. 5, pp. 450–457, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Frickmann, N. G. Schwarz, D. F. Wiemer et al., “Food and drinking water hygiene and intestinal protozoa in deployed German soldiers,” European Journal of Microbiology and Immunology, vol. 3, no. 1, pp. 53–60, 2013. View at Publisher · View at Google Scholar
  4. H. Frickmann, N. G. Schwarz, H.-U. Holtherm et al., “Compliance with antimalarial chemoprophylaxis in German soldiers: a 6-year survey,” Infection, vol. 41, no. 2, pp. 311–320, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Wiemer, U. Loderstaedt, H. von Wulffen et al., “Real-time multiplex PCR for simultaneous detection of Campylobacter jejuni, Salmonella, Shigella and Yersinia species in fecal samples,” International Journal of Medical Microbiology, vol. 301, no. 7, pp. 577–584, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Frickmann, D. Dekker, K. Boahen et al., “Increased detection of invasive enteropathogenic bacteria in pre-incubated blood culture materials by real-time PCR in comparison with automated incubation in Sub-Saharan Africa,” Scandinavian Journal of Infectious Diseases, vol. 45, no. 8, pp. 616–622, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. J. J. Verweij, D. Laeijendecker, E. A. T. Brienen, L. Van Lieshout, and A. M. Polderman, “Detection of Cyclospora cayetanensis in travellers returning from the tropics and subtropics using microscopy and real-time PCR,” International Journal of Medical Microbiology, vol. 293, no. 2-3, pp. 199–202, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. J. J. Verweij, R. A. Blangé, K. Templeton et al., “Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR,” Journal of Clinical Microbiology, vol. 42, no. 3, pp. 1220–1223, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. H. G. M. Niesters, “Quantitation of viral load using real-time amplification techniques,” Methods, vol. 25, no. 4, pp. 419–429, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Frickmann, K. Tenner-Racz, P. Eggert et al., “Influence of parasite density and sample storage time on the reliability of entamoeba histolytica-specific PCR from formalin-fixed and paraffin-embedded tissues,” Diagnostic Molecular Pathology, vol. 22, no. 4, pp. 236–244, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. G. P. Richards, M. A. Watson, R. L. Fankhauser, and S. S. Monroe, “Genogroup I and II noroviruses detected in stool samples by real-time reverse transcription-PCR using highly degenerate universal primers,” Applied and Environmental Microbiology, vol. 70, no. 12, pp. 7179–7184, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Kroneman, H. Vennema, K. Deforche et al., “An automated genotyping tool for enteroviruses and noroviruses,” Journal of Clinical Virology, vol. 51, no. 2, pp. 121–125, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. J.-L. A. N. Murk, E. R. Heddema, D. L. J. Hess, J. A. Bogaards, C. M. J. E. Vandenbroucke-Grauls, and Y. J. Debets-Ossenkopp, “Enrichment broth improved detection of extended-spectrum-beta-lactamase-producing bacteria in throat and rectal surveillance cultures of samples from patients in intensive care units,” Journal of Clinical Microbiology, vol. 47, no. 6, pp. 1885–1887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. T.-D. Huang, P. Bogaerts, C. Berhin, A. Guisset, and Y. Glupczynski, “Evaluation of brilliance ESBL agar, a novel chromogenic medium for detection of extended-spectrum-beta-lactamase-producing Enterobacteriaceae,” Journal of Clinical Microbiology, vol. 48, no. 6, pp. 2091–2096, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Ongut, A. E. Daloglu, B. O. Baysan et al., “Evaluation of a chromogenic medium for detection of extended-spectrum-beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae strains,” Clinical Laboratory, vol. 60, no. 7, pp. 1213–1215, 2014. View at Publisher · View at Google Scholar
  16. H. Frickmann, M. Christner, M. Donat et al., “Rapid discrimination of Haemophilus influenzae, H. parainfluenzae, and H. haemolyticus by fluorescence in situ hybridization (FISH) and two matrix-assisted laser-desorption-ionization time-of-flight mass spectrometry (MALDI-TOF-MS) platforms,” PLoS ONE, vol. 8, no. 4, Article ID e63222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. A. K. da Silva, J.-C. Le Saux, S. Parnaudeau, M. Pommepuy, M. Elimelech, and F. S. Le Guyader, “Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II,” Applied and Environmental Microbiology, vol. 73, no. 24, pp. 7891–7897, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Svraka, E. Duizer, H. Vennema et al., “Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005,” Journal of Clinical Microbiology, vol. 45, no. 5, pp. 1389–1394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Connor, C. K. Porter, B. Swierczewski, and M. S. Riddle, “Diarrhoea during military deployment: current concepts and future directions,” Current Opinion in Infectious Diseases, vol. 25, no. 5, pp. 546–554, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. I. N. Okeke, “Diarrheagenic Escherichia coli in sub-Saharan Africa: status, uncertainties and necessities,” Journal of Infection in Developing Countries, vol. 3, no. 11, pp. 817–842, 2009. View at Google Scholar · View at Scopus
  21. R. E. Black, “Pathogens that cause travelers' diarrhea in Latin America and Africa,” Reviews of infectious diseases, vol. 8, supplement 2, pp. S131–S135, 1986. View at Publisher · View at Google Scholar · View at Scopus
  22. R. E. Black, “Epidemiology of travelers' diarrhea and relative importance of various pathogens,” Reviews of Infectious Diseases, vol. 12, supplement 1, pp. S73–S79, 1990. View at Publisher · View at Google Scholar · View at Scopus
  23. C. A. Hart, R. M. Batt, and J. R. Saunders, “Diarrhoea caused by Escherichia coli,” Annals of Tropical Paediatrics, vol. 13, no. 2, pp. 121–131, 1993. View at Google Scholar · View at Scopus
  24. S. L. Becker, J. Vogt, S. Knopp et al., “Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests,” BMC Infectious Diseases, vol. 13, article 37, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Kundig, P. Chevalley, and D. Genné, “Norovirus gastroenteritis: frequent, often epidemic, with potentially severe complications,” Revue Medicale Suisse, vol. 9, no. 401, pp. 1806–1808, 2013 (French). View at Google Scholar · View at Scopus
  26. L. Barclay, G. Park, E. Vega et al., “Infection control for norovirus,” Clinical Microbiology and Infection, vol. 20, no. 8, pp. 731–740, 2014. View at Publisher · View at Google Scholar
  27. M. Iturriza-Gómara and B. Lopman, “Norovirus in healthcare settings,” Current Opinion in Infectious Diseases, vol. 27, no. 5, pp. 437–443, 2014. View at Publisher · View at Google Scholar
  28. P. Godoy, G. Ferrrus, N. Torner et al., “High incidence of norovirus GII.4 outbreaks in hospitals and nursing homes in Catalonia (Spain), 2010-2011,” Epidemiology and Infection, vol. 43, no. 4, pp. 725–733, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. F. R. Lin, Y. H. Shen, C. W. Fang et al., “Incidence of and factors associated with false positives in laboratory diagnosis of norovirus infection by amplification of the RNA-dependent RNA polymerase gene,” PLoS ONE, vol. 9, no. 9, Article ID e109876, 2014. View at Publisher · View at Google Scholar
  30. M. S. Riddle, J. W. Sanders, S. D. Putnam, and D. R. Tribble, “Incidence, etiology, and impact of diarrhea among long-term travelers (US military and similar populations): a systematic review,” American Journal of Tropical Medicine and Hygiene, vol. 74, no. 5, pp. 891–900, 2006. View at Google Scholar · View at Scopus
  31. H. K. de Jong, C. M. Parry, T. van der Poll, and W. J. Wiersinga, “Host-pathogen interaction in invasive salmonellosis,” PLoS Pathogens, vol. 8, no. 10, Article ID e1002933, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Gryseels and P. L. Gigase, “The prevalence of intestinal parasites in two suburbs of Kinshasa (Zaire) and their relation to domestic water supplies,” Tropical and Geographical Medicine, vol. 37, no. 2, pp. 129–132, 1985. View at Google Scholar · View at Scopus
  33. R. Wumba, A. Enache-Angoulvant, M. Develoux et al., “Prevalence of opportunistic digestive parasitic infections in Kinshasa, Democratic Republic of Congo. Results of a preliminary study in 50 aids patients,” Medecine Tropicale, vol. 67, no. 2, pp. 145–148, 2007. View at Google Scholar · View at Scopus
  34. M. A. Babiker, M. S. M. Ali, and E. S. Ahmed, “Frequency of intestinal parasites among food-handlers in Khartoum, Sudan,” Eastern Mediterranean Health Journal, vol. 15, no. 5, pp. 1098–1104, 2009. View at Google Scholar · View at Scopus
  35. H. A. Saeed and H. H. Hamid, “Bacteriological and parasitological assessment of food handlers in the Omdurman area of Sudan,” Journal of Microbiology, Immunology and Infection, vol. 43, no. 1, pp. 70–73, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Bowen-Jones, “Infection and cross-infection in a paediatric gastro-enteritis unit,” Curationis, vol. 12, no. 3-4, pp. 30–33, 1989. View at Google Scholar · View at Scopus
  37. C. N. Kamalaratnam, G. Kang, C. Kirubakaran et al., “A prospective study of nosocomial enteric pathogen acquisition in hospitalized children in South India,” Journal of Tropical Pediatrics, vol. 47, no. 1, pp. 46–49, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Lopez-Gigosos, M. Campins, M. J. Calvo et al., “Effectiveness of the WC/rBS oral cholera vaccine in the prevention of traveler's diarrhea: a prospective cohort study,” Human Vaccines and Immunotherapeutics, vol. 9, no. 3, pp. 692–698, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Parés, M. Comas, D. Dorcaratto et al., “Adaptation and validation of the Bristol scale stool form translated into the Spanish language among health professionals and patients,” Revista Espanola de Enfermedades Digestivas, vol. 101, no. 5, pp. 312–316, 2009. View at Google Scholar · View at Scopus
  40. B. P. Chumpitazi, M. M. Lane, D. I. Czyzewski, E. M. Weidler, P. R. Swank, and R. J. Shulman, “Creation and initial evaluation of a stool form scale for children,” The Journal of Pediatrics, vol. 157, no. 4, pp. 594–597, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. M. M. Lane, D. I. Czyzewski, B. P. Chumpitazi, and R. J. Shulman, “Reliability and validity of a modified bristol stool form scale for children,” The Journal of Pediatrics, vol. 159, no. 3, pp. 437.e1–441.e1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. P. Martinez and G. R. de Azevedo, “The Bristol stool form scale: its translation to Portuguese, cultural adaptation and validation,” Revista Latino-Americana de Enfermagem, vol. 20, no. 3, pp. 583–589, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Blessmann, H. Buss, P. A. T. Nu et al., “Real-time PCR for detection and differentiation of Entamoeba histolytica and Entamoeba dispar in fecal samples,” Journal of Clinical Microbiology, vol. 40, no. 12, pp. 4413–4417, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. J. A. Platts-Mills, J. Gratz, E. Mduma et al., “Association between stool enteropathogen quantity and disease in Tanzanian children using TaqMan Array Cards: a nested case-control study,” American Journal of Tropical Medicine and Hygiene, vol. 90, no. 1, pp. 133–138, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Lindsay, J. B. Ochieng, U. N. Ikumapayi et al., “Quantitative PCR for detection of Shigella improves ascertainment of Shigella burden in children with moderate-to-severe diarrhea in low-income countries,” Journal of Clinical Microbiology, vol. 51, no. 6, pp. 1740–1746, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Yavzori, N. Uriel, N. Porat et al., “Development of molecular tests for rapid detection of enteropathogens,” Harefuah, vol. 138, no. 9, pp. 758–805, 2000 (Hebrew). View at Google Scholar · View at Scopus
  47. I. Zollner-Schwetz and R. Krause, “Therapy of acute gastroenteritis: role of antibiotics,” Clinical Microbiology and Infection, 2015. View at Publisher · View at Google Scholar
  48. P. Connor and M. J. Farthing, “Travellers' diarrhoea: a military problem?” Journal of the Royal Army Medical Corps, vol. 145, no. 2, pp. 95–101, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. C. D. Ericsson, “Travellers' diarrhoea,” International Journal of Antimicrobial Agents, vol. 21, no. 2, pp. 116–124, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Layer and V. Andresen, “Review article: rifaximin, a minimally absorbed oral antibacterial, for the treatment of travellers' diarrhoea,” Alimentary Pharmacology and Therapeutics, vol. 31, no. 11, pp. 1155–1164, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. K. L. Hopkins, S. Mushtaq, J. F. Richardson et al., “In vitro activity of rifaximin against clinical isolates of Escherichia coli and other enteropathogenic bacteria isolated from travellers returning to the UK,” International Journal of Antimicrobial Agents, vol. 43, no. 5, pp. 431–437, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Steffen, D. R. Hill, and H. L. DuPont, “Traveler’s diarrhea: a clinical review,” Journal of the American Medical Association, vol. 313, no. 1, pp. 71–80, 2015. View at Publisher · View at Google Scholar
  53. G. Peirano, K. B. Laupland, D. B. Gregson, and J. D. D. Pitout, “Colonization of returning travelers with CTX-M-producing Escherichia coli,” Journal of Travel Medicine, vol. 18, no. 5, pp. 299–303, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Paltansing, J. A. Vlot, M. E. M. Kraakman et al., “Extended-spectrum β-lactamase-producing enterobacteriaceae among travelers from the Netherlands,” Emerging Infectious Diseases, vol. 19, no. 8, pp. 1206–1213, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Lübbert, L. Straube, C. Stein et al., “Colonization with extended-spectrum beta-lactamase-producing and carbapenemase-producing Enterobacteriaceae in international travelers returning to Germany,” International Journal of Medical Microbiology, vol. 305, no. 1, pp. 148–156, 2015. View at Publisher · View at Google Scholar
  56. S. M. Belderok, A. van den Hoek, J. A. Kint, M. F. Schim van der Loeff, and G. J. B. Sonder, “Incidence, risk factors and treatment of diarrhoea among Dutch travellers: reasons not to routinely prescribe antibiotics,” BMC Infectious Diseases, vol. 11, article 295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Kantele, “A call to restrict prescribing antibiotics for travellers' diarrhea—travel medicine practitioners can play an active role in preventing the spread of antimicrobial resistance,” Travel Medicine and Infectious Disease, vol. 13, no. 3, pp. 213–214, 2015. View at Publisher · View at Google Scholar
  58. S. Vandersee, M. Hannemann, F. Herrmann, and P. Becker, “Multiresistente erreger bei patienten des deutschen Bundeswehr-Einsatzlazaretts in Masar-e Scharif,” Hygiene & Medizin, vol. 36, pp. 384–392, 2011 (German). View at Google Scholar
  59. M. Li, R. D. Specian, R. D. Berg, and E. A. Deitch, “Effects of protein malnutrition and endotoxin on the intestinal mucosal barrier to the translocation of indigenous flora in mice,” Journal of Parenteral and Enteral Nutrition, vol. 13, no. 6, pp. 572–578, 1989. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Vaishnavi, “Translocation of gut flora and its role in sepsis,” Indian Journal of Medical Microbiology, vol. 31, no. 4, pp. 334–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Gatt, B. S. Reddy, and J. MacFie, “Review article: bacterial translocation in the critically ill—evidence and methods of prevention,” Alimentary Pharmacology and Therapeutics, vol. 25, no. 7, pp. 741–757, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. M. J. Matar, A. Safdar, and K. V. I. Rolston, “Relationship of colonization with vancomycin-resistant enterococci and risk of systemic infection in patients with cancer,” Clinical Infectious Diseases, vol. 42, no. 10, pp. 1506–1507, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. D. M. Weinstock, M. Conlon, C. Iovino et al., “Colonization, bloodstream infection, and mortality caused by vancomycin-resistant enterococcus early after allogeneic hematopoietic stem cell transplant,” Biology of Blood and Marrow Transplantation, vol. 13, no. 5, pp. 615–621, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. J. B. Bossaer, P. D. Hall, and E. Garrett-Mayer, “Incidence of vancomycin-resistant enterococci (VRE) infection in high-risk febrile neutropenic patients colonized with VRE,” Supportive Care in Cancer, vol. 19, no. 2, pp. 231–237, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. E. J. Haas, T. E. Zaoutis, P. Prasad, M. Li, and S. E. Coffin, “Risk factors and outcomes for vancomycin-resistant Enterococcus bloodstream infection in children,” Infection Control and Hospital Epidemiology, vol. 31, no. 10, pp. 1038–1042, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Ubeda, Y. Taur, R. R. Jenq et al., “Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans,” The Journal of Clinical Investigation, vol. 120, no. 12, pp. 4332–4341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. K. F. Bodmann and B. Grabein, “Expertenkommission der Paul-Ehrlich-Gesellschaft für Chemotherapie e.V. Empfehlungen zur kalkulierten parenteralen Initialtherapie bakterieller Erkrankungen bei Erwachsenen. Update 2010,” Chemotherapy Journal, vol. 19, pp. 179–255, 2010 (German). View at Google Scholar
  68. A. F. Sadeghabadi, A. Ajami, R. Fadaei et al., “Widespread antibiotic resistance of diarrheagenic Escherichia coli and Shigella species,” Journal of Research in Medical Sciences, vol. 19, supplement 1, pp. S51–S55, 2014. View at Google Scholar · View at Scopus