Skip to main content
Top
Published in: Diseases of the Colon & Rectum 6/2004

01-06-2004 | Original Contribution

Delay of the First Onset of Pouchitis by Oral Intake of the Probiotic Strain Lactobacillus rhamnosus GG

Authors: Martijn P. Gosselink, M.D., W. Rudolph Schouten, M.D., Ph.D., Leo M. C. van Lieshout, M.Sc., Willem C. J. Hop, M.Sc., Ph.D., Jon D. Laman, M.Sc., Ph.D., Johanneke G. H. Ruseler-van Embden, M.Sc., Ph.D.

Published in: Diseases of the Colon & Rectum | Issue 6/2004

Login to get access

PURPOSE:

Proctocolectomy with ileal pouch-anal anastomosis is the operation of choice for patients with refractory or fulminant ulcerative colitis. The most common long-term complication in these patients is pouchitis. This study was designed to investigate the efficacy of probiotic Lactobacillus rhamnosus GG in long-term delaying the first onset of pouchitis.

METHODS:

Between 1989 and 2001, a consecutive series of 127 patients presenting with ulcerative colitis underwent an ileal pouch-anal anastomosis at the Erasmus Medical Center in Rotterdam. Histopathologic investigation of the resected specimens revealed unsuspected Crohn’s disease in five patients. Postoperative complications resulted in pouch excision in five patients. The remaining 117 patients were included in this study. All episodes of pouchitis occurring in this group were analyzed. Pouchitis was diagnosed on the basis of clinical symptoms and endoscopic and histologic features. The 39 patients, who underwent an ileal pouch-anal anastomosis between 1996 and 2001, started immediately after the operation with the daily intake of L. rhamnosus GG in a fermented product. The 78 patients, in whom an ileal pouch-anal anastomosis was performed between 1989 and 1996, received no L. rhamnosus GG.

RESULTS:

Except for the duration of follow-up, the patient characteristics, indications for proctocolectomy, number of postoperative complications, and functional outcome were similar in both groups. First episodes of pouchitis were observed less frequently in patients with a daily intake of L. rhamnosus GG (cumulative risk at 3 years: 7 vs. 29 percent; P = 0.011).

CONCLUSIONS:

Daily intake of fermented products containing L. rhamnosus GG provides significant clinical benefit, without side effects. Based on the results of this study, we recommend a daily intake of Lactobacillus rhamnosus GG (dose 1–2 × 1010 bacteria) to delay the first onset of pouchitis.
Literature
1.
go back to reference Parks, AG, Nicholls, RJ 1978Proctocolectomy without ileostomy for ulcerative colitisBMJ2858 Parks, AG, Nicholls, RJ 1978Proctocolectomy without ileostomy for ulcerative colitisBMJ2858
2.
go back to reference Utsunomiya, J, Iwama, T, Imajo, M, et al. 1980Total colectomy, mucosal proctectomy, and ileoanal anastomosisDis Colon Rectum2345966 Utsunomiya, J, Iwama, T, Imajo, M,  et al. 1980Total colectomy, mucosal proctectomy, and ileoanal anastomosisDis Colon Rectum2345966
3.
go back to reference Johnson, E, Carlsen, E, Nazir, M, Nygaard, K 2001Morbidity and functional outcome after restorative proctocolectomy for ulcerative colitisEur J Surg167405 Johnson, E, Carlsen, E, Nazir, M, Nygaard, K 2001Morbidity and functional outcome after restorative proctocolectomy for ulcerative colitisEur J Surg167405
4.
go back to reference Fazio, VW, Ziv, Y, Church, JM, et al. 1995Ileal pouch-anal anastomoses complications and function in 1005 patientsAnn Surg2221207 Fazio, VW, Ziv, Y, Church, JM,  et al. 1995Ileal pouch-anal anastomoses complications and function in 1005 patientsAnn Surg2221207
5.
go back to reference Karlbom, U, Raab, Y, Ejerblad, S, Graf, W, Thorn, M, Pahlman, L 2000Factors influencing the functional outcome of restorative proctocolectomy in ulcerative colitisBr J Surg8714018 Karlbom, U, Raab, Y, Ejerblad, S, Graf, W, Thorn, M, Pahlman, L 2000Factors influencing the functional outcome of restorative proctocolectomy in ulcerative colitisBr J Surg8714018
6.
go back to reference Pemberton, JH 1993The problem with pouchitisGastroenterology104120911 Pemberton, JH 1993The problem with pouchitisGastroenterology104120911
7.
go back to reference Keighley, MR 1994Pouchitis. Br J Surg8110912 Keighley, MR 1994Pouchitis. Br J Surg8110912
8.
go back to reference Meagher, AP, Farouk, R, Dozois, RR, Kelly, KA, Pemberton, JH 1998J ileal pouch-anal anastomosis for chronic ulcerative colitis: complications and long-term outcome in 1310 patientsBr J Surg858003 Meagher, AP, Farouk, R, Dozois, RR, Kelly, KA, Pemberton, JH 1998J ileal pouch-anal anastomosis for chronic ulcerative colitis: complications and long-term outcome in 1310 patientsBr J Surg858003
9.
go back to reference Lohmuller, JL, Pemberton, JH, Dozois, RR, Ilstrup, D, van Heerden, J 1990Pouchitis and extraintestinal manifestations of inflammatory bowel disease after ileal pouch-anal anastomosisAnn Surg2116229 Lohmuller, JL, Pemberton, JH, Dozois, RR, Ilstrup, D, van Heerden, J 1990Pouchitis and extraintestinal manifestations of inflammatory bowel disease after ileal pouch-anal anastomosisAnn Surg2116229
10.
go back to reference Madden, MV, Farthing, MJ, Nicholls, RJ 1990Inflammation in ileal reservoirs: ‘pouchitis’Gut312479 Madden, MV, Farthing, MJ, Nicholls, RJ 1990Inflammation in ileal reservoirs: ‘pouchitis’Gut312479
11.
go back to reference Sandborn, WJ 1994Pouchitis following ileal pouch-anal anastomosis: definition, pathogenesis, and treatmentGastroenterology107185660 Sandborn, WJ 1994Pouchitis following ileal pouch-anal anastomosis: definition, pathogenesis, and treatmentGastroenterology107185660
12.
go back to reference Shepherd, NA, Hulten, L, Tytgat, GN, et al. 1989Pouchitis. Int J Colorectal Dis420529 Shepherd, NA, Hulten, L, Tytgat, GN,  et al. 1989Pouchitis. Int J Colorectal Dis420529
13.
go back to reference Shen, B, Achkar, JP, Lashner, BA, et al. 2001Endoscopic and histologic evaluation together with symptom assessment are required to diagnose pouchitisGastroenterology1212617 Shen, B, Achkar, JP, Lashner, BA,  et al. 2001Endoscopic and histologic evaluation together with symptom assessment are required to diagnose pouchitisGastroenterology1212617
14.
go back to reference Penna, C, Dozois, R, Tremaine, W, et al. 1996Pouchitis after ileal pouch-anal anastomosis for ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitisGut382349 Penna, C, Dozois, R, Tremaine, W,  et al. 1996Pouchitis after ileal pouch-anal anastomosis for ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitisGut382349
15.
go back to reference Stahlberg, D, Gullberg, K, Liljeqvist, L, Hellers, G, Lofberg, R 1996Pouchitis following pelvic pouch operation for ulcerative colitis: incidence, cumulative risk, and risk factorsDis Colon Rectum3910128 Stahlberg, D, Gullberg, K, Liljeqvist, L, Hellers, G, Lofberg, R 1996Pouchitis following pelvic pouch operation for ulcerative colitis: incidence, cumulative risk, and risk factorsDis Colon Rectum3910128
16.
go back to reference Svaninger, G, Nordgren, S, Oresland, T, Hulten, L 1993Incidence and characteristics of pouchitis in the Kock continent ileostomy and the pelvic pouchScand J Gastroenterol28695700 Svaninger, G, Nordgren, S, Oresland, T, Hulten, L 1993Incidence and characteristics of pouchitis in the Kock continent ileostomy and the pelvic pouchScand J Gastroenterol28695700
17.
go back to reference Sandborn, WJ, Tremaine, WJ, Batts, KP, Pemberton, JH, Phillips, SF 1994Pouchitis after ileal pouch-anal anastomosis: a Pouchitis Disease Activity IndexMayo Clin Proc6940915 Sandborn, WJ, Tremaine, WJ, Batts, KP, Pemberton, JH, Phillips, SF 1994Pouchitis after ileal pouch-anal anastomosis: a Pouchitis Disease Activity IndexMayo Clin Proc6940915
18.
go back to reference Hurst, RD, Molinari, M, Chung, TP, Rubin, M, Michelassi, F 1996Prospective study of the incidence, timing and treatment of pouchitis in 104 consecutive patients after restorative proctocolectomyArch Surg131497502 Hurst, RD, Molinari, M, Chung, TP, Rubin, M, Michelassi, F 1996Prospective study of the incidence, timing and treatment of pouchitis in 104 consecutive patients after restorative proctocolectomyArch Surg131497502
19.
go back to reference Setti Carraro, P, Talbot, IC, Nicholls, RJ 1994Long-term appraisal of the histological appearances of the ileal reservoir mucosa after restorative proctocolectomy for ulcerative colitisGut3517217 Setti Carraro, P, Talbot, IC, Nicholls, RJ 1994Long-term appraisal of the histological appearances of the ileal reservoir mucosa after restorative proctocolectomy for ulcerative colitisGut3517217
20.
go back to reference Mowschenson, PM, Critchlow, JF, Peppercorn, MA 2000Ileoanal pouch operation: long-term outcome with or without diverting ileostomyArch Surg1354636 Mowschenson, PM, Critchlow, JF, Peppercorn, MA 2000Ileoanal pouch operation: long-term outcome with or without diverting ileostomyArch Surg1354636
21.
go back to reference Hurst, RD, Chung, TP, Rubin, M, Michelassi, F 1998The implications of acute pouchitis on the long-term functional results after restorative proctocolectomyInflamm Bowel Dis42804 Hurst, RD, Chung, TP, Rubin, M, Michelassi, F 1998The implications of acute pouchitis on the long-term functional results after restorative proctocolectomyInflamm Bowel Dis42804
22.
go back to reference Korsgen, S, Keighley, MR 1997Causes of failure and life expectancy of the ileoanal pouchInt J Colorectal Dis1248 Korsgen, S, Keighley, MR 1997Causes of failure and life expectancy of the ileoanal pouchInt J Colorectal Dis1248
23.
go back to reference Lepisto, A, Luukkonen, P, Jarvinen, HJ 2002Cumulative failure rate of ileal pouch-anal anastomosis and quality of life after failureDis Colon Rectum45128994 Lepisto, A, Luukkonen, P, Jarvinen, HJ 2002Cumulative failure rate of ileal pouch-anal anastomosis and quality of life after failureDis Colon Rectum45128994
24.
go back to reference Fleshner, PR, Vasiliauskas, EA, Kam, LY, et al. 2001High level perinuclear antineutrophil cytoplasmic antibody (pANCA) in ulcerative colitis patients before colectomy predicts the development of chronic pouchitis after ileal pouch-anal anastomosisGut496717 Fleshner, PR, Vasiliauskas, EA, Kam, LY,  et al. 2001High level perinuclear antineutrophil cytoplasmic antibody (pANCA) in ulcerative colitis patients before colectomy predicts the development of chronic pouchitis after ileal pouch-anal anastomosisGut496717
25.
go back to reference Ruseler-van Embden, JG, Schouten, WR, Lieshout, LM 1994Pouchitis: result of microbial imbalance?Gut3565864 Ruseler-van Embden, JG, Schouten, WR, Lieshout, LM 1994Pouchitis: result of microbial imbalance?Gut3565864
26.
go back to reference Ouwehand, AC, Salminen, S, Isolauri, E 2002Probiotics: an overview of beneficial effectsAntonie Van Leeuwenhoek8227989 Ouwehand, AC, Salminen, S, Isolauri, E 2002Probiotics: an overview of beneficial effectsAntonie Van Leeuwenhoek8227989
27.
go back to reference Gionchetti, P, Rizzello, F, Helwig, U, et al. 2003Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trialGastroenterology12412029 Gionchetti, P, Rizzello, F, Helwig, U,  et al. 2003Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trialGastroenterology12412029
28.
go back to reference Gionchetti, P, Rizzello, F, Venturi, A, et al. 2000Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trialGastroenterology1193059 Gionchetti, P, Rizzello, F, Venturi, A,  et al. 2000Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trialGastroenterology1193059
29.
go back to reference Gorbach SL, Goldin BR. Lactobacillus strains and methods of isolation. United States, 1989, US patent 4,839,281. Gorbach SL, Goldin BR. Lactobacillus strains and methods of isolation. United States, 1989, US patent 4,839,281.
30.
go back to reference Schultz, M, Sartor, RB 2000Probiotics and inflammatory bowel diseasesAm J Gastroenterol95S1921 Schultz, M, Sartor, RB 2000Probiotics and inflammatory bowel diseasesAm J Gastroenterol95S1921
31.
go back to reference Malin, M, Suomalainen, H, Saxelin, M, Isolauri, E 1996Promotion of IgA immune response in patients with Crohn’s disease by oral bacteriotherapy with Lactobacillus GGAnn Nutr Metab4013745 Malin, M, Suomalainen, H, Saxelin, M, Isolauri, E 1996Promotion of IgA immune response in patients with Crohn’s disease by oral bacteriotherapy with Lactobacillus GGAnn Nutr Metab4013745
32.
go back to reference Siitonen, S, Vapaatalo, H, Salminen, S, et al. 1990Effect of Lactobacillus GG yoghurt in prevention of antibiotic associated diarrhoeaAnn Med22579 Siitonen, S, Vapaatalo, H, Salminen, S,  et al. 1990Effect of Lactobacillus GG yoghurt in prevention of antibiotic associated diarrhoeaAnn Med22579
33.
go back to reference Gorbach, SL, Chang, TW, Goldin, B 1987Successful treatment of relapsing Clostridium difficile colitis with Lactobacillus GGLancet21519 Gorbach, SL, Chang, TW, Goldin, B 1987Successful treatment of relapsing Clostridium difficile colitis with Lactobacillus GGLancet21519
34.
go back to reference Hilton, E, Kolakowski, P, Singer, C, Smith, M 1997Efficacy of Lactobacillus GG as a diarrheal preventive in travelersJ Travel Med4413 Hilton, E, Kolakowski, P, Singer, C, Smith, M 1997Efficacy of Lactobacillus GG as a diarrheal preventive in travelersJ Travel Med4413
35.
go back to reference Pant, AR, Graham, SM, Allen, SJ, et al. 1996Lactobacillus GG and acute diarrhoea in young children in the tropicsJ Trop Pediatr421625 Pant, AR, Graham, SM, Allen, SJ,  et al. 1996Lactobacillus GG and acute diarrhoea in young children in the tropicsJ Trop Pediatr421625
36.
go back to reference Friedman, G, George, J 2000Treatment of refractory “pouchitis” with prebiotic and probiotic therapyGastroenterology118A190 Friedman, G, George, J 2000Treatment of refractory “pouchitis” with prebiotic and probiotic therapyGastroenterology118A190
37.
go back to reference Ruseler-van Embden, JG, Lieshout, LM, Gosselink, MJ, Marteau, P 1995Inability of Lactobacillus casei strain GG, L. acidophilus, and Bifidobacterium bifidum to degrade intestinal mucus glycoproteinsScand J Gastroenterol3067580 Ruseler-van Embden, JG, Lieshout, LM, Gosselink, MJ, Marteau, P 1995Inability of Lactobacillus casei strain GG, L. acidophilus, and Bifidobacterium bifidum to degrade intestinal mucus glycoproteinsScand J Gastroenterol3067580
38.
go back to reference Gibson, GR, Beatty, ER, Wang, X, Cummings, JH 1995Selective stimulation of bifidobacteria in the human colon by oligofructose and inulinGastroenterology10897582 Gibson, GR, Beatty, ER, Wang, X, Cummings, JH 1995Selective stimulation of bifidobacteria in the human colon by oligofructose and inulinGastroenterology10897582
39.
go back to reference Kalliomaki, M, Salminen, S, Arvilommi, H, Kero, P, Koskinen, P, Isolauri, E 2001Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trialLancet35710769 Kalliomaki, M, Salminen, S, Arvilommi, H, Kero, P, Koskinen, P, Isolauri, E 2001Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trialLancet35710769
40.
go back to reference Shibolet, O, Karmeli, F, Eliakim, R, et al. 2002Variable response to probiotics in two models of experimental colitis in ratsInflamm Bowel Dis8399406 Shibolet, O, Karmeli, F, Eliakim, R,  et al. 2002Variable response to probiotics in two models of experimental colitis in ratsInflamm Bowel Dis8399406
41.
go back to reference Kuisma, J, Mentula, S, Jarvinen, H, Kahri, A, Saxelin, M, Farkkila, M 2003Effect of Lactobacillus rhamnosus GG on ileal pouch inflammation and microbial floraAliment Pharmacol Ther1750915 Kuisma, J, Mentula, S, Jarvinen, H, Kahri, A, Saxelin, M, Farkkila, M 2003Effect of Lactobacillus rhamnosus GG on ileal pouch inflammation and microbial floraAliment Pharmacol Ther1750915
42.
go back to reference Ulisse, S, Gionchetti, P, D’Alo, S, et al. 2001Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: effects of probiotic treatmentAm J Gastroenterol9626919 Ulisse, S, Gionchetti, P, D’Alo, S,  et al. 2001Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: effects of probiotic treatmentAm J Gastroenterol9626919
43.
go back to reference Korhonen, R, Korpela, R, Saxelin, M, Maki, M, Kankaanranta, H, Moilanen, E 2001Induction of nitric oxide synthesis by probiotic Lactobacillus rhamnosus GG in J774 macrophages and human T84 intestinal epithelial cellsInflammation2522332 Korhonen, R, Korpela, R, Saxelin, M, Maki, M, Kankaanranta, H, Moilanen, E 2001Induction of nitric oxide synthesis by probiotic Lactobacillus rhamnosus GG in J774 macrophages and human T84 intestinal epithelial cellsInflammation2522332
44.
go back to reference Miettinen, M, Vuopio-Varkila, J, Varkila, K 1996Production of human tumor necrosis factor alpha, interleukin-6, and interleukin-10 is induced by lactic acid bacteriaInfect Immun6454035 Miettinen, M, Vuopio-Varkila, J, Varkila, K 1996Production of human tumor necrosis factor alpha, interleukin-6, and interleukin-10 is induced by lactic acid bacteriaInfect Immun6454035
45.
go back to reference Langhendries, JP, Detry, J, Hees, J, et al. 1995Effect of a fermented infant formula containing viable bifidobacteria on the fecal flora composition and pH of healthy full-term infantsJ Pediatr Gastroenterol Nutr2117781 Langhendries, JP, Detry, J, Hees, J,  et al. 1995Effect of a fermented infant formula containing viable bifidobacteria on the fecal flora composition and pH of healthy full-term infantsJ Pediatr Gastroenterol Nutr2117781
46.
go back to reference Kailasapathy, K, Chin, J 2000Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium sppImmunol Cell Biol78808 Kailasapathy, K, Chin, J 2000Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium sppImmunol Cell Biol78808
47.
go back to reference Fujiwara, S, Hashiba, H, Hirota, T, Forstner, JF 1997Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramideAppl Environ Microbiol6350612 Fujiwara, S, Hashiba, H, Hirota, T, Forstner, JF 1997Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramideAppl Environ Microbiol6350612
48.
go back to reference Rolfe, RD 2000The role of probiotic cultures in the control of gastrointestinal healthJ Nutr130396S402S Rolfe, RD 2000The role of probiotic cultures in the control of gastrointestinal healthJ Nutr130396S402S
49.
go back to reference Isolauri, E, Joensuu, J, Suomalainen, H, Luomala, M, Vesikari, T 1995Improved immunogenicity of oral D x RRV reassortant rotavirus vaccine by Lactobacillus casei GGVaccine133102 Isolauri, E, Joensuu, J, Suomalainen, H, Luomala, M, Vesikari, T 1995Improved immunogenicity of oral D x RRV reassortant rotavirus vaccine by Lactobacillus casei GGVaccine133102
50.
go back to reference Isolauri, E, Juntunen, M, Rautanen, T, Sillanaukee, P, Koivula, T 1991A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in childrenPediatrics88907 Isolauri, E, Juntunen, M, Rautanen, T, Sillanaukee, P, Koivula, T 1991A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in childrenPediatrics88907
51.
go back to reference Heuschen, UA, Autschbach, F, Allemeyer, EH, et al. 2001Long-term follow-up after ileoanal pouch procedure: algorithm for diagnosis, classification, and management of pouchitisDis Colon Rectum4448799 Heuschen, UA, Autschbach, F, Allemeyer, EH,  et al. 2001Long-term follow-up after ileoanal pouch procedure: algorithm for diagnosis, classification, and management of pouchitisDis Colon Rectum4448799
Metadata
Title
Delay of the First Onset of Pouchitis by Oral Intake of the Probiotic Strain Lactobacillus rhamnosus GG
Authors
Martijn P. Gosselink, M.D.
W. Rudolph Schouten, M.D., Ph.D.
Leo M. C. van Lieshout, M.Sc.
Willem C. J. Hop, M.Sc., Ph.D.
Jon D. Laman, M.Sc., Ph.D.
Johanneke G. H. Ruseler-van Embden, M.Sc., Ph.D.
Publication date
01-06-2004
Publisher
Springer-Verlag
Published in
Diseases of the Colon & Rectum / Issue 6/2004
Print ISSN: 0012-3706
Electronic ISSN: 1530-0358
DOI
https://doi.org/10.1007/s10350-004-0525-z

Other articles of this Issue 6/2004

Diseases of the Colon & Rectum 6/2004 Go to the issue