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https://doi.org/10.1038/s41430-020-0607-6
REVIEW ARTICLE
Abstract
Recently, relationship between gut microbiota composition and development of obesity has been pointed. However, the
gut microbiota composition of individual with obesity is not known yet. Therefore, this systematic review aimed to
evaluate differences in profile of gut microbiota between individuals with obesity and individuals with normal weight. A
search performed on August 2019 in the databases Pubmed, Scopus, Web of Science, Cochrane library, Lilacs and gray
literature using the terms: “microbiota”, “microbiome”, “obesity”, “obesity morbid”, and “humans”. Studies assessing
the gut microbiota composition in adults with obesity and lean were included. Quality assessment was performed by
Newcastle–Ottawa Quality Assessment Scale. Of the 12,496 studies, 32 were eligible and included in this review.
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Individuals with obesity have a greater Firmicutes/Bacteroidetes ratio, Firmicutes, Fusobacteria, Proteobacteria,
Mollicutes, Lactobacillus (reuteri), and less Verrucomicrobia (Akkermansia muciniphila), Faecalibacterium
(prausnitzii), Bacteroidetes, Methanobrevibacter smithii, Lactobacillus plantarum and paracasei. In addition, some
bacteria had positive correlation and others negative correlation with obesity. Individuals with obesity showed profile of
gut microbiota different than individual lean. These results may help in advances of the diagnosis and treatment of
obesity.
The eligibility criteria were based on the PICOS strat- Data extraction
egy: Population (P), Intervention (I), Comparison (C),
Outcome (O), Study design (S). The literature search was The data extracted from the studies included in this sys-
carried out on August 2019 using five scientific databases: tematic review was summarized in Table 1, giving the
Medline via Pubmed, Scopus, Web of Science, Food Sci- following information: author and year of publication,
ence and Technology Abstracts (FSTA), Cochrane library, country and period of study/seasons (when informed),
Lilacs, and gray literature (Tripdatabase, Open Gray, sample size and characterization of the study population,
Google Scholar, Digital Library of Theses and Disserta- method used to evaluate the gut microbiota and bacteria
tions and the Universidade de São Paulo). We followed the analyzed (if applicable), and outcomes.
PRISMA statement to carry out the present systematic
review [15].
The search strategy combined MESH (Medline), DeCs Results
(VHL) terms, and free terms using the boolean operators
“AND” and “OR”. “Microbiota”, “microbiome”, “obesity”, Literature search
and “morbid obesity” were the terms used in the search. The
search protocols for each scientific database can be found in Of the 12,496 studies found in the search (scientific literature
the supplementary material. A complementary search was (n = 9881—Pubmed (n = 2800), Scopus (n = 3393), Web of
carried out in the references of studies included. science (n = 2426), FSTA (n = 887), Cochrane library (n =
The studies identified were imported to the EndNote 300), Lilacs (n = 75)), and gray literature (n = 2615)), the full
Web Software (Thomson Reuters, New York, USA), and texts of only 53 articles were read, after the removal of
duplicate articles were identified and excluded. duplicates and screening of the title and abstract (Fig. 1). One
The present systematic review was registered in the thesis was not available for full-text reading. Thirty-two
International Prospective Register of Systematic Reviews articles are included and are described in Table 1.
(PROSPERO) under the number: CRD42018107414
(https://www.crd.york.ac.uk/PROSPERO/). Quality and risk of bias
Eligibility criteria The quality scores of the studies can be found in Table 1.
Three articles [17–19] received the maximum score and
Observational human studies and clinical trials that eval- seven [17, 20, 21] showed good quality with eight points.
uated the gut microbiota composition in adults with obe- Two articles did not explain the recruitment process
sity and in those of normal weight by any validated [22, 23]. So they were excluded from the systematic review,
technique, written in English, Spanish or Portuguese, due to a high risk of bias.
were included.
Studies with animal models, children, teenagers and Studies characteristics
pregnant; clinical trials with no gut microbiota composition
baseline data; evaluation of oral, stomach, skin or oro- Of the 32 studies included, three found no difference
pharyngeal microbiota; studies not compared with lean between the gut microbiota of individuals with obesity and
individuals; and studies with a high risk of bias (poor normal weight [17–19]. Differences found between the gut
quality), were excluded. microbiota compositions are shown in the next sections.
Quality assessment and risk of bias Diversity, richness, and total number of bacteria
The studies included were submitted to a quality assess- Verdam et al. [24], Dorminianni et al. [20], and De la
ment by the Newcastle–Ottawa Quality Assessment Scale Cuesta-Zuluaga et al. [25] identified less diversity in indi-
[16]. This instrument includes three domains: selection, viduals with obesity, while Kocelak et al. [12] and Kasai
comparability, and outcomes. The selection domain is et al. [26] found greater diversity and a larger total number
composed of by four items, comparability of one item, of bacteria. The microbiota was richer in individuals with
and outcomes of three items. The article could receive obesity [26, 27].
one star in each item, receiving a maximum four stars
in selection, one or two in comparability, and three in Firmicutes/bacteroidetes ratio
outcomes [16]. A high risk of bias occurred when some
domain did not receive star, and in this case, the article One study showed a lower Firmicutes/Bacteroidetes ratio in
was excluded. individuals with obesity [11], but other studies found the
Profile of the gut microbiota of adults with obesity: a systematic review
Table 1 Characteristics, summary, and quality score of studies included in systematic review.
Author Country Characteristics of population n Method of gut microbiota evaluation Outcomes NOS score
Period (n men) BMI (kg/m²) age (years) (bacteria analyzed)
of study
Schwiertz Germany 98 individuals (♂ n = 34) qPCR (Clostridium leptum, Clostridium Ruminococcus flavefaciens spp, 8
et al. [11] Age: 47 ± 13 coccoides, E. cylindroide, Lactobacilli/ Firmicutes, and Firmicutes/
Lean (n = 30 BMI 18.5–24.9) Enterococci, Ruminococcus flavefaciens Bacteroidetes ratio were lower and
Overweight (n = 35, BMI 25–30) spp., Veilonella, Bacteroides, Bacteroidetes higher in individuals with
Obese (n = 33, BMI > 30) Prevotella, Bifidobacterium, overweight and obesity, and
Methanobrevibacter) Bifidobacterium, Methanobrevibacter
and Clostridium leptum were lower in
individuals with obesity, compared
with lean.
Positive correlation between BMI and
Bifidobacterium, Methanobrevibacter.
Zuo et al. China 104 individuals Quantification of bacteria isolated from Bacteroides and Clostridium 8
[33] Lean (n = 52, ♂ n = 26, BMI feces and incubated (Escherichia coli, perfringens were lower in individuals
20.26 ± 1.50, age 33.02 ± 10.37) Enterococci, Lactobacilli, with obesity. Enterococci tended to be
Obese (n = 52, ♂ n = 34, BMI Bifidobacteria, Clostridium perfringens, higher in individuals affected by obesity
30.79 ± 2.80, age 34.65 ± 11.91) Bacteroides) (no significance).
Million et al. France 115 individuals qPCR (Methanobrevibacter smithii, Individuals with obesity showed lower 7
[41] Lean (n = 47, ♂ n = 24, BMI 22.1 ± Bacteroidetes, Firmicutes, Methanobrevibacter smithii,
1.8, age 42.6 ± 17.5) Lactobacillus, Lactococcus latis, and Lactobacillus paracasei, Lactobacillus
Obese (n = 68, ♂ n = 31, BMI Bifidobacterium) plantarum and Bifidoacterium animalis,
43.6 ± 7.8, age 50.5 ± 14.4) and higher Lactobacillus and
Lactobacillus reuteri, compared
with lean.
Lactobacillus reuteri increased,
Bifidobacterium animalis and
Methanobrevibacter smithii decreased
were associated with obesity.
Munukka Finland 85 women Flow cytometry, 16S rRNA Women with obesity and metabolic 7
et al. [40] Lean (n = 11, BMI 21.6 ± 2.0, age hybridization, and DNA staining disorder showed higher Eubacterium
31 ± 14) (Atopobium cluster, Bacteroides group, rectale-Clostridium coccoides,
Obese without metabolic disorder Bifidobacterium spp., enteric bacteria, Firmicutes/Bacteroidetes ratio and
(n = 47, BMI 29.1 ± 2.9, age 39 ± 9) Eubacterium rectale- Clostridium Eubacterium rectale/Bacteroidetes
Obese with metabolic disorder coccoides group, and Faecalibacterium compared with other groups and higher
(n = 27, BMI 30.9 ± 2.9, age 42 ± 8) prausnitzii) gram-negative bacteria compared with
lean only. Eubacterium rectale/
Bacteroidetes ratio was higher in
women affected by obesity without
metabolic disorder compared with lean.
Positive correlation between BMI and
Eubacterium rectale-Clostridium
coccoides and Eubacterium rectale/
Bacteroidetes ratio, and negative
correlation between BMI and
Bacteroides.
Patil et al. India 20 individuals Sequencing and qPCR (Archaea and Archaea and Bacteroides were higher in 5
[35] Underweight (n = 5, BMI 16.46 ± Bacteroides) individuals with obesity, decreasing
1.34, median age 23) after bariatric surgery and becoming like
Lean (n = 5, BMI 23.56 ± 0.82, the lean individual.
median age 44)
Obese (n = 5, BMI 44.62 ± 7.49,
median age 45)
Obese post bariatric surgery (n = 5,
BMI 31.63 ± 3.68, median age 50)
Bezerra et al. Brazil October ♀ n = 32 Quantification of bacteria isolated of No difference in gut microbiota 6
[18] to April Lean (n = 13, BMI 21.9 ± 2.1, age feces and incubated (Bifidobacterium composition between different
26 (24–27)) spp. and Lactobacillus spp.) nutritional status.
Obese (n = 19, BMI 45.8 ± 4.7, age
34 (31–47))
Kocelak Poland 80 individuals Quantification of bacteria isolated of Individuals with obesity showed higher 5
et al. [12] Lean (n = 30, BMI 23.2 (22.5–23.9), feces and incubated (Bacteroides bacteria total. Gram-positive and gram-
age 42.6 (38.1–47.1)) ovatus, Clostridium septicum, variables cocci only cultured on fecal
obese (n = 50, BMI 35.7 Clostridium perfringens, staphylococcus sample of obese.
(34.3–37.1), age 51.9 (48.1–55.7)) aureus, echerichia coli)
Million et al. France 263 individuals qPCR (Firmicutes, Bacteroidetes, Lactobacillus reuteri was higher in 5
[14] Anorexia (n = 15, ♂ n = 1, BMI Escherichia coli, Metanobevibacter individuals with overweight and obesity
13.5 (11.7–14.6), age 27.3 ± 10.8) smithii, Latobacillus reuteri, and Lactobacillus reuteri was associated
Lean (n = 76, ♂ n = 40, BMI 22.4 Lactobacillus plantarum, Lactobacillus with overweight and obesity.
(20.7–23.7), age 49.5 ± 18.6) hamnosus, Lactobacillus fermentum and Bacteroidetes and Escherichia coli were
Overweight (n = 38, ♂ n = 32, BMI Lactobacillus acidophilus, lower in individual with obesity
27.1 (25.9–28.6), age 54.1 ± 17.8) Bifidobacterium animalis) compared with overweight and lean, and
Obese (n = 134), ♂ n = 65, BMI Metanobrevibacter smithii and
40.0 (36.4–46.8), age 51.8 ± 14.7 Bifidobacterium animalis were lower
L. Crovesy et al.
Table 1 (continued)
Author Country Characteristics of population n Method of gut microbiota evaluation Outcomes NOS score
Period (n men) BMI (kg/m²) age (years) (bacteria analyzed)
of study
Table 1 (continued)
Author Country Characteristics of population n Method of gut microbiota evaluation Outcomes NOS score
Period (n men) BMI (kg/m²) age (years) (bacteria analyzed)
of study
Table 1 (continued)
Author Country Characteristics of population n Method of gut microbiota evaluation Outcomes NOS score
Period (n men) BMI (kg/m²) age (years) (bacteria analyzed)
of study
Table 1 (continued)
Author Country Characteristics of population n Method of gut microbiota evaluation Outcomes NOS score
Period (n men) BMI (kg/m²) age (years) (bacteria analyzed)
of study
♀ women, ♂ men, BMI body mass index, DNA desoxyribonucleic acid, FISH fluorescence in situ hybridization, NOS Newcastle–Ottawa Scale,
rRNA ribosomal ribonucleic acid, qPCR quantitative polymerase chain reaction quantitative, T2D type 2 diabetes, USA United State of America.
inverse result, with higher Firmicutes/Bacteroidetes ratio in and another study found higher Mollicutes class [29], while
individual with obesity [10, 24, 26, 28–30]. a third showed lower Methanobacteria [31] in individuals
with obesity.
Microbiota profile and obesity Rikenellaceae, Ruminococcaceae, and Veillonellaceae
families were less present in individuals with obesity [34]. At
Individuals with obesity showed higher Firmicutes counts the genus level, individuals with obesity had higher count of
[10, 13, 28, 30–32] and lower Bacteroidetes counts Alistipes, Anaerococcus, Coprococcus, Parvimonas [32],
[10, 14, 26, 32–34]. However, some studies found lower Fusobacterium [32, 38], Enterococcus [38], Prevotella,
Firmicutes [11, 34] and higher Bacteroidetes Megasphaera, Meganomas, Acidaminococcus [27], Bifido-
[11, 13, 31, 35, 36] in individual with obesity. Fusobacteria bacterium [30, 39], Lactobacillus [13, 14, 21, 27], Cateni-
[32, 36] and Proteobacteria [13, 27, 36] phyla increased, bacterium [34], Dorea, Bacteroides, Escherichia-Shiguela
while the Ignavibacteriae [37] and Verrucobacteria [13], Lactobacillus/Leuconostoc/Predicoccus [30], and the
(Akkermansia municiphila) [13] decreased. In addition, one Eubacteriumrectale/Bacteroidetes ratio [40], and lower
study showed higher counts for the Archaea kingdom [32], counts of Desulfovibrio, Finegoldia, Lachnoanaerobaculum,
L. Crovesy et al.
Identification
Records identified through 2615 records identified
correlations were found between the BMI and Bifido-
database searching through grey literature bacterium, Methanobrevibacter [11], Eubacterium rectale-
(n=9881)
Clostridium coccuides, Eubacterium rectale/Bacteroidetes
Records duplicates excluded
ratio [40], Roseburia intestinalis, Enterobacter aerogenes,
(n=4160) Klebsiella pneumniea, Vibrio, Yersina spp. [24], Mollicutes
[29], Firmicutes, Clostridium leptum, Lactobacillus/Leu-
Screening
absorption of calories, a reduction in the secretion of the The presence of divergent results between different stu-
anorexigenic hormones (GLP-1, PYY, and leptin) and dies can be caused by many factors, such as the techniques
satiety, increases fat storage in the adipose tissue, and used to analyze the gut microbiota, different primer designs
damage to the gut barrier contributing with translocation of and different DNA extraction techniques [11, 54], the
lipopolysaccharide and inflammation. These changes con- population studied, diet, gender, latitude of the study site,
tribute to the development of obesity [46, 48]. Although the and the season. The gut microbiota is easily affected, and it
mechanism causing an imbalance in the gut microbiota is is difficult to control all the elements that affect the gut
known, the bacteria involved in this process have not been microbiota composition [55]. Most studies did not evaluate
determined yet [48]. the components that influence the gut microbiota, and
The relationship between Firmicutes/Bacteroidetes ratio therefore it is difficult to understand the possible differences
and obesity appears to have also been confirmed in humans. found between the results of the different studies.
Only one study showed lower Firmicutes/Bacteroidetes Amongst these factors, the diet appears to have a greater
ratio in individuals with obesity; however, these authors influence on the gut microbiota composition. Thus, the
considered Bacteroides and Prevotella as Bacteroidetes focus of the present article was a comparison between the
phylum [11], which may have resulted in this phylum being gut microbiota of individuals with obesity and normal
overestimated. Firmicutes and Bacteroidetes are dominant weight individuals, who have different dietary patterns. In
in the gut microbiota, corresponding to 90% of bacteria [4]. addition, the studies were carried out in different countries
The Bacteroidetes have been associated with adequate body with distinct food habits that affect the gut microbiota
weight but the Firmicutes with obesity. The Bacteroidetes composition [55]. Most of the studies were carried out with
have a positive correlation with a reduction of body fat [2], single population except those of Yasir et al. [13] and
whereas the relationship between Firmicutes and obesity Escobar et al. [34]. From the information reported in these
can be associated with a greater energy harvest. The Fir- articles, it was possible to show different dietary patterns
micutes have more carbohydrate metabolism enzymes, exerted different influences on the gut microbiota compo-
which contribute to the metabolization of this macronutrient sition, not only on body weight, making the study of the
allowed for a greater energy absortion [49]. microbiota with respect to obesity more complex.
Lactobacillus genus belongs to Firmicutes phylum, an Other important point to discuss is the metabolites pro-
increase in this genus has been associated with obesity [49]. duces by the bacteria of the microbiota. Of the metabolites
Amongst the bacteria of this genus, Lactobacillus reuteri highlighted, the short-chain fatty acids can exert different
[14, 40] has been correlated with a higher BMI. However, effects on the host and can help or hinder the host meta-
despite the association between Lactobacillus and obesity, it bolism. Short-chain fatty acids influence the metabolism of
appears that some of the bacteria (Lactobacillus paracasei energy, lipids, glucose, and cholesterol, in addition con-
and Lactobacillus plantarum) of this phylum have a pro- tribute to fat storage in the adipose tissue and the immune
tective effect against weight gain. Lactobacillus paracasei system function [56]. Patil et al. [35] observed that the gut
and Lactobacillus plantarum produce bacteriocins with microbiota of individuals with obesity produced twice as
antibacterial action, preventing the growth of bacterial much short-chain fatty acids as compared with that of lean
pathogens that cause dysbiosis [50]. individuals, propionate being present in the greatest pro-
The Proteobacteria is associated with dysbiosis, leading portion [11]. Few studies have explored the role of meta-
to metabolic diseases such as obesity. When the Proteo- bolites in the host metabolism.
bacteria increases there is a reduction in mucus production Furthermore, the impact of the gut microbiota composi-
causing damage to the gut barrier and a low-grade inflam- tion on body weight must be considered. Although some
mation [51]. Fusobacteria and Fusobacterium are oppor- studies have associated alterations in the gut microbiota
tunist pathogenic bacteria, increasing in individuals with with metabolic changes, leading to weight gain and con-
obesity. This result was also found by Goa et al. [23]. sequently to the development of obesity [2, 8, 9], there are
Faecalibacterium prausnitzii is a butyrate producing still doubts as to whether obesity leads to changes in the gut
bacterium with anti-inflammatory and protective effects microbiota composition or whether changes in the gut
against obesity [52]. Akkermansia muciniphila (Verruco- microbiota lead to obesity [57]. Studies evaluating the
microbia) is involved in the metabolism of mucin, impact of weight loss in individual with obesity have shown
degrading and stimulating the mucin in host gut. Besides changes in the gut microbiota [58, 59]. Pajecki et al. [59]
the control of mucus, this bacterium also interacts with the showed alteration in the gut microbiota composition in
host metabolism, maintaining the integrity of the intestinal individual with severe obesity after bariatric surgery, and
barrier, and modulating other bacteria of the gut microbiota, the bacteria showed different contributions to the weight
favoring eubiosis [53]. loss process. In addition, the diet appears to have greater
L. Crovesy et al.
impact on changes in the gut microbiota than surgery alone Publisher’s note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
[60].
From the gut microbiota composition can predict the
results of the intervention on weight loss. In addition, References
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