The aim of the study was to investigate the effects of fibre-rich rye bread and yoghurt containing Lactobacillus GG (LGG) on intestinal transit time and bowel function, and to test whether they have an interaction in cases of self-reported constipation.
The study was carried out as a two-by-two factorial design.
A total of 59 healthy women with self-reported constipation, recruited by advertisement.
After a baseline period, the subjects were randomized into four diet groups: (1) rye bread+LGG yoghurt, (2) rye bread, (3) LGG yoghurt, and (4) control. The 3-week dietary intervention was followed by a 3-week follow-up period. During each period, total intestinal transit time was measured and the subjects recorded faecal frequency and consistency, difficulty in defecation and gastrointestinal symptoms.
The rye bread shortened total intestinal transit time (mean difference, −0.7; CI95, −1.1 to −0.2; P=0.007), increased faecal frequency (0.3; CI95, 0.1 to 0.5; P=0.001), softened faeces (−0.3; CI95, −0.4 to −0.2; P<0.001) and made defecation easier (−0.4; CI95, −0.5 to −0.2; P<0.001), but also increased gastrointestinal symptoms (1.6; CI95, 0.7 to 2.4; P<0.001) compared to the low-fibre toast consumed in the LGG and control groups. There were fewer symptoms in the rye bread+LGG group compared to the rye bread group (−1.3; CI95, −2.4 to −0.2; P=0.027).
Fibre-rich rye bread can be recommended in the treatment of constipation, and the simultaneous consumption of LGG yoghurt relieves the adverse gastrointestinal effects associated with increased intake of fibre.
Valio Ltd, R&D, and Fazer Bakeries Ltd.
Constipation is a common complaint of the gastrointestinal tract. One in five Western women report that they suffer from the complaint (Walter et al., 2002). Constipation is related to increasing age, female gender, lower socioeconomic status, low consumption of fibre and the Western lifestyle (Garrigues et al., 2004; Higgins and Johanson, 2004). According to the Rome II criteria, when no organic cause is found, constipation is considered to be functional and the diagnosis of functional constipation can be based on the patients' own reports (Thompson et al., 1999). A widely accepted definition of constipation involves the presence of at least two of the following symptoms: fewer than three bowel movements per week and/or difficulty in defecation – straining, hard stools, sensation of incomplete evacuation or sensation of anorectal blockage (Thompson et al., 1999). The treatment of functional constipation is based on dietary and other lifestyle modifications, and the role of dietary fibre is generally accepted in the prevention and treatment of constipation (Loening-Baucke et al., 2004). In Finland, the daily intake of dietary fibre by women – 18 g (Männistö et al., 2003) – is less than the Nordic recommendation of 25–35 g per day (Becker et al., 2004). The laxative effect of dietary fibre is based on increased stool output, accelerated colonic transit time, the binding of bile acids and the production of short-chain fatty acids and gas (Read and Eastwood, 1992). It can be hypothesized that rye bread, because of its high fibre content, relieves constipation. Whole-meal rye bread has been shown to increase faecal output and frequency, and shorten intestinal transit time compared to wheat bread, in healthy men and women (Grasten et al., 2000), but to our knowledge the effect has not so far been studied in subjects with chronic constipation.
It has been hypothesized that lactic acid bacteria may have a function in relieving constipation (Salminen et al., 1993; Koebnick et al., 2003). Lactobacillus rhamnosus strain GG (LGG; ATCC 53103) is a well-documented strain of lactobacilli. It has been shown to be of benefit in many gastrointestinal disorders as well as in enhancing the immune system (Saxelin, 1997; Szajewska and Mrukowicz, 2003; Vaarala, 2003). Some preliminary data on the potential positive effect of LGG on bowel function exist, showing normalization of stool consistency (Ling et al., 1992) and possibly a slight increase of bowel movements in healthy adults (Benno et al., 1996) and elderly constipated patients (Salminen and Salminen, 1997) during LGG supplementation.
The aim of our study was to investigate whether, in women with self-reported constipation, rye bread rich in fibre or yoghurt containing LGG have effects on intestinal transit time and bowel function, and whether there is a synergistic interaction between these two supplementations.
Women suffering from constipation were recruited for the study. The study population consisted of 59 women with self-reported constipation. The subjects' own feelings about reduced/less-frequent bowel movements as well as straining at defecation were considered to be self-reported constipation. There were no dietary inclusion criteria. Subjects with intestinal or other diseases that could affect bowel function were excluded.
The study was carried out as a two-by-two factorial design. After a 1-week baseline period, the subjects were randomized into one of the four following intervention groups:
Rye bread+LGG group: Instructions for minimum consumption 8 × 40 g fibre-rich rye bread, 2 × 150 g LGG yoghurt. Additional bread allowed – any kind/any amount.
Rye bread group: Minimum consumption 8 × 40 g fibre-rich rye bread, no LGG products. Additional bread allowed – any kind/any amount.
LGG group: Maximum consumption 8 × 24 g low-fibre toast, 2 × 150 g LGG yoghurt. Additional bread allowed – low fibre only.
Control group: Maximum consumption 8 × 24 g low-fibre toast and no LGG products. Additional bread allowed – low fibre only. (For amounts actually consumed, see Table 2.)
The fibre-rich rye bread contained 12.3 g fibre/100 g (Real®, Fazer Bakeries Ltd, Lahti, Finland), the low-fibre toast contained 4.5 g fibre/100 g (Suomi Paahtis, Fazer Bakeries Ltd, Vantaa, Finland), and the LGG yoghurt contained ⩾5 × 107 CFU LGG/g (Gefilus® apricot-flavoured yoghurt, Valio Ltd, Riihimäki, Finland). The study lasted 7 weeks. After a 1-week baseline, the 3-week intervention period began and was followed by a 3-week follow-up period. During the baseline and the follow-up periods there were no dietary restrictions.
During the baseline week, the first and last weeks of the intervention and the last week of the follow-up, the subjects kept a daily diary of their bowel functions. They reported the number and consistency of stools (−1=loose, 0=normal, 1=hard), difficulty of defecation (−1=easy, 0=normal, 1=straining at defecation), and abdominal pain, flatulence, borborygmi, abdominal bloating, loose stools and hard stools (0=no symptoms, 1=mild, 2=moderate, 3=severe symptoms). Lifestyle factors such as amount of exercise, use of medication, intake of liquids, and consumption of coffee and tea were also reported by the subjects.
After the baseline, the intervention and the follow-up periods, the subjects filled in a validated dietary-fibre intake-frequency questionnaire (Jäkälä et al., 1994). The intake of fibre was calculated using the Micro-Nutrica programme based on data files of Finnish foods (Rastas et al., 1989).
Measurement of total intestinal transit time
Total intestinal transit time (TITT) was measured three times: during the baseline week, during the last week of the intervention, and during the last week of the follow-up. TITTs were measured using radiopaque Sitzmarks® capsules (Konsyl, Texas, USA), each containing 24 polyvinyl chloride rings, which could be seen on X-ray. At the beginning of each TITT measurement, the study subjects ingested one Sitzmarks® capsule, and then for the next 5 days, collected all their faeces. The frozen faecal samples were X-rayed, using a Bennet Model D-50 M and Kodak T-mat G films. TITT was calculated with the following formula (Corazziari et al., 1987):
in which n is the number of PVC rings appearing in the faeces on different investigation days (=d) (i=1, 2, 3, 4 and 5) and N is the total number of PVC rings appearing in the faeces over a period of 5 days.
The sample size calculation was based on the intestinal transit time. Assuming that no interaction between LGG and rye bread exists, with 16 subjects per group, the true difference of 24 h (s.d. 24 h) has an 80% chance of being detected at a 5% significance level.
Baseline characteristics were compared in the four groups, using one-way analysis of variance (ANOVA) or the χ2 test, whichever was appropriate. The variables describing bowel functions and gastrointestinal symptoms during the 1-week baseline and the 1-week follow-up are expressed as means of 7 days, and are based on the subjects' own records. The main outcome variables, bowel functions and gastrointestinal symptoms during the intervention, were the means of 7 or 14 days based on the first or third intervention weeks or a combination of both weeks. The two-way ANOVA was first carried out to test the interaction between rye bread and LGG in the context of the main outcome variables. The interactions were nonsignificant, and the effects of rye bread and LGG were analysed in separate analyses using the analysis of covariance (ANCOVA), where the corresponding baseline level of the main outcome variable was included as a continuous covariate. The results of group comparisons are given as baseline-adjusted means with 95% confidence intervals (CI95). Pairwise comparisons between the four study groups were performed using one-way ANOVA and Fisher's LSD test. A P value of <0.05 was considered significant. Data were analysed using SPSS, version 12.0.
The study protocol was accepted by the local ethics committee. Informed, written consent was obtained from all the subjects.
The study comprised 59 women with self-reported constipation (mean age 41 years, range 18–57 years). The baseline characteristics of the study groups are given in Table 1. Mean age in the control group was 5–8 years higher than in the other groups, but this was not considered to be a confounding factor.
No differences between the groups were discerned either in the bowel function variables during the baseline period or the lifestyle variables (exercise, medication, liquid intake and consumption of coffee or tea) during any of the study periods (data not shown). During the baseline period, during which no additional bread was supplied to the subjects, the mean daily intake of fibre was higher in the control group (24.9 g) than in the other groups (rye bread+LGG group, 17.1 g; rye bread group, 19.9 g; LGG group, 15.1 g; P=0.016), but during the follow-up period no differences between the groups were discerned (rye bread+LGG group, 15.5 g; rye bread group, 15.7 g; LGG group, 14.3 g; control group, 17.0 g; P=0.864).
Diet compliance during the intervention was good: all the subjects in the rye bread+LGG group and the LGG group reported a daily consumption of 2 × 150 g yoghurt as instructed. Even though the subjects in the rye bread+LGG and rye bread groups consumed slightly less rye bread than the eight slices/day they were instructed to eat (mean daily consumption six slices and 7.5 slices, respectively), the intake of dietary fibre during the intervention was significantly higher in these two rye bread groups than in the two low-fibre toast groups (Table 2).
Fibre-rich rye bread significantly improved bowel function (Figures 1, 2 3 and 4). During the 3-week dietary intervention, in the rye bread groups the frequency of bowel movements was higher (mean difference, 0.3 defections/day; CI95, 0.1 to 0.5; P=0.001), defecation was easier (−0.4; CI95, −0.5 to −0.2; P<0.001) and stools were softer (−0.3; CI95, −0.4 to −0.2; P<0.001) compared to the low-fibre toast groups. An interesting result was that LGG yoghurt tended to increase the effect of rye bread on all the bowel function variables, although neither the main effect nor the interactions were statistically significant.
Gastrointestinal side effects (abdominal pain, flatulence, borborygmi, abdominal bloating, loose and/or hard stools) occurred in both the groups supplemented with rye bread (Figure 4). During the 3-week intervention, the symptom score in the rye bread groups was consistently higher than in the low-fibre groups (mean difference, 1.6; CI95, 0.7 to 2.4; P<0.001). The gastrointestinal symptoms, mainly flatulence and abdominal bloating, were strongest during the first week of the dietary intervention, when the baseline-adjusted means were 4.7 for the rye bread groups and 2.6 for the low-fibre toast groups (mean difference, 2.1; CI95, 1.1 to 3.0; P<0.001). The difference diminished during the intervention, thus, during the last intervention week, there were only slightly more symptoms in the rye bread groups than in the low-fibre toast groups (baseline-adjusted means, 3.6 vs 2.7; mean difference, 0.9; CI95 0.1 to 0.9; P=0.039). LGG yoghurt relieved the gastrointestinal symptoms caused by rye bread. The baseline adjusted symptom scores were 3.5 for the rye bread+LGG group and 4.8 for the rye bread group (mean difference, −1.3; CI95, −2.4 to −0.2; P=0.027). During the last intervention week, there were fewer symptoms in the LGG groups compared to the non-LGG groups (baseline-adjusted means, 2.7 vs 3.7; mean difference, −0.9; CI95, −1.8 to 0.0; P=0.050).
Rye bread significantly shortened TITT compared to low-fibre toast (mean difference, −0.7 days; CI95, −1.1 to −0.2; P=0.007, Figure 5). LGG tended to improve the positive effect of rye bread: at the end of the 3-week intervention, the baseline-adjusted means of the TITTs were 2.6 days in the rye bread+LGG group, 3.0 days in the rye bread group, 3.4 days in the LGG group and 3.5 days in the control group.
Based on the dietary interventions of fibre-rich rye bread and LGG yoghurt, the main results of the study were the relieving effect of rye bread on constipation and the positive effect of LGG yoghurt on gastrointestinal symptoms in women with self-reported constipation. Changes in bowel function were mainly based on the subjects' own reports, recorded in a diary. An objective measurement of bowel function, the TITT measurement, gave results similar to the subjective records. Since collection of stool samples is time consuming and awkward, and our results indicate that subjective records of bowel function were reliable, it can be concluded that objective measurements may not always be needed when self-reporting, free-living volunteers are used.
The results of our study clearly show the effectiveness of fibre-rich rye bread in the treatment of constipation. This accords with those of a study by Grasten et al. (2000) in which rye bread had positive effects on bowel function in healthy men and women. LGG yoghurt did not have a significant independent effect on bowel function, but it did tend to shorten TITT. A slight increase in faecal frequency has been reported in previous studies (Benno et al., 1996; Salminen and Salminen, 1997). In this study, the effect of LGG yoghurt might also have been based on components of yoghurt/milk other than LGG, since a placebo dairy product was not used. The effect of rye bread, too, may be based on many nutrients, but dietary fibre is the most likely explanation for the improvement in bowel function. This study shows a positive synergistic effect of a candidate prebiotic, rye fibre (Korakli et al., 2002; Karppinen et al., 2003), and a probiotic, LGG, on bowel function.
At the beginning of the rye bread intervention, troublesome gastrointestinal side effects occurred. However, this did not come as a surprise, since it is known that an increased intake of dietary fibre causes flatulence and abdominal bloating (Read and Eastwood, 1992; Roberfroid, 2000; Cummings et al., 2001). Our results support the adaptation hypothesis, according to which a continuous intake of dietary fibre relieves symptoms. The adaptation may be the result of an increase in the number of bacteria and/or the number of species capable of fermenting rye fibre, followed by an increase in species capable of utilizing a sudden excess of gas, both of which, together with the short-chain fatty acids thus produced, enter the colon; the consequence of this may be a new equilibrium between the gas-producing and gas-utilizing bacteria (Salyers, 1995).
The role of LGG yoghurt and Lactobacillus GG in relieving gastrointestinal symptoms is worth noting. It may support the growth of other bacteria capable of metabolizing gases, but the exact mechanism is unknown. In our study, the intake of rye fibre was almost 20% lower in the rye fibre+LGG group compared to the rye bread group, which may have affected the results of gastrointestinal symptoms and also the TITTs. Further studies on colonic microbiota and their changes during rye bread or LGG yoghurt administration are needed before one can speculate further about the mechanisms.
A low intake of dietary fibre is related to constipation (Garrigues et al., 2004; Higgins and Johanson 2004). The mean intake of dietary fibre by our study subjects during the baseline week (19.2 g/day) is less than the Nordic recommendation (25–35 g/day) (Becker et al., 2004) but similar to the daily intake by Finnish women in general (18 g/day) (Männistö et al., 2003). This may be one – but not the only – reason for their constipation. The intake of dietary fibre differed between the groups at baseline and therefore the statistical tests of the effect of dietary interventions were carried out taking into account these baseline differences. The results were similar when baseline differences were ignored.
The subjects may have considered constipation to be merely straining at defecation. A subjective feeling of constipation does not necessarily include less-frequent bowel movements, which is the generally accepted definition of constipation in medicine. It is known that subjects' records and the observed frequency of their bowel movements correlate poorly (Sandler et al., 1990). Thus, it is understandable that the mean faecal frequency of our study population during the baseline week was as high as once a day. However, the subjects reported that they suffered from problems in bowel function.
In conclusion, in the present study fibre-rich rye bread clearly relieved constipation: it significantly increased faecal frequency, softened stools, made defecation easier and shortened TITT. Rye bread also increased unpleasant gastrointestinal symptoms at the beginning of consumption, but the simultaneous consumption of LGG yoghurt may have relieved some of the symptoms. Thus, in the treatment of constipation, a combination of fibre-rich rye bread and LGG yoghurt can be recommended in order to improve bowel function, causing only mild adverse gastrointestinal effects.
Becker W, Lyhne N, Pedersen AN, Aro A, Fogelholm M, Phórsdottir I et al. (2004). Nordic Nutrition Recommendations 2004 – integrating nutrition and physical activity. Scand J Nutr 48, 178–187.
Benno Y, He F, Hosoda M, Hashimodo H, Kojima T, Yamazaki K et al. (1996). Effects of Lactobacillus GG yoghurt on human intestinal microecology in Japanese subjects. Nutr Today 31 (Suppl 1), 9S–11S.
Corazziari E, Materia E, Bausano G, Torsoli A, Badiali D, Fanucci A et al. (1987). Laxative consumption in chronic nonorganic constipation. J Clin Gastroenterol 9, 427–430.
Cummings JH, Macfarlane GT, Englyst HN (2001). Prebiotic digestion and fermentation. Am J Clin Nutr 73 (2 Suppl), 415S–420S.
Garrigues V, Galvez C, Ortiz V, Ponce M, Nos P, Ponce J (2004). Prevalence of constipation: agreement among several criteria and evaluation of the diagnostic accuracy of qualifying symptoms and self-reported definition in a population-based survey in Spain. Am J Epidemiol 159, 520–526.
Grasten SM, Juntunen KS, Poutanen KS, Gylling HK, Miettinen TA, Mykkänen HM (2000). Rye bread improves bowel function and decreases the concentrations of some compounds that are putative colon cancer risk markers in middle-aged women and men. J Nutr 130, 2215–2221.
Higgins PD, Johanson JF (2004). Epidemiology of constipation in North America: a systematic review. Am J Gastroenterol 99, 750–759.
Jäkälä E, Korpela R, Mykkänen H (1994). Validity and reliability of a short interview method in measuring the intake of dietary fibre (abstract). Scand J Nutr 38 (Suppl 29), 5.
Karppinen S, Myllymäki O, Forssel P, Poutanen K (2003). Fructan content of rye and rye products. Cereal Chem 80, 168–171.
Koebnick C, Wagner I, Leitzmann P, Stern U, Zunft HJ (2003). Probiotic beverage containing Lactobacillus casei Shirota improves gastrointestinal symptoms in patients with chronic constipation. Can J Gastroenterol 17, 655–659.
Korakli M, Ganzle MG, Vogel RF (2002). Metabolism by bifidobacteria and lactic acid bacteria of polysaccharides from wheat and rye, and exopolysaccharides produced by Lactobacillus sanfranciscensis. J Appl Microbiol 92, 958–965.
Ling WH, Hänninen O, Mykkänen H, Heikura M, Salminen S, von Wright A (1992). Colonization and fecal enzyme activities after oral Lactobacillus GG administration in elderly nursing home residents. Ann Nutr Metab 36, 162–166.
Loening-Baucke V, Miele E, Staiano A (2004). Fiber (glucomannan) is beneficial in the treatment of childhood constipation. Pediatrics 113, e259–e264.
Männistö S, Ovaskainen M-L, Valsta L (2003). The National FINDIET 2002 Study. National Public Health Institute: Helsinki.
Rastas M, Seppänen R, Knuts L-R, Karvetti R-L, Varo P (1989). Nutrient Composition of Foods. Publications of the Social Insurance Institution: Helsinki, Finland, p 461.
Read NW, Eastwood MA (1992). Gastrointestinal physiology and function. In: Schweizer TF, Edwards CA (eds). Dietary Fibre – A Component of Food. Springer-Verlag: Germany. pp 103–117.
Roberfroid M (2000). Nondigestible oligosaccharides. Clin Rev Food Sci Nutr 40, 461–480.
Salminen S, Salminen E (1997). Lactulose, lactic acid bacteria, intestinal microecology and mucosal protection. Scand J Gastroenterol 32 (Suppl 222), 45–48.
Salminen S, Deighton M, Gorbach S (1993). Lactic acid bacteria in health and disease. In: Salminen S, von Wright A (eds). Lactic Acid Bacteria. Marcel Dekker, Inc.: USA. pp 199–225.
Salyers AA (1995). Fermentation of polysaccharides by human colonic anaerobes. In: Cherbut C, Barry JL, Lairon D, Durand M (eds). Dietary Fibre. Mechanisms of Action in Human Physiology and Metabolism. John Libbey Eurotext: Paris. pp 29–35.
Sandler RS, Jordan MC, Shelton BJ (1990). Demographic and dietary determinants of constipation in the US population. Am J Public Health 80, 185–189.
Saxelin M (1997). Lactobacillus GG – A human probiotic strain with thorough clinical documentation. Food Rev Int 13, 293–313.
Szajewska H, Mrukowicz JZ (2003). Probiotics in prevention of antibiotic-associated diarrhea: meta-analysis. J Pediatr 142, 85.
Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA (1999). Functional bowel disorders and functional abdominal pain. Gut 45 (Suppl 2), II43–II47.
Vaarala O (2003). Immunological effects of probiotics with special reference to lactobacilli. Clin Exp Allergy 33, 1634–1640.
Walter S, Hallbook O, Gotthard R, Bergmark M, Sjodahl R (2002). A population-based study on bowel habits in a Swedish community: prevalence of faecal incontinence and constipation. Scand J Gastroenterol 37, 911–916.
We are grateful to Director Pekka Kulonen from Oululainen Flour Mill and Director Risto Viskari from Fazer Bakeries Ltd for supplying the study breads, to Tuija Poussa, MSc, for assistance with statistical analysis, to Professor Heikki Vapaatalo for helpful advice in preparing the manuscript, and to Mimi Ponsonby, MA, for correcting the English. Financial support information: Rye bread and yoghurt were provided by the manufacturers, Fazer Ltd and Valio Ltd.
Guarantor: R Korpela.
Contributors: S-MH, RK and MS contributed to the design of the study, S-MH conducted the recruitment, intervention and data collection, and LP wrote the manuscript with the other authors' co-operation.
About this article
Cite this article
Hongisto, S., Paajanen, L., Saxelin, M. et al. A combination of fibre-rich rye bread and yoghurt containing Lactobacillus GG improves bowel function in women with self-reported constipation. Eur J Clin Nutr 60, 319–324 (2006). https://doi.org/10.1038/sj.ejcn.1602317
- rye bread
- Lactobacillus GG
- bowel function
European society of neurogastroenterology and motility guidelines on functional constipation in adults
Neurogastroenterology & Motility (2020)
Probiotic research priorities for the healthy adult population: A review on the health benefits of Lactobacillus rhamnosus GG and Bifidobacterium animalis subspecies lactis BB-12
Cogent Food & Agriculture (2018)
Alimentary Pharmacology & Therapeutics (2016)
Systematic review with meta-analysis: effect of fibre supplementation on chronic idiopathic constipation in adults
Alimentary Pharmacology & Therapeutics (2016)
World Journal of Gastroenterology (2016)