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. 2008 Nov 28;31(1):59–66. doi: 10.1007/s11357-008-9081-0

Probiotics modulate the Bifidobacterium microbiota of elderly nursing home residents

Sampo J Lahtinen 1,3, Liisa Tammela 2, Jaakko Korpela 1, Riikka Parhiala 1, Henri Ahokoski 1, Hannu Mykkänen 2, Seppo J Salminen 1,✉
PMCID: PMC2645989  PMID: 19234769

Abstract

Gut Bifidobacterium microbiota of the elderly has been suggested to differ from that of adults, possibly promoting the risk of infections and gut barrier dysfunction. Specific probiotics may improve the gut barrier. In this randomized, placebo-controlled intervention study, 66 elders consumed a fermented oat drink containing probiotic Bifidobacterium longum 46 and B. longum 2C or a non-fermented placebo oat drink for 6 months. Faecal samples were collected before, during and after the intervention. Levels of faecal bifidobacteria were determined using species-specific quantitative PCR and plate counting. The Bifidobacterium levels in the elderly were high and the species composition diverse. Probiotic intervention increased the levels bifidobacteria significantly. Specifically, the levels of B. catenulatum, B. bifidum and B. breve were enhanced. Consumption of the fermented oat drink itself was also associated with certain changes in microbiota. In conclusion, Bifidobacterium microbiota of elderly subjects may be modulated by probiotic administration. In some healthy elderly populations, Bifidobacterium microbiota may be more abundant and diverse than previously suggested.

Keywords: Bifidobacterium, Probiotics, Elderly, Microbiota, Oat

Introduction

Gut microbiota plays a critical role in maintaining human health throughout life. A healthy, diverse microbiota contributes to pathogen resistance and interacts with the host immune system. The impact of commensal microbes to colonization resistance against pathogens and healthy diversity are important to host health. Intestinal bifidobacteria in particular have received attention, due to their association with ‘typical healthy intestinal microbiota’ and their proposed health benefits (Leahy et al. 2005). Age-related changes in the gut microbiota composition include decreased species diversity and decreased levels of beneficial bacteria, and this may be associated with increased susceptibility to pathogen action and infection (Hopkins et al. 2001). Gut microbiota changes among the elderly may derive from dietary changes, changes in immune response, hospitalization, increased intestinal transit times and lack of physical activity, recurrent infections, and frequent use of antibiotics (Bartosch et al. 2004). Studies relying on traditional culturing methods have suggested that compared with healthy adults, the numbers of genus Bifidobacterium are decreased in the elderly (Gavini et al. 2001; Mitsuoka and Hayakawa 1972; Mutai and Tanaka 1987; Woodmansey et al. 2004). However, in studies based on culture-independent methods, decrease in the numbers of bifidobacteria has not been observed (Bartosch et al. 2004; He et al. 2003).

Constipation and diarrhoea are common among the elderly, in particular in institutionalized subjects. Therefore, modulation and balancing of the gut function and microbiota composition of the elderly is desirable. Probiotics have been proposed as potential modulators of gut microbiota and function (Ouwehand et al. 2002). Despite the potential benefits of probiotics in this age group, few studies have been conducted in the elderly population. We hypothesized that specific probiotics chosen for this target group would improve gut Bifidobacterium microbiota composition and diversity, thereby improving the gut barrier. Using a species-specific quantitative PCR (qPCR) method and a traditional culturing method, we assessed the efficacy of an oat product fermented with two probiotic Bifidobacterium strains, specifically designed for the elderly, in the improvement of the gastrointestinal Bifidobacterium composition of elderly nursing-home residents.

Materials and methods

Study subjects and products

The study population consisted of 66 elderly nursing-home residents participating in placebo-controlled clinical intervention trial, which was approved by the Kuopio University and Kuopio University Hospital Ethical Committee. The subjects were randomized into two groups. The probiotic group (n = 33, aged 84 ± 8 years) was administered daily with fermented and flavoured oat drink containing 109 cfu ml−1Bifidobacterium longum 46 (DSM 14583) and B. longum 2C (DSM 14579) for six months, while the placebo group (n = 33; aged 83 ± 7 years) consumed a non-fermented artificially acidified and flavoured oat drink, which did not contain probiotic or starter cultures. Stool samples were collected by the nursing home staff at the baseline, and after 2, 4 and 6 months of intervention, as well as after a 2-month wash-out period. Complete or nearly complete sets of stool samples were obtained from 31 and 28 subjects in the probiotic and placebo groups, respectively. Of the subjects lacking a complete set of samples, one subject in the probiotic group and four subjects in the placebo group were missing the 8-month wash-out sample. Due to the distance between the location of the sample collection (Kuopio, Finland) and the location of the sample analysis (Turku, Finland), stool samples were shipped and stored at −20°C until the analysis.

Quantification of culturable bifidobacteria by plate counts

Stool samples were homogenized and serially diluted with phosphate buffered saline (pH 7.2) and spread on blood-liver agar plates (Nissui, Tokyo, Japan). Plates were covered from light and incubated anaerobically in an anaerobic hood (80% N2, 10% CO2, 10% H2) at 37°C for 3 days. Bifidobacterium colonies were identified by colony morphology and the identification was confirmed by PCR using Bifidobacterium genus-specific primers (see below). Colonies were enumerated and the results were expressed as colony-forming units per gram of stool.

Quantification of total and species-specific bifidobacteria PCR

Bacterial DNA was isolated from 1:10 diluted homogenized stool samples using the QIAamp DNA Stool Mini Kit (Qiagen, Hilden, Germany) according to the manufacturer’s instructions, and stored at −20°C until use. Total bifidobacteria and nine Bifidobacterium species were quantified using quantitative real-time PCR. Apart from the genus Bifidobacterium and the species assumed to be the most commonly detected in the samples (B. longum and B. adolescentis), the presence of specific Bifidobacterium species was first determined by qualitative PCR as described by Rinne et al. (2005). Samples which were found positive in the qualitative assay were subsequently subjected to quantitative PCR. The species-specific primers and probes used in this study have been described and validated earlier by Langendijk et al. (1995) (total Bifidobacterium), Gueimonde et al. (2007) (B. angulatum, B. adolescentis, B. bifidum, B. breve, B. catenulatum group, B. dentium), Matsuki et al. (1999) (B. longum and B. infantis) and Lahtinen et al. (2006) (B. animalis). Specificity of the primers was further investigated in silico by comparing the oligonucleotide sequences with BLAST database search program (Altschul et al. 1997). In the case of the B. animalis primers, a mismatch with certain strains of B. infantis was detected. The composition of reaction mixture was: 10.5 μl of H2O, 0.5 μl of 3′ primer, 0.5 μl of 5′ primer, 12.5 μl of SYBR Green, and 1 μl of template DNA. Thermal cycling (Applied Biosystems) consisted of the following time and temperature profile: 95°C for 10 min, and 40 × 95°C for 15 s, annealing temperature for 1 min and 35°C for 15 s.

Statistics

Following logarithmic conversion, Student’s t-test was used to determine differences between the treatment groups in the baseline levels of specific species, and in the number of different species harboured by the subjects. Paired t-test was used to test whether the levels of bifidobacteria or the number of different species harboured in both groups differed between the baseline and the subsequent time points.

Results

Genus Bifidobacterium was detected in all subjects by both culturing and qPCR. The baseline level of total bifidobacteria in the study population was log 9.94 cells g−1 (SD 0.68) assessed culture-independently by qPCR (no difference between the groups). Probiotic intervention resulted in elevated levels of total bifidobacteria as measured by qPCR, but this increase was significant only at 2 months, while at 4 months there was a trend for increased Bifidobacterium levels (Table 1). In the placebo group, the levels of total bifidobacteria remained unchanged throughout the study. The average level of culturable bifidobacteria at the baseline was log 8.39 cfu g−1 (SD 1.07; no difference between the groups). In the probiotic group, the level of culturable bifidobacteria was higher throughout the intervention compared with the baseline level (Table 1), and remained elevated 2 months after the intervention had ceased. In the placebo group the level of culturable bifidobacteria was elevated at 4 months of the study but not at other time points. The Bifidobacterium species diversity, as assessed by the average number of species harboured by the elderly subjects at the baseline, was 3.2 (SD 1.64) Bifidobacterium species per subject. There was no difference between the probiotic group (3.1 species; SD 1.59) and the placebo group (3.3 species; SD 1.73) at the baseline. No significant changes in the average number of different species were observed in either group during the study.

Table 1.

The mean levels (SD) of culturable (measured by plating) and total (measured by qPCR) fecal Bifidobacterium microbiota of elderly subjects at the baseline, and the differences observed during the study between the baseline and the subsequent time points. Results presented as log cells g−1 (n.s. not significant)

Genus Bifidobacterium Probiotic group (n = 31) Placebo group (n = 28)
Plating qPCR Plating qPCR
Baseline 8.45 (0.97) 9.87 (0.71) 8.33 (1.18) 10.03 (0.65)
2 months +0.37 +0.21 n.s. n.s.
P = 0.014 a P = 0.040
4 months +0.39 +0.22 +0.54 n.s.
P = 0.041 P = 0.098 P = 0.015
6 months +0.32 n.s. n.s. n.s.
P = 0.074
Wash-out +0.49 n.s. n.s. n.s.
P = 0.013
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aSignificant difference between the baseline and the respective time point

At the baseline, B. longum was the most prevalent Bifidobacterium species detected by qPCR, being present in nearly all subjects generally at high levels (Table 2). B. adolescentis was detected in 33.9% of the subjects and, when present, the levels of this species were as high as those of B. longum. B. animalis was surprisingly frequent in both groups, being present in 67.8% of the subjects at the baseline, albeit at low levels. B. bifidum and B. breve were relatively frequent species at the baseline, while B. catenulatum was detected in 20.3% of the subjects. Both B. dentium and B. infantis were detected in 13.6% of the subjects, both at low levels. B. angulatum was not detected in any of the stool samples during the study. The baseline levels of the Bifidobacterium species did not differ between the groups, apart from B. animalis and B. bifidum, which were detected by qPCR more frequently and at higher levels in the placebo group at the baseline compared with the probiotic intervention group (Table 2).

Table 2.

The prevalence (%) and the mean baseline levelsa (SD) of nine species of Bifidobacterium in the fecal samples (n.d. not detected)

Species Probiotic group (n = 31) Placebo group (n = 28) All subjects (n = 59) Differenceb
Prevalence log cells g−1 Prevalence log cells g−1 Prevalence log cells g−1
B. adolescentis 35.5 8.48 (1.41) 32.1 8.71 (1.59) 33.9 8.58 (1.47) n.s.
B. angulatum 0 n.d. 0 n.d. 0 n.d. n.s.
B. animalis/lactis 54.8 6.82 (0.64) 82.9 7.24 (0.74) 67.8 7.04 (0.72) P = 0.042
B. bifidum 29.0 7.20 (1.35) 57.1 8.90 (1.27) 42.4 8.16 (1.54) P = 0.001
B. breve 48.4 7.29 (1.26) 39.3 7.70 (1.10) 44.1 7.45 (1.19) n.s.
B. catenulatum groupc 19.4 7.43 (1.64) 21.4 7.61 (1.55) 20.3 7.51 (1.56) n.s.
B. dentium 9.7 6.34 (0.49) 17.9 6.65 (0.69) 13.6 6.53 (0.61) n.s.
B. infantis 16.1 7.52 (0.57) 9.8 8.02 (0.84) 13.6 7.72 (0.69) n.s.
B. longum 100 8.69 (1.60) 89.3 8.49 (1.61) 94.9 8.60 (1.60) n.s.
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aAverage faecal level of cells in subjects positive for the species, as determined by qPCR

bSignificant difference between the groups in the average level of the species

cIncludes B. catenulatum and B. pseudocatenulatum

The intervention resulted in several species-specific changes in the faecal Bifidobacterium microbiota of the elderly subjects, as detected by qPCR (Table 3). The probiotic administration but not the placebo increased the levels of B. bifidum and B. breve significantly throughout the intervention. The level of B. catenulatum was significantly increased in the probiotic group from the baseline after 2 months, 4 months, and 6 months of intervention, while in the placebo group the increase was significant only at 2 months. In the case of B. adolescentis, no changes were detected in the probiotic group during the administration, but in the placebo group elevated levels were observed at 4 and 6 months into the study. The levels of B. animalis were significantly lower at 2 months compared to the baseline in both probiotic and placebo groups. Following the initial reduction, the levels of B. animalis tended to increase during the reminder of study, but this was significant only in the placebo group at 4 months and after the wash-out. No changes were observed in the levels of B. infantis, B. dentium and B. longum during the study.

Table 3.

Differences in the mean faecal levels of Bifidobacterium species between the baseline levels and subsequent time points observed during the study. Results expressed as ±log cells g−1

Speciesa Probiotic group (n = 31) Placebo group (n = 28)
2 months 4 months 6 months 8 months 2 months 4 months 6 months 8 months
B. adolescentis n.s. n.s. n.s. n.s. n.s. +0.72 P = 0.010 +0.47 P = 0.025 n.s.
B. animalis −0.42 P = 0.015 b n.s. n.s. +0.40 P = 0.089 −0.69 P < 0.001 +0.46 P = 0.003 n.s. +0.52 P = 0.018
B. bifidum +0.90 P = 0.015 +1.14 P = 0.005 +1.38 P = 0.004 +0.65 P = 0.062 n.s. n.s. n.s. n.s.
B. breve +0.67 P = 0.011 +0.85 P = 0.005 +0.97 P = 0.006 +0.44 P = 0.058 n.s n.s. n.s. n.s
B. catenulatum groupc +1.09 P = 0.005 +0.86 P = 0.015 +0.94 P = 0.025 n.s. +1.20 P = 0.049 +1.04 P = 0.066 n.s. n.s.
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aB. dentium, B. infantis and B. longum were excluded from the table as no differences in the levels of these species were observed during the study

bSignificant difference between the baseline and the respective time point

cIncludes B. catenulatum and B. pseudocatenulatum

Discussion

Bifidobacterium longum 46 and B. longum 2C are two probiotic strains isolated from healthy elderly subjects (Salminen et al. 2002). The strains are safe for human consumption (Mäkeläinen et al. 2003) and capable of antimicrobial activity (Hütt et al. 2006; Lahtinen et al. 2007) and toxin binding (Halttunen et al. 2007; Nybom et al. 2007). The strains are capable of adhesion to intestinal mucus and displacement of adhered pathogens from mucus (Collado et al. 2007, 2008). Moreover, the consumption of these probiotics by the elderly results in beneficial effects on health. In a randomized controlled study conducted in Helsinki, Finland, the administration of B. longum 46 and B. longum 2C resulted in normalized bowel movements in institutionalized elderly subjects (Pitkälä et al. 2007). Moreover, the probiotic administration was associated with enhanced immune function in the elderly subjects, and the changes observed in the immune parameters correlated with changes in the intestinal microbiota composition (Ouwehand et al. 2008a). In the current clinical trial, we confirm the capability of these strains to beneficially modulate the composition of intestinal Bifidobacterium microbiota in institutionalized elderly subjects, in particular the culturable proportion of the Bifidobacterium microbiota. Moreover, we demonstrate that in contrast with many earlier reports, elderly subjects in this study may harbour an abundant and diverse Bifidobacterium microbiota.

Ageing is thought to be associated with changes in the intestinal microbiota components, including decreased levels of the genus Bifidobacterium. In this study, the faecal level of Bifidobacterium and the species diversity were high in the elderly nursing home subjects at the baseline. The levels of Bifidobacterium observed in this study were within the same range as commonly found in healthy adults, and also comparable to what was recently reported for healthy institutionalized elders from Helsinki, Finland (Ouwehand et al. 2008a) and healthy free-living elders from Kuopio, Finland (Ouwehand et al. 2008b). The observed high levels of bifidobacteria may relate to the high food intake and the lack of constipation among the study subjects, and possibly to the fact that the intake of dietary fibre is typically high in the Kuopio region. All subjects were consuming the food served at the institute and made to correspond with the nutrition recommendations (Nordic Council of Ministers 2004). The high levels of Bifidobacterium are somewhat contradictory to earlier culture-based studies, which have suggested that the levels of bifidobacteria are decreased at old age (Gavini et al. 2001; Mitsuoka et al. 1974; Mutai and Tanaka 1987; Woodmansey et al. 2004). One possible explanation for the differences between this study and the earlier culture-based studies is that rather than lowering the absolute levels of bifidobacteria, ageing may change the species composition and thereby the culturability of bacteria. Age-related differences in the Bifidobacterium species composition have been reported previously (Gavini et al. 2001; Woodmansey et al. 2004). Shifts in the species composition may affect the plating results because some species grow better in laboratory conditions than others.

Despite the high initial levels observed, the levels of culturable and total bifidobacteria were positively affected by the probiotic treatment. Based on plate counting, the levels of culturable bifidobacteria in the probiotic group were significantly higher than the baseline levels throughout the intervention, and remained elevated after the 2-month wash-out period. In the placebo group, increased levels of culturable bifidobacteria were observed only at 4 months of the study. Assessed culture-independently, the administration of the probiotic product resulted in increased levels of total Bifidobacterium, while the placebo product had no effect. These results suggest that the changes in the Bifidobacterium microbiota induced by probiotic intervention may to be more pronounced in the culturable proportion of Bifidobacterium microbiota than in the total numbers of this genus.

The Bifidobacterium species composition of the elderly subjects was found to be diverse. Probiotic intervention resulted in changes in the composition of the Bifidobacterium microbiota composition—a result which is inline with earlier reports from studies with probiotics (Ouwehand et al. 2008a) and synbiotics (Bartosch et al. 2005; Ouwehand et al. 2008b). The most common species was B. longum, which was present at high levels in almost all of the subjects at the baseline. The frequency of this species in our study (89.3%) was higher than in many previous culture-dependent studies (Gavini et al. 2001; Mutai and Tanaka 1987; Silvi et al. 2003), but in line with the recent results obtained by culture-independent methods (Ouwehand et al. 2008a, 2008b). The administration of the oat drink containing two strains of B. longum did not affect faecal levels of this species, possibly because the initial levels of this species were already high. However, the probiotic administration resulted in significant changes in the levels of many other Bifidobacterium species. Consumption of the probiotic product increased the levels of B. catenulatum throughout the intervention, whereas in the placebo group, increase in B. catenulatum was observed only at 2 months into the study. This suggests that oat drink itself has a beneficial effect on B. catenulatum, possibly due to the proposed prebiotic effects of oat components (Mälkki and Virtanen 2001), but this effect may be further enhanced by the use of probiotics. Administration of the probiotic product but not placebo resulted in steady and significant increase in the levels of B. bifidum and B. breve. The frequency of B. breve was somewhat surprising, as this species is thought to be more typical of infant gut microbiota (Gavini et al. 2001; Mitsuoka et al. 1974). When present, B. bifidum and B. breve seldom represented the dominant Bifidobacterium species in the samples, but were nevertheless present at notable levels. B. angulatum was not detected from any of the subjects, although Woodmansey et al. (2004) identified B. angulatum as the predominant Bifidobacterium species in British elderly subjects, as analysed by culturing and cellular fatty acid profiles. This difference may be related to dietary or genetic differences among the study populations, or the different methodologies applied.

B. adolescentis (sensu stricto) was detected less frequently than previously reported (Gavini et al. 2001; Mutai and Tanaka 1987; Silvi et al. 2003), but when present, B. adolescentis was a dominant part of the Bifidobacterium microbiota in the elderly. Administration of placebo oat drink increased the levels of B. adolescentis, possibly due to the effects of oat components such as the oat fibre including ß-glucan. It is not known why such an effect only occurred in the placebo group. It is possible that the administration of probiotics favoured Bifidobacterium species other than B. adolescentis, increasing the competition between the species. Several culture-based studies have suggested that B. infantis is found exclusively in infants (Mitsuoka et al. 1974; Mutai and Tanaka 1987; Woodmansey et al. 2004), but in this study B. infantis was detected in 13.6% of the elderly subjects. It is possible that due to the close relatedness to B. longum (Sakata et al. 2002), B. infantis has earlier been overlooked as a component of adult and elderly gut microbiota. B. animalis was found to be commonly present in the elderly subjects at low levels. Traditionally, B. animalis has not been considered a component of normal human gut microbiota, but B. animalis subsp. lactis has been reported the most common Bifidobacterium species in commercial probiotic products in Europe (Gueimonde et al. 2004). Although the subjects consumed a controlled diet during the study, the dietary origin of this species cannot be completely ruled out. It is possible that the presence of B. animalis has been overlooked in the earlier culture-based studies, as B. animalis may grow slowly on nutrient media used normally for the culturing of Bifidobacterium, and it may be difficult to detect minor components of complex microbiota due to overgrowth of dominant species. In addition, as B. animalis has not been thought to be a component of normal human microbiota, it often has been excluded from culture-independent analyses of human gut microbiota. According to the current results, B. animalis was usually present at low levels, representing less than 1% of the total genus Bifidobacterium, and this may also partly explain why B. animalis has not been detected frequently in many earlier reports. Taken together, the results of the current study are in agreement with the results reported recently for institutionalized elderly subjects from Helsinki, Finland. Nevertheless, differences in the baseline prevalence of certain species, in particular B. adolescentis and B. animalis, can be observed between the two elderly populations. The baseline differences in the microbiota composition as well as the possible dietary, genetic and environmental factors may partly explain why the changes in the Bifidobacterium microbiota associated with the probiotic intervention were somewhat different between the two study populations, with the probiotic intervention enhancing the levels of B. adolescentis in the elders from Helsinki area and the levels of B. bifidum and B. breve in the elders from Kuopio area. In both study populations, the levels of B. catenulatum increased as a result of the probiotic intervention.

In conclusion, the results of this study demonstrate that the Bifidobacterium microbiota of the elderly may be modified by probiotic intervention. Such intervention may affect a number of different species other than the administered species, in particular the culturable proportion of the Bifidobacterium microbiota. Moreover, this study suggests that the average level and the species diversity of Bifidobacterium microbiota of the elderly may be considerably higher in certain populations than previously thought. Certain species which previously have not been associated with Bifidobacterium microbiota of elderly subjects were found to be relatively frequent in faecal samples in this population. Future research in this required to further study the impact of probiotic therapies on gut metabolism, pathogen resistance and intestinal function of elderly subjects.

Acknowledgements

Bioferme (Kaarina, Finland) is thanked for providing the test oat products used in the study. Dr. Miguel Gueimonde is thanked for helpful discussions. Sampo Lahtinen was funded by the ABS Graduate School.

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