A systematic review and meta-analysis of the association between giardia lamblia and endemic pediatric diarrhea in developing countries

Clinical Infectious Diseases

Volumn 55, Issue SUPPL. 4, 2012, Pages

  Muhsen, Khitam ^a   Levine, Myron M ^a  

^a University of Maryland School of Medicine Center for Vaccine Development   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE DIARRHEA; DEVELOPING COUNTRY; DISEASE ASSOCIATION; DISEASE TRANSMISSION; ENDEMIC DISEASE; FECES ANALYSIS; GIARDIA LAMBLIA; GIARDIASIS; HUMAN; INFANT; INFANTILE DIARRHEA; NEWBORN; PREVALENCE; PRIORITY JOURNAL; PROTIST LIFE CYCLE STAGE; REVIEW;

ASYMPTOMATIC DISEASES; CHILD, PRESCHOOL; COHORT STUDIES; DEVELOPING COUNTRIES; DIARRHEA; EPIDEMIOLOGIC RESEARCH DESIGN; FEMALE; GIARDIA LAMBLIA; GIARDIASIS; HUMANS; INFANT; INFANT, NEWBORN; MALE; MULTICENTER STUDIES AS TOPIC;

EID: 84870018865     PISSN: 10584838     EISSN: 15376591     Source Type: Journal    
DOI: 10.1093/cid/cis762     Document Type: Review

References (174)

1. Marquardt WC, Demaree RS, Grieve RB. Giardia and giardiosis. Parasitology and vector biology. 2nd ed. San Diego, CA: Academic Press, 2000:89-96.
2. Adam RD. Biology of Giardia lamblia. Clin Microbiol Rev 2001; 14:447-75. (Pubitemid 32642745)
3. Ankarklev J, Jerlstrom-Hultqvist J, Ringqvist E, Troell K, Svard SG. Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 2010; 8:413-22.
4. Farthing MJ. Giardiasis. Gastroenterol Clin North Am 1996; 25:493-515. (Pubitemid 26335820)
5. Lane S, Lloyd D. Current trends in research into the waterborne parasite Giardia. Crit Rev Microbiol 2002; 28:123-47. (Pubitemid 34779348)
6. Nakano T, Binka FN, Afari EA, et al. Survey of enteropathogenic agents in children with and without diarrhoea in Ghana. J Trop Med Hyg 1990; 93:408-12.
7. Nimri LF, Meqdam M. Enteropathogens associated with cases of gastroenteritis in a rural population in Jordan. Clin Microbiol Infect 2004; 10:634-9. (Pubitemid 39077051)
8. Yoder JS, Harral C, Beach MJ. Giardiasis surveillance - United States, 2006-2008. MMWR Surveill Summ 2010; 59:15-25.
9. European Centre for Disease Prevention and Control. Annual epidemiological report on communicable diseases in Europe 2010. European Center for Disease Prevention and Control: Stockholm, Sweden, 2010.
10. Lebwohl B, Deckelbaum RJ, Green PH. Giardiasis. Gastrointest Endosc 2003; 57:906-13. (Pubitemid 47231348)
11. Katz DE, Heisey-Grove D, Beach M, Dicker RC, Matyas BT. Prolonged outbreak of giardiasis with two modes of transmission. Epidemiol Infect 2006; 134:935-41. (Pubitemid 44336366)
12. al-Bwardy MA, Ramia S, al-Frayh AR, et al. Bacterial, parasitic and viral enteropathogens associated with diarrhoea in Saudi children. Ann Trop Paediatr 1988; 8:26-30.
13. Khan MM, Iqbal J, Ghafoor A, Burney MI. Aetiologic agents of diarrhoeal diseases in hospitalised children in Rawalpindi, Pakistan. J Diarrhoeal Dis Res 1988; 6:228-31.
14. Nash TE, Herrington DA, Losonsky GA, Levine MM. Experimental human infections with Giardia lamblia. J Infect Dis 1987; 156:974-84. (Pubitemid 18017076)
15. Rendtorff RC, Holt CJ. The experimental transmission of human intestinal protozoan parasites. IV. Attempts to transmit Endamoeba coli and Giardia lamblia cysts by water. Am J Hyg 1954; 60:327-38.
16. White KE, Hedberg CW, Edmonson LM, Jones DB, Osterholm MT, MacDonald KL. An outbreak of giardiasis in a nursing home with evidence for multiple modes of transmission. J Infect Dis 1989; 160:298-304. (Pubitemid 19189023)
17. Shaw PK, Brodsky RE, Lyman DO, et al. A communitywide outbreak of giardiasis with evidence of transmission by a municipal water supply. Ann Intern Med 1977; 87:426-32. (Pubitemid 8217081)
18. Keystone JS, Krajden S, Warren MR. Person-to-person transmission of Giardia lamblia in day-care nurseries. Can Med Assoc J 1978; 119:241-2, 247-8.
19. Addiss DG, Davis JP, Roberts JM, Mast EE. Epidemiology of giardiasis in Wisconsin: increasing incidence of reported cases and unexplained seasonal trends. Am J Trop Med Hyg 1992; 47:13-9.
20. Lopez CE, Dykes AC, Juranek DD, et al. Waterborne giardiasis: a communitywide outbreak of disease and a high rate of asymptomatic infection. Am J Epidemiol 1980; 112:495-507. (Pubitemid 10029552)
21. Birkhead G, Vogt RL. Epidemiologic surveillance for endemic Giardia lamblia infection in Vermont. The roles of waterborne and person-to-person transmission. Am J Epidemiol 1989; 129:762-8. (Pubitemid 19094254)
22. Black RE, Dykes AC, Sinclair SP, Wells JG. Giardiasis in day-care centers: evidence of person-to-person transmission. Pediatrics 1977; 60:486-91. (Pubitemid 8208130)
23. Nygard K, Schimmer B, Sobstad O, et al. A large community outbreak of waterborne giardiasis-delayed detection in a non-endemic urban area. BMC Public Health 2006; 6:141.
24. Stanton B, Silimperi DR, Khatun K, et al. Parasitic, bacterial and viral pathogens isolated from diarrhoeal and routine stool specimens of urban Bangladeshi children. J Trop Med Hyg 1989; 92:46-55. (Pubitemid 19074378)
25. Nimri LF, Elnasser Z, Batchoun R. Polymicrobial infections in children with diarrhoea in a rural area of Jordan. FEMS Immunol Med Microbiol 2004; 42:255-9. (Pubitemid 39208555)
26. Shetty N, Narasimha M, Raghuveer TS, Elliott E, Farthing MJ, Macaden R. Intestinal amoebiasis and giardiasis in southern Indian infants and children. Trans R Soc Trop Med Hyg 1990; 84:382-4. (Pubitemid 20204319)
27. Hollm-Delgado MG, Gilman RH, Bern C, et al. Lack of an adverse effect of Giardia intestinalis infection on the health of Peruvian children. Am J Epidemiol 2008; 168:647-55.
28. Loening WE, Coovadia YM, van den Ende J. Aetiological factors of infantile diarrhoea: a community-based study. Ann Trop Paediatr 1989; 9:248-55. (Pubitemid 20037554)
29. Bilenko N, Levy A, Dagan R, Deckelbaum RJ, El-On Y, Fraser D. Does co-infection with Giardia lamblia modulate the clinical characteristics of enteric infections in young children? Eur J Epidemiol 2004; 19:877-83. (Pubitemid 41184412)
30. Veenemans J, Mank T, Ottenhof M, et al. Protection against diarrhea associated with Giardia intestinalis is lost with multi-nutrient supplementation: a study in Tanzanian children. PLoS Negl Trop Dis 2011; 5:e1158.
31. Abramson JH. WINPEPI (PEPI-for-Windows): computer programs for epidemiologists. Epidemiol Perspect Innov 2004; 1:6.
32. Higgins JP, Thompson SG. Quantifying heterogeneity in a metaanalysis. Stat Med 2002; 21:1539-58.
33. Sterne JA, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 2001; 54:1046-55. (Pubitemid 32888370)
34. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629-34. (Pubitemid 27387172)
35. Borenstein M, Hedges L, Higgins J, Rothstein H. Comprehensive meta-analysis version 2. Englewood, NJ: Biostat, 2005.
36. Muller N, von Allmen N. Recent insights into the mucosal reactions associated with Giardia lamblia infections. Int J Parasitol 2005; 35:1339-47. (Pubitemid 41484147)
37. Roxstrom-Lindquist K, Palm D, Reiner D, Ringqvist E, Svard SG. Giardia immunity - an update. Trends Parasitol 2006; 22:26-31. (Pubitemid 43017201)
38. Eckmann L. Mucosal defences against Giardia. Parasite Immunol 2003; 25:259-70. (Pubitemid 38021456)
39. Buret AG. Pathophysiology of enteric infections with Giardia duodenalis. Parasite 2008; 15:261-5.
40. Cotton JA, Beatty JK, Buret AG. Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol 2011; 41:925-33.
41. Gillin FD, Reiner DS, Boucher SE. Small-intestinal factors promote encystation of Giardia lamblia in vitro. Infect Immun 1988; 56:705-7. (Pubitemid 18058806)
42. Rendtorff RC. The experimental transmission of human intestinal protozoan parasites. II. Giardia lamblia cysts given in capsules. Am J Hyg 1954; 59:209-20.
43. Weniger BG, Blaser MJ, Gedrose J, Lippy EC, Juranek DD. An outbreak of waterborne giardiasis associated with heavy water runoff due to warm weather and volcanic ashfall. Am J Public Health 1983; 73:868-72. (Pubitemid 13032832)
44. Isaac-Renton JL, Philion JJ. Factors associated with acquiring giardiasis in British Columbia residents. Can J Public Health 1992; 83:155-8.
45. Hoque ME, Hope VT, Kjellstrom T, Scragg R, Lay-Yee R. Risk of giardiasis in Aucklanders: a case-control study. Int J Infect Dis 2002; 6:191-7.
46. Hoque ME, Hope VT, Scragg R, Kjellstrom T. Children at risk of giardiasis in Auckland: a case-control analysis. Epidemiol Infect 2003; 131:655-62. (Pubitemid 37062886)
47. Gray SF, Gunnell DJ, Peters TJ. Risk factors for giardiasis: a casecontrol study in Avon and Somerset. Epidemiol Infect 1994; 113:95-102. (Pubitemid 24255394)
48. Dennis DT, Smith RP, Welch JJ, et al. Endemic giardiasis in New Hampshire: a case-control study of environmental risks. J Infect Dis 1993; 167:1391-5. (Pubitemid 23146189)
49. Balcioglu IC, Limoncu E, Ertan P, Yereli K, Ozbilgin A, Onag A. Incidence of giardiasis among siblings in Turkey. Pediatr Int 2003; 45:311-3. (Pubitemid 36995103)
50. Chute CG, Smith RP, Baron JA. Risk factors for endemic giardiasis. Am J Public Health 1987; 77:585-7. (Pubitemid 17056048)
51. Porter JD, Gaffney C, Heymann D, Parkin W. Food-borne outbreak of Giardia lamblia. Am J Public Health 1990; 80:1259-60. (Pubitemid 20323300)
52. Mintz ED, Hudson-Wragg M, Mshar P, Cartter ML, Hadler JL. Foodborne giardiasis in a corporate office setting. J Infect Dis 1993; 167:250-3. (Pubitemid 23002872)
53. Meyers JD, Kuharic HA, Holmes KK. Giardia lamblia infection in homosexual men. Br J Vener Dis 1977; 53:54-5. (Pubitemid 8057763)
54. Keystone JS, Keystone DL, Proctor EM. Intestinal parasitic infections in homosexual men: prevalence, symptoms and factors in transmission. Can Med Assoc J 1980; 123:512-4.
55. Phillips SC, Mildvan D, William DC, Gelb AM, White MC. Sexual transmission of enteric protozoa and helminths in a venerealdisease- clinic population. N Engl J Med 1981; 305:603-6. (Pubitemid 12201111)
56. Pakianathan MR, McMillan A. Intestinal protozoa in homosexual men in Edinburgh. Int J STD AIDS 1999; 10:780-4.
57. Pereira MG, Atwill ER, Barbosa AP. Prevalence and associated risk factors for Giardia lamblia infection among children hospitalized for diarrhea in Goiania, Goias State, Brazil. Rev Inst Med Trop Sao Paulo 2007; 49:139-45. (Pubitemid 47041686)
58. Coles CL, Levy A, Dagan R, Deckelbaum RJ, Fraser D. Risk factors for the initial symptomatic Giardia infection in a cohort of young Arab-Bedouin children. Ann Trop Paediatr 2009; 29:291-300.
59. Mahmud MA, Chappell C, Hossain MM, Habib M, Dupont HL. Risk-factors for development of first symptomatic Giardia infection among infants of a birth cohort in rural Egypt. Am J Trop Med Hyg 1995; 53:84-8.
60. Boontanom P, Mungthin M, Tan-Ariya P, Naaglor T, Leelayoova S. Epidemiology of giardiasis and genotypic characterization of Giardia duodenalis in preschool children of a rural community, central Thailand. Trop Biomed 2011; 28:32-9.
61. Ratanapo S, Mungthin M, Soontrapa S, et al. Multiple modes of transmission of giardiasis in primary schoolchildren of a rural community, Thailand. Am J Trop Med Hyg 2008; 78:611-5. (Pubitemid 351845165)
62. Sprong H, Caccio SM, van der Giessen JW. Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis 2009; 3:e558.
63. Eligio-Garcia L, Cortes-Campos A, Jimenez-Cardoso E. Genotype of Giardia intestinalis isolates from children and dogs and its relationship to host origin. Parasitol Res 2005; 97:1-6. (Pubitemid 41215263)
64. Monis PT, Andrews RH, Mayrhofer G, Ey PL. Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infect Genet Evol 2003; 3:29-38. (Pubitemid 36437584)
65. Moore G, Cross W, McGuire D, et al. Epidemic giardiasis at a ski resort. N Engl J Med 1969; 281:402-27.
66. Flanagan PA. Giardia - diagnosis, clinical course and epidemiology. A review. Epidemiol Infect 1992; 109:1-22.
67. Addy PA, Antepim G, Frimpong EH. Prevalence of pathogenic Escherichia coli and parasites in infants with diarrhoea in Kumasi, Ghana. East Afr Med J 2004; 81:353-7.
68. Albert MJ, Faruque AS, Faruque SM, Sack RB, Mahalanabis D. Casecontrol study of enteropathogens associated with childhood diarrhea in Dhaka, Bangladesh. J Clin Microbiol 1999; 37:3458-64. (Pubitemid 29491074)
69. Al-Gallas N, Bahri O, Bouratbeen A, Ben Haasen A, Ben Aissa R. Etiology of acute diarrhea in children and adults in Tunis, Tunisia, with emphasis on diarrheagenic Escherichia coli: prevalence, phenotyping, and molecular epidemiology. Am J Trop Med Hyg 2007; 77:571-82. (Pubitemid 351844340)
70. Bodhidatta L, McDaniel P, Sornsakrin S, Srijan A, Serichantalergs O, Mason CJ. Case-control study of diarrheal disease etiology in a remote rural area in Western Thailand. Am J Trop Med Hyg 2010; 83:1106-9.
71. Casalino M, Yusuf MW, Nicoletti M, et al. A two-year study of enteric infections associated with diarrhoeal diseases in children in urban Somalia. Trans R Soc Trop Med Hyg 1988; 82:637-41.
72. Chatterjee BD, Thawani G, Sanyal SN. Etiology of acute childhood diarrhoea in Calcutta. Trop Gastroenterol 1989; 10:158-66.
73. Echeverria P, Taylor DN, Lexsomboon U, et al. Case-control study of endemic diarrheal disease in Thai children. J Infect Dis 1989; 159:543-8. (Pubitemid 19065903)
74. El-Hakim MA, El-Sahn A. Association of parasites and diarrhoea among children less than five years of age in a rural area in Egypt. J Egypt Public Health Assoc 1996; 71:439-63.
75. Gambhir IS, Jaiswal JP, Nath G. Significance of Cryptosporidium as an aetiology of acute infectious diarrhoea in elderly Indians. Trop Med Int Health 2003; 8:415-9. (Pubitemid 36733591)
76. Gascon J, Vargas M, Schellenberg D, et al. Diarrhea in children under 5 years of age from Ifakara, Tanzania: a case-control study. J Clin Microbiol 2000; 38:4459-62. (Pubitemid 32244534)
77. Gassama A, Sow PS, Fall F, et al. Ordinary and opportunistic enteropathogens associated with diarrhea in Senegalese adults in relation to human immunodeficiency virus serostatus. Int J Infect Dis 2001; 5:192-8. (Pubitemid 34059579)
78. Georges MC, Roure C, Tauxe RV, et al. Diarrheal morbidity and mortality in children in the Central African Republic. Am J Trop Med Hyg 1987; 36:598-602. (Pubitemid 17099476)
79. Gracey M, Burke V, Robinson J. Patterns of intestinal infection in Australian Aboriginal children. Ann Trop Paediatr 1983; 3:35-9. (Pubitemid 13067216)
80. Haque R, Mondal D, Karim A, et al. Prospective case-control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Clin Infect Dis 2009; 48:1191-7.
81. Hassan EM, el-Meneza SA, el-Rashidy Z, Rashad R, Rabie S, Fahmy SA. Detection of enteropathogens in diarrhoeal diseases among malnourished Egyptian infant and children. J Egypt Public Health Assoc 1989; 64:461-74.
82. Huilan S, Zhen LG, Mathan MM, et al. Etiology of acute diarrhoea among children in developing countries: a multicentre study in five countries. Bull World Health Organ 1991; 69:549-55.
83. Korzeniowski OM, Dantas W, Trabulsi LR, Guerrant RL. A controlled study of endemic sporadic diarrhoea among adult residents of southern Brazil. Trans R Soc Trop Med Hyg 1984; 78:363-9.
84. Menon BS, Abdullah S, Mahamud F, et al. Low prevalence of Cryptosporidium parvum in hospitalized children in Kota Bharu, Malaysia. Southeast Asian J Trop Med Public Health 2001; 32:319-22. (Pubitemid 33641783)
85. Mertens TE, Wijenayake R, Pinto MR, et al. Microbiological agents associated with childhood diarrhoea in the dry zone of Sri Lanka. Trop Med Parasitol 1990; 41:115-20. (Pubitemid 20145132)
86. Mubashir M, Khan A, Baqai R, et al. Causative agents of acute diarrhoea in the first 3 years of life: hospital-based study. J Gastroenterol Hepatol 1990; 5:264-70. (Pubitemid 20375187)
87. Nahrevanian H, Assmar M, Samin MG. Cryptosporidiosis among immunocompetent patients with gastroenteritis in Iran: a comparison with other enteropathogenic parasites. J Microbiol Immunol Infect 2007; 40:154-6. (Pubitemid 46999321)
88. Ogunsanya TI, Rotimi VO, Adenuga A. A study of the aetiological agents of childhood diarrhoea in Lagos, Nigeria. J Med Microbiol 1994; 40:10-4. (Pubitemid 24041817)
89. Opintan JA, Newman MJ, Ayeh-Kumi PF, et al. Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg 2010; 83:936-43.
90. Orlandi PP, Magalhaes GF, Matos NB, et al. Etiology of diarrheal infections in children of Porto Velho (Rondonia, Western Amazon region, Brazil). Braz J Med Biol Res 2006; 39:507-17.
91. Orlandi PP, Silva T, Magalhaes GF, et al. Enteropathogens associated with diarrheal disease in infants of poor urban areas of Porto Velho, Rondonia: a preliminary study. Mem Inst Oswaldo Cruz 2001; 96:621-5. (Pubitemid 33704161)
92. Oyofo BA, Subekti D, Tjaniadi P, et al. Enteropathogens associated with acute diarrhea in community and hospital patients in Jakarta, Indonesia. FEMS Immunol Med Microbiol 2002; 34:139-46.
93. Paniagua GL, Monroy E, Garcia-Gonzalez O, Alonso J, Negrete E, Vaca S. Two or more enteropathogens are associated with diarrhoea in Mexican children. Ann Clin Microbiol Antimicrob 2007; 6:17.
94. Sallon S, el-Shawwa R, Khalil M, et al. Diarrhoeal disease in children in Gaza. Ann Trop Med Parasitol 1994; 88:175-82. (Pubitemid 24201902)
95. Sanchez-Vega JT, Tay-Zavala J, Aguilar-Chiu A, et al. Cryptosporidiosis and other intestinal protozoan infections in children less than one year of age in Mexico City. Am J Trop Med Hyg 2006; 75:1095-8. (Pubitemid 351627488)
96. Simango C, Dindiwe J. The aetiology of diarrhoea in a farming community in Zimbabwe. Trans R Soc Trop Med Hyg 1987; 81: 552-3.
97. Ming ZF, Xi ZD, Dong CS, et al. Diarrhoeal disease in children less than one year of age at a children's hospital in Guangzhou, People's Republic of China. Trans R Soc Trop Med Hyg 1991; 85:667-9.
98. Meng CY, Smith BL, Bodhidatta L, et al. Etiology of diarrhea in young children and patterns of antibiotic resistance in Cambodia. Pediatr Infect Dis J 2011; 30:331-5.
99. Househam KC, Dove MG, Smith MS. Enteropathogens associated with acute infantile diarrhoea in Bloemfontein, South Africa. J Trop Pediatr 1987; 33:287-8.
100. Ajjampur SS, Rajendran P, Ramani S, et al. Closing the diarrhoea diagnostic gap in Indian children by the application of molecular techniques. J Med Microbiol 2008; 57(Pt 11):1364-8.
101. Na'was TE, Abo-Shehada MN. A study of the bacterial and parasitic causes of acute diarrhoea in northern Jordan. J Diarrhoeal Dis Res 1991; 9:305-9.
102. Stintzing G, Mollby R, Habte D. Enterotoxigenic Escherichia coli and other enteropathogens in paediatric diarrhoea in Addis Ababa. Acta Paediatr Scand 1982; 71:279-86. (Pubitemid 12165811)
103. Hoge CW, Echeverria P, Rajah R, et al. Prevalence of Cyclospora species and other enteric pathogens among children less than 5 years of age in Nepal. J Clin Microbiol 1995; 33:3058-60.
104. Rajeshwari K, Jaggi N, Aggarwal V, Kalra KK, Mittal SK, Baveja U. Determinants of symptomatic giardiasis in childhood. Trop Gastroenterol 1996; 17:70-6.
105. Haque R, Roy S, Kabir M, Stroup SE, Mondal D, Houpt ER. Giardia assemblage A infection and diarrhea in Bangladesh. J Infect Dis 2005; 192:2171-3. (Pubitemid 41779218)
106. Bhandari N, Bahl R, Dua T, Kumar R, Srivastava R. Role of protozoa as risk factors for persistent diarrhea. Indian J Pediatr 1999; 66:21-6. (Pubitemid 29313525)
107. Sullivan PB, Marsh MN, Phillips MB, et al. Prevalence and treatment of giardiasis in chronic diarrhoea and malnutrition. Arch Dis Child 1991; 66:304-6.
108. Yakoob J, Abbas Z, Beg MA, et al. Prevalences of Giardia lamblia and Cryptosporidium parvum infection in adults presenting with chronic diarrhoea. Ann Trop Med Parasitol 2010; 104:505-10.
109. Mukhopadhyay C, Wilson G, Pradhan D, Shivananda PG. Intestinal protozoal infestation profile in persistent diarrhea in children below age 5 years in western Nepal. Southeast Asian J Trop Med Public Health 2007; 38:13-9.
110. Guerrant RL, Kirchhoff LV, Shields DS, et al. Prospective study of diarrheal illnesses in northeastern Brazil: patterns of disease, nutritional impact, etiologies, and risk factors. J Infect Dis 1983; 148:986-97. (Pubitemid 14206300)
111. Newman RD, Moore SR, Lima AA, Nataro JP, Guerrant RL, Sears CL. A longitudinal study of Giardia lamblia infection in north-east Brazilian children. Trop Med Int Health 2001; 6:624-34. (Pubitemid 32830482)
112. Zaki AM, DuPont HL, el Alamy MA, et al. The detection of enteropathogens in acute diarrhea in a family cohort population in rural Egypt. Am J Trop Med Hyg 1986; 35:1013-22. (Pubitemid 17172954)
113. Schorling JB, Wanke CA, Schorling SK, McAuliffe JF, de Souza MA, Guerrant RL. A prospective study of persistent diarrhea among children in an urban Brazilian slum. Patterns of occurrence and etiologic agents. Am J Epidemiol 1990; 132:144-56. (Pubitemid 20203312)
114. Chunge RN, Nagelkerke N, Karumba PN, et al. Longitudinal study of young children in Kenya: intestinal parasitic infection with special reference to Giardia lamblia, its prevalence, incidence and duration, and its association with diarrhoea and with other parasites. Acta Trop 1991; 50:39-49.
115. Molbak K, Wested N, Hojlyng N, et al. The etiology of early childhood diarrhea: a community study from Guinea-Bissau. J Infect Dis 1994; 169:581-7.
116. Black RE, Lopez de Romana G, Brown KH, Bravo N, Bazalar OG, Kanashiro HC. Incidence and etiology of infantile diarrhea and major routes of transmission in Huascar, Peru. Am J Epidemiol 1989; 129:785-99. (Pubitemid 19094256)
117. Baqui AH, Sack RB, Black RE, et al. Enteropathogens associated with acute and persistent diarrhea in Bangladeshi children less than 5 years of age. J Infect Dis 1992; 166:792-6.
118. Hasan KZ, Pathela P, Alam K, et al. Aetiology of diarrhoea in a birth cohort of children aged 0-2 year(s) in rural Mirzapur, Bangladesh. J Health Popul Nutr 2006; 24:25-35. (Pubitemid 43984536)
119. Kaminsky RG. Parasitism and diarrhoea in children from two rural communities and marginal barrio in Honduras. Trans R Soc Trop Med Hyg 1991; 85:70-3.
120. Valentiner-Branth P, Steinsland H, Fischer TK, et al. Cohort study of Guinean children: incidence, pathogenicity, conferred protection, and attributable risk for enteropathogens during the first 2 years of life. J Clin Microbiol 2003; 41:4238-45. (Pubitemid 37099690)
121. Boeke CE, Mora-Plazas M, Forero Y, Villamor E. Intestinal protozoan infections in relation to nutritional status and gastrointestinal morbidity in Colombian school children. J Trop Pediatr 2010; 56:299-306.
122. Fraser D, Bilenko N, Deckelbaum RJ, Dagan R, El-On J, Naggan L. Giardia lamblia carriage in Israeli Bedouin infants: risk factors and consequences. Clin Infect Dis 2000; 30:419-24. (Pubitemid 30205282)
123. Fraser D, Dagan R, Naggan L, et al. Natural history of Giardia lamblia and Cryptosporidium infections in a cohort of Israeli Bedouin infants: a study of a population in transition. Am J Trop Med Hyg 1997; 57:544-9. (Pubitemid 27500457)
124. Shah N, DuPont HL, Ramsey DJ. Global etiology of travelers' diarrhea: systematic review from 1973 to the present. Am J Trop Med Hyg 2009; 80:609-14.
125. Riddle MS, Sanders JW, Putnam SD, Tribble DR. Incidence, etiology, and impact of diarrhea among long-term travelers (US military and similar populations): a systematic review. Am J Trop Med Hyg 2006; 74:891-900. (Pubitemid 46774414)
126. Black RE. Pathogens that cause travelers' diarrhea in Latin America and Africa. Rev Infect Dis 1986; 8(suppl 2):S131-5.
127. Back E, Jonsson M, Wadstrom T. Enterotoxin-producing bacteria stools from Swedish United Nations soldiers in Cyprus. Infection 1978; 6:116-20. (Pubitemid 8361851)
128. Shlim DR, Hoge CW, Rajah R, Rabold JG, Echeverria P. Is Blastocystis hominis a cause of diarrhea in travelers? A prospective controlled study in Nepal. Clin Infect Dis 1995; 21:97-101.
129. 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. (Pubitemid 43736379)
130. Paschke C, Apelt N, Fleischmann E, et al. Controlled study on enteropathogens in travellers returning from the tropics with and without diarrhoea. Clin Microbiol Infect 2011; 17:1194-200.
131. Pandey P, Bodhidatta L, Lewis M, et al. Travelers' diarrhea in Nepal: an update on the pathogens and antibiotic resistance. J Travel Med 2011; 18:102-8.
132. DuPont HL, Olarte J, Evans DG, Pickering LK, Galindo E, Evans DJ. Comparative susceptibility of Latin American and United States students to enteric pathogens. N Engl J Med 1976; 295:1520-1. (Pubitemid 8014698)
133. Brodsky RE, Spencer HC Jr., Schultz MG. Giardiasis in American travelers to the Soviet Union. J Infect Dis 1974; 130:319-23.
134. Bolivar R, Conklin RH, Vollet JJ, et al. Rotavirus in travelers' diarrhea: study of an adult student population in Mexico. J Infect Dis 1978; 137:324-7. (Pubitemid 8309151)
135. Echeverria P, Blacklow NR, Zipkin C, et al. Etiology of gastroenteritis among Americans living in the Philippines. Am J Epidemiol 1979; 109:493-501. (Pubitemid 10201099)
136. Hoge CW, Shlim DR, Rajah R, et al. Epidemiology of diarrhoeal illness associated with coccidian-like organism among travellers and foreign residents in Nepal. Lancet 1993; 341:1175-9. (Pubitemid 23137113)
137. Gascon J, Vargas M, Quinto L, Corachan M, Jimenez de Anta MT, Vila J. Enteroaggregative Escherichia coli strains as a cause of traveler's diarrhea: a case-control study. J Infect Dis 1998; 177:1409-12. (Pubitemid 28194290)
138. Schultsz C, van den Ende J, Cobelens F, et al. Diarrheagenic Escherichia coli and acute and persistent diarrhea in returned travelers. J Clin Microbiol 2000; 38:3550-4.
139. Andersson T, Forssell J, Sterner G. Outbreak of giardiasis: effect of a new antiflagellate drug, tinidazole. Br Med J 1972; 2:449-51.
140. Merson MH, Morris GK, Sack DA, et al. Travelers' diarrhea in Mexico. A prospective study of physicians and family members attending a congress. N Engl J Med 1976; 294:1299-305.
141. Cevallos A, Carnaby S, James M, Farthing JG. Small intestinal injury in a neonatal rat model of giardiasis is strain dependent. Gastroenterology 1995; 109:766-73.
142. Read C, Walters J, Robertson ID, Thompson RC. Correlation between genotype of Giardia duodenalis and diarrhoea. Int J Parasitol 2002; 32:229-31. (Pubitemid 34112630)
143. Aydin AF, Besirbellioglu BA, Avci IY, Tanyuksel M, Araz E, Pahsa A. Classification of Giardia duodenalis parasites in Turkey into groups A and B using restriction fragment length polymorphism. Diagn Microbiol Infect Dis 2004; 50:147-51. (Pubitemid 39335852)
144. Al-Mohammed HI. Genotypes of Giardia intestinalis clinical isolates of gastrointestinal symptomatic and asymptomatic Saudi children. Parasitol Res 2011; 108:1375-81.
145. Ajjampur SS, Sankaran P, Kannan A, et al. Giardia duodenalis assemblages associated with diarrhea in children in South India identified by PCR-RFLP. Am J Trop Med Hyg 2009; 80:16-9.
146. Molina N, Minvielle M, Grenovero S, Salomon C, Basualdo J. High prevalences of infection with Giardia intestinalis genotype B among children in urban and rural areas of Argentina. Ann Trop Med Parasitol 2011; 105:299-309.
147. Paintlia AS, Descoteaux S, Spencer B, et al. Giardia lamblia groups A and B among young adults in India. Clin Infect Dis 1998; 26:190-1. (Pubitemid 28068181)
148. Sahagun J, Clavel A, Goni P, et al. Correlation between the presence of symptoms and the Giardia duodenalis genotype. Eur J Clin Microbiol Infect Dis 2008; 27:81-3. (Pubitemid 350197877)
149. Homan WL, Mank TG. Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol 2001; 31:822-6. (Pubitemid 32524167)
150. Kohli A, Bushen OY, Pinkerton RC, et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg 2008; 102:718-25.
151. Lebbad M, Petersson I, Karlsson L, et al. Multilocus genotyping of human Giardia isolates suggests limited zoonotic transmission and association between assemblage B and flatulence in children. PLoS Negl Trop Dis 2011; 5:e1262.
152. Mahmud MA, Chappell CL, Hossain MM, Huang DB, Habib M, DuPont HL. Impact of breast-feeding on Giardia lamblia infections in Bilbeis, Egypt. Am J Trop Med Hyg 2001; 65:257-60. (Pubitemid 32847821)
153. Miotti PG, Gilman RH, Santosham M, Ryder RW, Yolken RH. Agerelated rate of seropositivity of antibody to Giardia lamblia in four diverse populations. J Clin Microbiol 1986; 24:972-5. (Pubitemid 17193351)
154. Wright RA, Spencer HC, Brodsky RE, Vernon TM. Giardiasis in Colorado: an epidemiologic study. Am J Epidemiol 1977; 105:330-6. (Pubitemid 8086388)
155. Morrow AL, Reves RR, West MS, Guerrero ML, Ruiz-Palacios GM, Pickering LK. Protection against infection with Giardia lamblia by breast-feeding in a cohort of Mexican infants. J Pediatr 1992; 121:363-70.
156. Walterspiel JN, Morrow AL, Guerrero ML, Ruiz-Palacios GM, Pickering LK. Secretory anti-Giardia lamblia antibodies in human milk: protective effect against diarrhea. Pediatrics 1994; 93:28-31. (Pubitemid 24012124)
157. Gillin FD, Reiner DS, Wang CS. Human milk kills parasitic intestinal protozoa. Science 1983; 221:1290-2. (Pubitemid 13001279)
158. Hernell O, Ward H, Blackberg L, Pereira ME. Killing of Giardia lamblia by human milk lipases: an effect mediated by lipolysis of milk lipids. J Infect Dis 1986; 153:715-20. (Pubitemid 16133753)
159. Neto UF, Martins MCD, Lima FLD, Patricio FRS, Toledo MRF. Asymptomatic environmental enteropathy among slum-dwelling infants. J Am Coll Nutr 1994; 13:51-6. (Pubitemid 24037981)
160. Anderson CM, Langford RF. Bacterial content of small intestine of children in health, in coeliac disease, and in fibrocystic disease of pancreas. Br Med J 1958; 1:803-6.
161. Fagundes-Neto U, Viaro T, Wehba J, Patricio FR, Machado NL. Tropical enteropathy (environmental enteropathy) in early childhood: a syndrome caused by contaminated environment. J Trop Pediatr 1984; 30:204-9. (Pubitemid 14049854)
162. dos Reis JC, de Morais MB, Oliva CA, Fagundes-Neto U. Breath hydrogen test in the diagnosis of environmental enteropathy in children living in an urban slum. Dig Dis Sci 2007; 52:1253-8. (Pubitemid 46626168)
163. Zenian A, Gillin FD. Interactions of Giardia lamblia with human intestinal mucus: enhancement of trophozoite attachment to glass. J Protozool 1985; 32:664-8. (Pubitemid 16204086)
164. Singer SM, Nash TE. The role of normal flora in Giardia lamblia infections in mice. J Infect Dis 2000; 181:1510-2. (Pubitemid 30252567)
165. Hanevik K, Hausken T, Morken MH, et al. Persisting symptoms and duodenal inflammation related to Giardia duodenalis infection. J Infect 2007; 55:524-30. (Pubitemid 350082473)
166. Kent GP, Greenspan JR, Herndon JL, et al. Epidemic giardiasis caused by a contaminated public water supply. Am J Public Health 1988; 78:139-43. (Pubitemid 18036050)
167. Prucca CG, Rivero FD, Lujan HD. Regulation of antigenic variation in Giardia lamblia. Annu Rev Microbiol 2011; 65:611-30.
168. Nash TE, Herrington DA, Levine MM, Conrad JT, Merritt JW Jr. Antigenic variation of Giardia lamblia in experimental human infections. J Immunol 1990; 144:4362-9. (Pubitemid 20187781)
169. Nash TE. Surface antigenic variation in Giardia lamblia. Mol Microbiol 2002; 45:585-90. (Pubitemid 34989167)
170. Nash TE, Lujan HT, Mowatt MR, Conrad JT. Variant-specific surface protein switching in Giardia lamblia. Infect Immun 2001; 69:1922-3. (Pubitemid 32187657)
171. Singer SM, Elmendorf HG, Conrad JT, Nash TE. Biological selection of variant-specific surface proteins in Giardia lamblia. J Infect Dis 2001; 183:119-24. (Pubitemid 32043049)
172. Ali SA, Hill DR. Giardia intestinalis. Curr Opin Infect Dis 2003; 16:453-60. (Pubitemid 37267264)
173. McCardell BA, Madden JM, Stanfield JT, Tall BD, Stephens MJ. Binding of cholera toxin to Giardia lamblia. J Clin Microbiol 1987; 25:1786-8. (Pubitemid 17135195)
174. Ljungstrom I, Holmgren J, Svennerholm AM, Ferrante A. Changes in intestinal fluid and mucosal immune responses to cholera toxin in Giardia muris infection and binding of cholera toxin to Giardia muris trophozoites. Infect Immun 1985; 50:243-9. (Pubitemid 15239216)