Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests

BMC Infectious Diseases

Jürg Utzinger^1,11  François Chappuis⁴  Eliézer K N’Goran^1,12  Lisette van Lieshout^1,14  Pascal Lutumba³  Marleen Boelaert⁸  Michael A Miles⁷  Fransiska Meyanti²  Suman Rijal^1,13  Moussa Sacko⁵  Emmanuel Bottieau⁹  Jan Jacobs⁹  Cedric P Yansouni⁹  Lutz von Müller^1,15  Hanspeter Marti¹  Katja Polman^1,10  David C Warhurst⁷  Marcus Panning⁶  Stefanie Knopp^1,11  Jürg Vogt^1,11  Sören L Becker^1,15 

[1]Department of Medical Services and Diagnostic, Swiss Tropical and Public Health Institute, Basel, Switzerland

[2]Centre for Tropical Medicine, Faculty of Medicine, Gadjah Mada University, Yogyakarta, Indonesia

[3]Université de Kinshasa, Kinshasa, Democratic Republic of the Congo

[4]Division of Humanitarian and International Medicine, Geneva University Hospitals, Geneva, Switzerland

[5]Institut National de Recherche en Santé Publique, , Bamako, Mali

[6]Department of Virology, University of Freiburg, Freiburg, Germany

[7]Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom

[8]Department of Public Health, Institute of Tropical Medicine, Antwerp, Belgium

[9]Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp, Belgium

[10]Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium

[11]University of Basel, Basel, Switzerland

[12]Département Environnement et Santé, Centre Suisse de Recherches Scientifiques en Côte d’Ivoire, Abidjan, Côte d’Ivoire

[13]Department of Internal Medicine, B P Koirala Institute of Health Sciences, Dharan, Nepal

[14]Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands

[15]Institute of Medical Microbiology and Hygiene, University of Saarland Hospital, Homburg/Saar, Germany

关键词: Virus;    Persistent diarrhoea;    Intestinal protozoa;    Helminths;    Gastroenterology;    Digestive disorders;    Diagnosis;    Clinical microbiology;    Bacteria;   

Others  :  1158517
DOI  :  10.1186/1471-2334-13-37

 received in 2012-09-17, accepted in 2013-01-14,  发布年份 2013

【 摘 要 】

Background

Persistent digestive disorders account for considerable disease burden in the tropics. Despite advances in understanding acute gastrointestinal infections, important issues concerning epidemiology, diagnosis, treatment and control of most persistent digestive symptomatologies remain to be elucidated. Helminths and intestinal protozoa are considered to play major roles, but the full extent of the aetiologic spectrum is still unclear. We provide an overview of pathogens causing digestive disorders in the tropics and evaluate available reference tests.

Methods

We searched the literature to identify pathogens that might give rise to persistent diarrhoea, chronic abdominal pain and/or blood in the stool. We reviewed existing laboratory diagnostic methods for each pathogen and stratified them by (i) microscopy; (ii) culture techniques; (iii) immunological tests; and (iv) molecular methods. Pathogen-specific reference tests providing highest diagnostic accuracy are described in greater detail.

Results

Over 30 pathogens may cause persistent digestive disorders. Bacteria, viruses and parasites are important aetiologic agents of acute and long-lasting symptomatologies. An integrated approach, consisting of stool culture, microscopy and/or specific immunological techniques for toxin, antigen and antibody detection, is required for accurate diagnosis of bacteria and parasites. Molecular techniques are essential for sensitive diagnosis of many viruses, bacteria and intestinal protozoa, and are increasingly utilised as adjuncts for helminth identification.

Conclusions

Diagnosis of the broad spectrum of intestinal pathogens is often cumbersome. There is a need for rapid diagnostic tests that are simple and affordable for resource-constrained settings, so that the management of patients suffering from persistent digestive disorders can be improved.

【 授权许可】

   
2013 Becker et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Bartram J, Cairncross S: Hygiene, sanitation, and water: forgotten foundations of health. PLoS Med 2010, 7:e1000367.
• [2]WHO: Diarrhoeal disease. Fact sheet no. 330. August 2009. Geneva: World Health Organization; 2009.
• [3]Murray CJL, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, et al.: Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012, 380:2197-2223.
• [4]Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, et al.: Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012, 380:2095-2128.
• [5]Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD: 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 2012, 12:136-141.
• [6]Pawlowski SW, Warren CA, Guerrant R: Diagnosis and treatment of acute or persistent diarrhea. Gastroenterology 2009, 136:1874-1886.
• [7]Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, Hatz CF: Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly 2012, 142:w13727.
• [8]Pullan RL, Brooker SJ: The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors 2012, 5:81.
• [9]Hotez PJ, Molyneux DH, Fenwick A, Ottesen E, Ehrlich Sachs S, Sachs JD: Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Med 2006, 3:e102.
• [10]Utzinger J: A research and development agenda for the control and elimination of human helminthiases. PLoS Negl Trop Dis 2012, 6:e1646.
• [11]Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Ehrlich Sachs S, Sachs JD, Savioli L: Control of neglected tropical diseases. N Engl J Med 2007, 357:1018-1027.
• [12]Hotez P: Hookworm and poverty. Ann N Y Acad Sci 2008, 1136:38-44.
• [13]Hotez PJ, Fenwick A, Savioli L, Molyneux DH: Rescuing the bottom billion through control of neglected tropical diseases. Lancet 2009, 373:1570-1575.
• [14]Conteh L, Engels T, Molyneux DH: Socioeconomic aspects of neglected tropical diseases. Lancet 2010, 375:239-247.
• [15]King CH: Parasites and poverty: the case of schistosomiasis. Acta Trop 2010, 113:95-104.
• [16]Cavalli A, Bamba SI, Traore MN, Boelaert M, Coulibaly Y, Polman K, Pirard M, Van Dormael M: Interactions between Global Health Initiatives and country health systems: the case of a neglected tropical diseases control program in Mali. PLoS Negl Trop Dis 2010, 4:e798.
• [17]Marchal B, Van Dormael M, Pirard M, Cavalli A, Kegels G, Polman K: Neglected tropical disease (NTD) control in health systems: the interface between programmes and general health services. Acta Trop 2011, 120(Suppl 1):S177-S185.
• [18]Amazigo UV, Leak SG, Zoure HG, Njepuome N, Lusamba-Dikassa PS: Community-driven interventions can revolutionise control of neglected tropical diseases. Trends Parasitol 2012, 28:231-238.
• [19]Robays J, Lefevre P, Lutumba P, Lubanza S, Kande Betu Ku Mesu V, Van der Stuyft P, Boelaert M: Drug toxicity and cost as barriers to community participation in HAT control in the Democratic Republic of Congo. Trop Med Int Health 2007, 12:290-298.
• [20]Kibadi K, Boelaert M, Kayinua M, Minuku JB, Muyembe-Tamfum JJ, Portaels F, Lefevre P: Therapeutic itineraries of patients with ulcerated forms of Mycobacterium ulcerans (Buruli ulcer) disease in a rural health zone in the Democratic Republic of Congo. Trop Med Int Health 2009, 14:1110-1116.
• [21]Brun R, Blum J, Chappuis F, Burri C: Human African trypanosomiasis. Lancet 2010, 375:148-159.
• [22]Birx D, de Souza M, Nkengasong JN: Laboratory challenges in the scaling up of HIV, TB, and malaria programs: the interaction of health and laboratory systems, clinical research, and service delivery. Am J Clin Pathol 2009, 131:849-851.
• [23]Yansouni CP, Bottieau E, Lutumba P, Winkler AS, Lynen L, Büscher P, Jacobs J, Gillet P, Lejon V, Alirol E, et al.: Rapid diagnostic tests for neurological infections in Central Africa. Lancet Infect Dis 2013. in press
• [24]Yansouni CP, Bottieau E, Chappuis F, Phoba MF, Lunguya O, Ifeka BB, Jacobs J: Rapid diagnostic tests for a coordinated approach to fever syndromes in low-resource settings. Clin Infect Dis 2012, 55:610-611.
• [25]Lacour M, Zunder T, Huber R, Sander A, Daschner F, Frank U: The pathogenetic significance of intestinal Candida colonization - a systematic review from an interdisciplinary and environmental medical point of view. Int J Hyg Environ Health 2002, 205:257-268.
• [26]Abba K, Sinfield R, Hart CA, Garner P: Pathogens associated with persistent diarrhoea in children in low and middle income countries: systematic review. BMC Infect Dis 2009, 9:88.
• [27]Moore SR: Update on prolonged and persistent diarrhea in children. Curr Opin Gastroenterol 2011, 27:19-23.
• [28]Pfeiffer ML, Dupont HL, Ochoa TJ: The patient presenting with acute dysentery - a systematic review. J Infect 2012, 64:374-386.
• [29]Barratt JL, Harkness J, Marriott D, Ellis JT, Stark D: A review of Dientamoeba fragilis carriage in humans: several reasons why this organism should be considered in the diagnosis of gastrointestinal illness. Gut Microbes 2011, 2:3-12.
• [30]Scanlan PD: Blastocystis: past pitfalls and future perspectives. Trends Parasitol 2012, 28:327-334.
• [31]Janda JM, Abbott SL: The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 2010, 23:35-73.
• [32]Granato PA, Chen L, Holiday I, Rawling RA, Novak-Weekley SM, Quinlan T, Musser KA: Comparison of premier CAMPY enzyme immunoassay (EIA), ProSpecT Campylobacter EIA, and ImmunoCard STAT! CAMPY tests with culture for laboratory diagnosis of Campylobacter enteric infections. J Clin Microbiol 2010, 48:4022-4027.
• [33]Bartlett JG, Gerding DN: Clinical recognition and diagnosis of Clostridium difficile infection. Clin Infect Dis 2008, 46(Suppl 1):S12-S18.
• [34]Planche T, Aghaizu A, Holliman R, Riley P, Poloniecki J, Breathnach A, Krishna S: Diagnosis of Clostridium difficile infection by toxin detection kits: a systematic review. Lancet Infect Dis 2008, 8:777-784.
• [35]Lemee L, Dhalluin A, Testelin S, Mattrat MA, Maillard K, Lemeland JF, Pons JL: Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (Toxin A), and tcdB (Toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol 2004, 42:5710-5714.
• [36]Kaur P, Chakraborti A, Asea A: Enteroaggregative Escherichia coli: an emerging enteric food borne pathogen. Interdiscip Perspect Infect Dis 2010, 2010:254159.
• [37]Ochoa TJ, Barletta F, Contreras C, Mercado E: New insights into the epidemiology of enteropathogenic Escherichia coli infection. Trans R Soc Trop Med Hyg 2008, 102:852-856.
• [38]Szakal DD, Schneider G, Pal T: A colony blot immune assay to identify enteroinvasive Escherichia coli and Shigella in stool samples. Diagn Microbiol Infect Dis 2003, 45:165-171.
• [39]Gould LH, Bopp C, Strockbine N, Atkinson R, Baselski V, Body B, Carey R, Crandall C, Hurd S, Kaplan R, et al.: Recommendations for diagnosis of shiga toxin-producing Escherichia coli infections by clinical laboratories. MMWR Recomm Rep 2009, 58:1-14.
• [40]Hermos CR, Janineh M, Han LL, McAdam AJ: Shiga toxin-producing Escherichia coli in children: diagnosis and clinical manifestations of O157:H7 and non-O157:H7 infection. J Clin Microbiol 2011, 49:955-959.
• [41]Nataro JP, Kaper JB: Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998, 11:142-201.
• [42]Guion CE, Ochoa TJ, Walker CM, Barletta F, Cleary TG: Detection of diarrheagenic Escherichia coli by use of melting-curve analysis and real-time multiplex PCR. J Clin Microbiol 2008, 46:1752-1757.
• [43]Wiener RS, Della-Latta P, Schluger NW: Effect of nucleic acid amplification for Mycobacterium tuberculosis on clinical decision making in suspected extrapulmonary tuberculosis. Chest 2005, 128:102-107.
• [44]Giouleme O, Paschos P, Katsaros M, Papalexi F, Karabatsou S, Masmanidou M, Koliouskas D: Intestinal tuberculosis: a diagnostic challenge - case report and review of the literature. Eur J Gastroenterol Hepatol 2011, 23:1074-1077.
• [45]Bhan MK, Bahl R, Bhatnagar S: Typhoid and paratyphoid fever. Lancet 2005, 366:749-762.
• [46]Kariuki S: Typhoid fever in sub-Saharan Africa: challenges of diagnosis and management of infections. J Infect Dev Ctries 2008, 2:443-447.
• [47]Gordon MA: Invasive nontyphoidal Salmonella disease: epidemiology, pathogenesis and diagnosis. Curr Opin Infect Dis 2011, 24:484-489.
• [48]Niyogi SK: Shigellosis. J Microbiol 2005, 43:133-143.
• [49]Marth T, Schneider T: Whipple disease. Curr Opin Gastroenterol 2008, 24:141-148.
• [50]Shears P: Recent developments in cholera. Curr Opin Infect Dis 2001, 14:553-558.
• [51]Neogi SB, Chowdhury N, Asakura M, Hinenoya A, Haldar S, Saidi SM, Kogure K, Lara RJ, Yamasaki S: A highly sensitive and specific multiplex PCR assay for simultaneous detection of Vibrio cholerae, Vibrio parahaemolyticus and Vibrio vulnificus. Lett Appl Microbiol 2010, 51:293-300.
• [52]Bockemühl J, Roggentin P: Intestinal yersiniosis. Clinical importance, epidemiology, diagnosis, and prevention. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2004, 47:685-691. in German
• [53]M’Ikanatha NM, Dettinger LA, Perry A, Rogers P, Reynolds SM, Nachamkin I: Culturing stool specimens for Campylobacter spp., Pennsylvania, USA. Emerg Infect Dis 2012, 18:484-487.
• [54]Shanholtzer CJ, Peterson LR, Olson MN, Gerding DN: Prospective study of gram-stained stool smears in diagnosis of Clostridium difficile colitis. J Clin Microbiol 1983, 17:906-908.
• [55]Schuster FL, Ramirez-Avila L: Current world status of Balantidium coli. Clin Microbiol Rev 2008, 21:626-638.
• [56]Stark D, van Hal S, Marriott D, Ellis J, Harkness J: Irritable bowel syndrome: a review on the role of intestinal protozoa and the importance of their detection and diagnosis. Int J Parasitol 2007, 37:11-20.
• [57]Stensvold CR, Nielsen HV, Molbak K, Smith HV: Pursuing the clinical significance of Blastocystis - diagnostic limitations. Trends Parasitol 2009, 25:23-29.
• [58]Zhang X, Qiao J, Wu X, Da R, Zhao L, Wei Z: In vitro culture of Blastocystis hominis in three liquid media and its usefulness in the diagnosis of blastocystosis. Int J Infect Dis 2012, 16:e23-e28.
• [59]Verweij JJ, Blange RA, Templeton K, Schinkel J, Brienen EA, van Rooyen MA, van Lieshout L, Polderman AM: Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol 2004, 42:1220-1223.
• [60]van Lieshout L, Verweij JJ: Newer diagnostic approaches to intestinal protozoa. Curr Opin Infect Dis 2010, 23:488-493.
• [61]Caccio SM, Pozio E: Advances in the epidemiology, diagnosis and treatment of cryptosporidiosis. Expert Rev Anti Infect Ther 2006, 4:429-443.
• [62]Davies AP, Chalmers RM: Cryptosporidiosis. BMJ 2009, 339:b4168.
• [63]Ortega YR, Sanchez R: Update on Cyclospora cayetanensis, a food-borne and waterborne parasite. Clin Microbiol Rev 2010, 23:218-234.
• [64]Verweij JJ, Mulder B, Poell B, van Middelkoop D, Brienen EA, van Lieshout L: Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Mol Cell Probes 2007, 21:400-404.
• [65]Stark D, Barratt J, Roberts T, Marriott D, Harkness J, Ellis J: Comparison of microscopy, two xenic culture techniques, conventional and real-time PCR for the detection of Dientamoeba fragilis in clinical stool samples. Eur J Clin Microbiol Infect Dis 2010, 29:411-416.
• [66]Qvarnstrom Y, James C, Xayavong M, Holloway BP, Visvesvara GS, Sriram R, da Silva AJ: Comparison of real-time PCR protocols for differential laboratory diagnosis of amebiasis. J Clin Microbiol 2005, 43:5491-5497.
• [67]Fotedar R, Stark D, Beebe N, Marriott D, Ellis J, Harkness J: Laboratory diagnostic techniques for Entamoeba species. Clin Microbiol Rev 2007, 20:511-532.
• [68]Clark CG, Diamond LS: Methods for cultivation of luminal parasitic protists of clinical importance. Clin Microbiol Rev 2002, 15:329-341.
• [69]Kebede A, Verweij J, Dorigo-Zetsma W, Sanders E, Messele T, van Lieshout L, Petros B, Polderman T: Overdiagnosis of amoebiasis in the absence of Entamoeba histolytica among patients presenting with diarrhoea in Wonji and Akaki, Ethiopia. Trans R Soc Trop Med Hyg 2003, 97:305-307.
• [70]Kebede A, Verweij JJ, Petros B, Polderman AM: Misleading microscopy in amoebiasis. Trop Med Int Health 2004, 9:651-652.
• [71]Nagaty IM, Hegazi MM: Dot-ELISA copro-antigen and direct stool examination in diagnosis of giardiasis patients. J Egypt Soc Parasitol 2007, 37:641-648.
• [72]ten Hove RJ, van Lieshout L, Brienen EA, Perez MA, Verweij JJ: Real-time polymerase chain reaction for detection of Isospora belli in stool samples. Diagn Microbiol Infect Dis 2008, 61:280-283.
• [73]Murphy SC, Hoogestraat DR, Sengupta DJ, Prentice J, Chakrapani A, Cookson BT: Molecular diagnosis of cystoisosporiasis using extended-range PCR screening. J Mol Diagn 2011, 13:359-362.
• [74]Didier ES, Weiss LM: Microsporidiosis: not just in AIDS patients. Curr Opin Infect Dis 2011, 24:490-495.
• [75]Didier ES, Weiss LM: Microsporidiosis: current status. Curr Opin Infect Dis 2006, 19:485-492.
• [76]Verweij JJ, Ten Hove R, Brienen EA, van Lieshout L: Multiplex detection of Enterocytozoon bieneusi and Encephalitozoon spp. in fecal samples using real-time PCR. Diagn Microbiol Infect Dis 2007, 57:163-167.
• [77]Scholz T, Garcia HH, Kuchta R, Wicht B: Update on the human broad tapeworm (genus diphyllobothrium), including clinical relevance. Clin Microbiol Rev 2009, 22:146-160.
• [78]Wicht B, Yanagida T, Scholz T, Ito A, Jimenez JA, Brabec J: Multiplex PCR for differential identification of broad tapeworms (Cestoda: Diphyllobothrium) infecting humans. J Clin Microbiol 2010, 48:3111-3116.
• [79]Steinmann P, Cringoli G, Bruschi F, Matthys B, Lohourignon LK, Castagna B, Maurelli MP, Morgoglione ME, Utzinger J, Rinaldi L: FLOTAC for the diagnosis of Hymenolepis spp. infection: proof-of-concept and comparing diagnostic accuracy with other methods. Parasitol Res 2012, 111:749-754.
• [80]Brunetti E, White AC Jr: Cestode infestations: hydatid disease and cysticercosis. Infect Dis Clin North Am 2012, 26:421-435.
• [81]Katz N, Chaves A, Pellegrino J: A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop São Paulo 1972, 14:397-400.
• [82]WHO: Bench aids for the diagnosis of intestinal parasites. Geneva: World Health Organization; 1994.
• [83]Basuni M, Muhi J, Othman N, Verweij JJ, Ahmad M, Miswan N, Rahumatullah A, Aziz FA, Zainudin NS, Noordin R: A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. AmJTrop Med Hyg 2011, 84:338-343.
• [84]Soukhathammavong P, Sayasone S, Harimanana AN, Akkhavong A, Thammasack S, Phoumindr N, Choumlivong K, Keoluangkhot V, Phongmany S, Akkhavong K, et al.: Three cases of intestinal capillariasis in Lao People’s Democratic Republic. AmJTrop Med Hyg 2008, 79:735-738.
• [85]Attia RA, Tolba ME, Yones DA, Bakir HY, Eldeek HE, Kamel S: Capillaria philippinensis in Upper Egypt: has it become endemic? AmJTrop Med Hyg 2012, 86:126-133.
• [86]Montes M, Sawhney C, Barros N: Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis 2010, 23:500-504.
• [87]Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, van Lieshout L: Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg 2009, 103:342-346.
• [88]Keiser J, Duthaler U, Utzinger J: Update on the diagnosis and treatment of food-borne trematode infections. Curr Opin Infect Dis 2010, 23:513-520.
• [89]Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, Steinmann P, Rinaldi L, Cringoli G, N’Goran EK, Utzinger J: Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis 2010, 4:e754.
• [90]Henke-Gendo C, Ganzenmueller T, Kluba J, Harste G, Raggub L, Heim A: Improved quantitative PCR protocols for adenovirus and CMV with an internal inhibition control system and automated nucleic acid isolation. J Med Virol 2012, 84:890-896.
• [91]van Maarseveen NM, Wessels E, de Brouwer CS, Vossen AC, Claas EC: Diagnosis of viral gastroenteritis by simultaneous detection of adenovirus group F, astrovirus, rotavirus group a, norovirus genogroups I and II, and sapovirus in two internally controlled multiplex real-time PCR assays. J Clin Virol 2010, 49:205-210.
• [92]Kantola K, Sadeghi M, Antikainen J, Kirveskari J, Delwart E, Hedman K, Soderlund-Venermo M: Real-time quantitative PCR detection of four human bocaviruses. J Clin Microbiol 2010, 48:4044-4050.
• [93]Dare RK, Fry AM, Chittaganpitch M, Sawanpanyalert P, Olsen SJ, Erdman DD: Human coronavirus infections in rural Thailand: a comprehensive study using real-time reverse-transcription polymerase chain reaction assays. J Infect Dis 2007, 196:1321-1328.
• [94]Dierssen U, Rehren F, Henke-Gendo C, Harste G, Heim A: Rapid routine detection of enterovirus RNA in cerebrospinal fluid by a one-step real-time RT-PCR assay. J Clin Virol 2008, 42:58-64.
• [95]Center for Disease Control and Prevention: Guidelines for appropriate evaluations of HIV testing technologies in Africa. Available at: http://www.who.int/diagnostics_laboratory/publications/EN_HIVEval_Guide.pdf webcite (accessed online: 26 December 2012)
• [96]Branson BM: The future of HIV testing. J Acquir Immune Defic Syndr 2010, 55(Suppl 2):S102-S105.
• [97]Baumgarte S, de Souza Luna LK, Grywna K, Panning M, Drexler JF, Karsten C, Huppertz HI, Drosten C: Prevalence, types, and RNA concentrations of human parechoviruses, including a sixth parechovirus type, in stool samples from patients with acute enteritis. J Clin Microbiol 2008, 46:242-248.
• [98]Martiny D, Busson L, Wybo I, El Haj RA, Dediste A, Vandenberg O: Comparison of the Microflex LT and Vitek MS systems for routine identification of bacteria by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 2012, 50:1313-1325.
• [99]Bessede E, Delcamp A, Sifre E, Buissonniere A, Megraud F: New methods for detection of campylobacters in stool samples in comparison to culture. J Clin Microbiol 2011, 49:941-944.
• [100]Kuhn KG, Falkenhorst G, Ceper T, Dalby T, Ethelberg S, Molbak K, Krogfelt KA: Detection of antibodies to Campylobacter in humans using enzyme-linked immunosorbent assays: a review of the literature. Diagn Microbiol Infect Dis 2012, 74:113-118.
• [101]Yaqing H, Wenping Z, Zhiyi Y, Xionghu W, Shouyi Y, Hong Y, Yingchun D, Guifang H: Detection of human Enterovirus 71 reverse transcription loop-mediated isothermal amplification (RT-LAMP). Lett Appl Microbiol 2012, 54:233-239.
• [102]Yamazaki W: Sensitive and rapid detection of Campylobacter jejuni and Campylobacter coli using loop-mediated isothermal amplification. Methods Mol Biol 2013, 943:267-277.
• [103]Parry CM, Wijedoru L, Arjyal A, Baker S: The utility of diagnostic tests for enteric fever in endemic locations. Expert Rev Anti Infect Ther 2011, 9:711-725.
• [104]Gilman RH, Terminel M, Levine MM, Hernandez-Mendoza P, Hornick RB: Relative efficacy of blood, urine, rectal swab, bone-marrow, and rose-spot cultures for recovery of Salmonella typhi in typhoid fever. Lancet 1975, 305:1211-1213.
• [105]Baker S, Favorov M, Dougan G: Searching for the elusive typhoid diagnostic. BMC Infect Dis 2010, 10:45.
• [106]Joost I, Speck K, Herrmann M, von Müller L: Characterisation of Clostridium difficile isolates by slpA and tcdC gene sequencing. Int J Antimicrob Agents 2009, 33(Suppl 1):S13-S18.
• [107]Bartlett JG: Clostridium difficile: progress and challenges. Ann N Y Acad Sci 2010, 1213:62-69.
• [108]de Jong E, de Jong AS, Bartels CJ, Van Der Rijt-Van Den Biggelaar C, Melchers WJ, Sturm PD: Clinical and laboratory evaluation of a real-time PCR for Clostridium difficile toxin A and B genes. Eur J Clin Microbiol Infect Dis 2012, 31:2219-2225.
• [109]Reller ME, Lema CA, Perl TM, Cai M, Ross TL, Speck KA, Carroll KC: Yield of stool culture with isolate toxin testing versus a two-step algorithm including stool toxin testing for detection of toxigenic Clostridium difficile. J Clin Microbiol 2007, 45:3601-3605.
• [110]Crobach MJ, Dekkers OM, Wilcox MH, Kuijper EJ: European Society of Clinical Microbiology and Infectious Diseases (ESCMID): data review and recommendations for diagnosing Clostridium difficile infection (CDI). Clin Microbiol Infect 2009, 15:1053-1066.
• [111]Robert-Koch-Institut: Abschließende Darstellung und Bewertung der epidemiologischen Erkenntnisse im EHEC O104:H4 Ausbruch. Berlin: Deutschland 2011; 2011. (in German). Available at: http://www.rki.de/DE/Content/InfAZ/E/EHEC/EHEC-Abschlussbericht.html webcite (accessed online: 30 August 2012)
• [112]Donoghue HD, Holton J: Intestinal tuberculosis. Curr Opin Infect Dis 2009, 22:490-496.
• [113]Jeyanathan M, Boutros-Tadros O, Radhi J, Semret M, Bitton A, Behr MA: Visualization of mycobacterium avium in Crohn’s tissue by oil-immersion microscopy. Microbes Infect 2007, 9:1567-1573.
• [114]Yu H, Liu Y, Wang Y, Peng L, Li A, Zhang Y: Clinical, endoscopic and histological differentiations between Crohn’s disease and intestinal tuberculosis. Digestion 2012, 85:202-209.
• [115]Honscha G, Von Groll A, Valenca M, Ramos DF, Sanchotene K, Scaini CJ, Ribeiro MO, da Silva PE: The laboratory as a tool to qualify tuberculosis diagnosis. Int J Tuberc Lung Dis 2008, 12:218-220.
• [116]Yardley JH, Hendrix TR: Combined electron and light microscopy in Whipple’s disease. Demonstration of “bacillary bodies” in the intestine. Bull Johns Hopkins Hosp 1961, 109:80-98.
• [117]Raoult D, Birg ML, La Scola B, Fournier PE, Enea M, Lepidi H, Roux V, Piette JC, Vandenesch F, Vital-Durand D, et al.: Cultivation of the bacillus of Whipple’s disease. N Engl J Med 2000, 342:620-625.
• [118]Raoult D, Fenollar F, Birg ML: Culture of T. whipplei from the stool of a patient with Whipple’s disease. N Engl J Med 2006, 355:1503-1505.
• [119]Dobell C: The discovery of the intestinal protozoa of man. Proc R Soc Med 1920, 13:1-15.
• [120]Allen AVH, Ridley DS: Further observations on the formol-ether concentration technique for faecal parasites. J Clin Pathol 1970, 23:545-546.
• [121]Utzinger J, Botero-Kleiven S, Castelli F, Chiodini PL, Edwards H, Kohler N, Gulletta M, Lebbad M, Manser M, Matthys B, et al.: Microscopic diagnosis of sodium acetate-acetic acid-formalin-fixed stool samples for helminths and intestinal protozoa: a comparison among European reference laboratories. Clin Microbiol Infect 2010, 16:267-273.
• [122]Becker SL, Lohourignon LK, Speich B, Rinaldi L, Knopp S, N’Goran EK, Cringoli G, Utzinger J: Comparison of the Flotac-400 dual technique and the formalin-ether concentration technique for diagnosis of human intestinal protozoon infection. J Clin Microbiol 2011, 49:2183-2190.
• [123]Sharp SE, Suarez CA, Duran Y, Poppiti RJ: Evaluation of the Triage Micro Parasite Panel for detection of Giardia lamblia, Entamoeba histolytica/Entamoeba dispar, and Cryptosporidium parvum in patient stool specimens. J Clin Microbiol 2001, 39:332-334.
• [124]Chalmers RM, Davies AP: Clinical cryptosporidiosis. Exp Parasitol 2010, 124:138-146.
• [125]Diamond LS, Clark CG: A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. J Eukaryot Microbiol 1993, 40:340-344.
• [126]Haque R, Neville LM, Hahn P, Petri WA Jr: Rapid diagnosis of Entamoeba infection by using Entamoeba and Entamoeba histolytica stool antigen detection kits. J Clin Microbiol 1995, 33:2558-2561.
• [127]Fotedar R, Stark D, Beebe N, Marriott D, Ellis J, Harkness J: PCR detection of Entamoeba histolytica, Entamoeba dispar, and Entamoeba moshkovskii in stool samples from Sydney, Australia. J Clin Microbiol 2007, 45:1035-1037.
• [128]Ximenez C, Moran P, Rojas L, Valadez A, Gomez A: Reassessment of the epidemiology of amebiasis: state of the art. Infect Genet Evol 2009, 9:1023-1032.
• [129]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 2009, 28:1045-1053.
• [130]de Vlas SJ, Gryseels B: Underestimation of Schistosoma mansoni prevalences. Parasitol Today 1992, 8:274-277.
• [131]Booth M, Vounatsou P, N’Goran EK, Tanner M, Utzinger J: The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d’Ivoire. Parasitology 2003, 127:525-531.
• [132]Speich B, Knopp S, Mohammed KA, Khamis IS, Rinaldi L, Cringoli G, Rollinson D, Utzinger J: Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasit Vectors 2010, 3:71.
• [133]García LS, Bruckner DA: Diagnostic medical parasitology. Washington D.C: ASM Press; 2001.
• [134]Tarafder MR, Carabin H, Joseph L, Balolong E Jr, Olveda R, McGarvey ST: Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a ‘gold standard’. Int J Parasitol 2010, 40:399-404.
• [135]Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J: Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis 2008, 2:e331.
• [136]Berhe N, Medhin G, Erko B, Smith T, Gedamu S, Bereded D, Moore R, Habte E, Redda A, Gebre-Michael T, et al.: Variations in helminth faecal egg counts in Kato-Katz thick smears and their implications in assessing infection status with Schistosoma mansoni. Acta Trop 2004, 92:205-212.
• [137]Goodman D, Haji HJ, Bickle QD, Stoltzfus RJ, Tielsch JM, Ramsan M, Savioli L, Albonico M: A comparison of methods for detecting the eggs of Ascaris, Trichuris, and hookworm in infant stool, and the epidemiology of infection in Zanzibari infants. Am J Trop Med Hyg 2007, 76:725-731.
• [138]Steinmann P, Du ZW, Wang LB, Wang XZ, Jiang JY, Li LH, Marti H, Zhou XN, Utzinger J: Extensive multiparasitism in a village of Yunnan province, People’s Republic of China, revealed by a suite of diagnostic methods. Am J Trop Med Hyg 2008, 78:760-769.
• [139]Knopp S, Rinaldi L, Khamis IS, Stothard JR, Rollinson D, Maurelli MP, Steinmann P, Marti H, Cringoli G, Utzinger J: A single FLOTAC is more sensitive than triplicate Kato-Katz for the diagnosis of low-intensity soil-transmitted helminth infections. Trans R Soc Trop Med Hyg 2009, 103:347-354.
• [140]Steinmann P, Utzinger J, Du ZW, Zhou XN: Multiparasitism: a neglected reality on global, regional and local scale. Adv Parasitol 2010, 73:21-50.
• [141]Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P: Strongyloidiasis - the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg 2009, 103:967-972.
• [142]Verweij JJ, van Lieshout L: Intestinal parasitic infections in an industrialized country; a new focus on children with better DNA-based diagnostics. Parasitology 2011, 138:1492-1498.
• [143]Becker SL, Sieto B, Silué KD, Adjossan L, Kone S, Hatz C, Kern WV, N’Goran EK, Utzinger J: Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis 2011, 5:e1292.
• [144]World Gastroenterology Organization: WGO practice guideline. Management of strongyloidiasis. Available at: http://www.worldgastroenterology.org/assets/downloads/en/pdf/guidelines/15_management_strongyloidiasis_en.pdf webcite (accessed online: 1 August 2012)
• [145]Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H: A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg 1991, 45:518-521.
• [146]Feely NM, Waghorn DJ, Dexter T, Gallen I, Chiodini P: Strongyloides stercoralis hyperinfection: difficulties in diagnosis and treatment. Anaesthesia 2010, 65:298-301.
• [147]Kramme S, Nissen N, Soblik H, Erttmann K, Tannich E, Fleischer B, Panning M, Brattig N: Novel real-time PCR for the universal detection of Strongyloides species. J Med Microbiol 2011, 60:454-458.
• [148]Engels D, Sinzinkayo E, Gryseels B: Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. Am J Trop Med Hyg 1996, 54:319-324.
• [149]Utzinger J, Booth M, N’Goran EK, Müller I, Tanner M, Lengeler C: Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 2001, 122:537-544.
• [150]Midzi N, Butterworth AE, Mduluza T, Munyati S, Deelder AM, van Dam GJ: Use of circulating cathodic antigen strips for the diagnosis of urinary schistosomiasis. Trans R Soc Trop Med Hyg 2009, 103:45-51.
• [151]Clerinx J, Van Gompel A: Schistosomiasis in travellers and migrants. Travel Med Infect Dis 2011, 9:6-24.
• [152]Coulibaly JT, Knopp S, N’Guessan NA, Silué KD, Fürst T, Lohourignon LK, Brou JK, N’Gbesso YK, Vounatsou P, N’Goran EK, et al.: Accuracy of urine circulating cathodic antigen (CCA) test for Schistosoma mansoni diagnosis in different settings of Côte d’Ivoire. PLoS Negl Trop Dis 2011, 5:e1384.
• [153]Shane HL, Verani JR, Abudho B, Montgomery SP, Blackstock AJ, Mwinzi PN, Butler SE, Karanja DM, Secor WE: Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in Western Kenya. PLoS Negl Trop Dis 2011, 5:e951.
• [154]ten Hove RJ, Verweij JJ, Vereecken K, Polman K, Dieye L, van Lieshout L: Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Trans R Soc Trop Med Hyg 2008, 102:179-185.
• [155]Obeng BB, Aryeetey YA, de Dood CJ, Amoah AS, Larbi IA, Deelder AM, Yazdanbakhsh M, Hartgers FC, Boakye DA, Verweij JJ, et al.: Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Ann Trop Med Parasitol 2008, 102:625-633.
• [156]Wardlaw T, Salama P, Brocklehurst C, Chopra M, Mason E: Diarrhoea: why children are still dying and what can be done. Lancet 2010, 375:870-872.
• [157]Clark B, McKendrick M: A review of viral gastroenteritis. Curr Opin Infect Dis 2004, 17:461-469.
• [158]Soares CC, Volotao EM, Albuquerque MC, da Silva FM, de Carvalho TR, Nozawa CM, Linhares RE, Santos N: Prevalence of enteric adenoviruses among children with diarrhea in four Brazilian cities. J Clin Virol 2002, 23:171-177.
• [159]Seto D, Chodosh J, Brister JR, Jones MS: Using the whole-genome sequence to characterize and name human adenoviruses. J Virol 2011, 85:5701-5702.
• [160]Grandien M, Pettersson CA, Svensson L, Uhnoo I: Latex agglutination test for adenovirus diagnosis in diarrheal disease. J Med Virol 1987, 23:311-316.
• [161]Gleaves CA, Militoni J, Ashley RL: An enzyme immunoassay for the direct detection of adenovirus in clinical specimens. Diagn Microbiol Infect Dis 1993, 17:57-59.
• [162]Caballero S, Guix S, El-Senousy WM, Calico I, Pinto RM, Bosch A: Persistent gastroenteritis in children infected with astrovirus: association with serotype-3 strains. J Med Virol 2003, 71:245-250.
• [163]Dalton RM, Roman ER, Negredo AA, Wilhelmi ID, Glass RI, Sanchez-Fauquier A: Astrovirus acute gastroenteritis among children in Madrid, Spain. Pediatr Infect Dis J 2002, 21:1038-1041.
• [164]Jartti T, Hedman K, Jartti L, Ruuskanen O, Allander T, Soderlund-Venermo M: Human bocavirus - the first 5 years. Rev Med Virol 2012, 22:46-64.
• [165]Don M, Soderlund-Venermo M, Hedman K, Ruuskanen O, Allander T, Korppi M: Don’t forget serum in the diagnosis of human bocavirus infection. J Infect Dis 2011, 203:1031-1032. author reply 1032–1033
• [166]Green KY, et al.: Caliciviridae: the noroviruses. In Fields virology. 5th edition. Edited by Knipe D. Philadelphia, PA, USA: Lippincott Williams & Wilkins; 2007:949-979.
• [167]Burton-MacLeod JA, Kane EM, Beard RS, Hadley LA, Glass RI, Ando T: Evaluation and comparison of two commercial enzyme-linked immunosorbent assay kits for detection of antigenically diverse human noroviruses in stool samples. J Clin Microbiol 2004, 42:2587-2595.
• [168]Morillo SG, Luchs A, Cilli A, Ribeiro CD, Calux SJ, Carmona Rde C, Timenetsky Mdo C: Norovirus 3rd Generation kit: an improvement for rapid diagnosis of sporadic gastroenteritis cases and valuable for outbreak detection. J Virol Meth 2011, 173:13-16.
• [169]Gunson RN, Collins TC, Carman WF: The real-time detection of sapovirus. J Clin Virol 2006, 35:321-322.
• [170]Esper F, Ou Z, Huang YT: Human coronaviruses are uncommon in patients with gastrointestinal illness. J Clin Virol 2010, 48:131-133.
• [171]Baroco AL, Oldfield EC: Gastrointestinal cytomegalovirus disease in the immunocompromised patient. Curr Gastroenterol Rep 2008, 10:409-416.
• [172]Nasri D, Bouslama L, Pillet S, Bourlet T, Aouni M, Pozzetto B: Basic rationale, current methods and future directions for molecular typing of human enterovirus. Expert Rev Mol Diagn 2007, 7:419-434.
• [173]Tapia G, Cinek O, Witso E, Kulich M, Rasmussen T, Grinde B, Ronningen KS: Longitudinal observation of parechovirus in stool samples from Norwegian infants. J Med Virol 2008, 80:1835-1842.
• [174]Harvala H, Simmonds P: Human parechoviruses: biology, epidemiology and clinical significance. J Clin Virol 2009, 45:1-9.
• [175]Wolffs PF, Bruggeman CA, van Well GT, van Loo IH: Replacing traditional diagnostics of fecal viral pathogens by a comprehensive panel of real-time PCRs. J Clin Microbiol 2011, 49:1926-1931.
• [176]Pang XL, Lee B, Boroumand N, Leblanc B, Preiksaitis JK, Yu Ip CC: Increased detection of rotavirus using a real time reverse transcription-polymerase chain reaction (RT-PCR) assay in stool specimens from children with diarrhea. J Med Virol 2004, 72:496-501.
• [177]Jothikumar N, Kang G, Hill VR: Broadly reactive TaqMan assay for real-time RT-PCR detection of rotavirus in clinical and environmental samples. J Virol Meth 2009, 155:126-131.
• [178]Bhaijee F, Subramony C, Tang SJ, Pepper DJ: Human immunodeficiency virus-associated gastrointestinal disease: common endoscopic biopsy diagnoses. Patholog Res Int 2011, 2011:247923.
• [179]Lowe AM, Yansouni CP, Behr MA: Causality and gastrointestinal infections: Koch, Hill, and Crohn’s. Lancet Infect Dis 2008, 8:720-726.
• [180]Zimmermann MB, Chassard C, Rohner F, N’Goran EK, Nindjin C, Dostal A, Utzinger J, Ghattas H, Lacroix C, Hurrell RF: The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d’Ivoire. Am J Clin Nutr 2010, 92:1406-1415.
• [181]Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S: Host-gut microbiota metabolic interactions. Science 2012, 336:1262-1267.
• [182]Clemente JC, Ursell LK, Parfrey LW, Knight R: The impact of the gut microbiota on human health: an integrative view. Cell 2012, 148:1258-1270.
• [183]Prasad RN, Virk KJ: Malaria as a cause of diarrhoea - a review. P N G Med J 1993, 36:337-341.
• [184]Reisinger EC, Fritzsche C, Krause R, Krejs GJ: Diarrhea caused by primarily non-gastrointestinal infections. Nat Clin Pract Gastroenterol Hepatol 2005, 2:216-222.
• [185]Spiller R, Garsed K: Postinfectious irritable bowel syndrome. Gastroenterology 2009, 136:1979-1988.