Original Paper Ann Nutr Metab 1992;36:162-166
Departments of Physiology, Clinical Nutrition and Pharmaceutical Chemistry', University of Kuopio, Finland; Valio Research and Development Centre, Helsinki, Finland
Key Words
Feces Lactobacillus GG, P-Glucuronidase Urease Glycocholic acid hydrolase Elderly
Colonization and Fecal Enzyme Activities after Oral Lactobacillus GG Administration in Elderly Nursing Home Residents
Abstract
This study was undertaken to investigate the effect of 2-week oral administration of a Lactobacillus-GG-fermented whey drink on fecal enzymes in elderly nursing home residents com plaining of difficulties in defecation. The study was divided into three 2-week periods: baseline (2 dl placebo drink/day); Lactobacillus GG treatment (2 dl of a Lactobacillir.v-GG-fcrmented whey drink containing 108 efu lactobacilli/ml); follow up (2 dl placebo drink). Administration of the fermented whey drink resulted in colonization of feces by Lactobacillus GG in all the subjects. Glycocholic acid hydrolase activity and tryptic activity were significantly decreased at the end of the treat ment period. The effect of Lactobacillus GG treatment on bowel function was less evident. Although the consistency of the stools appeared to normalize, no significant changes in the fecal frequency, weight and pH were observed. The results indicated that a Lactobacillus-GG-fermented whey drink can change the bacterial metabolism, and has no significant effect on bowel function.
Introduction
Constipation is a common problem of the elderly [1], The accumulation of fecal content in the large bowel promotes the prédomina-
Received: September 2, 1991 Accepted: January 24. 1992
tion of putrefactive bacteria. Since certain bacteria produce large quantities of enzymes [2-4] which are potentially important in gen erating toxicants and carcinogens [5], toxic compounds are produced and consequently
W.H. Ling Department of Physiology University of Kuopio P.O. Box 1627 SF—70211 Kuopio (Finland)
© 1992 S. Karger AG. Basel 0250-6807/92/ 0363-0162S2.75/0
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/19/2018 7:54:12 AM
W.H. Linga O. Hanninena H. Mykkanenb M. Heikurab S. Salminend A. Von Wrightc
Subjects and Methods Twelve subjects volunteered to participate in the study. The age of the participants varied from 78 to 91 years. They complained of difficulties in defecation, and were therefore given a glass of prune juice (2 dl) daily. This protocol was discontinued at the start of the study. Five of the subjects used laxatives regularly. Four subjects who had a fecal frequency at least once a day left the study after the first 2-week period. Two subjects were taken into hospital during the study. Therefore, for only 6 persons were stools collected dur ing all three periods of the study. The study was divided into three 2-week periods: a baseline observation period: treatment with the Lactobacillus-GG-krmenicd whey drink, and a follow-up period. During the first 2-weck period the subjects had a glass (1 dl) of apple-peach drink twice a day. During the next 2-week period the apple-peach drink was replaced by the same quantity of Lactobacillus-GGfermented apricot-peach whey drink. The composition of whey drink was (per 100 ml): energy 240 kJ. protein !.4g. fat 0.1 g, carbohydrate 12.5g, lactose < 1.0g. The Lactobacillus GG content was 10s efu Lactobacil lus GGIm\. In the last 2-wcck period apple-peach drink was served again. Intake of fibre and liquids was assessed by a questionnaire filled by the staff. All stools during the second week of each 2-week period were collected. The hardness of the stools was assessed by the subjects themselves, and the fecal pH value was recorded by nurses. The fecal samples were
frozen, weighed, and kept at -21 °C until the analysis for fecal enzyme activities. Fecal samples were analyzed for total Lactobacillus GG as described by Saxelin et al. [7], Serial dilutions were prepared from each sample and the culturing was completed using MRS agar plates. Plates were incu bated anaerobically for 78 h and the number of typical Lactobacillus GG colonies was calculated. Fecal |5-glucuronidase and |S-glucosidasc activities were determined using the method described by Free man [10]. Fecal tryptic activity was measured as de scribed by Midtvedt et al. [11]. For the assay of fecal urease activity, the enzyme reaction was run at 37 °C (pH 7.4) in a total volume of 1.0 ml containing a final concentration of 0.02 mol/l potassium phosphate buffer, 10 mmol/l urea, and 0.2 ml fecal extract. The reaction was stopped by addi tion of 0.2 N sulfuric acid (9.0 ml). Ammonia was determined using a specific electrode after \0 N so dium hydroxide (1.0 ml) had been added. The estima tion of urease activity also included a measurement of fecal ammonia in the blank tubes. The reaction was linear for 30 min. For determination of the activity of glycocholic acid hydrolase, the method described by Nair et al. [ 12] was used with modification. The enzyme reaction was run at 37 °C (pH 5.8) in a total volume of 1.0 ml containing (final concentration) 0.02 mol/l potassium phosphate buffer, 1 mmol/l glycocholic acid (Sigma), and 0.1 ml fecal supernatant. Enzyme activity was ter minated by the addition of 20% trichloroacetic acid (1.0 ml), and the suspension was centrifuged. The su pernatant fluid (0.3 ml) was assayed for glycine spcctrophotometrically with the aid of ninhydrin. The esti mation of hydrolase activity also included a measure ment of fecal amino acids in the blank lubes. The reac tion was linear for 15 min. Results are presented as means ± SD. Data were analyzed over time using the Wilcoxon signed rank test.
Results
Lactobacillus GG treatment was effective in colonizing the intestine of the elderly. After 2 weeks of Lactobacillus GG whey drink treatment the level of Lactobacillus GG was about 107efu/g feces. Prior to GG administra tion. Lactobacillus GG could not be detected (detection limit 103 efu) in the fecal samples
163
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absorbed into the gut wall and the general cir culation. Lactobacillus GG, originally isolated from a healthy human resists digestive acids and adheres to the intestinal mucosa, and colo nizes the human intestinal tract [6. 7], There is increasing evidence that Lactobacillus-fer mented products can alter the balance of the human intestinal flora to suppress putrefac tive fermentation [8. 9]. thereby diminishing the host's exposure to toxic metabolites. This study was undertaken to investigate the effect of oral administration of a Lactobacilhis-GG-fermented whey drink on fecal en zyme activities and some parameters of bowel function in elderly nursing home residents.
Table 1. Effect of Lactobacillus GG administration on fecal enzyme activities in elderly nursing home resi dents Enzyme
Baseline (n = 6)
GG period (n = 6)
Follow-up (n = 6)
P-Glucuronidase, nmol/min/mg protein p-Glucosidase, nmol/min/mg protein Glycocholic acid hydrolase, nmol/min/mg protein Urease, nmol/min/mg protein Tryptic activity, mg/kg of feces
6.00± 1.97 12.08 ±4.60 15.53 ± 7.85 75.35±44.60 204 ±252
4.74 ± 1.57 1 1.14 ± 5.89 10.15 ±5.44* 46.07 ±38.81 132 ± 189*
5.00 ±2.40 11.28 ±4.96 16.68 ±9.01 68.82 ±46.93 155 ± 188
Each value represents the mean ± SD. * p < 0.05 in the Wilcoxon signed rank test.
Baseline (n = 6 )
GG period Follow-up (n = 6) (n = 6)
pH 7.1 ±0.7 6.6 ±0.9 6.9±0.4 Weight, g/dav 90±25 79 ± 16 69 ±19 ------------------------------------------------------------------Each value represents the mean ± SD. -------------------------------------------------------------------
of 10 participants but was found in 2 persons at the level of 103 cfu/g feces. During the fol low-up period fecal Lactobacillus GG was found in 2 subjects at the level of about 105 cfu/g of feces. Glycocholic acid hydrolase and tryptic ac tivities were significantly decreased (p < 0.05), and p-glucuronidase and urease tended to decrease with Lactobacillus GG treatment (table 1). The activities of the enzymes in creased during the follow-up period. There was no change in P-glucosidase activity during the Lactobacillus GG treatment.
164
Table 3. Effect of Lactobacillus GG administration on fecal quality and frequency in elderly nursing home residents
Quality Soft. % Normal, % Hard. % Fecal frequency. times/week
Baseline (n = 6)
GG period Follow-up (n = 6) (n = 6)
21 38 41
12 55 33
7 70 23
5.7 ±2.0
5.5 ±2.3
5.0 ±1.4
The effects of Lactobacillus GG treatment on bowel function were not as clear as those on the fecal enzymes. There were no signifi cant changes in the weight or the pH of the feces (table 2). The percentage of feces classi fied as hard decreased during Lactobacillus GG administration and remained at the lower level throughout the follow-up period. No changes in fecal frequency were observed (ta ble 3). The liquid and fiber intakes of the subjects remained unchanged during the three study periods.
I.ing/Hänninen/Mykkänen/Hcikura/ Salminen/Von Wright
Fecal Enzyme Activities Decreased by Lactobacillus GG
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/19/2018 7:54:12 AM
Table 2. Effect of Lactobacillus GG administration on the pH and weight of the feces in elderly nursing home residents
Discussion
Some putrefactive bacteria are known to produce large amounts of ß-glucuronidase, glycocholic acid hydrolase and urease, while laclobacilli produce lower levels of these cnyzmes [2-4]. In the present investigation, the mean fecal glycocholic acid hydrolase ac tivity decreased significantly, and the activi ties of ß-glucuronidase and urease decreased by 20 and 38% (not statistically significant) after 2 weeks of Lactobacillus GG administra tion. This trend towards a reduction in en zyme activities coincided with an increase in fecal Lactobacillus GG content in all the sub jects. Lactobacilli produce an intermediate amount of ß-glucosidase [3], and in the present study ß-glucosidase did not decrease during Lactobacillus GG intake. It has been reported that Lactobacillus sp. strain GG produced a substance with a potent inhibitory activity against a wide range of anaerobic bacterial species [13], which may result in antagonism against some colonic bacteria influencing enzyme activity in the colon. Lowered activity of glycocholic acid hy drolase (after administration of Lactobacillus GG) results in decreased formation of free
bile acids and probably the conversion of sec ondary bile acids from primary acids. Many experiments have indicated that free bile acids are cocarcinogenic orcomutagenic. Sec ondary bile acids are more toxic than primary ones, and increase the risk of colon cancer [14], It has been known that bacterial [3-glucuronidase and urease are potentially impor tant in generating toxicants and carcinogens [5, 15, 16], The lowered enzymatic activities after a 2-week Lactobacillus GG administra tion suggest that oral Lactobacillus GG intake may alter the production of toxic compounds in the colon. The consistency of the stools tended to normalize during Lactobacillus GG treat ment. However, no improvement in bowel function was observed. It is possible that the function of the colon and rectum was not affected by colonization with Lactobacillus GG. Alternatively, the period of Lactobacillus GG treatment was not long enough to in fluence bowel function.
Acknowledgements This work is supported by the Foundation for Nutrition Research. Helsinki. Finland.
References
1- 8. 2 Hill MJ. Drasar MS: Degradation of bile salts by human intestinal bacte ria. Gut 1968:9:22-27. 3 Hawksworth G. Drasar BS. Hill MJ: Intestinal bacteria and the hydroly sis of glycosidic bonds. J Med Mi crobiol 1971:4:451-459.
4 Drasar BS. Hill MJ: Human Intesti nal Flora. London. Academic Press. 1974, pp 103-123. 5 Gorbach SL, Goldin BR: The intes tinal microfiora and the colon can cer connection. Rev Infect Dis 1990: 12(suppl):s252—s261. 6 Deneke CF. McGowan K. Thorne GM. Gorbach SL: Attachment of enterotoxigenic Escherichia enti to human intestinal cells. Infect Immun 1983:39:1102-1106.
7 Saxelin M. Elo S. Salminen S. Vapaatalo H: Dose response colonisa tion of faeces after oral administra tion of Lactobacillus casei strain GG. Microb Ecol Halth Dis 1991:4: 209-214. 8 Goldin B. Gorbach SL: The effect of milk and Lactobacillus feeding on human intestinal bacterial enzyme activity. Am J Clin Nutr 1984:39: 756-761.
165
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1 Sonnenberg A, Koch TR: Epidemi ology of constipation in the United States. Dis Colon Rectum 1989:32:
12 Nair PP, Gordon M, Rcback J: The enzymatic cleavage of the carbonnitrogen bond in 3a.7a.l2a-trihydroxy-5(}-cholan-24-oylglycinc. J Bi ol Chcm 1967:242:7-11. 13 Silva M, Jacous V. Deneke C, Gorbach SL: Antimicrobial substance from a human Lactobacillus strain. Antimicrob Agents Chemother 1987:31:1231-1233. 14 Adlercreutz H: Western diet and western diseases: Some hormonal and biochemical mechanisms and associations. Scand J Clin Lab In vest 1990:50(suppl 201 ):3—23.
15 William RT: Toxicologic implica tions of biotransformation by intes tinal microflora. Toxicol Appl Phar macol 1972:23:769-781. 16 Chipman JK: Biles as a source of potential reactive metabolism. Tox icology 1982:25:99-111.
166
Ling/Hannincn/Mykkanen/Hcikura/ Salminen/Von Wright
Fecal Enzyme Activities Decreased by Lactobacillus GG
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/19/2018 7:54:12 AM
9 Hitchins A, McDonough FE: Pro phylactic and therapeutic aspects of fermented milk. Am J Clin Nutr 1989:49:675-684. 10 Freeman HJ: Effects of differing pu rified cellulose, pectin, and hemicellulose fibre on fecal enzymes in 1.2dimethylhydrazine-induced rat co lon carcinogenesis. Cancer Res 1986;46:5529-5532. 11 Midtvcdt T, Carlstedt-Duke B. Hoverstad T. Midtvedl AC. Norin KE, Saxerholt H: Establishment of bio chemically active intestine ecosys tem in ex-germfree rats. Appl Envi ron Microbiol 1987:53:2866-2871.
Departments of Physiology, Clinical Nutrition and Pharmaceutical Chemistry', University of Kuopio, Finland; Valio Research and Development Centre, Helsinki, Finland
Key Words
Feces Lactobacillus GG, P-Glucuronidase Urease Glycocholic acid hydrolase Elderly
Colonization and Fecal Enzyme Activities after Oral Lactobacillus GG Administration in Elderly Nursing Home Residents
Abstract
This study was undertaken to investigate the effect of 2-week oral administration of a Lactobacillus-GG-fermented whey drink on fecal enzymes in elderly nursing home residents com plaining of difficulties in defecation. The study was divided into three 2-week periods: baseline (2 dl placebo drink/day); Lactobacillus GG treatment (2 dl of a Lactobacillir.v-GG-fcrmented whey drink containing 108 efu lactobacilli/ml); follow up (2 dl placebo drink). Administration of the fermented whey drink resulted in colonization of feces by Lactobacillus GG in all the subjects. Glycocholic acid hydrolase activity and tryptic activity were significantly decreased at the end of the treat ment period. The effect of Lactobacillus GG treatment on bowel function was less evident. Although the consistency of the stools appeared to normalize, no significant changes in the fecal frequency, weight and pH were observed. The results indicated that a Lactobacillus-GG-fermented whey drink can change the bacterial metabolism, and has no significant effect on bowel function.
Introduction
Constipation is a common problem of the elderly [1], The accumulation of fecal content in the large bowel promotes the prédomina-
Received: September 2, 1991 Accepted: January 24. 1992
tion of putrefactive bacteria. Since certain bacteria produce large quantities of enzymes [2-4] which are potentially important in gen erating toxicants and carcinogens [5], toxic compounds are produced and consequently
W.H. Ling Department of Physiology University of Kuopio P.O. Box 1627 SF—70211 Kuopio (Finland)
© 1992 S. Karger AG. Basel 0250-6807/92/ 0363-0162S2.75/0
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/19/2018 7:54:12 AM
W.H. Linga O. Hanninena H. Mykkanenb M. Heikurab S. Salminend A. Von Wrightc
Subjects and Methods Twelve subjects volunteered to participate in the study. The age of the participants varied from 78 to 91 years. They complained of difficulties in defecation, and were therefore given a glass of prune juice (2 dl) daily. This protocol was discontinued at the start of the study. Five of the subjects used laxatives regularly. Four subjects who had a fecal frequency at least once a day left the study after the first 2-week period. Two subjects were taken into hospital during the study. Therefore, for only 6 persons were stools collected dur ing all three periods of the study. The study was divided into three 2-week periods: a baseline observation period: treatment with the Lactobacillus-GG-krmenicd whey drink, and a follow-up period. During the first 2-weck period the subjects had a glass (1 dl) of apple-peach drink twice a day. During the next 2-week period the apple-peach drink was replaced by the same quantity of Lactobacillus-GGfermented apricot-peach whey drink. The composition of whey drink was (per 100 ml): energy 240 kJ. protein !.4g. fat 0.1 g, carbohydrate 12.5g, lactose < 1.0g. The Lactobacillus GG content was 10s efu Lactobacil lus GGIm\. In the last 2-wcck period apple-peach drink was served again. Intake of fibre and liquids was assessed by a questionnaire filled by the staff. All stools during the second week of each 2-week period were collected. The hardness of the stools was assessed by the subjects themselves, and the fecal pH value was recorded by nurses. The fecal samples were
frozen, weighed, and kept at -21 °C until the analysis for fecal enzyme activities. Fecal samples were analyzed for total Lactobacillus GG as described by Saxelin et al. [7], Serial dilutions were prepared from each sample and the culturing was completed using MRS agar plates. Plates were incu bated anaerobically for 78 h and the number of typical Lactobacillus GG colonies was calculated. Fecal |5-glucuronidase and |S-glucosidasc activities were determined using the method described by Free man [10]. Fecal tryptic activity was measured as de scribed by Midtvedt et al. [11]. For the assay of fecal urease activity, the enzyme reaction was run at 37 °C (pH 7.4) in a total volume of 1.0 ml containing a final concentration of 0.02 mol/l potassium phosphate buffer, 10 mmol/l urea, and 0.2 ml fecal extract. The reaction was stopped by addi tion of 0.2 N sulfuric acid (9.0 ml). Ammonia was determined using a specific electrode after \0 N so dium hydroxide (1.0 ml) had been added. The estima tion of urease activity also included a measurement of fecal ammonia in the blank tubes. The reaction was linear for 30 min. For determination of the activity of glycocholic acid hydrolase, the method described by Nair et al. [ 12] was used with modification. The enzyme reaction was run at 37 °C (pH 5.8) in a total volume of 1.0 ml containing (final concentration) 0.02 mol/l potassium phosphate buffer, 1 mmol/l glycocholic acid (Sigma), and 0.1 ml fecal supernatant. Enzyme activity was ter minated by the addition of 20% trichloroacetic acid (1.0 ml), and the suspension was centrifuged. The su pernatant fluid (0.3 ml) was assayed for glycine spcctrophotometrically with the aid of ninhydrin. The esti mation of hydrolase activity also included a measure ment of fecal amino acids in the blank lubes. The reac tion was linear for 15 min. Results are presented as means ± SD. Data were analyzed over time using the Wilcoxon signed rank test.
Results
Lactobacillus GG treatment was effective in colonizing the intestine of the elderly. After 2 weeks of Lactobacillus GG whey drink treatment the level of Lactobacillus GG was about 107efu/g feces. Prior to GG administra tion. Lactobacillus GG could not be detected (detection limit 103 efu) in the fecal samples
163
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absorbed into the gut wall and the general cir culation. Lactobacillus GG, originally isolated from a healthy human resists digestive acids and adheres to the intestinal mucosa, and colo nizes the human intestinal tract [6. 7], There is increasing evidence that Lactobacillus-fer mented products can alter the balance of the human intestinal flora to suppress putrefac tive fermentation [8. 9]. thereby diminishing the host's exposure to toxic metabolites. This study was undertaken to investigate the effect of oral administration of a Lactobacilhis-GG-fermented whey drink on fecal en zyme activities and some parameters of bowel function in elderly nursing home residents.
Table 1. Effect of Lactobacillus GG administration on fecal enzyme activities in elderly nursing home resi dents Enzyme
Baseline (n = 6)
GG period (n = 6)
Follow-up (n = 6)
P-Glucuronidase, nmol/min/mg protein p-Glucosidase, nmol/min/mg protein Glycocholic acid hydrolase, nmol/min/mg protein Urease, nmol/min/mg protein Tryptic activity, mg/kg of feces
6.00± 1.97 12.08 ±4.60 15.53 ± 7.85 75.35±44.60 204 ±252
4.74 ± 1.57 1 1.14 ± 5.89 10.15 ±5.44* 46.07 ±38.81 132 ± 189*
5.00 ±2.40 11.28 ±4.96 16.68 ±9.01 68.82 ±46.93 155 ± 188
Each value represents the mean ± SD. * p < 0.05 in the Wilcoxon signed rank test.
Baseline (n = 6 )
GG period Follow-up (n = 6) (n = 6)
pH 7.1 ±0.7 6.6 ±0.9 6.9±0.4 Weight, g/dav 90±25 79 ± 16 69 ±19 ------------------------------------------------------------------Each value represents the mean ± SD. -------------------------------------------------------------------
of 10 participants but was found in 2 persons at the level of 103 cfu/g feces. During the fol low-up period fecal Lactobacillus GG was found in 2 subjects at the level of about 105 cfu/g of feces. Glycocholic acid hydrolase and tryptic ac tivities were significantly decreased (p < 0.05), and p-glucuronidase and urease tended to decrease with Lactobacillus GG treatment (table 1). The activities of the enzymes in creased during the follow-up period. There was no change in P-glucosidase activity during the Lactobacillus GG treatment.
164
Table 3. Effect of Lactobacillus GG administration on fecal quality and frequency in elderly nursing home residents
Quality Soft. % Normal, % Hard. % Fecal frequency. times/week
Baseline (n = 6)
GG period Follow-up (n = 6) (n = 6)
21 38 41
12 55 33
7 70 23
5.7 ±2.0
5.5 ±2.3
5.0 ±1.4
The effects of Lactobacillus GG treatment on bowel function were not as clear as those on the fecal enzymes. There were no signifi cant changes in the weight or the pH of the feces (table 2). The percentage of feces classi fied as hard decreased during Lactobacillus GG administration and remained at the lower level throughout the follow-up period. No changes in fecal frequency were observed (ta ble 3). The liquid and fiber intakes of the subjects remained unchanged during the three study periods.
I.ing/Hänninen/Mykkänen/Hcikura/ Salminen/Von Wright
Fecal Enzyme Activities Decreased by Lactobacillus GG
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/19/2018 7:54:12 AM
Table 2. Effect of Lactobacillus GG administration on the pH and weight of the feces in elderly nursing home residents
Discussion
Some putrefactive bacteria are known to produce large amounts of ß-glucuronidase, glycocholic acid hydrolase and urease, while laclobacilli produce lower levels of these cnyzmes [2-4]. In the present investigation, the mean fecal glycocholic acid hydrolase ac tivity decreased significantly, and the activi ties of ß-glucuronidase and urease decreased by 20 and 38% (not statistically significant) after 2 weeks of Lactobacillus GG administra tion. This trend towards a reduction in en zyme activities coincided with an increase in fecal Lactobacillus GG content in all the sub jects. Lactobacilli produce an intermediate amount of ß-glucosidase [3], and in the present study ß-glucosidase did not decrease during Lactobacillus GG intake. It has been reported that Lactobacillus sp. strain GG produced a substance with a potent inhibitory activity against a wide range of anaerobic bacterial species [13], which may result in antagonism against some colonic bacteria influencing enzyme activity in the colon. Lowered activity of glycocholic acid hy drolase (after administration of Lactobacillus GG) results in decreased formation of free
bile acids and probably the conversion of sec ondary bile acids from primary acids. Many experiments have indicated that free bile acids are cocarcinogenic orcomutagenic. Sec ondary bile acids are more toxic than primary ones, and increase the risk of colon cancer [14], It has been known that bacterial [3-glucuronidase and urease are potentially impor tant in generating toxicants and carcinogens [5, 15, 16], The lowered enzymatic activities after a 2-week Lactobacillus GG administra tion suggest that oral Lactobacillus GG intake may alter the production of toxic compounds in the colon. The consistency of the stools tended to normalize during Lactobacillus GG treat ment. However, no improvement in bowel function was observed. It is possible that the function of the colon and rectum was not affected by colonization with Lactobacillus GG. Alternatively, the period of Lactobacillus GG treatment was not long enough to in fluence bowel function.
Acknowledgements This work is supported by the Foundation for Nutrition Research. Helsinki. Finland.
References
1- 8. 2 Hill MJ. Drasar MS: Degradation of bile salts by human intestinal bacte ria. Gut 1968:9:22-27. 3 Hawksworth G. Drasar BS. Hill MJ: Intestinal bacteria and the hydroly sis of glycosidic bonds. J Med Mi crobiol 1971:4:451-459.
4 Drasar BS. Hill MJ: Human Intesti nal Flora. London. Academic Press. 1974, pp 103-123. 5 Gorbach SL, Goldin BR: The intes tinal microfiora and the colon can cer connection. Rev Infect Dis 1990: 12(suppl):s252—s261. 6 Deneke CF. McGowan K. Thorne GM. Gorbach SL: Attachment of enterotoxigenic Escherichia enti to human intestinal cells. Infect Immun 1983:39:1102-1106.
7 Saxelin M. Elo S. Salminen S. Vapaatalo H: Dose response colonisa tion of faeces after oral administra tion of Lactobacillus casei strain GG. Microb Ecol Halth Dis 1991:4: 209-214. 8 Goldin B. Gorbach SL: The effect of milk and Lactobacillus feeding on human intestinal bacterial enzyme activity. Am J Clin Nutr 1984:39: 756-761.
165
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1 Sonnenberg A, Koch TR: Epidemi ology of constipation in the United States. Dis Colon Rectum 1989:32:
12 Nair PP, Gordon M, Rcback J: The enzymatic cleavage of the carbonnitrogen bond in 3a.7a.l2a-trihydroxy-5(}-cholan-24-oylglycinc. J Bi ol Chcm 1967:242:7-11. 13 Silva M, Jacous V. Deneke C, Gorbach SL: Antimicrobial substance from a human Lactobacillus strain. Antimicrob Agents Chemother 1987:31:1231-1233. 14 Adlercreutz H: Western diet and western diseases: Some hormonal and biochemical mechanisms and associations. Scand J Clin Lab In vest 1990:50(suppl 201 ):3—23.
15 William RT: Toxicologic implica tions of biotransformation by intes tinal microflora. Toxicol Appl Phar macol 1972:23:769-781. 16 Chipman JK: Biles as a source of potential reactive metabolism. Tox icology 1982:25:99-111.
166
Ling/Hannincn/Mykkanen/Hcikura/ Salminen/Von Wright
Fecal Enzyme Activities Decreased by Lactobacillus GG
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/19/2018 7:54:12 AM
9 Hitchins A, McDonough FE: Pro phylactic and therapeutic aspects of fermented milk. Am J Clin Nutr 1989:49:675-684. 10 Freeman HJ: Effects of differing pu rified cellulose, pectin, and hemicellulose fibre on fecal enzymes in 1.2dimethylhydrazine-induced rat co lon carcinogenesis. Cancer Res 1986;46:5529-5532. 11 Midtvcdt T, Carlstedt-Duke B. Hoverstad T. Midtvedl AC. Norin KE, Saxerholt H: Establishment of bio chemically active intestine ecosys tem in ex-germfree rats. Appl Envi ron Microbiol 1987:53:2866-2871.
