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Impact of coffee consumption on the gut microbiota: A human volunteer study
Muriel Jaquet, Isabelle Rochat, Julie Moulin, Christophe Cavin, Rodrigo Bibiloni
Nestl Research Center, Nutrition and Health Department, CH-1000 Lausanne 26, Vers-chez-les-Blanc, Switzerland
a b s t r a c t a r t i c l e i n f o
Article history:
Received 10 November 2008
Received in revised form 14 January 2009
Accepted 15 January 2009
Keywords:
Microbiota
Coffee
RT-PCR DGGE
FISH
The impact of a moderate consumption of an instant coffee on the general composition of the human
intestinal bacterial population was assessed in this study. Sixteen (16) healthy adult volunteers consumed a
daily dose of 3 cups of coffee during 3 weeks. Faecal samples were collected before and after the
consumption of coffee, and the impact of the ingestion of the product on the intestinal bacteria as well as the
quantication of specic bacterial groups was assessed using nucleic acid-based methods. Although faecal
proles of the dominant microbiota were not signicantly affected after the consumption of the coffee (Dice's
similarity index=92%, n=16), the population of Bidobacterium spp. increased after the 3-week test period
(P=0.02). Moreover, in some subjects, there was a specic increase in the metabolic activity of Bidobac-
terium spp. Our results show that the consumption of the coffee preparation resulting from water co-
extraction of green and roasted coffee beans produce an increase in the metabolic activity and/or numbers of
the Bidobacterium spp. population, a bacterial group of reputed benecial effects, without major impact on
the dominant microbiota.
2009 Elsevier B.V. All rights reserved.
1. Introduction
The key role of the complexcolonic microbiota ingut healthhas been
largely addressed during the last years. The gut microbial community
has been shown to affect a wide range of biological processes including
gut maturation and angiogenesis (Stappenbeck et al., 2002), develop-
ment of innate immunity (Mazmanian et al., 2005), production of
vitamins (Hill, 1997), biotransformation of endogenous and exogenous
compounds (Blaut and Clavel, 2007), dietary energy harvest, and
recently, regulation of the host fat storage (Bckhed et al., 2004).
Considerable attention has been devoted to studying how diet can
impact both the composition and metabolism of the gut microbiota.
The conversion of dietary components by intestinal bacteria leads
to the formation of a large variety of compounds, with either benecial
or adverse effects on humanhealth. Carbohydrate-rich diets can have a
signicant effect on the numbers of viable butyrate-producing bacteria
in the gut, like the clostridial clusters IV and XIVa (Ruminococcus/
Faecalibacterium and Roseburia/Eubacterium respectively, which com-
prise over 50% of the bacteria in the human large intestine). Butyrate is
the preferredenergysource for colonic epithelial cells andis thought to
play an important role in maintaining colonic health in humans by
activating apoptosis and cell cycle arrest (Roediger, 1982; Heerdt et al.,
1994). Indigestible bres can also selectively stimulate the growth of
species of Bidobacterium, a genus of bacteria of reputed benecial
effects (Lee et al., 1993; Gibson and Wang, 1994; Jiang et al., 1996;
Schiffrinet al., 1995; Singhet al., 1997; Marteauet al., 2002; Rayment et
al., 2002). Plant lignans and avonoids, generally considered as non-
nutritive substances, could be transformed by intestinal bacteria into
estrogen-like compounds with antioxidant effects. For instance,
lignan-transforming activity was identied on strains of the genera
Bacteroides, Clostridium, Eggerthella, Eubacterium, and Ruminococcus
isolated from human faeces (Blaut and Clavel, 2007).
Coffee is one of the most popular beverages at a global level,
appreciated not only for its taste, but also for its stimulating
properties. Coffee beverages contain signicant amounts of soluble
bre (mainly galactomannans and arabinogalactan-proteins) and
phenolic compounds (chlorogenic acids), which are well utilised by
the human faecal microbiota. Although traditionally considered as
containing low nutritional value, regular coffee drinking has been
shown to impact on several aspects of health. Most of this evidence
was obtained either from in vitro studies using static batch fermenta-
tions with faecal slurries (Plumb et al., 1999; Couteau et al., 2001;
Borrelli et al., 2004; Gniechwitz et al., 2007, 2008), or in human
intervention studies with by-products of spent coffee grounds, an
industrial waste (Umemura et al., 2004; Asano et al., 2004).
The aimof this human trial was to evaluate the impact of a moderate
consumption of an instant coffee product on both the metabolic activity
and bacterial composition of the intestinal microbiota.
2. Materials and methods
2.1. Subjects
Sixteen (16) healthy adults (7 males, 9 females), aged between 21
and 57 years, with no history of gastrointestinal problems volunteered
for the study. The protocol was carefully explained to the volunteers,
International Journal of Food Microbiology 130 (2009) 117121
Corresponding author. Tel.: +41 21 785 8676; fax: +41 21 785 8544.
E-mail address: rodrigo.bibiloni@rdls.nestle.com (R. Bibiloni).
0168-1605/$ see front matter 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2009.01.011
Contents lists available at ScienceDirect
International Journal of Food Microbiology
j our nal homepage: www. el sevi er. com/ l ocat e/ i j f oodmi cr o
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and their written informed consent was obtained. Inclusion criteria
consisted of the following: no intake of antibiotics, laxatives or other
gastrointestinal medications 3 months prior to the beginning of the
study, no consumption of yogurt or products containing bidobac-
teria, lactobacilli or prebiotics (oligosaccharide-containing products or
supplements) 3 weeks before the beginning of the study, consumption
of up to 3 cups of coffee/day, body mass index [BMI; body weight (kg)/
height (m
2
)] between 20 and 30, and no simultaneous participation in
other study. Volunteers were asked to keep records of concomitant
medication, adverse effects or any other comments.
2.2. Study design
The study had a longitudinal design, and consisted of a 3-week
pre-treatment period during which the volunteers were instructed to
start a partial diet restriction, followed by a 3-week treatment period
during which they consumed a coffee test product (3 cups/day). The
partial diet restriction consisted in no consumption of yogurts, or
fermented milks containing bidobacteria, lactobacilli, or prebiotics,
and no cereal breakfast or whole grain bread during the whole study.
No other coffee product other than the test product was allowed
during the study. A faecal sample was collected from each volunteer
before the beginning of the treatment period (baseline), and at the end
of the 3 weeks of coffee consumption. All faecal samples were
immediately frozen at 80 C until further analysis. The study was
approved by the local Ethics Committee (Commission d'Ethique de la
Recherche Clinique, Lausanne), reference 36/07.
2.3. Coffee product
Sachets containing 3.4 g of instant coffee powder resulting from
water co-extraction of green and roasted coffee beans, were provided
to the volunteers. Prior to consumption, coffee powders were
dissolved in heated tap water to a volume of 150 to 200 ml according
to the taste of the volunteers. Three cups of coffee/day were consumed
orally during 3 weeks.
2.4. Analysis of faecal microbiota by RT-PCR DGGE
Bacterial RNAs were extracted from faecal samples using the
BioRobot EZ1 apparatus (Qiagen, Germany), according to the manu-
facturer's instructions. Briey, faecal samples (1/10 [wt/vol] in sterile
phosphate buffered saline) were homogenised in a bead-beater for
2 min in sterile microcentrifuge tubes containing 0.3 g of glass beads
and 750 l of QIAzol lysis reagent. After the addition of 150 l of
chloroform:isoamylalcohol (24:1), samples were vortexed for 15 s and
let stand for 23 min at room temperature. Finally, samples were
centrifuged at 12,000 g for 15 min at 4 C and 300 l of the supernatant
was loaded into the BioRobot apparatus. RNA were eluted in 200 l of
elution buffer, and amplied by RT-PCR (Qiagen OneStep RT-PCR kit)
targeting the V3 region of the 16S rRNA gene. RT-PCRs were
performed using the universal bacterial primers HDA1-GC and
HDA2, and a previously described programme (Tannock et al., 2004).
Denaturing gradient gel electrophoresis were performed using a
DCode apparatus (Bio-Rad) and 6% polyacrylamide gels with a 3055%
gradient of 7 M urea and 40% (v/v) formamide that increased in the
direction of electrophoresis. Samples were run along with a DGGE
reference marker containing PCR products of the following species
(Lactobacillus johnsonii NCC533, Lactobacillus helveticus ATCC15009,
Lactococcus lactis LM0230, Bidobacterium breve NCC452, Bidobac-
terium longum NCC3001, and Bidobacterium lactis NCC362, uncul-
tured bacterium clone pDP 867). Electrophoretic runs were in TAE
buffer (40 mM Tris, 20 mM acetic acid, 1 mM EDTA) at 130 V and 60 C
for 270 min. Gels were stained with SYBR Safe 1(Invitrogen, USA) for
30 min, rinsed with deionized water, and viewed by UV transillumi-
nation. DGGE proles were compared by determining the Dice's
similarity coefcient (D
SC
) using the Bionumerics software package
(version 4.01, Applied Maths) at a sensitivity of 12%. All gels were
normalized using the DGGE marker before analysis.
2.5. Identication of fragments eluted from RT-PCR DGGE gels
DNA fragments of interest were excised from the polyacrylamide
gel using sterile scalpel blades, placed in 100 l diffusion buffer (0.5 M
ammoniumacetate, 10 mMmagnesiumacetate, 1 mMEDTA, 0.1% SDS,
pH 8.0) and stored at 20 C until use. DNA was recovered and treated
with S1 nuclease (Roche, Mannheim, Germany) as described pre-
viously (Tannock et al., 2004). S1 nuclease-treated DNA fragments
were used as templates in PCR with HDA primers prior to ligation in a
cloning vector. The amplicons were cloned and sequenced as
described previously (Bibiloni et al., 2008). The retrieved sequences
were phylogenetically classied using the RDP Classiers (defaults
parameters) (Wang et al., 2007). Although of short length, the
sequences gave high-resolution chromatograms and provided suf-
cient taxonomic power for bacterial identication (Snart et al., 2006).
2.6. Determination of selected bacterial groups by FISH
Selected bacterial groups were enumerated in faecal samples with
specic probes by uorescent in situ hybridization (Harmsen et al.,
2002). The sequences and target groups for the probes are shown in
Table 1. Total cell numbers were counted by nucleic acid staining with
4,6-diamidino-2-phenylindole, and the bacterial populations were
recorded as percentage of the total cell count.
2.7. Statistical analysis
Based on the data distribution, particularly due to the presence of
outliers, non-parametric Wilcoxon signed rank tests were performed
on FISH results (SAS software, version 8.2). No correction for multiple
comparisons was performed on these results.
3. Results
3.1. Fecal microbiota proles generated by RNA-DGGE
Similarity analysis of the RT-PCR DGGE proles generated from
bacterial RNA before and after the consumption of the coffee product
did not reveal differences in each individual. Pairwise calculations
showed that proles were 92% similar (D
SC
). No clustering due to the
consumption of coffee was observed when all individuals were
compared (Fig. 1). RT-PCR DGGE gels were generated with amplicons
produced using bacterial universal primers; however, only the
dominant bacterial population representing over 1% of the total
population is reected in the gels (Muyzer et al., 1993). Proles were
individually unique as reported previously (Zoetendal et al., 1998).
Despite this high similarity of the whole prole, some specic bands
were more intensely stained in some of the post-consumption
samples, especially in the lower part of the gel (high-G+C bacteria).
Table 1
Probes used for FISH analysis
Probe Target bacterial group Sequence 5-3
Erec482 Clostridium/Eubacterium GCT TCT TAG TCA RGT ACC G
Bac303 Bacteroides/Prevotella CCA ATG TGG GGG ACC TT
Wbif164 Bidobacterium CAT CCG GYA TTA CCA CCC
Eco1531 Enterobacteriaceae CAC CGT AGT GCC TCG TCA TCA
Lab158 Lactobacillus/Enterococcus GGT ATT AGC AYC TGT TTC CA
118 M. Jaquet et al. / International Journal of Food Microbiology 130 (2009) 117121
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3.2. Sequence analysis of DGGE bands
Distinct 16S rRNA gene fragments that were more apparent in the
proles after the consumption of coffee than in those before the
consumption were excised from the gel, cloned and sequenced.
Alignment of the sequences with sequences using the RDP Classier
resulted in identication of the bacterial origins. The identity of the
sequences is shown in Table 2. We focused on fragments in the lower
part of the gels because alterations to proles were commonly
detected there. Four individuals showed an increased staining in the
bands corresponding to the genus Bidobacterium (98100% identity,
RDP Classier) after the consumption of coffee, and four individuals
showed an increased staining in bands corresponding to butyrate-
producing bacteria (Lachnospiraceae [100% identity], Roseburia [100%
identity]). One band (band #3) gave insufcient quality for taxonomic
analysis. One individual showed increased intensity of a band
corresponding to a member of the Actinobacteria phylum. The
maximum condence value attributed to this sequence was at the
family level (Coriobacteriaceae [100% identity]).
3.3. Enumeration of selected bacterial groups by FISH
The population of selected bacterial groups present in all
volunteers before and after the consumption of coffee are shown in
Fig. 2. Bacterial counts were determined by FISH technology and are
expressed as log
10
cells/g faeces. The total number of bacteria detected
in faeces did not differ between pre and post consumption of the
coffee product (P=0.27). Likewise, little or no signicant differences
were observed in the numbers of Clostridium/Eubacterium group, En-
terobacteriaceae family, Bacteroides/Prevotella group, and Lactobacil-
lus/Entrococcus group. In contrast, the consumption of the coffee
product during 3 weeks resulted in a signicant increase in numbers
of Bidobacterium spp. (P=0.02).
The impact of coffee consumption was not the same for all
volunteers. The largest increase in bidobacterial numbers after coffee
consumption was observed for those volunteers showing the lowest
initial bidobacterial levels. This phenomenon was previously
reported for the consumption of oligosaccharide-containing biscuits
(Tuohy et al., 2001). Twelve of the sixteen volunteers showed an
increase in bidobacterial numbers (ve of them of over 0.5 log
10
cells/g), and in four volunteers bidobacterial levels decreased after
the consumption of coffee. However, we could not nd a strong
correlation on those individuals harbouring an already high initial
bidobacterial counts (between log
10
8.5 and log
10
9.5) to assess a
systematic behaviour.
4. Discussion
The popularity of coffee is attributed not only to its taste and
aroma, but also to its physiological effects and psychoactive proper-
ties. Yet, scientic medical research about coffee, its absorption,
distribution, metabolism, and excretion in the human body is very
recent. Coffee has its advocates and its opponents when it comes to
the effects of coffee drinking on health. Acknowledging that there
have been many contradictory results in relationship to confounding
factors, evidence amassed to date from epidemiological studies
Fig. 1. RNA-DGGE gels of faecal samples using bacterial universal primers. Proles represent abundance and/or metabolic activity of dominant bacterial species before and after (T)
coffee consumption for each volunteer (represented by letters). Ld: Ladder used to normalize the gels. Interesting bands are indicated with numbered arrows.
Table 2
Taxonomic assignment of selected RT-PCR DGGE bands according to the RDP classier
Band # Superkingdom CV Phylum CV Class CV Order CV Family CV Genus CV
1 Bacteria 100% Firmicutes 100% Clostridia 100% Clostridiales 100% Lachnospiraceae 94% Catonella 15%
2 Bacteria 100% Firmicutes 100% Clostridia 100% Clostridiales 100% Lachnospiraceae 99% Lachnospira 94%
4 Bacteria 100% Firmicutes 100% Clostridia 100% Clostridiales 100% Lachnospiraceae 100%
5 Bacteria 100% Proteobacteria 100% Alphaproteobacteria 100% Rhizobiales 100% Methylobacteriaceae 87% Methylobacterium 87%
6 Bacteria 100% Actinobacteria 100% Actinobacteria 100% Bidobacteriales 100% Bidobacteriaceae 100% Bidobacterium 100%
7 Bacteria 100% Actinobacteria 100% Actinobacteria 100% Coriobacteriales 100% Coriobacteriaceae 100%
8 Bacteria 100% Bacteroidetes 100% Bacteroidetes 99% Bacteroidales 99% Prevotellaceae 96% Prevotella 94%
9 Bacteria 100% Firmicutes 92% Clostridia 92% Clostridiales 92% Lachnospiraceae 77% Coprococcus 14%
10 Bacteria 100% Firmicutes 100% Clostridia 100% Clostridiales 100% Lachnospiraceae 100%
11 Bacteria 100% Firmicutes 100% Clostridia 100% Clostridiales 100% Lachnospiraceae 100% Roseburia 100%
12 Bacteria 100% Actinobacteria 100% Actinobacteria 100% Bidobacteriales 99% Bidobacteriaceae 99% Bidobacterium 99%
13 Bacteria 100% Actinobacteria 100% Actinobacteria 100% Bidobacteriales 100% Bidobacteriaceae 100% Bidobacterium 100%
14 Bacteria 100% Actinobacteria 100% Actinobacteria 100% Bidobacteriales 98% Bidobacteriaceae 98% Bidobacterium 98%
For each sequence, the taxonomic assignments as well as the condence value (CV) for each class are listed.
119 M. Jaquet et al. / International Journal of Food Microbiology 130 (2009) 117121
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suggest that coffee consumption may help prevent many chronic
diseases, like type 2 diabetes, arteriosclerosis, and some types of
cancer (Schilter et al., 2001; Drea and da Costa, 2005; Higdon and
Frei, 2006). Among its various constituentsmore than a thousand
compounds have been described (Spiller, 1998) most of which may
affect human healthcaffeine is by far the best studied and the one
that is responsible for the mild stimulant effect on the central nervous
system stimulatory and benecial properties on alertness, mood, and
physical and psychomotor performances. It is likely, however, that
some of the proposed benets of daily coffee consumption might be
related to other constituents, such as alkaloids, chlorogenic acids and
other phenolic compounds, bers, and minerals.
The complex microbial ecosystem of the human gastrointestinal
tract, in particular that contained in the colon, has been shown to
metabolise many dietary ingredients, especially those that escape
digestion. On one side, our study demonstrates that a moderate
consumption of coffee has a targeted effect on particular members of
the colonic microbiota (represented in faeces), principally bidobac-
teria, without a major impact on the dominant bacterial groups. On
the other side, RNA extracted from the bacterial cells is mostly rRNA
and can be used as an indicator of metabolic activity because the
ribosome-per-cell ratio is roughly proportional to the growth rate of
bacteria (Dunne et al., 1999). As these DGGE gels were produced using
rRNA as template for the RT-PCR reactions, the proles represent
mostly metabolically active bacteria, or those that multiply more
rapidly. Consequently, differences in staining reveal bacterial groups
contained in the faeces that become more active or increase in amount
after the consumption of coffee.
Although our study cannot discriminate which coffee component
is responsible for this effect (chlorogenic acids and bers contained in
coffee are known to be metabolised by the gut microbiota), it
illustrates a means of modulating the human microbiota through
coffee consumption. Given that the gut ora has a major role in human
nutrition and health, some of the benecial effects of coffee
components may be ascribed to the microora involved in their
metabolism. Instant coffee, for example, is recognized as an important
source of soluble polysaccharides containing around 20% of arabino-
galactan proteins (Leloup, 2006). Prebiotic properties of arabinoga-
lactan proteins may be a result of the increased levels of short chain
fatty acids such as butyrate and propionate (Redgwell and Fischer,
2005; Michel et al., 1998).
A few attempts to evaluate the contribution of the gut microbiota
to the metabolism of coffee components have been performed with
the aid of in vitro model systems to simulate the intestinal conditions
using faecal slurries. Although far from reality, these studies have
indicated that the gut microbiota is implicated in the metabolism of
melanoidins (Ames et al., 1999), bers (Gniechwitz et al., 2007), and
chlorogenic acids (Plumb et al., 1999). Traditional culture methods
have been used to isolate and characterize colonic bacteria able to
hydrolise chlorogenic acids (Couteau et al., 2001). Two studies
performed in Japan explored the impact of mannooligosaccharides
produced from spent coffee grounds (a coffee waste) on the cultivable
faecal microbiota (Asano et al., 2004; Umemura et al., 2004). The
classical microbiological methods employed for the analysis of the
faecal microbiota give a partial representation of the impact on the gut
ecosystem because it has been estimated that more than 60% of the
faecal bacteria cannot be cultured due to their fastidious requirements
for anaerobiosis and nutritional needs. Nevertheless, these studies
illustrated the impact of a by-product from the food industry in the
microbiota of humans.
Our study has not been tailored to address a particular health
condition, but may sway future strategies to identify a specic
population with low bidobacterial numbers in their gastrointestinal
tract where coffee consumption may have an important impact. These
groups include the elderly (Hopkins et al., 2001), or people under-
going antibiotic therapy (Jernberg et al., 2000). In our study, we have
shown that healthy volunteers with lower initial bidobacterial
populations in faeces displayed the largest increases following the
consumption of coffee. Some individuals also showed increased
metabolic activity for bidobacterial species after drinking coffee.
Although these results cannot be directly related to the consumption
of the product, it suggests that the consumption of coffee may prove
useful for increasing bidobacterial numbers or metabolic activity of
those individuals with lowered colonic bidobacterial numbers. The
health benets or the biological relevance associated with these
ndings have still to be assessed.
Acknowledgements
The authors would like to thank Maurice Beaumont, Anny Blondel-
Lubrano, and Sylviane Oguey-Araymon for their assistance in the
recruitment of the volunteers and the submission of documents to the
Ethical Committee, and to Lutz Krause for his support on the
bioinformatics analysis. The dedication of the human volunteers
who participated in this study is gratefully acknowledged.
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