Extra-intestinal and long term consequences of Giardia duodenalis infections

World Journal of Gastroenterology

Volumn 19, Issue 47, 2013, Pages 8974-8985

  Halliez, Marie C M ^a,b   Buret, André G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b ROUEN UNIVERSITY HOSPITAL   (France)

Author keywords

Extra intestinal manifestations of enteritis; Failure to thrive; Giardiasis; Inflammatory disorders; Post infectious irritable bowel syndrome

Indexed keywords

ANTIINFECTIVE AGENT; CORTICOSTEROID; IMMUNOGLOBULIN E; METRONIDAZOLE;

ARTHRITIS; CELL PROLIFERATION; CHRONIC FATIGUE SYNDROME; COGNITIVE DEFECT; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE TRANSMISSION; GIARDIA LAMBLIA; GIARDIASIS; HUMAN; IMMUNE RESPONSE; INCIDENCE; IRRITABLE COLON; MUSCLE NECROSIS; PARASITE CLEARANCE; PATHOPHYSIOLOGY; PREVALENCE; REVIEW; SOCIOECONOMICS; STUNTING;

EXTRA-INTESTINAL MANIFESTATIONS OF ENTERITIS; FAILURE TO THRIVE; GIARDIASIS; INFLAMMATORY DISORDERS; POST-INFECTIOUS IRRITABLE BOWEL SYNDROME;

ANTIPROTOZOAL AGENTS; COGNITION DISORDERS; FAILURE TO THRIVE; GIARDIA LAMBLIA; GIARDIASIS; GROWTH DISORDERS; HUMANS; IRRITABLE BOWEL SYNDROME; NUTRITIONAL STATUS; TIME FACTORS; TREATMENT OUTCOME;

EID: 84890950148     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i47.8974     Document Type: Review

References (129)

1. World Health Organization. WHO guidelines for drinking water quality launched in 2004. Available from: URL: http//www.who.int/water_sanitation_health/dwq/gdwq3/en/
2. Savioli L, Smith H, Thompson A. Giardia and Cryptosporid-ium join the 'Neglected Diseases Initiative'. Trends Parasitol 2006; 22: 203-208 [PMID: 16545611]
3. Roxström-Lindquist K, Palm D, Reiner D, Ringqvist E, Svärd SG. Giardia immunity--an update. Trends Parasitol 2006; 22: 26-31 [PMID: 16303332]
4. Jensen LA, Marlin JW, Dyck DD, Laubach HE. Prevalence of multi-gastrointestinal infections with helminth, protozoan and Campylobacter spp. in Guatemalan children. J Infect Dev Ctries 2009; 3: 229-234 [PMID: 19759480]
5. Thompson RC. Echinococcus, Giardia and Cryptospo-ridium: observational studies challenging accepted dogma. Parasitology 2009; 136: 1529-1535 [PMID: 19366481 DOI: 10.1017/S0031182009005897]
6. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 2011; 24: 110-140 [PMID: 21233509 DOI: 10.1128/CMR.00033-10]
7. Buret A, denHollander N, Wallis PM, Befus D, Olson ME. Zoonotic potential of giardiasis in domestic ruminants. J Infect Dis 1990; 162: 231-237 [PMID: 2355197]
8. Solaymani-Mohammadi S, Singer SM. Giardia duodenalis: the double-edged sword of immune responses in giardia-sis. Exp Parasitol 2010; 126: 292-297 [PMID: 20599999 DOI: 10.1016/j.exppara.2010.06.014]
9. McDowall RM, Peregrine AS, Leonard EK, Lacombe C, Lake M, Rebelo AR, Cai HY. Evaluation of the zoonotic potential of Giardia duodenalis in fecal samples from dogs and cats in Ontario. Can Vet J 2011; 52: 1329-1333 [PMID: 22654138]
10. Cotton JA, Beatty JK, Buret AG. Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol 2011; 41: 925-933 [PMID: 21683702 DOI: 10.1016/ j.ijpara.2011.05.002]
11. Gillon J, Al-Thamery D, Ferguson A. Features of small intestinal pathology (epithelial cell kinetics, intraepithelial lymphocytes, disaccaridases) in a primary Giardia muris infection. Gut 1982; 23: 498-506 [PMID: 7076025]
12. Vinayak VK, Khanna R, Kum K. Kinetics of intraepithelium and lamina propria lymphocyte responses during Giardia lamblia infection in mice. Microb Pathog 1991; 10: 343-350 [PMID: 1836523]
13. Scott KG, Yu LC, Buret AG. Role of CD8+ and CD4+ T lymphocytes in jejunal mucosal injury during murine giardiasis. Infect Immun 2004; 72: 3536-3542 [PMID: 15155662]
14. Beatty J, Akierman S, Rioux K, Beck P, McKnight W, Feener T, Wallace J, Buret AG. Gut microbiota bioflm disruptions by Giardia: pathology in human enterocytes and germ-free mice. Experimental Biology 2013; Boston Convention & Exhibition Center April 20-24 [Meeting Abstracts]
15. Robertson LJ, Hanevik K, Escobedo AA, Mørch K, Lange-land N. Giardiasis--why do the symptoms sometimes never stop? Trends Parasitol 2010; 26: 75-82 [PMID: 20056486]
16. Buret A, Gall DG, Olson ME. Growth, activities of enzymes in the small intestine, and ultrastructure of microvillous border in gerbils infected with Giardia duodenalis. Parasitol Res 1991; 77: 109-114 [PMID: 2027878]
17. Buret AG. Pathophysiology of enteric infections with Giar-dia duodenalius. Parasite 2008; 15: 261-265 [PMID: 18814692]
18. Chin AC, Teoh DA, Scott KG, Meddings JB, Macnaughton WK, Buret AG. Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect Immun 2002; 70: 3673-3680 [PMID: 12065509]
19. Troeger H, Epple HJ, Schneider T, Wahnschaffe U, Ullrich R, Burchard GD, Jelinek T, Zeitz M, Fromm M, Schulzke JD. Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut 2007; 56: 328-335 [PMID: 16935925]
20. Koot BG, ten Kate FJ, Juffrie M, Rosalina I, Taminiau JJ, Benninga MA. Does Giardia lamblia cause villous atrophy in children?: A retrospective cohort study of the histo-logical abnormalities in giardiasis. J Pediatr Gastroenterol Nutr 2009; 49: 304-308 [PMID: 19525873 DOI: 10.1097/ MPG.0b013e31818de3c4]
21. Ankarklev J, Jerlström-Hultqvist J, Ringqvist E, Troell K, Svärd SG. Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 2010; 8: 413-422 [PMID: 20400969 DOI: 10.1186/1471-2334-10-4]
22. Buret AG, Bhargava A. Modulatory mechanisms of entero-cyte apoptosis by viral, bacterial and parasitic pathogens. Crit Rev Microbiol 2013 Jun 9; Epub ahead of print [PMID: 23297858 DOI: 10.3109/1040841X.2012.746952]
23. Panaro MA, Cianciulli A, Mitolo V, Mitolo CI, Acquafredda A, Brandonisio O, Cavallo P. Caspase-dependent apopto-sis of the HCT-8 epithelial cell line induced by the parasite Giardia intestinalis. FEMS Immunol Med Microbiol 2007; 51: 302-309 [PMID: 17714487]
24. O'Hara JR, Buret AG. Mechanisms of intestinal tight junc-tional disruption during infection. Front Biosci 2008; 13: 7008-7021 [PMID: 18508712]
25. Stadelmann B, Merino MC, Persson L, Svärd SG. Arginine consumption by the intestinal parasite Giardia intestina-lis reduces proliferation of intestinal epithelial cells. PLoS One 2012; 7: e45325 [PMID: 23028934 DOI: 10.137/journal. pone.0045325.Epub]
26. Scott KG, Meddings JB, Kirk DR, Lees-Miller SP, Buret AG. Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology 2002; 123: 1179-1190 [PMID: 12360480]
27. Gillrie MR, Krishnegowda G, Lee K, Buret AG, Robbins SM, Looareesuwan S, Gowda DC, Ho M. Src-family kinase dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood 2007; 110: 3426-3435 [PMID: 17693580]
28. Maia-Brigagão C, Morgado-Díaz JA, De Souza W. Giardia disrupts the arrangement of tight, adherens and desmosom-al junction proteins of intestinal cells. Parasitol Int 2012; 61: 280-287 [PMID: 22146155 DOI: 10.1016/j.pqrint.2011.11.002. Epub]
29. Teoh DA, Kamieniecki D, Pang G, Buret AG. Giardia lamblia rearranges F-actin and alpha-actinin in human colonic and duodenal monolayers and reduces transepithelial electrical resistance. J Parasitol 2000; 86: 800-806 [PMID: 10958459]
30. Buret AG, Mitchell K, Muench DG, Scott KG. Giardia lam-blia disrupts tight junctional ZO-1 and increases permeability in non-transformed human small intestinal epithelial monolayers: effects of epidermal growth factor. Parasitology 2002; 125: 11-19 [PMID: 12166516]
31. Erlandsen SL, Chase DG. Morphological alterations in the microvillous border of villous epithelial cells produced by intestinal microorganisms. Am J Clin Nutr 1974; 27: 1277-1286 [PMID: 4447094]
32. Jonas A, Flanagan PR, Forstner GG. Pathogenesis of muco-sal injury in the blind loop syndrome. Brush border enzyme activity and glycoprotein degradation. J Clin Invest 1977; 60: 1321-1330 [PMID: 410830]
33. Torres MF, Uetanabaro AP, Costa AF, Alves CA, Farias LM, Bambirra EA, Penna FJ, Vieira EC, Nicoli JR. Infuence of bacteria from the duodenal microbiota of patients with symptomatic giardiasis on the pathogenicity of Giardia duo-denalis in gnotoxenic mice. J Med Microbiol 2000; 49: 209-215 [PMID: 10707940]
34. Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, Sears CL, Lima AA, Guerrant RL. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg 2008; 102: 718-725 [PMID: 18485429 DOI: 10.1016/ j.trstmh.2008.03.002.Epub]
35. LoGalbo PR, Sampson HA, Buckley RH. Symptomatic giar-diasis in three patients with X-linked agammaglobulinemia. J Pediatr 1982; 101: 78-80 [PMID: 7201017]
36. Hacker VL, Stark D, Thomas S. Validation of the stroke aphasic depression questionnaire using the brief assessment schedule depression cards in an acute stroke sample. Br J Clin Psychol 2010; 49: 123-127 [PMID: 19712541 DOI: 10.1348/014466509X467440.Epub]
37. Farthing MJ, Mata L, Urrutia JJ, Kronmal RA. Natural history of Giardia infection of infants and children in rural Guatemala and its impact on physical growth. Am J Clin Nutr 1986; 43: 395-405 [PMID: 3953479]
38. Ettehad GH, Daryani A, Nemati A. Effect of Giardia infection on nutritional status in primary schoolchildren, in northwest Iran. Pak J Biol Sci 2010; 13: 229-234 [PMID: 20464945]
39. Ignatius R, Gahutu JB, Klotz C, Steininger C, Shyirambere C, Lyng M, Musemakweri A, Aebischer T, Martus P, Harms G, Mockenhaupt FP. High prevalence of Giardia duodenalis Assemblage B infection and association with underweight in Rwandan children. PLoS Negl Trop Dis 2012; 6: e1677 [PMID: 22720102 DOI: 10.137/journal.pntd.0001677.Epub]
40. Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 2002; 359: 564-571 [PMID: 11867110]
41. Niehaus MD, Moore SR, Patrick PD, Derr LL, Lorntz B, Lima AA, Guerrant RL. Early childhood diarrhea is associated with diminished cognitive function 4 to 7 years later in children in a northeast Brazilian shantytown. Am J Trop Med Hyg 2002; 66: 590-593 [PMID: 12201596]
42. Olson ME, McAllister TA, Deselliers L, Morck DW, Cheng KJ, Buret AG, Ceri H. Effects of giardiasis on production in a domestic ruminant (lamb) model. Am J Vet Res 1995; 56: 1470-1474 [PMID: 8585658]
43. Geurden T, Vercruysse J, Claerebout E. Field testing of a fen-bendazole treatment combined with hygienic and management measures against a natural Giardia infection in calves. Vet Parasitol 2006; 142: 367-371 [PMID: 16959430]
44. Geurden T, Vandenhoute E, Pohle H, Casaert S, De Wilde N, Vercruysse J, Claerebout E. The effect of a fenbenda-zole treatment on cyst excretion and weight gain in calves experimentally infected with Giardia duodenalis. Vet Parasitol 2010; 169: 18-23 [PMID: 20089358 DOI: 10.1016/ j,vetpar.2009.12.027.Epub]
45. Sweeny JP, Ryan UM, Robertson ID, Jacobson C. Cryp-tosporidium and Giardia associated with reduced lamb carcase productivity. Vet Parasitol 2011; 182: 127-139 [PMID: 21719199 DOI: 10.1016/j.vetpar.2011.05.050.Epub]
46. Cantey PT, Roy S, Lee B, Cronquist A, Smith K, Liang J, Beach MJ. Study of nonoutbreak giardiasis: novel findings and implications for research. Am J Med 2011; 124: 1175.e1-1175.e8 [PMID: 22014792 DOI: 10.1016/ j.amjmed.2011.06.012.Epub]
47. Barraquer I. Sur la coïncidence de la lambliase et de cer-taineslésions du fond de l'oeil. Bulletin de la Sociétéde Patholo-gie Exotique 1938; 31: 55-58
48. Pettoello Mantovani M, Giardino I, Magli A, di Martino L, Guandalini S. Intestinal giardiasis associated with ophthal-mologic changes. J Pediatr Gastroenterol Nutr 1990; 11: 196-200 [PMID: 2395058]
49. Corsi A, Nucci C, Knafelz D, Bulgarini D, Di Iorio L, Polito A, De Risi F, Ardenti Morini F, Paone FM. Ocular changes associated with Giardia lamblia infection in children. Br J Ophthalmol 1998; 82: 59-62 [PMID: 9536883]
50. Carlson DW, Finger DR. Beaver fever arthritis. J Clin Rheu-matol 2004; 10: 86-88 [PMID: 17043473]
51. Borman P, Seçkin U, Ozoran K. Beaver fever--a rare cause of reactive arthritis. J Rheumatol 2001; 28: 683 [PMID: 11296987]
52. Hill Gaston JS, Lillicrap MS. Arthritis associated with enteric infection. Best Pract Res Clin Rheumatol 2003; 17: 219-239 [PMID: 12787523]
53. Gaston JS, Cox C, Granfors K. Clinical and experimental evidence for persistent Yersinia infection in reactive arthritis. Arthritis Rheum 1999; 42: 2239-2242 [PMID: 10524699]
54. Giacometti A, Cirioni O, Antonicelli L, D'Amato G, Silvestri C, Del Prete MS, Scalise G. Prevalence of intestinal parasites among individuals with allergic skin diseases. J Parasitol 2003; 89: 490-492 [PMID: 12880246]
55. Di Prisco MC, Hagel I, Lynch NR, Jiménez JC, Rojas R, Gil M, Mata E. Association between giardiasis and allergy. Ann Allergy Asthma Immunol 1998; 81: 261-265 [PMID: 9759805]
56. Hardin JA, Buret AG, Olson ME, Kimm MH, Gall DG. Mast cell hyperplasia and increased macromolecular uptake in an animal model of giardiasis. J Parasitol 1997; 83: 908-912 [PMID: 9379297]
57. Pietrzak A, Chodorowska G, Urban J, Bogucka V, Dybiec E. Cutaneous manifestation of giardiasis - case report. Ann Ag-ric Environ Med 2005; 12: 299-303 [PMID: 16457489]
58. Nenoff P, Domula E, Willing U, Herrmann J. Giardia lamblia--cause of urticaria and pruritus or accidental association?. Hautarzt 2006; 57: 518-520, 521-522 [PMID: 15875147]
59. Cervelló A, Alfaro A, Chumillas MJ. Hypokalemic myopa-thy induced by Giardia lamblia. N Engl J Med 1993; 329: 210-211 [PMID: 8515799]
60. Genovese A, Spadaro G, Santoro L, Gasparo Rippa P, On-orati AM, Marone G. Giardiasis as a cause of hypokalemic myopathy in congenital immunodefciency. Int J Clin Lab Res 1996; 26: 132-135 [PMID: 8856367]
61. Addiss DG, Lengerich EJ. Hypokalemic myopathy induced by Giardia lamblia. N Engl J Med 1994; 330: 66-67 [PMID: 8259154]
62. Araújo NS, Mundim MJ, Gomes MA, Amorim RM, Viana JC, Queiroz RP, Rossi MA, Cury MC. Giardia duodenalis: pathological alterations in gerbils, Meriones unguiculatus, infected with different dosages of trophozoites. Exp Parasitol 2008; 118: 449-457 [PMID: 18083166]
63. Simsek Z, Zeyrek FY, Kurcer MA. Effect of Giardia infection on growth and psychomotor development of children aged 0-5 years. J Trop Pediatr 2004; 50: 90-93 [PMID: 15088797]
64. Botero-Garcés JH, García-Montoya GM, Grisales-Patiño D, Aguirre-Acevedo DC, Alvarez-Uribe MC. Giardia intesti-nalis and nutritional status in children participating in the complementary nutrition program, Antioquia, Colombia, May to October 2006. Rev Inst Med Trop Sao Paulo 2009; 51: 155-162 [PMID: 19551290]
65. Thompson RC, Reynoldson JA, Mendis AH. Giardia and giardiasis. Adv Parasitol 1993; 32: 71-160 [PMID: 8237618]
66. Lengerich EJ, Addiss DG, Juranek DD. Severe giardiasis in the United States. Clin Infect Dis 1994; 18: 760-763 [PMID: 8075266]
67. Koruk I, Simsek Z, Tekin Koruk S, Doni N, Gürses G. Intestinal parasites, nutritional status and physchomotor development delay in migratory farm worker's children. Child Care Health Dev 2010; 36: 888-894 [PMID: 20645989 DOI: 10.1111/ j.1365-2214.2010.01126.x]
68. Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL. Association of early childhood diarrhea and cryptosporidiosis with impaired physical ftness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am J Trop Med Hyg 1999; 61: 707-713 [PMID: 10586898]
69. Veenemans J, Mank T, Ottenhof M, Baidjoe A, Mbugi EV, Demir AY, Wielders JP, Savelkoul HF, Verhoef H. 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 [PMID: 21666789 DOI: 10.137/journal.pntd.0001158.Epub]
70. Bergman P, Graham J. An approach to "failure to thrive". Aust Fam Physician 2005; 34: 725-729 [PMID: 16184203]
71. Loewenson R, Mason PR, Patterson BA. Giardiasis and the nutritional status of Zimbabwean schoolchildren. Ann Trop Paediatr 1986; 6: 73-78 [PMID: 2428298]
72. 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: 419-424 [PMID: 10722422]
73. Heyman M, Boudraa G, Sarrut S, Giraud M, Evans L, Tou-hami M, Desjeux JF. Macromolecular transport in jejunal mucosa of children with severe malnutrition: a quantitative study. J Pediatr Gastroenterol Nutr 1984; 3: 357-363 [PMID: 6737179]
74. Springer SC, Key JD. Vitamin B12 defciency and subclinical infection with Giardia lamblia in an adolescent with agam-maglobulinemia of Bruton. J Adolesc Health 1997; 20: 58-61 [PMID: 9007660]
75. Olness K. Effects on brain development leading to cognitive impairment: a worldwide epidemic. J Dev Behav Pediatr 2003; 24: 120-130 [PMID: 12692458]
76. Ajjampur SS, Koshy B, Venkataramani M, Sarkar R, Joseph AA, Jacob KS, Ward H, Kang G. Effect of cryptosporidial and giardial diarrhoea on social maturity, intelligence and physical growth in children in a semi-urban slum in south India. Ann Trop Paediatr 2011; 31: 205-212 [PMID: 21781414 DOI: 10.1179/1465328111Y.0000000003]
77. Celiksöz A, Aciöz M, Deǧerli S, Cinar Z, Elaldi N, Erandaç M. Effects of giardiasis on school success, weight and height indices of primary school children in Turkey. Pediatr Int 2005; 47: 567-571 [PMID: 16190966]
78. Quihui L, Morales GG, Méndez RO, Leyva JG, Esparza J, Valencia ME. Could giardiasis be a risk factor for low zinc status in schoolchildren from northwestern Mexico? A cross-sectional study with longitudinal follow-up. BMC Public Health 2010; 10: 85 [PMID: 20170531 DOI: 10.1186/1471-2458-10-85]
79. Quihui-Cota L, Méndez Estrada RO, Astiazarán-García H, Morales-Figueroa GG, Moreno-Reyes MJ, Cuadras-Romo D, Canett-Romero R. Changes in serum zinc levels associated with giardiasis and dietary zinc intake in mice. Biol Trace Elem Res 2012; 145: 396-402 [PMID: 21952867 DOI: 10.1007/ s12011-011-9208-5.Epub]
80. de Deungria M, Rao R, Wobken JD, Luciana M, Nelson CA, Georgieff MK. Perinatal iron deficiency decreases cytochrome c oxidase (CytOx) activity in selected regions of neonatal rat brain. Pediatr Res 2000; 48: 169-176 [PMID: 10926291]
81. Veenemans J, Schouten LR, Ottenhof MJ, Mank TG, Uges DR, Mbugi EV, Demir AY, Kraaijenhagen RJ, Savelkoul HF, Verhoef H. Effect of preventive supplementation with zinc and other micronutrients on non-malarial morbidity in Tanzanian pre-school children: a randomized trial. PLoS One 2012; 7: e41630 [PMID: 22870238 DOI: 10.1371/journal. pome.0041630.Epub]
82. Naess H, Nyland M, Hausken T, Follestad I, Nyland HI. Chronic fatigue syndrome after Giardia enteritis: clinical characteristics, disability and long-term sickness absence. BMC Gastroenterol 2012; 12: 13 [PMID: 22316329 DOI: 10.1186/1471-230X-12-13]
83. Mørch K, Hanevik K, Rortveit G, Wensaas KA, Eide GE, Hausken T, Langeland N. Severity of Giardia infection associated with post-infectious fatigue and abdominal symptoms two years after. BMC Infect Dis 2009; 9: 206 [PMID: 20003489 DOI: 10.1186/1471-2334-9-206]
84. Mørch K, Hanevik K, Rortveit G, Wensaas KA, Lange-land N. High rate of fatigue and abdominal symptoms 2 years after an outbreak of giardiasis. Trans R Soc Trop Med Hyg 2009; 103: 530-532 [PMID: 19185898 DOI: 10.1016/ j.trstmh.2009.01.010.Epub]
85. Wood NJ. Infection: Giardia lamblia is associated with an increased risk of both IBS and chronic fatigue that persists for at least 3 years. Nat Rev Gastroenterol Hepatol 2011; 8: 597 [PMID: 21989158 DOI: 10.1038/nrgastro.2011.176]
86. Wensaas KA, Langeland N, Hanevik K, Mørch K, Eide GE, Rortveit G. Irritable bowel syndrome and chronic fatigue 3 years after acute giardiasis: historic cohort study. Gut 2012; 61: 214-219 [PMID: 21911849 DOI: 10.1136/gutjnl-2011-300220. Epub]
87. Hanevik K, Kristoffersen EK, Sørnes S, Mørch K, Næss H, Rivenes AC, Bødtker JE, Hausken T, Langeland N. Immu-nophenotyping in post-giardiasis functional gastrointestinal disease and chronic fatigue syndrome. BMC Infect Dis 2012; 12: 258 [PMID: 23061432 DOI: 10.1186/1471-2334-12-258]
88. Natelson BH, Haghighi MH, Ponzio NM. Evidence for the presence of immune dysfunction in chronic fatigue syndrome. Clin Diagn Lab Immunol 2002; 9: 747-752 [PMID: 12093668]
89. Whitehead WE, Palsson O, Jones KR. Systematic review of the comorbidity of irritable bowel syndrome with other disorders: what are the causes and implications? Gastroenterol-ogy 2002; 122: 1140-1156 [PMID: 11910364]
90. Rodríguez LA, Ruigómez A. Increased risk of irritable bowel syndrome after bacterial gastroenteritis: cohort study. BMJ 1999; 318: 565-566 [PMID: 10037630]
91. Spiller RC. Role of infection in irritable bowel syndrome. J Gastroenterol 2007; 42 Suppl 17: 41-47 [PMID: 17238025]
92. Dizdar V, Gilja OH, Hausken T. Increased visceral sensitivity in Giardia-induced postinfectious irritable bowel syndrome and functional dyspepsia. Effect of the 5HT3-antag-onist ondansetron. Neurogastroenterol Motil 2007; 19: 977-982 [PMID: 17973637]
93. Hanevik K, Dizdar V, Langeland N, Hausken T. Development of functional gastrointestinal disorders after Giardia lamblia infection. BMC Gastroenterol 2009; 9: 27 [PMID: 19383162 DOI: 10.1186/1471-230X-9-27]
94. Spiller R. Clinical update: irritable bowel syndrome. Lancet 2007; 369: 1586-1588 [PMID: 17499587]
95. Thabane M, Marshall JK. Post-infectious irritable bowel syndrome. World J Gastroenterol 2009; 15: 3591-3596 [PMID: 19653335 DOI: 10.3748/wjg.15.3591]
96. Törnblom H, Lindberg G, Nyberg B, Veress B. Full-thickness biopsy of the jejunum reveals infammation and enteric neuropathy in irritable bowel syndrome. Gastroenterology 2002; 123: 1972-1979 [PMID: 12454854]
97. Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 2004; 126: 693-702 [PMID: 14988823]
98. Choudhury BK, Shi XZ, Sarna SK. Gene plasticity in colonic circular smooth muscle cells underlies motility dysfunction in a model of postinfective IBS. Am J Physiol Gastrointest Liver Physiol 2009; 296: G632-G642 [PMID: 19136376 DOI: 10.1152/ ajpgi.90673.2008.Epub]
99. Farthing MJ. Giardiasis. Gastroenterol Clin North Am 1996; 25: 493-515 [PMID: 8863037]
100. D'Anchino M, Orlando D, De Feudis L. Giardia lamblia infections become clinically evident by eliciting symptoms of irritable bowel syndrome. J Infect 2002; 45: 169-172 [PMID: 12387773]
101. Grazioli B, Matera G, Laratta C, Schipani G, Guarnieri G, Spiniello E, Imeneo M, Amorosi A, Focà A, Luzza F. Giardia lamblia infection in patients with irritable bowel syndrome and dyspepsia: a prospective study. World J Gastroenterol 2006; 12: 1941-1944 [PMID: 16610003]
102. 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 [PMID: 17070814]
103. Hanevik K, Hausken T, Morken MH, Strand EA, Mørch K, Coll P, Helgeland L, Langeland N. Persisting symptoms and duodenal infammation related to Giardia duodenalis infection. J Infect 2007; 55: 524-530 [PMID: 17964658]
104. Parkes GC, Brostoff J, Whelan K, Sanderson JD. Gastrointestinal microbiota in irritable bowel syndrome: their role in its pathogenesis and treatment. Am J Gastroen-terol 2008; 103: 1557-1567 [PMID: 18513268 DOI: 10.1111/ j.1572-0241.2008.01869.x.Epub]
105. Ghoshal UC, Ranjan P. Post-infectious irritable bowel syndrome: the past, the present and the future. J Gastroenterol Hepatol 2011; 26 Suppl 3: 94-101 [PMID: 21443719 DOI: 10.111/j.1440-1746.2011.06643.x]
106. Collins SM, Bercik P. The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 2009; 136: 2003-2014 [PMID: 19457424 DOI: 10.1053/ j.gastro.2009.01.075]
107. Collins SM, Denou E, Verdu EF, Bercik P. The putative role of the intestinal microbiota in the irritable bowel syndrome. Dig Liver Dis 2009; 41: 850-853 [PMID: 19740713 DOI: 10.1016/j.dld.2009.07.023]
108. Camilleri M, Di Lorenzo C. Brain-gut axis: from basic understanding to treatment of IBS and related disorders. J Pedi-atr Gastroenterol Nutr 2012; 54: 446-453 [PMID: 22027566 DOI: 10.1097/MPG.0b013e31823d34c3]
109. Bravo JA, Julio-Pieper M, Forsythe P, Kunze W, Dinan TG, Bienenstock J, Cryan JF. Communication between gastrointestinal bacteria and the nervous system. Curr Opin Pharmacol 2012; 12: 667-672 [PMID: 23041079 DOI: 10.1016/ j.coph.2012.09.010]
110. Fichna J, Storr MA. Brain-Gut Interactions in IBS. Front Pharmacol 2012; 3: 127 [PMID: 22783191 DOI: 10.3389/fphar.2012.00127]
111. Forsythe P, Kunze WA. Voices from within: gut microbes and the CNS. Cell Mol Life Sci 2013; 70: 55-69 [PMID: 22638926 DOI: 10.1007/s00018-012-1028-z]
112. Kalischuk LD, Buret AG. A role for Campylobacter jejuni-induced enteritis in infammatory bowel disease? Am J Physi-ol Gastrointest Liver Physiol 2010; 298: G1-G9 [PMID: 19875702 DOI: 10.1152/qjpgi.00193.2009.Epub]
113. Kurita A, Maguchi H, Takahashi K, Katanuma A, Osanai M, Kin T, Yane K, Hashigo S, Ohtsubo M. Small pancreatic cancer with giardiasis: a case report. Pancreas 2010; 39: 943-945 [PMID: 20664486 DOI: 10.1097/MPA.0b013e3181d7883c]
114. Furukawa M, Lee L, Ikegami T, Maeda T, Nishiyama K, Itaba S, Funakoshi A. Giardiasis in the pancreas accompanied by pancreatic cancer. Pancreas 2011; 40: 168-169 [PMID: 21160381 DOI: 10.1097/MPA.0b013e3181f6a1b9]
115. Mitchell CM, Bradford CM, Kapur U. Giardia lamblia tro-phozoites in an ultrasound-guided fne-needle aspiration of a pancreatic mucinous neoplasm. Diagn Cytopathol 2011; 39: 352-353 [PMID: 20730892 DOI: 10.1002/dc.21425.Epub]
116. Nagasaki T, Komatsu H, Shibata Y, Yamaguchi H, Nakashima M. A rare case of gallbladder cancer with giardiasis. Nihon Shokakibyo Gakkai Zasshi 2011; 108: 275-279 [PMID: 21307633]
117. Sarna SK. Lessons Learnt from Post-Infectious IBS. Front Physi-ol 2011; 2: 49 [PMID: 21897820 DOI: 10.2289/fphys.2011.00049. Epub]
118. Andersen YS, Gillin FD, Eckmann L. Adaptive immunity-dependent intestinal hypermotility contributes to host defense against Giardia spp. Infect Immun 2006; 74: 2473-2476 [PMID: 16552082]
119. Li E, Zhou P, Singer SM. Neuronal nitric oxide synthase is necessary for elimination of Giardia lamblia infections in mice. J Immunol 2006; 176: 516-521 [PMID: 16365445]
120. Li E, Zhao A, Shea-Donohue T, Singer SM. Mast cell-mediated changes in smooth muscle contractility during mouse giardiasis. Infect Immun 2007; 75: 4514-4518 [PMID: 17620354]
121. Buret A, Hardin JA, Olson ME, Gall DG. Pathophysiology of small intestinal malabsorption in gerbils infected with Giardia lamblia. Gastroenterology 1992; 103: 506-513 [PMID: 1634068]
122. Bénéré E, Van Assche T, Van Ginneken C, Peulen O, Cos P, Maes L. Intestinal growth and pathology of Giardia duode-nalis assemblage subtype A(I), A(II), B and E in the gerbil model. Parasitology 2012; 139: 424-433 [PMID: 22216783 DOI: 10.1017/S0031182011002137]
123. Gomes MA, de Oliveira DR, de Freitas SE, de Pinho Viana M, Borges EL. Effect of giardiasis combined with low-protein diet on intestinal absorption of glucose and electrolytes in gerbils. Exp Parasitol 2012; 131: 448-451 [PMID: 22659230 DOI: 10.1016/j.exppara.2012.04.016]
124. Valencia ME, McNeill G, Haggarty P, Moya SY, Pinelli A, Quihui L, Davalos R. Energetic consequences of mild Giar-dia intestinalis infestation in Mexican children. Am J Clin Nutr 1995; 61: 860-865 [PMID: 7702032]
125. 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: 624-634 [PMID: 11555428]
126. Muniz-Junqueira MI, Queiroz EF. Relationship between protein-energy malnutrition, vitamin A, and parasitoses in living in Brasília. Rev Soc Bras Med Trop 2002; 35: 133-141 [PMID: 12011921]
127. Sackey ME, Weigel MM, Armijos RX. Predictors and nutritional consequences of intestinal parasitic infections in rural Ecuadorian children. J Trop Pediatr 2003; 49: 17-23 [PMID: 12630715]
128. Matos SM, Assis AM, Prado Mda S, Strina A, Santos LA, Jesus SR, Barreto ML. Giardia duodenalis infection and anthropometric status in preschoolers in Salvador, Bahia State, Brazil. Cad Saude Publica 2008; 24: 1527-1535 [PMID: 18670676]
129. Lander RL, Lander AG, Houghton L, Williams SM, Costa-Ribeiro H, Barreto DL, Mattos AP, Gibson RS. Factors influencing growth and intestinal parasitic infections in preschoolers attending philanthropic daycare centers in Salvador, Northeast Region of Brazil. Cad Saude Publica 2012; 28: 2177-2188 [PMID: 23147959]