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Applied and Environmental Microbiology, October 2001, p. 4939-4942, Vol. 67, No. 10
INSERM U 290,
Paris,1 Département de
gastroentérologie, Hôpital Européen Georges Pompidou,
AP-HP, 75908 Paris,2 Laboratoire de
Biologie, Conservatoire National des Arts et Métiers, 75003 Paris,3 INRA, CR de Jouy-en-Josas,
78352 Jouy en Josas,4 and Laboratoire de
Microbiologie, INRA, CR de Clermont-Ferrand/Theix, 63122 Saint
Genes-Champanelle,5 France
Received 2 April 2001/Accepted 1 August 2001
The composition of the human cecal microbiota is poorly known
because of sampling difficulties. Samples of cecal fluid from eight
subjects were collected via an intestinal tube. Feces were also
collected. Total anaerobes, facultative anaerobes, bifidobacteria, and
Bacteroides were enumerated by culture methods, and the
predominant phylogenetic groups were quantified by molecular
hybridization using a set of six rRNA-targeted probes. The numbers of
strict anaerobes, bifidobacteria, Bacteroides, and members
of the Clostridium coccoides group and Clostridium
leptum subgroup were lower in the cecum. Facultative anaerobes
represented 25% of total bacteria in the cecum versus 1% in the feces.
The indigenous microbiota plays an
important part in colonic physiology and may be involved in the
pathogenesis of large-bowel diseases, such as cancer and Crohn's
disease (7, 10, 23, 24). It is well established that
microbiota patterns differ depending on the gastrointestinal site, with
differences clearly observed between the stomach, upper small bowel,
lower small bowel, and rectum (9, 10, 11, 17). The
ecological conditions in the cecum (i.e., the initial part of the right
colon) differ from those encountered in the distal colon (based on
fecal samples). The cecum receives substrates which escape digestion in
the small bowel, has higher concentrations of volatile fatty acids, and has a lower pH (9, 11, 16, 17). Few authors have attempted to describe the composition of the human cecal microbiota (4, 13,
16, 19), owing to sampling difficulties and the need to maintain
anaerobic conditions from sampling to counting. Several methods have
been used, such as sampling of sudden-death victims (16),
use of a pyxigraphy capsule (19), needle probing during surgery (4), and intestinal intubation with a long tube
(13). These techniques have inherent advantages and
limitations. Only intubation and pyxigraphy can be performed in healthy
subjects, and both can be repeated to study the stability of the flora
or the influence of various parameters on its composition. Colonic samples of sufficient volume are difficult to obtain because of their
viscosity and the difficulties in ensuring adequate anaerobic conditions. It was previously shown that a long tube could be used to
sample the chyme in the right colon (11, 17). Using an
intubation technique, Gorbach et al. demonstrated in three subjects
that the cecum contained 100 times more bacteria than the terminal
ileum (13). This study aimed to compare the composition of
the cecal and fecal microbiota in healthy humans. Recent studies of the
fecal microbiota indicate the necessity of molecular evaluation of this
ecosystem, and until now such methods have not been employed for cecal analysis.
Eight healthy volunteers (four men and four women aged 22 to 27 years)
gave informed written consent to the study protocol, which was approved
by the local Ethics Committee. None had a history of gastrointestinal
disease, laxative use, or recent treatment with antibiotics. They were
asked to avoid fermented dairy products for 15 days and were otherwise
allowed normal diets. The day before sampling, at 0900 they were
nasally intubated with a double-lumen tube. The distal extremity of the
first lumen had a rubber bag containing 30 g of mercury which
could be inflated with air to accelerate its progression through the
small bowel (11, 17). The sampling lumen consisted of a
vinyl tube with an internal diameter of 3.5 mm (Portex, Hythe Kent,
United Kingdom). It was multiperforated at its extremity, which was
located 3 cm above the rubber bag. Its other end was closed with a
stopcock. Progression of the tube was monitored fluoroscopically. When
the sampling port had reached the ileum, the sampling lumen was flushed
with 30 ml of nitrogen gas and the stopcock was closed; when it had reached the cecum (approximately 6 to 10 h after introduction), the tube was fixed to the nose, the rubber bag was deflated, the sampling lumen was flushed again with 30 ml of nitrogen gas, and subjects were asked to remain in a semirecumbent position to avoid further progression of the tube. The subjects received standard meals
at 1200 and 1930, and the following day they received a standard
breakfast at 800 and a meal at 1200. The meals consisted of two eggs in
the evening and 100 g of steak for lunch, mashed potatoes, 30 g of cheese (Gruyere), 100 g of white bread, and 30 g of
butter. Breakfast consisted of 250 ml of coffee, 10 g of
hydrolyzed milk, 10 g of sucrose, 100 g of white bread, 30 g
of butter, and 30 g of strawberry jam. The volunteers were allowed to drink water or tea ad libitum; smoking was not permitted. At 1400, on the second day, 2 to 10 ml of cecal contents was sampled by suction
using a sterile syringe equipped with a stopcock connected to the
stopcock of the sampling lumen. When sampling was unsuccessful, 5 to 10 ml of nitrogen gas was flushed into the sampling lumen to ensure its
patency and gentle suction was again applied every 10 min until a
sample was obtained. Fecal samples were obtained on the same day,
before cecal sampling. The subjects voided their feces into a box,
which allowed immediate introduction of stools into an anaerobic system
(Anaerocult; Merck, Darmstadt, Germany). The closed boxes
containing feces and the tight syringes containing the cecal samples
were transferred within 10 min to an anaerobic chamber. Samples were
diluted using anaerobic dilution solution containing (in grams/liter):
NaCl, 5; glucose, 2; cysteine-HCl, 0.3. They were homogenized by
magnetic stirring to give a 10-fold dilution (wet weight/volume), which
was then serially diluted down to 10 Total RNA was extracted from frozen fecal (200 mg) and cecal (400 µl)
material, as described by Doré et al. (8), using 0.1 g of zirconium beads. RNA concentration of extracts was
determined by dot blot hybridization with the universal oligonucleotide
probe (8) using a standard Escherichia coli RNA
control (rRNA standards; Roche Diagnostics, Meylan,
France). 16S rRNA-targeted oligonucleotide probes are detailed in
Table 1. Dot blots were achieved as
previously described (8): serial dilutions of control RNA
(2 to 250 ng) from pure cultures (Bacteroides vulgatus
[ATCC 8482], Bifidobacterium longum [ATCC 15707],
E. coli [Boehringer Mannheim rRNA standards], Lactobacillus acidophilus [ATCC 4356], Eubacterium
siraeum [ATCC 29066], Ruminococcus productus [ATCC
27340]), and 100 to 200 ng of total RNA extracted from fecal and cecal
samples were blotted and hybridized with purified 32P-5' end-labeled
probes overnight at 42°C. Stringent washing was performed twice for
30 min with 1× SSC (1× SSC is 0.15 M NaCl plus 0.015 M sodium
citrate), 1% sodium dodecyl sulfate buffer at an experimentally
previously defined temperature depending on each probe (Table
1). Hybridization signals on dot blots were measured using radioimaging
with the Instant Imager (Packard Instruments). Microbial quantification for each group was expressed as the percentage of the total bacterial 16S rRNA (mean of duplicate measurements). Microorganism counts expressed as log 10 are reported per gram (wet weight) of cecal or
fecal contents. Data are expressed as means, with 95% confidence intervals in brackets. Comparisons between the cecal and fecal flora
were made using the Wilcoxon test. Statistical significance was
achieved if the P value was <0.05.
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.10.4939-4942.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Comparative Study of Bacterial Groups within the Human Cecal
and Fecal Microbiota
ABSTRACT
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11 in anaerobic
dilution solution. Aliquots (100 µl) of each dilution were evenly
spread on plates of freshly prepared media. Bifidobacteria were counted
using Beerens' medium (3). Plates were incubated in
anaerobic jars for 5 days at 37°C using the Anaerocult procedure (Merck) prior to counting. Bifidobacteria colonies were identified by
their fructose-6-phosphate-phospho-ketolase activity (21). Facultative anaerobes and Bacteroides were counted on brain
heart agar (Bio-Rad, Marne la Coquette, France), to which 1% of hemin solution (500 µg/ml) had been added. Facultative anaerobes were counted directly after 5 days of incubation at 37°C in aerobic conditions. For counting of Bacteroides bacteria, brain
heart agar plates were exposed for 1 h to air to select less extremely oxygen-sensitive microorganisms prior to incubation in strict anaerobic
conditions at 37°C for 48 h (5). Colonies were
transferred onto 1% sodium dodecyl sulfate-impregnated Nytran N
membranes (Schleicher & Schuell, Ecquevilly, France) and hybridized
with a Bacteroides group-specific probe as previously
described (8). To count total viable anaerobes, 1 ml of
each 10-fold dilution was inoculated in duplicate in 15 ml of
Wilkins-Chalgren agar (Difco, Detroit, Mich.) at 45°C. The inoculated
medium was then poured into 8- by 400-mm tubes, which were immediately
cooled to ensure prompt solidification and incubated for 14 days at
37°C (18).
TABLE 1.
Probes used in this study
At least 5 ml (5 to 50 ml) of cecal contents could be sampled in all
experiments. The sample could be obtained 2 h after the meal in 7 out of 11 experiments and between 2.5 and 3 h after the meal in
the other 4 experiments. We chose to sample the cecal chime 2 to 3 h after a standard meal, as proposed by Gorbach et al.
(13), based on previous reports that sampling was not
always possible after an overnight fast (17). Total viable
anaerobe counts as well as those of facultative anaerobes,
bifidobacteria, and Bacteroides in cecal and fecal samples
are shown in Table 2. Counts of total
viable anaerobes, bifidobacteria, and Bacteroides were
consistently lower in the cecal samples compared to those of feces.
Counts of facultative anaerobes did not differ significantly between
the cecal and fecal samples. Facultative anaerobes represented 25%
versus 1% of the total anaerobic flora in the cecum and feces, respectively. Relative quantification of the fecal and cecal microbial populations achieved by dot blot hybridization using 16S rRNA-targeted oligonucleotide probes specific to microbial group, genus, or species
is shown in Table 3. Strict anaerobic
bacterial populations represented by the Bacteroides,
Clostridium leptum, and Clostridium coccoides groups
were significantly lower in the cecum. Facultative anaerobes
represented by the Lactobacillus-Enterococcus group and
E. coli species showed much higher rRNA proportions in cecal contents.
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This study shows, using culture-dependent and culture-independent methods, that the cecal flora differs greatly from the fecal flora. Meals flush fluids, substrates, and bacteria from the upper gastrointestinal tract into the cecum, and this may influence the cecal flora. The bacterial density in the upper gastrointestinal tract (increasing from 105 CFU/ml in the jejunum to 106 CFU/ml in the ileum [24]) is low compared to that of the cecum (108 CFU/ml). Assuming that 500 ml of ileal fluid entered the cecum after the meal and that water absorption led to a final volume of 50 to 100 ml (6), bacterial concentration would be below 107 CFU/ml. In other words, endogenous bacteria passively flushed from the small intestine would account for less than 10% of the bacteria in the cecum. The total anaerobe counts were 100 times lower in the cecal contents than in the feces. Similar results have been obtained with other sampling techniques used to date (4, 13, 16, 19). Water absorption in the colon may partly explain the increased bacterial density in the feces relative to that of the cecum. However, the increase in dry matter between the cecum and feces is only 10-fold (17), whereas bacterial density increases 100-fold. Bacterial growth must therefore occur within and downstream of the right colon. Some microorganisms, such as methanogens, represent <0.003 to 0.03% of all bacteria in the right colon, compared to 5 to 12% or more in the feces (16, 19). On the other hand, the numbers of facultative anaerobes were similar in the cecal and fecal flora. Results obtained using molecular hybridization were consistent with those obtained from classical studies. Strict anaerobes analyzed using probes specific for the Bacteroides (Bacteroides, Porphyromonas, and Prevotella spp.) and Clostridium groups (Clostridium, Eubacterium, and Ruminococcus spp., essentially) represented 44% of fecal bacterial rRNA and only 13% of cecal bacterial rRNA. rRNA from E. coli and the Lactobacillus-Enterococcus group represented 50% of the cecal bacteria rRNA and only 7% of fecal bacterial rRNA. Facultative anaerobes, i.e., enterobacteria (mainly E. coli) and enterococci, are usually thought to have little physiological relevance because of their low densities in the feces relative to that of the dominant flora, except when the latter is weakened (for example, following antibiotic use) (23). As we observed that facultative anaerobes belong to the dominant microbiota in the cecum, this suggests that they may have an important physiological role at this site.
In conclusion, the human cecal flora differs quantitatively and qualitatively from the fecal flora. It harbors 100 times fewer anaerobes, while facultative anaerobes represent an important part. Studying the right-sided colonic flora would, thus, be more appropriate than studying feces for functions occurring in the cecum, such as fermentation of dietary fibers and endogenous substrates, or for diseases involving the right part of the colon, such as ileocecal Crohn's disease.
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FOOTNOTES |
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* Corresponding author. Mailing address: Département de gastroentérologie, Hôpital Européen Georges Pompidou, 20 rue Leblanc, 75908, Paris CEDEX 15, France. Phone: 33 1 5609 3555. Fax: 33 1 5609 3554. E-mail: philippe.marteau{at}egp.ap-hop-paris.fr.
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Applied and Environmental Microbiology, October 2001, p. 4939-4942, Vol. 67, No. 10
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.10.4939-4942.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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