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European Journal of Clinical Nutrition

https://doi.org/10.1038/s41430-020-0607-6

REVIEW ARTICLE

Profile of the gut microbiota of adults with obesity: a systematic review


Louise Crovesy1 Daniele Masterson2 Eliane Lopes Rosado1
● ●

Received: 27 May 2019 / Revised: 4 March 2020 / Accepted: 6 March 2020


© The Author(s), under exclusive licence to Springer Nature Limited 2020

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.

Introduction most frequent in the microbiota, corresponding to 90% of


the gut bacteria [4, 5].
Obesity is a growing public health problem throughout the On 2004, Bäckhed et al. [6] published the first article
world, affecting 650 million adults worldwide. Obesity is about the role of gut microbiota in the host metabolism,
difficult to control due to multiple etiological factors [1] including body weight control. Animal model and humans’
and amongst the causes the gut microbiota has been studies have been carried out to discover the composition of
highlighted [2]. the gut microbiota associated with obesity [2, 7–10].
The gut microbiota is composed mainly of bacteria fol- Experimental studies with animals have shown success
lowed by smaller proportions of fungi, virus and Archea [3]. in determining the association between the Firmicutes/
The main phyla of bacteria in the gut microbiota are Fir- Bacteroidetes ratio and obesity [2, 7, 8]. However, in
micutes, Bacteroidetes, Proteobacteria, Actinobacteria, and humans this affirmation has not been confirmed [9–12]. In
Verrucomicrobia. Firmicutes and Bacteroidetes are the addition, other phyla and bacteria genera have been asso-
ciated with obesity [11–14]. Therefore, we carried out a
systematic review aimed to evaluate the differences between
the profile of the gut microbiota of individuals with obesity
and individuals with lean.
Supplementary information The online version of this article (https://
doi.org/10.1038/s41430-020-0607-6) contains supplementary
material, which is available to authorized users.
Methods
* Louise Crovesy
louisecrovesy@yahoo.com.br
Search strategy and registration
1
Instituto de Nutrição Josué de Castro, Universidade Federal do Rio
de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil A systematic review was carried out to answer the question:
2
Library of Health Sciences Center, Universidade Federal do Rio de “Is the gut microbiota profile of individuals with obesity
Janeiro, Rio de Janeiro, Brazil different of lean individuals?”.
L. Crovesy et al.

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

compared with lean.


Negative correlation between BMI and
Bifidobacterium animalis, Escherichia
coli.
Simões et al. Finland Years: 20 twin pairs (♂ pairs n = 9) qPCR (Bacteroides spp. (Bacteoroides No difference in gut microbiota 9
[17] 1975–1979 Lean (BMI 22.9 ± 2.2, age 26 ± 3) thetataiotaomicron), E. rectale composition between different
Overweight (BMI 26.5 ± 1.2, age (Roseburia intestinalis), C. leptum nutritional status.
29 ± 3) (Anaerotruncus colibominis),
Obese (BMI 32.74 ± 2.1, age 28 ± 4) Atopobium (A. parulim),
Bifidobacterium, (B. longum)
Lactobacillus (Lactobacillus casei))
Teixeira Brazil ♀ n = 32 qPCR (Bifidobacterium longum, Women with obesity showed lower 6
et al. [39] Lean (n = 17, BMI 21.2 (20.6–21.9), Bifidobacterium catenulatum, Bifidobacterium, Bifidobacterium
age 28.05 ± 6.9) Bifidobacterium bifidum, longum, Clostridium coccoides and
Obese (n = 15, BMI 34,5 Bifidobacterium adolescentis, Clostridium leptum. Lactobacillus
(32.8–36.7), age 30.7 ± 5.7) Bifidobacterium breve, Akkermansia plantarum and Akkermansia (p = 0.006)
muciniphila, Clostridium coccoides, tended to be lower.
Clostridium leptum, Lactobacillus Negative correlation between BMI and
acidophilus, Lactobacillus paracase, Akkermansia muciphinila,
Lactobacillus plantarum, Lactobacillus Bifidobacterium, Bifidobacterium
rhamnosus, Lactobacillus casei) longum, Clostridium coccoides,
Clostridium leptum, Lactobacillus
plantarum.
Verdam et a. Netherland 28 individuals Sequencing Individuals with obesity showed lower 7
[24] May to Lean (n = 9, ♂ n = 3, BMI 22.2 ± diversity and Bacteroidetes/Firmicutes
September 0.7, age 23.3 ± 3.3) ratio, and higher amount of Clostridium
Obese (n = 19, ♂ n = 5, BMI 40.4 ± cluster IV and XIVa.
2.5, age 36.2 ± 2.4) Negative correlation between BMI and
Bacteroidetes/Firmicutes ratio,
Allistipes, and positive correlation
between BMI and Roseburia
intestinalis, Enterobacter aerogenes,
Klebsiella pneumniea, Vibrio,
Yersina spp.
Zak-Golab Poland 80 individuals Quantification of bacteria isolated of No difference in gut microbiota 5
et al. [19] Lean (n = 30, ♂ n = 6, BMI 23.7 feces and incubated (Bacteroides ovatus composition between different
(21.8–24.8), age 42.5 (32.0–52.0)) ATCC BAA-1296, Clostridium nutritional status.
Obese (n = 50, ♂ n = 11, BMI 35.4 septicum ATCC 12464, Clostridium
(30.6–38.7), age 53.5 (42.0–63.0)) perfringens ATCC 13124,
Staphylococcus aureus ATCC 25923,
and Escherichia coli ATCC 25922)
Escobar et al. – 126 individuals Sequencing Americans with obesity showed lower 7
[34] Colombian (n = 30, ♂ n = 16 - Lean Firmicutes, Bacteroides, Coprococcus,
(BMI 22.6 ± 1.7, age 33 ± 11), Oscillospira, Parabacteroides,
Overweight (BMI 27.1 ± 1.3, age Clostridiales, Rikenellaceae,
39 ± 9), Obese (BMI 32.6 ± 2.3, age Ruminococcaceae, and higher
43 ± 12)) Catenibacterium, while Colombians
European (n = 13, ♂ n = 10 - Lean affected with obesity showed lower
(BMI 22.5 ± 1.2, age 56 ± 9), Ruminococcaceae, Clostridiales,
Overweight (BMI 28.4 ± 0.8, age Dialister, Oscillospira, Akkermansia.
56 ± 9), Obese (BMI 32.8 ± 1.7, age Europeans with obesity showed lower
59 ± 6)) Bacteroides and higher Veillonellaceae.
Japanese (n = 11, ♂ n = 5 - Lean
(n = 10, BMI 20.1 ± 0.8, age 21 ± 1),
Overweight (n = 1, BMI 28, age 33))
South Korea (n = 18, ♂ n = 12 -
Lean (n = 14, BMI 22.5 ± 1.2, age
43 ± 16), Overweight (n = 4, BMI
28.5 ± 0.6, age 58 ± 13))
USA (♀ n = 54 twin - Lean (BMI
21.3 ± 1.0, age 26 ± 2), Overweight
(BMI 28.3 ± 0.6, age 26 ± 3), Obese
(BMI 41.7 ± 7.8, age 26 ± 3))
Fernandes Canada 94 individuals qPCR (Bacteroidetes/Prevotella Individuals with overweight and obesity 7
et al. [42] Lean (n = 52, ♂ n = 22, BMI 21.8 ± (Bacteroidetes), Clostridium coccoides, showed lower Escherichia coli.
0.3, age 32.0 ± 1.8) Clotridium leptum, Bifidobacteria, Negative correlation between BMI and
Overweight and obese (n = 42, ♂ Escherichia coli, Archea) Bacteroidetes.
n = 21, BMI 30.3 ± 0.7, ager 37.9 ±
2.0)
Rahat- Canada 22 individuals Sequencing Individuals with obesity showed higher 8
rozenbloo Lean (n = 11, ♂ n = 6, BMI 22.6 ± Firmicutes and Firmicutes/
et al. [28] 0.6, age 35.8 ± 4.2) Bacteroidetes ratio.
Profile of the gut microbiota of adults with obesity: a systematic review

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

Obese (n = 11, ♂ n = 9, BMI 30.1 ±


0.8, age 42.5 ± 3.9)
Dorminianni USA April 82 individuals (♂ n = 51) Sequencing Women with overweight had lower 9
et al. [20] 1985 to ♀ (n = 31, BMI 23.8 ± 4.69, age diversity.
June 1987 59.2 ± 12.67)
♂ (n = 51, BMI 25.0 ± 4.06, age
58.4 ± 13.18)
Kasai et al. Japan 56 individuals Terminal restriction fragment length Individuals with obesity showed higher 7
[26] 2012–2013 Lean (n = 23, ♂ n = 11, BMI 18.6 ± polymorphism diversity, richness, Firmicutes/
1.2, age 45.6 ± 9.6) Bacteroidetes ratio, and lower amounts
obese (n = 33, ♂ n = 20, BMI of Bacteroidetes.
27.8 ± 2.5, age 54.4 ± 8.2) Blautia hydrogenotorophica,
Coprococcus catus, Eubacterium
ventriosum, Ruminococcus bromiii and
Ruminococcus obeum were associated
with obesity.
While Bacteroidetes faecichinchilar,
Bacteroides thetaiotaomicron, Blautia
wexlerae, Clostridium bolteae,
Flavonifractor plautii. Bacteroidetes
faecichinchil and Bacteroides
thetaiotaomicron were associated
with lean.
Santos et al. Brazil October ♀ n = 40 qPCR (Mollicutes classes, Firmicutes Women with obesity showed higher 8
[29] to December Lean (n = 20, BMI 22.41 ± 2.04, age and Bacteroidetes) amount of Mollicutes and Firmicutes/
44 ± 9.3) Bacteroidetes ratio.
Obese (n = 20, BMI 36.45 ± 4.52, Positive correlation between BMI and
age 33 ± 12.04) Mollicutes.
Yasir et al. Saudi Arabia 46 individuals Sequencing Lean French showed higher bacterial 6
[13] and France Saudi (♂ n = 18 men – Lean (n = 9, species than other groups.
BMI 24.5 ± 3.2, age 28 ± 4), Obese French with obesity showed higher
(n = 9, BMI 46.0 ± 5.9, age 26 ± 3)) Proteobacteria, Bacteroidetes,
French (n = 28 – Lean (n = 16, ♂ Lactobacillus, Escherichia-Shiguela,
n = 7, BMI no data, age 34 ± 5), Bacteroides, Bacteroides fragilis,
Obese (n = 12, ♂ n = 7, BMI 38.3 ± Blautia wexlerae, Echerichia coli and
7.9, age 39 ± 13)) lower Clostridium, Faecalibacterium,
Bifidobacterium adolescentis, breve,
and Ruminococcus lactaris compared
with lean French, and lower
Ruminococcus, Verrucomicrobia,
Faecalibacterium, Bifidobacterium
adolescentis, and higher Bacteroides
fragilis, and Bifidobacterium bifidum
compared with lean Saudi.
Saudi with obesity showed higher
Firmicutes and Dorea compared with
lean Saudi, and lower Clostridium,
Bifidobacterium brevee and higher
Dorea, Blautiawex lerae and Rothia
mucilaginosa compared with lean
French.
Gemmatimonadetes, Lactobacillus
gasseri and reuteri were detected only
French with obesity, and Spirochaetae
and Elusimicrobia detected only lean
French.
French with obesity had higher
Verrucobacteria, Rothia mucilaginosa
and Ruminococcus bromii, and lower
Faecalibacterium, Blautia and
Bifidobacterium compared with Saudi
with obesity.
Andoh et al. Japan 20 individuals Sequencing Individuals with obesity showed higher 6
[32] Lean (n = 10, ♂ n = 5, BMI 16.6 ± Firmicutes, Fusobacteria, Alistipes,
1.0, age 45 (31–58)) Anaerococcus, Coprococcus,
Obese (n = 10, ♂ n = 5, BMI 38.1 ± Fusobacterium, Parvimonas,
3.5, age 41 (35–55)) Acidaminococcus intestine, Actinomyces
meyeri, Atopobium parvulum,
Bacteroides vulgates, Eubacterium
hadrum, Klebsiella pneumonia,
Roseburia faecis and lower Bacteroides,
Desulfovibrio, Faecalibacterium,
Finegoldia, Lachnoanaero baculum,
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

Olsenella, Clostridium ramosum,


Clostridium citroniae, Faecalibacterium
prausnitzii, Eubacterium desmolans,
Eubacterium fissicatena, and
Haldemania filiformis.
Hippe et al. – 68 individuals qPCR (Faecalibacterium prausnitzii) Individuals with obesity with or without 5
[43] Lean (n = 18, ♂ n = 3, BMI 21.2 ± T2D showed lower Faecalibacterium
1.9, age 26 ± 3) prausnitzii compared with lean.
Obese with T2D (n = 24, ♂ n = 14,
BMI 38.2 ± 5.1, age 58 ± 9)
Obese (n = 26, ♂ n = 4, BMI 43.9 ±
12.1, age 42 ± 15)
Selma et al. Spain 69 individuals qPCR (Echerichia coli, Bifidobacterium Individuals with overweight-obesity 5
[30] Clinical trial Lean (n = 20, ♂ n = 11, BMI 22.5 ± (B. longum), Lactobacillus/ showed higher Firmicutes, Clostridium
2.1) Leuconostoc/Pedicoccus (Lactobacillus leptum, Lactobacillus/Leuconostoc/
Overweight-obesity (n = 49, ♂ n = plantarum), Firmicutes, Clostridium Predicoccus, Bifidobacterium and
32, BMI 30.3 ± 3.4) leptum, Blautiacoccoides/ Firmicutes/Bacteroidetes ratio, and
Eubacteriumrectale (Blautia coccoides), lower Prevotella.
Bacteroides (Bacteroides ovatus), Positive correlation between BMI and
Prevotella (Prevotella bucalis), and Firmicutes, Clostridium leptum,
Gordonibacter (Gordonibacter Lactobacillus/Leuconostoc/Predicoccus,
pamelaeae)) and negative correlation between BMI
and Prevotella.
Blasco et al. Spain January 35 individuals Sequencing Individuals with obesity showed lower 6
[37] to September Lean (n = 18, ♂ n = 10, BMI 23.3 Ignavibacteriae.
(21.6–25.82), age 50 (39–56.25))
Obese (n = 17, ♂ n = 11, BMI 45.1
(39.1–47.45), age 53 (48–58))
Davis et al. USA May to 81individuals, ♂ n = 36 Sequencing Firmicutes (Dialister sp., Ruminococcus 8
[45] December BMI 28.3 ± 7.0 gnavus, Blautiaobeum,
Lean (27) Megasphaerasp., Oscillospira sp.) and
Overweight (27) Verrucobacteria (Akkermansia
Obese (27) muciniphila) had association with
Age 33 ± 13.3 obesity.
Fernandéz- Spain 2009 68 individuals qPCR (Akkermansia (Akkermansia Lactobacillus was higher in individuals 9
Navarro et al. to 2015 Lean (n = 20, ♂ n = 4, BMI 23.0 ± muciniphila CIP 107961), Bacteroidetes with obesity.
[21] 1.5, age 56.4 ± 10.1) group and Bacteroidetes-Prevotella- Positive correlation between BMI and
Overweight (n = 35, ♂ n = 17, BMI Porphiromonas (Bacteroides Lactobacillus.
27.5 ± 1.4, age 51.7 ± 11.7) thetaiotaomicron DSMZ 2079),
Obese (n = 13, ♂ n = 6, BMI 34.1 ± Bifidobacterium (Bifidobacterium
2.7, age 47.8 ± 10.2) longum NCIMB 8809),
Faecalibacterium (Faecalibacterium
prausnitzii DSMZ 17977), Clostridia
XIVa and Blautia coccoides-
Eubacterium rectale (Blautia coccoides
DSMZ 935), Lactobacillus group
(Lactobacillus gasseriIPLA IR7/5))
Kolida et al. Ukraine 61 individuals qPCR (Bacteroidetes, Firmicutes, Individuals with obesity showed lower 6
[10] March to May Underweight (n = 7, ♂ n = 2, Actinobacteria) Bacteroidetes and higher Firmicutes and
BMI < 18.5) Firmicutes/Bacteroidetes ratio.
Lean (n = 27, ♂ n = 7, BMI Positive correlation between BMI and
18.5–24.9) Firmicutes and Firmicutes/
Overweight (n = 16, ♂ n = 2, BMI Bacteroidetes ratio, and negative
25–29.9) correlation between BMI and
Obese (n = 11, ♂ n = 4, BMI ≥ 30) Bacteroidetes.
Age 44.2
Nistal et al. Spain 73 individuals Sequencing Individuals with obesity showed higher 7
[27] Lean (n = 20) bacterial richness and amount of
Obese (n = 53) Proteobacteria, Prevotella,
No data about BMI Megasphaera, Lactobacillus,
Age (20–60) Meganomas and Acidaminococcus, and
lower amount of Blautia, Osillospira,
Flavobacterium, Alkaliphillys and
Eubacterium, compared with lean.
De la Cuesta- Colombia July 441 individuals Sequencing Diversity was lower in individuals with 6
Zuluaga et al. to November Healthy lean (n = 91, ♂ n = 41, BMI obesity and individuals with
[25] 22.5 ± 1.6, age 36.8 ± 10.8) cardiovascular disease.
Non-healthy lean (n = 47, ♂ n = 22, Pathobiont-CAG and Lachnospiraceae-
BMI 23.0 ± 1.6, age 43.3 ± 11.8) CAG were associated with
Healthy overweight (n = 60, ♂ n = cardiovascular disease and obesity,
26, BMI 27.2 ± 1.3, age 38.4 ± 10.8)
Profile of the gut microbiota of adults with obesity: a systematic review

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

Non-healthy overweight (n = 111, ♂ while Ruminococcaceae and


n = 63, BMI 27.6 ± 1.4, age 41.5 ± Akkermansia were associated with lean.
10.9)
Healthy obese (n = 21, ♂ n = 6,
BMI 33.5 ± 2.6, age 43.1 ± 8.8)
Non-healthy obese (n = 111, ♂ n =
54, BMI 34.1 ± 3.6, age 42.7 ± 11.1)
Gao et al. China 551 individuals Sequencing Underweight showed higher alpha 7
[36] Underweight (n = 62 ♀ n = 49, diversity compared with the other
♂ n = 13, BMI ♀ 17.5 ± 1.0, ♂ groups. Bacteroidetes, Fusobacteria and
16.7 ± 1.1, age ♀ 38.0 ± 25.6, ♂ Proteobacteria were higher in
21.5 ± 5.5) individuals with obesity, compared with
Lean (n = 261 ♀ n = 168, ♂ n = 93, underweight.
BMI ♀ 20.7 ± 1.3, ♂ 21.3 ± 1.3, age
♀ 35.6 ± 14.3, ♂ 37.8 ± 17.3)
Overweight (n = 170 ♀ n = 55,
♂ n = 115, BMI ♀ 24.7 ± 1.3, ♂
25.1 ± 1.2, age ♀ 38.1 ± 12.6, ♂
41.7 ± 15.9)
Obese (n = 58 ♀ n = 20, ♂ n = 38,
BMI ♀ 31.7 ± 4.3, ♂ 31.2 ± 3.2, age
♀ 35.5 ± 4.3, ♂ 34.7 ± 3.2)
Jinatham Thailand 42 individuals qPCR (Bacteroidetes, Bacteroides, Bacteroidetes, Firmicutes, 8
et al. [31] Lean (n = 21, BMI 20.7 ± 0.4) Prevotella, Firmicutes, Roseburia e Staphylococcus, Akkermansia
Overweight (n = 10, BMI 27.4 ± Eubacterium rectale, Ruminococcus, muciniphila, Methanobacteria were
0.5) Lactobacillus, Enterococcus, lower in individuals with obesity,
Obese (n = 11, BMI 33.6 ± 1.0) Staphylococcus, Oscillospira, compared with lean. Ruminoccocus,
Age 27.6 ± 1.3 Faecalibacterium prausnitzii, Christensenella minuta, γ-
Chistensenella minuta, Actinobacteria, Proteobacteria, Akkermansia
γ-Proteobacteria, Fusobacterium, municiphila was lower in individuals
Akkermansia muciniphila, affected by obesity, compared with
Methanobacteria) overweight.
Negative correlation between BMI,
waist circumference and Firmicutes,
Staphylococcus, Akkermansia
municiphila, Methanobacteria.
Ottosson Sweden 674 individuals Sequencing Positive correlation between BMI and 7
et al. [44] Lean (BMI 22.3 ± 1.8) Lachnospiraceae (Blautia, Dorea, and
Overweight (BMI 27.1 ± 1.4) Ruminococcus), and negative
Obese (BMI 33.6 ± 3.3) Age 39.4 ± correlation between BMI and SHA-98.
13.5
Sarmiento Brazil 72 individuals FISH (Bacteroidetes fragilis, Individuals with obesity showed higher 8
et al. [38] Lean (n = 24, BMI 22.2 ± 1.8) Escherichia cpli, Enterococcus, bacterial density followed by individuals
Overweight (n = 24, BMI 27.1 ± Fusobacterium, Prevotella intermedia, with overweigh and lean.
1.3) prevotella nigrescens, Pseudomonas, Fusobacterium, Enterococcus,
Obese (n = 24, BMI 36.9 ± 6.0) Staphylococcus, Streptococcus, Echerichia coli were higher in
Age 39.6 ± 13.5 Acinetobacter) individuals with obesity, compared with
lean individuals.

♀ 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

conostoc/Predicoccus [30], Lactobacillus [21], Proteo-


Records after duplicates
removed (n=8336) bacteria, Actinobacteria, Spitochaetes, Blautia, Dorea,
Ruminococcus [44], and Firmicutes/Bacteroidetes ratio
Records excluded after reading [26].
title and abstract (n=8283)
Negative correlations were found between the BMI and
Bacteroides [40, 42], Clostridium coccoides, Clostridium
Eligibility

Full-text articles excluded (n=21):


−Short communication (n=2)
Full text assessed for −Thesis was not available (n=1)
leptum, Lactobacillus plantarum, Bifidobacterium, Bifido-
eligibility (n=53) −Did not compared lean and obese bacterium longum [39], Akkermansia muciphinila [31, 39],
(n=4)
−Included children and teenagers
Firmicutes, Staphylococcus, Methanobacteria [31], Bifido-
(n=2) bacterium animalis, Escherichia coli [14], Prevotella [30],
− Did not evaluated gut
microbiota (n=2) SHA-98 [44], Allistipes, and Bacteroidetes/Firmicutes ratio
−Intervention study (n=2)
[24].
Included

−Obesity group had overweight


Studies included in BMI (n= 5) Bacteroidetes faecichinchilar, Bacteroides thetaiotao-
qualitative synthesis (n=32) −Protocol (n=1)
−Poor quality (n=2)
micron, Blautia wexlerae, Clostridium bolteae, Flavoni-
fractor plautii [26], Ruminococcaceae, and Akkermansia
Fig. 1 Flow chart of selection process. [25] were associated with normal weight. On the other
hand, increases in Blautia hydrogenotorophica, Copro-
Olsenella [32], Faecalibacterium [13, 32], Bifidobacterium, coccus catus, Eubacterium ventriosum, Ruminococcus
Methanobrevibacter [11], Prevotella [30], Blautia, Flavo- bromii, Ruminococcus obeum [26], Firmicutes, Verruco-
bacterium, Alkaliphillys, Eubacterium [27], Staphylococcus bacteria [45] and Lactobacillus reuteri [14, 41], and
[31], Osillospira [27, 34], Dialister, Akkermansia, Copro- decreases in Bifidobacterium animalis and Methano-
coccus, Parabacteroides, Clostridiales [34], Clostridium, and brevibacter smithii were associated with obesity [41], and
Ruminococcus [13]. Pathobiont-CAG and Lachnospiraceae-CAG were asso-
The species more present in individuals with obesity ciated with cardiovascular disease and obesity [41].
were Lactobacillus reuteri [14, 41], Clostridium cluster IV
and XIVa [24], Clostridium leptum [30], Acidaminococcus
intestine, Actinomyces meyeri, Atopobium parvulum, Bac- Discussion
teroides vulgates, Eubacterium hadrum, Klebsiella pneu-
monia, Roseburia faecis [32], Bacteroides fragilis, Blautia Over the years the role that the gut microbiota composition
wexlerae, Escherichia coli, and Bifidobacterium bifidum exerts on human health influencing body weight control,
[13]. On the other hand, Akkermansia muciniphila [13, 31], has been shown [46]. This review observed controversy in
Clostridium leptum, Ruminococcus flavefaciens spp. [11], the diversity of the gut microbiota associated with obesity
Clostridium perfringens [33], Lactobacillus paracasei, with respect to higher or lower counts in individual with
Lactobacillus plantarum [41], Methanobrevibacter smithii, obesity, compared with lean. Some bacteria of the gut
Bifidoacterium animalis [14, 41], Escherichia coli [14, 42], microbiota were highlighted as higher in individual with
Ruminococcus lactaris, Rothia mucilaginosa, Bifido- obesity, such as Firmicutes, Proteobacteria, Fusobacteria,
bacterium adolescentis Bifidobacterium breve [13], Bifido- Firmicutes/Bacteroidetes ratio, and Lactobacillus, and oth-
bacterium longum, Clostridium coccoides, Clostridium ers as lower, such as Bacteroidetes, Faecalibacterium
leptum [37], Clostridium ramosum, Clostridium citroniae, prausnitzii, Akkermansia muciniphila, Methanobrevibacter
Faecalibacterium prausnitzii [32, 43], Eubacterium des- smithii, and Bifidobacterium animalis.
molans, Eubacterium fissicatena, and Haldemania filiformis The relationship between the gut microbiota and body
[32] were less present in individuals with obesity. weight control was discovered in the last decade [6]. Later a
study showed weight gains in germ-free mice receiving
Correlation between gut microbiota and obesity transplants of gut microbiota from individuals with obesity
[47]. The literature indicates an important influence of the
Some studies carried out correlations between the gut microbiota on body weight control. This changes in the gut
microbiota composition and the BMI (n = 15). Positive microbiota composition causes a greater extraction and
Profile of the gut microbiota of adults with obesity: a systematic review

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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