The Journal of Nutrition

Critical Review

Does Consumption of Fermented Foods

Modify the Human Gut Microbiota?
Leah T Stiemsma,1 Reine E Nakamura,2 Jennifer G Nguyen,3 and Karin B Michels1,4

1
Department of Epidemiology, Fielding School of Public Health, University of California, Los Angeles, CA, USA; 2 Department of
Integrative Biology and Physiology, University of California, Los Angeles, CA, USA; 3 Department of Biology, University of California, Los
Angeles, CA, USA; and 4 Institute for Prevention and Cancer Epidemiology, Faculty of Medicine and Medical Center, University of Freiburg,
Freiburg, Germany

ABSTRACT
The human microbiota is a key contributor to many aspects of human health and its composition is largely influenced
by diet. There is a growing body of scientific evidence to suggest that gut dysbiosis (microbial imbalance of the
intestine) is associated with inflammatory and immune-mediated diseases (e.g., inflammatory bowel disease and
asthma). Regular consumption of fermented foods (e.g., kimchi, kefir, etc.) may represent a potential avenue to counter
the proinflammatory effects of gut dysbiosis. However, an assessment of the available literature in this research area is
lacking. Here we provide a critical review of current human intervention studies that analyzed the effect of fermented
foods on the composition and/or function of the human gut microbiota. A total of 19 human intervention studies were
identified that met this search criteria. In this review, we discuss evidence that consumption of fermented foods may
modify the gut microbiota in humans. Further, there is cursory evidence to suggest that gut microbiota compositional
changes mediate associations between fermented food consumption and human health outcomes. Although promising,
there remains considerable heterogeneity in the human populations targeted in the intervention studies we identified.
Larger longitudinal feeding studies with longer follow-up are necessary to confirm and enhance the current data.
Further, future studies should consider analyzing microbiota function as a means to elucidate the mechanism linking
fermented food consumption with human health. This review highlights methodologic considerations for intervention
trials, emphasizing an expanse of research opportunities related to fermented food consumption in humans. J Nutr
2020;150:1680–1692.

Keywords: microbiota, fermented foods, lactic acid bacteria, yogurt, probiotics

Introduction dietary habits (3). For example, regular consumption of a diet

high in fat contributes to microbial dysbiosis by increasing the
The human microbiota is comprised of trillions of microbial
ratio of Firmicutes to Bacteroidetes (4).
cells and viruses that together have significant influences on
Probiotics are live microbes which, when ingested in
many aspects of human health and physiology (1). The term
adequate amounts, confer a health benefit to the host (5). In
microbiota refers to the microbial population (composition),
addition, in order for a microbe to be considered probiotic, it
whereas microbiome refers to the genetic makeup of this
also must adhere to the intestinal mucosa, because this is crucial
microbial population (2). Enhanced genomic strategies have
for microbial colonization of the gut (6). Proper adhesion to the
streamlined analysis of this microbial consortium, allowing
intestinal lining contributes to some of the benefits of consuming
for the characterization of un-culturable microbial taxa (1).
probiotic microbes, namely, protection from pathogen invasion
Application of these -omics strategies in humans suggests the
and modulation of intestinal immune cells (6). Consumption
microbiota may be modified by many environmental factors (3).
of probiotics or other beneficial microbial taxa via dietary
Dysbiosis is an imbalanced microbial state, often instigated by
vehicles may also modify the host gut microbiota composition
environmental factors such as broad-spectrum antibiotic usage,
toward a more balanced state and counteract the effects of
which kills both pathogenic and resident microbes, and poor
dysbiosis-promoting factors (7). In addition, many fermented
foods contain bioactive compounds as a result of microbial
Supported by National Cancer Institute, NIH T-32 training grant 5T32CA009142- fermentation (8). Regardless of whether or not the microbes
37 (to LTS). remain in the food, consumption of these compounds can confer
Author disclosures: The authors report no conflicts of interest.
Address correspondence to KBM (e-mail: [email protected]).
health benefits (8).
Abbreviations used: IBS, irritable bowel syndrome; LAB, lactic acid bacteria; LBP, There is also increasing evidence to support the role of
LPS-binding protein. specific genetic determinants as strong predictors of microbiota

Copyright  C The Author(s) on behalf of the American Society for Nutrition 2020.
Manuscript received December 10, 2019. Initial review completed January 21, 2020. Revision accepted March 2, 2020.
1680 First published online March 31, 2020; doi: https://doi.org/10.1093/jn/nxaa077.
composition (9, 10). For example, expression of specific genes cultures comprised of yeasts and bacteria [e.g., Kombucha
in early life is reported to influence gut microbiota composition SCOBY (symbiotic culture of bacteria and yeasts)] (17–19)
into adulthood (9). Further, in a study of 1126 twin pairs, re- (Table 1). There are many human intervention studies aimed
searchers identified heritable microbes and associations between at analyzing the effects on the gut microbiota of probiotic
specific gene loci and bacterial taxa (10). Thus, intervention fortification of fermented food products (e.g., a comparison
studies aimed at assessing the influence of dietary choices on the of the microbiota or other health effects after consumption
gut microbiota in humans are particularly challenging, because of yogurt fortified with Bifidobacteria spp. or yogurt without
each person’s microbiota may be genetically primed to react this taxon) (20, 21). The goal of this review is to assess the
differently to the same intervention. effect of spontaneously or multispecies starter-culture fermented
Fermented foods such as yogurt, sauerkraut, kimchi, and foods on the microbiota. Although common probiotic taxa
kefir contain relatively stable microbial ecosystems comprised may be used in the fermentation of the foods discussed in this
primarily of lactic acid bacteria (LAB) and LAB primary review, these taxa are primary fermenters of the food rather
metabolites (e.g., lactic acid) (8). Some LAB are considered than secondarily added to compare the probiotic effectiveness
probiotic (e.g., Lactobacillus spp.), whereas others are currently of that specific microbe. Articles comparing effects of specific
being studied to better characterize their probiotic potential probiotic-fortified fermentations are not included in this
(11). Nevertheless, these foods contain a variety of microbes review.
that exhibit health-promoting properties, which could be Each study included in this review meets the following
integrated into one’s diet as a means to support the health of criteria: 1) the study analyzed a spontaneously fermented
the gut microbiota. food or a food fermented with a multispecies starter culture
Fermentation is a common form of food preservation, in commonly used in the commercial production of these foods,
which a resilient microbial ecosystem prevents colonization 2) the study was a human intervention (feeding) study (no
by invading microbes that may cause spoilage (Erwinia spp., observational studies were included), and 3) the composition
Pseudomonas spp.), maintaining the integrity of the food and/or metabolic function of the gut (fecal) microbiota was
over long periods of time (8, 11). The initial microbial analyzed. Three researchers (LTS, REN, and JGN) inde-
inhabitants of these ecosystems are preferentially selected from pendently reviewed the scientific literature and consistently
the environment based on the particular nutrient components identified a total of 19 studies meeting these criteria using
and pH conditions of the food (4, 5). Over time, these the following search terms in the PubMed database: “mi-
initial microbes contribute to changes in the pH of the food, crobiome” or “microbiota” in combination with “fermented
resulting in colonization by a succession of microbial species food,” “fermented,” “kefir,” “yogurt,” “wine,” “kimchi,”
(12). For example, although cabbage fermentations like kimchi “sauerkraut,” “pickled food,” “cheese,” “fermented cabbage,”
and sauerkraut are typically colonized by LAB, the particular “fermented milk,” “kombucha,” “coffee,” and “fermented tea”
species and strains of LAB differ based on the acidity of the (Table 2).
food product (Leuconostoc mesenteroides dominates early in
the colonization of the food at a pH of 5.6–4.3, whereas
Lactobacillus sakei dominates later at a pH of 4.1) (13).
Observational and interventional studies in humans suggest The Micro- and Molecular Environment of
that consumption of fermented foods is associated with Fermented Foods and Their Potential Role
protection from metabolic and immune-mediated diseases (14–
in Human Health
16). However, whether modification of the gut microbiota
composition mediates this association has yet to be determined. The fermented foods discussed in this review are fermented
To assess the relevant empirical evidence, we reviewed published predominantly by LAB (e.g., Lactobacillus spp., Streptococcus
human intervention studies of fermented foods in which thermophilus), Bifidobacteria spp., and, in the case of red wine
the gut microbiota composition (via culture-dependent or and coffee, Saccharomyces yeasts (Table 1). Introduction of
culture-independent methods) and/or metabolic function (i.e., specific LAB and Bifidobacteria species and strains into both
production of bioactive metabolites) was analyzed. We present humans and animal models suggests these bacterial taxa are
the available data on the topic, discuss gaps in the scientific capable of modifying host metabolism and immunity (22–24).
literature and challenges in study design and implementation, In addition, Saccharomyces yeasts are reported to exhibit anti-
and make recommendations for future assessment of the gut inflammatory properties, which may contribute to immune-
microbiota through dietary interventions in humans. supporting characteristics of modest wine consumption
(25, 26).
Microbial fermentation can also modify the bioactive
properties of the food itself. Through the process of fer-
Fermented Foods Discussed in This mentation, many microbes participate in the conversion of
complex carbohydrates and phenolic compounds to bioactive
Review
metabolites (8, 27). Bioactive metabolites such as SCFAs
In this review, we assess the influence of spontaneous or are essential energy sources for host cells and are reported
multispecies starter-culture fermented food consumption on the to have significant impact on host immune, neuronal, and
composition and/or metabolic function of the human gut micro- metabolic functions (27–29). These particular metabolites also
biota. Fermented foods such as kimchi, sauerkraut, coffee, and modulate gut immune function and energy production by
pickled vegetables (pickles, olives, etc.) undergo a spontaneous colonic cells, affecting host–microbiota interactions (28, 30).
fermentation process and are subject to microbial colonization Thus, consumption of fermented foods may introduce both
that is influenced by the surrounding environment (13) (Table probiotic microbes and their beneficial by-products, alluding to
1). Yogurt, cheese, soy products, kefir, kombucha/fermented a mechanism by which these foods support aspects of human
teas, and wine are typically fermented with multispecies starter health.
Do fermented foods modify the gut microbiota? 1681
TABLE 1 Microbial compositions of fermented foods addressed in this review1

Mode of initial bacterial

Citations Type of fermented food Microbial components colonization
Unno et al. (31); Tillisch et al. (32); Fermented milk Lactobacillus brevis, Lactobacillus casei, Lactobacillus Starter culture
Veiga et al. (33); Yilmaz et al. (34) acidophilus, Bifidobacterium longum, and Streptococcus
thermophilus (31); Bifidobacterium animalis, S. thermophilus,
and Lactobacillus bulgaricus (32); B. animalis subsp. lactis, S.
thermophilus, Lactobacillus delbrueckii subsp. bulgaricus, and
Lactococcus lactis (33); Lactobacillus spp. (34)
Lisko et al. (19); Yang and Sheu (35) Yogurt L. acidophilus, Bifidobacterium lactis, L. bulgaricus, S. Starter culture
thermophilus, and L. casei (18 only)
Firmesse et al. (36); Lay et al. (37) Camembert cheese S. thermophilus, Lactobacillus spp., L. lactis, Leuconostoc, Hafnia Starter culture or spontaneous
alvei, and Geotrichum
Not specified in the study cited in Wine Predominantly Saccharomyces yeasts Starter culture
this review. General fermenters of
fermented soybean milk were
identified from Marzano
et al. (38).
Han et al. (15) Kimchi Lactobacillus spp. Spontaneous
Nielsen et al. (39) Sauerkraut Lactobacillus spp. (L. plantarum and L. brevis), Leuconostoc spp., Spontaneous
Weissella confusa, L. lactis, and Enterobacteriaceae
Not specified in the study cited in Coffee Primarily Klebsiella, Leuconostoc, LAB, Erwinia spp., Enterobacter Spontaneous
this review. General fermenters of spp. And a variety of yeasts (e.g., Kloeckera apis apicualata,
coffee were identified from Lee Candida guilliermondii, Saccharomyces cerevisiae)
et al. (40).
Yamamoto et al. (41) Fermented tea Aspergillus luchuensis var kawachii kitahara, Lactobacillus spp. (L. Starter culture
sakei, L. acidophilus, L. casei, L. plantarum), B. longum
Not specified in the study cited in Fermented soybean milk Lactobacillus paracasei, L. casei, Lactobacillus mali, and Starter culture
this review. General fermenters of Bifidobacterium breve
fermented soybean milk were
identified from Sirilun et al. (42).
Not specified in the study cited in Fermented plant extract Not specified Not specified
this review.
1
LAB, lactic acid bacteria.

Review of Human Intervention Studies Fermented milk.

According to a crossover intervention study of 6 healthy
Of the 19 studies identified in our literature search, 8 ana- women, consumption of fermented milk may be associated with
lyzed fermented milk, yogurt, or cheese; 4 analyzed red wine; changes in gut microbiota composition (31). Specifically, the
and 7 analyzed other varieties of fermented foods, including authors report increases in the Firmicutes:Bacteroidetes ratio
fermented tea, coffee, kimchi, fermented soybean milk, after consumption of fermented milk for 3 wk (31). Tillisch
sauerkraut, and fermented plant extract (Table 2). We did not et al. (32) reported in a double-blind parallel-group intervention
identify feeding studies that assessed the effect of pickled foods study comprised of 36 healthy adult women (12 received
(olives, pickles, etc.) on the gut microbiota. fermented milk, 11 received nonfermented milk, and 13 received
no intervention) that changes in midbrain connectivity were
associated with consumption of the fermented milk product for
Studies testing fermented dairy products 4 wk. However, in a post hoc analysis of the gut microbiota, the
Eight studies analyzed the gut microbiota after consumption authors report that these changes in neuronal activity were not
of fermented dairy products, including fermented milk, yogurt, mediated by shifts in the bacterial diversity of the gut (32). Thus,
and cheese. Fermented dairy products are typically fermented whether fermented milk products modify the gut microbiota of
by LAB (namely, Streptococcus thermophilus and Lactobacillus healthy participants remains inconclusive. The study by Unno
spp.) in addition to Bifidobacterium spp. (Table 1) (19, 31– et al. (31) was comprised of only 6 participants, limiting the
37). Camembert cheese is also fermented with Leuconostoc researchers’ ability to detect small to medium shifts in microbial
spp., Hafnia alvei, and Geotrichum fungi (Table 1) (36, 37). abundance. These studies also do not provide evidence of
These additional fermenters of the cheese could account for the gut microbiota mediating associations between fermented
the varied effects of its consumption on the gut microbiota. milk products and other physiological aspects in healthy
However, it is important to note that although the fermented participants.
milks and yogurts tested were fermented with similar bacteria, Two studies analyzed the gut microbiota after consumption
the specific LAB and amounts of LAB in each product are not of fermented milk among immune-compromised patients. Veiga
identical. These differences may account for the variability in et al. (33) analyzed the gut microbiota before and after fer-
results between the fermented milk and yogurt intervention mented milk consumption for 4 wk in 28 women with irritable
studies. bowel syndrome (IBS). After the intervention, the researchers

1682 Stiemsma et al.

 TABLE 2 Human dietary intervention studies assessing the effect of fermented food consumption on the composition and/or function of the gut microbiota1

Food product Frequency and Other health or

tested in the Duration of the dose of the Effect on the gut physiological
Citation Study design intervention Comparison made Participants intervention intervention microbiota observations
Veiga et al. (33) Parallel-group Fermented milk Microbiota of participants 28 women patients with IBS 4 wk 125 g, twice daily Decrease in Bilophila No other health outcomes
design who consumed fermented aged 20–69 y; 13 wadsworthia (a were assessed.
milk compared with the consumed fermented milk, pathobiont, P < 0.05), and
microbiota of participants 15 consumed placebo an increase in
who received placebo butyrate-producing
bacteria (P < 0.05). There
was also a significant
increase in SCFA
production (particularly
butyrate, P < 0.001) by
the gut microbiota.
Unno et al. (31) Crossover Fermented milk Microbiota after 6 healthy adult women aged 3 wk, followed by 140 mL, twice Decrease in members of the No other health outcomes
intervention consumption of fermented 20–24 y 3 wk of no daily Bacteroidetes phylum were assessed.
milk compared with the intervention (P < 0.05) and increase in
microbiota after weeks of (washout) members of the Firmicutes
no intervention (washout) phylum (P < 0.05).
Tillisch et al. (32) Parallel-group Fermented milk Microbiota of participants 36 healthy adult women aged 4 wk 125 g, twice daily There were no significant After an emotional
design who consumed fermented 18–55 y; 12 consumed changes in the gut attention task,
milk compared with the fermented milk, 11 microbiota composition consumption of
microbiota of participants consumed nonfermented after the intervention. fermented milk
who consumed milk, 13 received no resulted in reduced
nonfermented milk, or who intervention midbrain activity
received no intervention (P < 0.004).
Yilmaz et al. (34) Parallel-group Fermented milk Microbiota after 45 adult patients (18 y or 4 wk 200 mL, twice Lactobacillus counts Specifically, in patients
design consumption of fermented older) with inflammatory daily significantly increased in with Crohn disease
milk compared with the bowel disease; 25 treated the feces of the treatment (compared with those
microbiota of subjects with fermented milk, 20 group. with ulcerative colitis
who received no untreated in the treatment
intervention group), there was a
decrease in C-reactive
protein and an
increase in
hemoglobin. In
addition, in the last 2
wk, bloating scores
were reduced and
“feeling good” scores
increased (P < 0.05).
(Continued)

Do fermented foods modify the gut microbiota? 1683

1684
TABLE 2 (Continued)

Food product Frequency and Other health or

tested in the Duration of the dose of the Effect on the gut physiological
Citation Study design intervention Comparison made Participants intervention intervention microbiota observations

Stiemsma et al.
Lisko et al. (19) Parallel-group Yogurt Microbiota after consumption 6 healthy adults aged 6 wk 250 g, once daily Nonsignificant shifts in No other health outcomes
design of yogurt compared with 18–54 y Bifidobacteria spp. were were assessed.
the microbiota before observed.
consumption of yogurt
Yang and Sheu Parallel-group Yogurt Microbiota after consumption 38 Helicobacter 4 wk 200 mL, twice Intervention reduced the Intervention reduced H.
(35) design of yogurt compared with pylori–infected and 38 daily Escherichia pylori loads (P < 0.05)
the microbiota before healthy children aged coli:Bifidobacterium ratio and elevated serum
consumption of yogurt 4–12 y (P < 0.03) in H. IgA and pepsinogen II
pylori–infected children. concentrations
(P < 0.001).
Firmesse et al. Before and after Camembert Microbiota after consumption 12 healthy volunteers (no age 4 wk 40 g, twice daily Enterococcus faecalis No other health outcomes
(43) design cheese of cheese compared with specified) increased in abundance were assessed.
the microbiota before after the intervention
consumption of cheese period (P < 0.05).
Firmesse et al. Before and after Camembert Microbiota after consumption 12 healthy volunteers (no age 4 wk 40 g, twice daily High concentrations of Nitrate reductase activity
(36) design cheese of cheese compared with specified) Lactococcus lactis and decreased during the
the microbiota before Leuconostoc intervention.
consumption of cheese mesenteroides measured
in fecal samples during
the intervention. L.
mesenteroides persisted
15 d after the intervention
ended.
Clemente-Postigo Crossover Red wine Microbiota of participants 10 healthy adult males aged 20 d each, no 272 mL, once daily Red wine increased No significant differences
et al. (44) intervention who consumed red wine 45–50 y washouts (red wine and Prevotella abundance were observed for LPS
compared with the dealcoholized (P < 0.01), red wine or LBP concentrations
microbiota of participants red wine), 100 polyphenols (alcoholized between interventions.
who consumed mL gin once and dealcoholized) Reductions in
dealcoholized red wine, daily increased Bifidobacterium Prevotella and
and gin abundance (P < 0.01). Bifidobacterium
correlated with LPS
concentrations
(P < 0.05 and
P < 0.01,
respectively).
(Continued)
 TABLE 2 (Continued)

Food product Frequency and Other health or

tested in the Duration of the dose of the Effect on the gut physiological
Citation Study design intervention Comparison made Participants intervention intervention microbiota observations
Queipo-Ortuño et Crossover Red wine Microbiota of participants 10 healthy adult males aged 20 d each, no 272 mL, once daily Consumption of red wine Daily intake of red wine
al. (45) intervention who consumed red wine 45–50 y washouts (red wine and polyphenols increased polyphenols was
compared with the dealcoholized specific bacterial genera observed to decrease
microbiotas of participants red wine), 100 (e.g., Enterococcus, systolic and diastolic
who consumed mL gin once Prevotella, Bacteroides, blood pressures, and
dealcoholized red wine, daily and Bifidobacterium, triglyceride, total
and gin P < 0.05). cholesterol, HDL
cholesterol, C-reactive
protein, and
transaminase
concentrations
(P < 0.05).
Moreno-Indias et Crossover Red wine Microbiota of participants 10 healthy and 10 obese 4 wk, 15-d 272 mL, once daily Red wine and dealcoholized Red wine polyphenols
al. (46) intervention who consumed red wine adult males aged 45–50 y washout in (red wine and red wine (polyphenols) were associated with
compared with the between dealcoholized decreased the abundances reduction in BMI,
microbiotas of participants red wine) of Bifidobacteria, weight, and LDL:HDL
who consumed Lactobacillus, and cholesterol (P < 0.05),
dealcoholized red wine butyrate-producing among other markers
bacteria (P < 0.05) in of metabolic
obese adults. Further, red syndrome.
wine polyphenols reduced
LPS-producing bacteria in
obese patients (P < 0.05).
Barroso et al. (47) Parallel-group Red wine Microbiotas of participants in 20 healthy adults (age not 4 wk 250 mL, once daily Consumption of red wine No other health outcomes
design different polyphenol specified) grouped increased total diversity of were assessed.
metabolizing groups after according to their the gut microbiota
consumption of red wine polyphenol metabolizing (P < 0.01). This was driven
capacity by specific low-abundant
taxa; Slackia (P < 0.001),
Gordonibacter,
Oscillatoria, and
Veillonella (P < 0.05).
Inoguchi et al. (48) Crossover Fermented Microbiota of participants 10 healthy adults aged 2 wk 100 g, once daily Increase in Lactobacillus and Fecal sulfide decreased
intervention soybean milk who consumed fermented 21–25 y; 5 consumed decreased Clostridia after after fermented
soybean milk compared fermented soybean milk, 5 fermented soybean milk soybean milk
with the microbiota of consumed nonfermented consumption (P < 0.05). consumption
participants who soybean milk (P < 0.01).
consumed nonfermented
soybean milk
(Continued)

Do fermented foods modify the gut microbiota? 1685

 TABLE 2 (Continued)

1686
Food product Frequency and Other health or
tested in the Duration of the dose of the Effect on the gut physiological
Citation Study design intervention Comparison made Participants intervention intervention microbiota observations
Cheng et al. (49) Crossover Fermented Microbiota of participants 28 healthy adults aged 2 wk 250 mL, twice Decrease in coliform No other health outcomes
intervention soybean milk who consumed fermented 20–25 y; 14 consumed daily organisms and Clostridium were assessed.

Stiemsma et al.
soybean milk compared fermented soybean milk, perfringens (P < 0.05),
with the microbiota of 14 consumed increase in
participants who nonfermented soybean Bifidobacterium and
consumed nonfermented milk Lactobacillus spp.
soybean milk (P < 0.05).
Nielsen et al. (39) Parallel-group Lacto-fermented Microbiota of participants 34 patients with IBS aged 6 wk, followed by 75 g, once daily Both pasteurized and Both pasteurized and
design sauerkraut who consumed 16–65 y; 15 consumed a 2-wk unpasteurized sauerkraut unpasteurized
unpasteurized sauerkraut pasteurized sauerkraut, 19 follow-up led to significant gut sauerkraut resulted in
compared with the consumed unpasteurized microbiota compositional decreased IBS severity
microbiota of participants sauerkraut changes (P < 0.001). scores.
who consumed Sauerkraut-related LAB
pasteurized sauerkraut were significantly
increased in guts of
patients who consumed
unpasteurized sauerkraut.
Chiu et al. (50) Parallel-group Fermented plant Microbiota of participants 44 patients with 8 wk, followed by 30 mL, twice daily Individuals who consumed Consumption of
design extract who consumed fermented hypercholesterolemia a 2-wk the fermented plant fermented plant
plant extract compared aged 30–60 y; 22 received follow-up extract displayed extract increased total
with the microbiota of fermented plant extract, increased gut antioxidant capacity
participants who received 22 received placebo Bifidobacteria (P < 0.05) (P < 0.05) and
placebo and Lactobacillus spp. decreased the lipid
(P < 0.01) and decreased profile (P < 0.05).
E. coli and C. perfringens
(P < 0.05).
Han et al. (15) Parallel-group Kimchi Microbiota of participants 23 obese women aged 8 wk 60 g, thrice daily Significant increase in Negative correlation
design who consumed fresh 30–60 y; 12 consumed Bifidobacterium between
kimchi compared with the fresh kimchi, 11 consumed abundance after kimchi Bifidobacterium and
microbiota of participants fermented kimchi consumption for 8 wk. waist circumference
who consumed fermented Nonsignificant shifts in (P < 0.05). This group
kimchi other bacterial taxa. also observed
upregulation of genes
associated with
metabolism, immunity,
and digestion
(P < 0.05), which also
correlated with
bacterial taxa
(P < 0.05).
(Continued)
 No other health outcomes
observed a decrease in Bilophila wadsworthia (a pathobiont)

Increase in T regulatory
and an increase in butyrate-producing bacteria (33). They also

Other health or
physiological
observations

were assessed.
consumption of
observed an increase in SCFA production, specifically butyrate,

fermented tea
in the gut after consumption of fermented milk (33). Among

(P < 0.01).
cells after
45 adult patients with inflammatory bowel disease, researchers
reported increased Lactobacillus spp. counts in the feces of the
patients who consumed fermented milk for 4 wk (n = 25)
compared with untreated patients (n = 20) (34). This increase in
abundance of Lactobacillus spp. was accompanied by decreased

cluster XIVa and decrease

Increase in Bifidobacterium
in cluster IX (P < 0.05).
bloating scores and increased “feeling good” scores among the
Effect on the gut

Increase in Clostridium
patients (34). These 2 studies suggest the gut microbiota as a me-
microbiota

spp. (P < 0.05)

diator between fermented milk consumption and various health
outcomes among immune-compromised individuals. Compared
with studies in healthy participants, these works suggest that fer-
mented food consumption may be more effective at modulating
the gut microbiota among individuals with compromised gut
health.
2.14 g, once daily
Frequency and

intervention
dose of the

Yogurt.
We identified 2 studies that tested the effect of yogurt
3 cups/d

consumption on the gut microbiota. Consumption of yogurt

for 6 wk by 6 healthy participants was not linked to any
statistically significant shifts in bacterial abundance in the gut
(19). Conversely, a study by Yang and Sheu (35) reported that a
Duration of the
intervention

4-wk intervention with yogurt containing probiotic microbes

4 wk

3 wk

reduced the intestinal Escherichia coli:Bifidobacterium spp.

ratio in children infected with Helicobacter pylori compared
with controls (antibiotic consumption within 1 mo of study
start was an exclusion criterion). Notably, this intervention
also reduced H. pylori loads and elevated serum IgA con-
centrations in infected children, highlighting an avenue for
16 healthy adults aged

treatment of this infection with yogurt (35). Larger studies

9 healthy adults aged
Participants

and possibly studies of longer intervention duration testing

yogurt on the gut microbiota are necessary to shed more
25–47 y

21–57 y

light on the potential beneficial effects of consuming yogurt

products.

Camembert cheese.
Microbiota after consumption

Microbiota after consumption

of Cha-Koji compared with

We identified 2 studies that analyzed the gut microbiota

consumption of Cha-Koji

of coffee compared with

compositional effects of Camembert cheese consumption in

consumption of coffee
Comparison made

the microbiota before

the microbiota before

healthy volunteers (36, 43). Both studies reported increases in

specific microbial taxa in the guts of 12 participants consuming
Camembert cheese for 4 wk, some of which (Leuconostoc spp.)
IBS, irritable bowel syndrome; LAB, lactic acid bacteria; LBP, LPS-binding protein.

persisted in the gut 15 d after completing the intervention (36,

43). Of note, the bacteria Firmesse et al. (36, 43) identified
in the feces of these participants are colonizers of Camembert
cheese, suggesting that the gut microbiota was effectively
seeded by microbes found in this cheese. However, aside from
Fermented green
Food product

tea (Cha-Koji)
tested in the
intervention

the identification of cheese-colonizers in the guts of these

individuals, no additional microbiota compositional alterations
Coffee

were observed.
Collectively, there are too few studies in each of these
fermented dairy categories to suggest a particular pattern
of gut microbiota modulation after consumption of these
Study design
Before and after

Before and after

food products. Focusing specifically on fermented milk and

yogurt, there is some evidence to suggest that consumption of
design

design
TABLE 2 (Continued)

these dairy products alters the gut microbiota preferentially in

individuals with compromised gut health (33–35).

Studies testing red wine

Jaquet et al. (51)
Yamamoto et al.

Four studies analyzed the gut microbiota’s response to red wine

consumption (44–47). We did not identify any studies that
Citation

focused on other fermented alcoholic beverages, although gin

(41)

was used as a control in the studies by Queipo-Ortuño et al.

1

Do fermented foods modify the gut microbiota? 1687

(45) and Clemente-Postigo et al. (44). The specific fermenters of tea, sauerkraut, fermented plant extract, coffee, kimchi, and
the red wine tested in the following studies were not disclosed fermented soybean milk) on the gut microbiota (Table 2).
in these publications (45). However, the goal of these studies All 7 studies reported that consumption of the fermented
was to compare the effects of red wine polyphenols on the food tested modified the composition of the gut microbiota
gut microbiota, rather than the ethanol content. Red wine is (Table 2). Four studies analyzed the gut microbiota of
predominately fermented with Saccharomyces yeast (Table 1), healthy individuals, all of which reported increased abundances
which, in addition to the production of ethanol, has the ability of specific bacteria in the gut, which may exhibit health-
to modify the polyphenolic content of red wine (52). promoting properties (41, 48, 49, 51). Consumption of 250 mL
A 2017 study (47) analyzed the effect of red wine consump- soybean milk twice daily for 2 wk was associated with
tion on the gut microbiota composition in 20 healthy individu- increased abundance of Lactobacillus and Bifidobacteria spp.
als grouped according to their polyphenol metabolizing capacity and decreased coliform bacteria and Clostridium perfringens
(metabotypes). After 1 mo red wine consumption, researchers (49). Some of these findings were corroborated in a 2012
observed increased total gut microbial diversity driven primarily study (48); consumption of 100 g fermented soybean milk once
by shifts in abundances of specific bacterial genera (e.g., daily for 2 wk was associated with increased abundance of
Enterococcus, Prevotella, Bacteroides, and Bifidobacterium Lactobacillus spp. and decreased abundance of Clostridia spp.
spp.) (47). However, there was no association between red wine in 10 healthy adults. A 4-wk intervention study with Cha-Koji
consumption and the metabotype classifications, suggesting (fermented tea) increased the anti-inflammatory Clostridium
significant gut microbiota interindividual variability (47). cluster XIVa in the gut microbiota of 9 healthy adults (41). This
Moreno-Indias et al. (46) assessed the effect of red wine shift in gut bacterial abundance was accompanied by an increase
polyphenols on the gut microbiota of healthy and obese males. in systemic T-regulatory cells, suggesting the gut microbiota
The authors reported that consumption of both red wine as a mediator between Cha-Koji consumption and these
and dealcoholized red wine for 4 wk increased Bifidobacteria, anti-inflammatory effects (41). Finally, coffee consumption (3
Lactobacillus, and butyrate-producing bacteria (e.g., Faecal- cups/d) for 3 wk was linked to increased Bifidobacteria spp. in
ibacterium prausnitzii) and reduced LPS-producing bacteria the guts of 16 healthy adults (51). Notably, coffee beans are
(e.g., E. coli) in obese males only (46). Notably, there were no traditionally roasted before consumption. This study did not
significant gut microbiota compositional differences between compare roasted with unroasted coffee beans or caffeinated
the red wine and dealcoholized red wine interventions. This with decaffeinated coffee products, highlighting opportunities
suggests that polyphenol conversion by microbial fermentation, for future investigation.
rather than alcohol content, drove these gut microbiota changes Three studies analyzed the gut microbiotas of immune-
in the participants. compromised or metabolic syndrome patients (15, 39,
The same research group also conducted 2 crossover 50). Consumption of fermented plant extract for 8 wk by
intervention studies in 10 healthy male volunteers (44, 45). 22 hypercholesterolemic patients was reported to increase
Participants consumed 272 mL red wine, dealcoholized red beneficial microbes, Bifidobacteria and Lactobacillus spp., and
wine, or gin once daily for 20 d each (44, 45). Fecal samples were decrease potential pathogens, E. coli and C. perfringens (50).
collected for gut microbiota analysis after each intervention This shift in gut microbiota composition was accompanied by
period, but each study focused on different metabolic and an increased antioxidant capacity and decreased lipid profile of
immune outcomes (44, 45). Both studies reported similar these patients (50). In an 8-wk controlled clinical trial, kimchi
changes in the gut microbiota composition (i.e., increases in consumption was linked to an increase in Bifidobacteria spp.
Prevotella and Bifidobacteria spp.) after consumption of red abundance (15). Further, the abundance of Bifidobacterium
wine and dealcoholized red wine, in comparison with gin was inversely correlated with waist circumference (15). Lastly,
(44, 45). The 2012 study also reported reduction in systolic a 2018 intervention study by Nielsen et al. (39) compared the
and diastolic blood pressures, triglyceride concentrations, and effects of pasteurized and unpasteurized sauerkraut on the gut
total cholesterol and HDL cholesterol concentrations after microbiota composition. Fifteen IBS patients consumed 75 g
red wine polyphenol (red wine or dealcoholized red wine) pasteurized sauerkraut, whereas 19 IBS patients consumed
consumption (45). According to this group’s 2013 study, red unpasteurized sauerkraut for 6 wk (39). When the 2 groups
wine polyphenols had no effect on serum LPS or LPS-binding were compared, there was a higher abundance of sauerkraut
protein (LBP) concentrations (44). LAB in the fecal samples of patients in the unpasteurized group
These works provide preliminary evidence that red wine (39). However, both pasteurized and unpasteurized sauerkraut
consumption modifies the composition of the gut microbiota. were linked to decreased IBS severity scores (39). This suggests
Interestingly however, the effect of red wine consumption on that the beneficial effects of consuming sauerkraut may be
the gut microbiota may be driven primarily by the polyphenolic attributed more to the enhanced bioactive properties (e.g.,
content of red wine, rather than the ethanol content. Two microbial metabolic content of the food after fermentation) of
studies (45, 46) reported the polyphenol content of the red the fermented cabbage rather than the microbial content. An
wine and dealcoholized red wine tested, indicating that other avenue for future studies testing sauerkraut would be to include
than the ethanol content, these 2 beverages were very similar unfermented cabbage as a control, because this would allow
in their chemical compositions. Because similar effects on the researchers to determine whether fermentation of cabbage is
gut microbiota were observed with dealcoholized red wine, any truly linked to health benefits and/or changes in gut microbiota
positive effect of alcoholized red wine should be weighed against composition.
the carcinogenic effects of alcohol consumption. The studies discussed in this review provide evidence that
fermented food products induce compositional changes in the
gut microbiota. However, there are too few studies within each
Studies testing other fermented food products fermented food category to identify a pattern of microbiota
We identified 7 human intervention studies that assessed modulation that can be attributed to consumption of any
the effects of other fermented food products (fermented specific fermented food. Further, the bacterial and yeast species
1688 Stiemsma et al.
 A Group A

Washout
Intervention
B1 I1
Sample Sample
collection collection
Study Start
Study End
B0 Group B

Washout

Intervention
B1 I1
Sample Sample
Study Start collection collection
B0 Study End

B Product A Product B

Washout Washout

Intervention Intervention
B1 I1 B2 I2
Sample Sample Sample Sample
collection collection collection collection
Study Start
Study End
B0

FIGURE 1 Study design strategies for human dietary intervention studies. (A) Parallel-group study design. Participants are randomly assigned
to 1 intervention only. Samples are collected at B1 and I1. (B) Randomized crossover dietary intervention study design. Participants are randomly
assigned to an intervention sequence. For example, group A consumes product A first and product B second. Samples are collected at B1, I1,
B2, and I2. B0, beginning of study; B1, baseline 1; B2, baseline 2; I1, intervention 1; I2, intervention 2.

used to ferment these foods and the amount of each of these fermented food on the microbiota. While some feeding studies
fermenters within the food may also vary significantly between included only healthy participants, other interventions focussed
studies, increasing the variability of gut microbiota alterations on populations with particular disorders. It is likely that
observed after fermented food consumption (Table 1). Finally, fermented foods affect balanced microbiota differently than
many studies in which additional health outcomes were assessed microbial dysbiosis. Future studies need to account for the
suggest the microbiota as a mediator of the immune and baseline microbiota as an important predictor.
metabolic benefits linked with fermented food consumption.
However, sample size calculations for the analyses of microbiota Suggestions for human intervention study design
composition were not reported for these studies and the Two study designs are most commonly used in dietary
majority are insufficiently powered to conduct mediation interventions: the parallel-group design and the crossover study
analyses to confirm this. design.
In the parallel-group design, participants are randomly
assigned to ≥2 interventions (Figure 1A). Evaluations may
be made by comparing 1 (or more) interventions with a no-
Challenges and Areas for Future Research
intervention arm. This design is often employed when studying
There are very few published intervention studies for the the effect of an intervention on 1 group of participants (e.g.,
majority of the foods discussed in this review (some foods are healthy) and comparing the effects of the intervention to those
represented by only 1 human intervention study). Consequently, of participants in another group (e.g., diseased). However, the
the study designs used to conduct these dietary interventions parallel-group design presents many challenges with regard to
are rather heterogeneous. Other than the duration of the individual variability, particularly in studies aimed at analyzing
intervention, which averaged ∼4 wk for most studies, the the human microbiota. Alternatively, in the crossover design,
amount of fermented food consumed, the number of partici- individual variability is reduced because comparisons are made
pants included, and the comparisons made vary significantly within each participant. In this design, individuals are randomly
across studies (Table 2). The duration of intervention was assigned into intervention sequences (Figure 1B) and samples
generally not well justified. Therefore, a lack of change in are collected before and after each intervention in the sequence.
the microbiota composition may be simply due to insufficient Both designs are represented in studies discussed in this review;
intervention duration. A better understanding of the minimum additional benefits and pitfalls of each are discussed below.
number of weeks required for a specific fermented food to Currently no benchmark for the “normal” human micro-
be consumed to instigate changes in the microbiota will be biota exists against which to measure “change” of the micro-
essential to inform future research. Moreover, the choice of biota composition. There is significant baseline (noninforma-
the study population will likely impact the influence of the tive) variability in microbiota composition between individuals
Do fermented foods modify the gut microbiota? 1689
(53). The main bacterial colonizers of the gut microbiota can be researchers are currently excluding the potential influence of
grouped into 2 phyla: Bacteroidetes and Firmicutes (53). Even a large microbial population in the gut. There is growing
at this high taxonomic rank, the Bacteroidetes:Firmicutes ratio evidence that the mycobiota plays an equally significant role in
has been reported to differ by an order of magnitude between human health (56). Further, because many fermented foods are
healthy individuals (53). The genera and species that comprise colonized by both yeasts and bacteria, analysis of the fungal
these phyla are highly variable and the presence of specific populations would provide a more holistic view of the gut
species depends strongly on the individual’s genetic background microbial populations affected by fermented food consumption.
and environmental exposome (e.g., diet, medications) (53). In addition, changes in bacterial composition after a dietary
Further, there is differential responsiveness among people, with intervention do not necessarily translate to functional changes
one individual’s microbiota being responsive and another’s in the gut microbiota. Given that sample size is a limitation in
being resilient to dietary modifications (54). For example, human intervention studies, many studies lack statistical power
1 study used a parallel-group design to analyze the effect to conduct mediation analyses that might address whether
of inulin consumption on the gut microbiota compared with the microbiota mediates the association between fermented
placebo (maltodextrin) (55). The authors reported that the food consumption and other health outcomes. However, it
increase in Bifidobacteria after the intervention was largely may be possible to address this mechanistic gap by conducting
driven by the baseline Bifidobacteria abundances (55). Thus, functional analyses on the gut microbiota in addition to the
a key flaw in the parallel-group design is the inability to compositional assessment. Microbial metabolomics or meta-
distinguish between microbiota compositional changes induced transcriptomics (analysis of the microbiota’s gene expression)
by the food product and those induced by interindividual could be applied to intervention studies in the future as a means
differences at baseline. to elucidate the mechanisms by which diet-induced variation in
In addition, when using the parallel-group design, the microbiota composition can lead to changes in health outcomes.
study size needs to be generally double that of a crossover
design. In the crossover design, all participants complete
both interventions, effectively doubling the total number of
participants in each group. Although it may be necessary to Conclusions
use the parallel-group design when testing a product among In this review, we identified 19 human intervention studies that
2 different groups of participants (e.g., healthy compared with analyzed the effect of naturally fermented food consumption
diseased), this design should be avoided when analyzing the on the gut microbiota. Currently, the data are too sparse
effects of multiple interventions (e.g., fermented food compared to suggest that 1 particular fermented food modifies the
with nonfermented food). gut microbiota in a specific pattern. However, because the
The crossover design is often preferable for dietary inter- majority of these foods are colonized by LAB, Saccharomyces
ventions for the aforementioned reasons. However, this design yeasts, and Bifidobacteria spp., we conclude that consumption
has its own set of limitations. If the interventions tested are of foods comprised of these particular fermenters may be
of significant duration (e.g., several months), it can be difficult potential dietary targets to prevent or overcome gut dysbiosis in
to enroll and maintain participants in the study because the humans. Further, a number of studies identified compositional
sequence of intervention doubles or triples the length of the changes to the gut microbiota along with changes to immune
study. Secondly, gut microbiota composition can shift over time, or metabolic factors in the human host. This suggests the
regardless of whether an individual has introduced a major microbiota as a mediator between fermented food consumption
change to their lifestyle (53). Moreover, if the dynamics of and these health outcomes. However, future studies should
the exposure–microbiota association are not well understood, consider functional analyses (microbial metabolomics, meta-
carryover effects may dilute comparisons between intervention transcriptomics) to better characterize the mechanisms linking
sequences. However, these challenges may be mitigated by fermented food consumption to changes in human health.
collecting new baseline samples after a washout period and Researchers should also carefully consider the design of
before beginning the next intervention in the sequence. their intervention study. Crossover designs would enhance
Each study type presents its own challenges and advantages. the statistical power owing to paired comparisons. Further,
However, if the research question is aimed at analyzing the effect the mycobiota is extremely understudied in this research
of fermented foods compared with nonfermented foods on the area, highlighting a novel opportunity for future intervention
gut microbiota, rather than comparing the effect of fermented studies.
food consumption between 2 groups of people, the crossover
design is superior. This design reduces the impacts of genetic Acknowledgments
and environmental variability and allows for maintaining the The authors’ responsibilities were as follows—LTS and KBM:
same statistical power as a parallel-group study with a smaller conceptualized the study and have primary responsibility for
sample size. Ultimately, selecting an unbiased study design is the final content; LTS, REN, and JGN: conducted the literature
of the utmost importance because it can significantly affect the review; LTS: wrote the manuscript; REN and JGN: contributed
interpretation of the results collected. to the construction of Table 2 and reviewed and edited the
manuscript; KBM: critically reviewed and provided significant
Functional analyses and the gut mycobiome revisions to the manuscript; and all authors: read and approved
Two areas which future intervention studies might consider the final manuscript.
expanding on include 1) analysis of the gut mycobiota (the
fungal complement to the bacterial microbiota) and 2) analysis
of microbiota function via metabolomics and metagenomics.
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