ARE ENTEROTYPES IN OBESE MODIFIED BY BARIATRIC SURGERY, THE USE OF PROBIOTIC SUPPLEMENTS AND FOOD HABITS?

Giúlia Jager Maximowicz DE-OLIVEIRA Maria Eliana Madalozzo SCHIEFERDECKER Antonio Carlos L CAMPOS About the authors

ABSTRACT

Introduction:

Studies suggest that bariatric surgery, use of probiotic supplements and the dietary pattern can change enterotypes, as well as the entire microbial population.

Objective:

To verify the influence of bariatric surgery, the use of probiotic supplements and eating habits on enterotypes in obese patients.

Methods:

Articles published between the 2015 and 2020 were searched in Lilacs and PubMed with the headings: probiotics, eating behavior, food consumption, food, diet, microbiota, gastrointestinal microbiome, bariatric surgery, gastric bypass and the keyword enterotype in Portuguese, English and Spanish.

Results:

Of the 260 articles found, only studies carried out in obese adults relating changes in the enterotype after bariatric surgery or use of probiotics or dietary patterns and original articles were selected. In the end, eight papers on enterotype change and bariatric surgery were selected and categorized, four on the relationship between food consumption and microbiota and one on the effects of probiotics on enterotypes.

Conclusion:

The microbial structure is widely modified after bariatric surgery, since the use of probiotic supplement does not bring lasting changes. Enterotypes appear to be shaped by long-term dietary patterns, can modulate how nutrients are metabolized and can be a useful biomarker to improve clinical management.

HEADINGS:
Probiotic; Food consumption; Microbiota; Gastric bypass; Obesity

RESUMO

Introdução:

Estudos sugerem que a cirurgia bariátrica, uso de suplementos probióticos e o padrão alimentar podem mudar enterótipos, assim como toda a população microbiana.

Objetivo:

Verificar a influência da cirurgia bariátrica, do uso de suplementos probióticos e de hábitos alimentares nos enterótipos de pacientes obesos.

Métodos:

Foi realizada a busca de artigos publicados entre os anos de 2015 e 2020 nas bases de dados Lilacs e PubMed com os descritores: probióticos, comportamento alimentar, consumo alimentar, alimentação, dieta, microbiota, microbioma gastrointestinal, cirurgia bariátrica, bypass gástrico e a palavra-chave enterótipo em português, inglês e espanhol.

Resultados:

Dos 260 artigos encontrados, foram selecionados os estudos originais realizados em adultos obesos relacionando mudanças de enterótipo após cirurgia bariátrica, a padrões alimentares ou ao uso de probiótico. Ao final, foram selecionados e categorizados oito estudos sobre mudança de enterótipo e cirurgia bariátrica, quatro sobre relação entre consumo alimentar e microbiota e somente um sobre efeitos dos probióticos nos enterótipos.

Conclusão:

A estrutura microbiana é amplamente modificada após a cirurgia bariátrica. O uso de suplemento probiótico não parece trazer mudanças duradouras. Os enterótipos parecem ser moldados por padrões alimentares em longo prazo e podem modular como os nutrientes são metabolizados, podendo vir a ser um biomarcador útil para melhorar o manejo clínico de pacientes obesos.

DESCRITORES:
Probiótico; Consumo alimentar; Microbiota; Bypass gástrico; Obesidade

INTRODUCTION

By a multifactorial cause, obesity is closely linked to incorrect eating habits66 Vanessa Marieli CEGLAREK1 , Zoé Maria GUARESCHI1 , Gabriela MOREIRA-SOARES2 RC, ECKER-PASSARELLO1 , Sandra Lucinei BALBO1 , Maria Lúcia BONFLEUR1 SG. Derivação duodeno-jejunal reduz o acúmulo de lipídios no tecido adiposo marrom de ratos com obesidade hipotalâmica. 2020; 33: 1-5.. With the global obesity epidemic, bariatric surgery is now considered the most effective, prompt and long-lasting treatment for patients with morbid obesity1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.. The most performed techniques in the world are Roux-en-Y gastric bypass (RYGB) and vertical gastrectomy88 Dao MC, Belda E, Prifti E, Everard A, Kayser BD, Bouillot JL et al. Akkermansia muciniphila abundance is lower in severe obesity, but its increased level after bariatric surgery is not associated with metabolic health improvement. Am J Physiol Endocrinol Metab 2019; 317: E446-E459..

The intestinal microbiota is colonized by about 100 trillion bacteria which contribute to 3.3 million unique microbial genes and is unique to each individual2121 Tang ZZ, Chen G, Hong Q, Huang S, Smith HM, Shah RD et al. Multi-omic analysis of the microbiome and metabolome in healthy subjects reveals microbiome-dependent relationships between diet and metabolites. Front Genet 2019; 10. doi:10.3389/fgene.2019.00454.
https://doi.org/10.3389/fgene.2019.00454...
. After bariatric surgery, eating habits change, patients often use medications and supplements, including probiotics, there is an intense change in body weight, and patients often incorporate healthier lifestyle habits, such as physical activity. All of these factors together have the potential to influence the composition of the intestinal microbiota2121 Tang ZZ, Chen G, Hong Q, Huang S, Smith HM, Shah RD et al. Multi-omic analysis of the microbiome and metabolome in healthy subjects reveals microbiome-dependent relationships between diet and metabolites. Front Genet 2019; 10. doi:10.3389/fgene.2019.00454.
https://doi.org/10.3389/fgene.2019.00454...
.

The evaluation of individual’s microbiota is complex, since it is specific to each one. For this reason, the proposition arose to group intestinal bacteria in groups, called enterotypes1010 Festi D, Schiumerini R, Eusebi LH, Marasco G, Taddia M, Colecchia A. Gut microbiota and metabolic syndrome. World J Gastroenterol 2014; 20: 16079-16094.. A recent study analyzed faecal metagenomas of individuals from different countries using multidimensional cluster analysis and main components22 Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR et al. Enterotypes of the human gut microbiome. Nature 2011; 473: 174-180.. The authors were able to group faecal metagenomas into three different enterotypes, which were identified by relative amounts of any of the three dominant genera: Bacteroides (enterotype 1), Prevotella (enterotype 2) and Ruminococcus (enterotype 3). Interestingly, these enterotypes appear to be independent of nationality, gender, age or body mass index (BMI).

However, the results of another study2525 Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh S. Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Bone 2012; 23: 1-7. improvement that enterotypes may be strongly associated with the composition of the diet in long term. Enterotype 1, rich in Bacteroides, was strongly associated with the consumption of animal proteins and saturated fats. Enterotype 2, rich in Prevotella, was associated with a carbohydrate-based diet, composed of simple sugars and fibers. Enterotype 3, on the other hand, seems to be strongly related to individual health status1818 Seganfredo FB, Blume CA, Moehlecke M, Giongo A, Casagrande DS, Spolidoro JVN et al. Weight-loss interventions and gut microbiota changes in overweight and obese patients: a systematic review. Obes Rev 2017; 18: 832-851.. Although it is not known whether enterotypes may be associated with predisposition to certain disease states, these findings have improved that long-term dietary patterns may affect the state of the enterotype, a nutritional-microbiome connection and the pathophysiology in relation to those susceptible to the disease2525 Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh S. Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Bone 2012; 23: 1-7..

Oral administration of supplements with probiotic strains is associated with verified benefits for human health and its use has become usual even after bariatric surgery. Probiotics are living microorganisms that, since they already reside naturally in the healthy human microbiota, when used in an adequate dosage, are safe and confer benefits to the host1919 Shin JH, Jung S, Kim SA, Kang MS, Kim MS, Joung H et al. Differential effects of typical Korean versus american-style diets on gut microbial composition and metabolic profile in healthy overweight koreans: A randomized crossover trial. Nutrients 2019; 11. doi:10.3390/nu11102450.
https://doi.org/10.3390/nu11102450....
,2020 Song EJ, Han K, Lim TJ, Lim S, Chung MJ, Nam MH et al. Effect of probiotics on obesity-related markers per enterotype: a double-blind, placebo-controlled, randomized clinical trial. EPMA J 2020; 11: 31-51..

There is evidence that bariatric surgery induces changes in the intestinal microbiota11 Aron-Wisnewsky J, Prifti E, Belda E, Ichou F, Kayser BD, Dao MC et al. Major microbiota dysbiosis in severe obesity: Fate after bariatric surgery. Gut 2019; 68: 70-82.,1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13. and that each enterotype seems to be strongly associated with food choices, affecting the quantity of specific strains differently in the intestinal microbiota99 David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505: 559-563.,1919 Shin JH, Jung S, Kim SA, Kang MS, Kim MS, Joung H et al. Differential effects of typical Korean versus american-style diets on gut microbial composition and metabolic profile in healthy overweight koreans: A randomized crossover trial. Nutrients 2019; 11. doi:10.3390/nu11102450.
https://doi.org/10.3390/nu11102450....
,2121 Tang ZZ, Chen G, Hong Q, Huang S, Smith HM, Shah RD et al. Multi-omic analysis of the microbiome and metabolome in healthy subjects reveals microbiome-dependent relationships between diet and metabolites. Front Genet 2019; 10. doi:10.3389/fgene.2019.00454.
https://doi.org/10.3389/fgene.2019.00454...
. It is also known that the use of probiotics can also modulate the microbiota of the general population1313 Hou Q, Zhao F, Liu W, Lv R, Khine WWT, Han J et al. Probiotic-directed modulation of gut microbiota is basal microbiome dependent. Gut Microbes 2020; 00: 1-20.. However, studies in the literature that contemplate all of these themes have not been found.

Thus, the aim of this study was to verify the impact of bariatric surgery, the use of probiotics and eating habits on the enterotypes of obese patients.

METHODS

This is an integrative literature review, accomplished out based on: identification of the theme and selection of the research question, establishment of inclusion and exclusion criteria, identification of pre-selected and selected studies, categorization of selected studies, analysis and interpretation of results and presentation of the review33 Botelho LLR, Cunha CC de A, Macedo M. O Método Da Revisão Integrativa Nos Estudos Organizacionais. Gestão e Soc 2011; 5: 121..

The guiding question of this review was: “Can bariatric surgery, the use of probiotic supplements and eating habits affect or modify enterotypes in obese patients?”

The data collection period occurred between the months of May and June 2020 in the Pubmed and Lilacs databases. The following Health Sciences Descriptors (DeCS) and boolean combinations were used: “probiotics”, “eating behavior”, “food consumption”, “food”, “diet”, “microbiota”, “gastrointestinal microbiome”, “bariatric surgery “,” gastric bypass “,” obesity “and the keyword:” enterotype “.

Articles available in portuguese and english, in their entirety, that included changes in enterotypes after bariatric surgery, the use of probiotics or related to dietary patterns were included. Only original articles published and indexed in the referred databases in the last five years were included. Review articles, studies in animals and children and those in which the population was not obese were excluded.

From those selected, data of interest were collected for analysis using a collection instrument that embrace publication, sample, objectives, methodology used and main results of each study. For the tabulation of probiotic studies, in addition to the items previously mentioned, a description of the strains used was added.

Data analysis was performed in a descriptive and comparative way and the studies were categorized into three tables. Those who showed changes in the composition of the intestinal microbiota in individuals undergoing bariatric surgery, studies that related the changes to food consumption and those who studied the use of some probiotic supplementation.

RESULTS

After associating the terms, 237 articles were found indexed in the Pubmed database and 23 in Lilacs. After reading the titles, were excluded the duplicates, those that did not meet the inclusion criteria and those that were not relevant to the theme. At the end of the search, 13 articles were selected then analyzed and discussed (Figure 1).

FIGURE 1
Flowchart of the selection of articles included in the review

Of the 13 studies, eight were aimed at changing the microbiota after bariatric surgery; four related the enterotypes with eating habits; and one examined the influence of the use of probiotic supplementation on the microbiota.

Studies that evaluated changes in the composition of the intestinal microbiota after bariatric surgery (Table 1) point out that there was a change in enterotypes, an increase in alpha diversity, a relative increase in Proteobacteria, Bacteroidetes and Fusobacteria phyla. Such changes occur from the first three months44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373.,55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505.,1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.,1717 Sánchez-Alcoholado L, Gutiérrez-Repiso C, Gómez-Pérez AM, García-Fuentes E, Tinahones FJ, Moreno-Indias I. Gut microbiota adaptation after weight loss by Roux-en-Y gastric bypass or sleeve gastrectomy bariatric surgeries. Surg Obes Relat Dis 2019; 15: 1888-1895. post-surgical and can extend for up to 10 years2222 Tremaroli V, Karlsson F, Werling M, Ståhlman M, Kovatcheva-Datchary P, Olbers T et al. Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation. Cell Metab 2015; 22: 228-238.. However, one study88 Dao MC, Belda E, Prifti E, Everard A, Kayser BD, Bouillot JL et al. Akkermansia muciniphila abundance is lower in severe obesity, but its increased level after bariatric surgery is not associated with metabolic health improvement. Am J Physiol Endocrinol Metab 2019; 317: E446-E459. has not found significant changes in the compositions of enterotypes over time.

TABLE 1
Changes in the composition of the intestinal microbiota in individuals undergoing bariatric surgery

Regarding the studies that analyzed changes in enterotypes related to food consumption (Table 2), there was a change in enterotypes Prevotella to Bacteroidetes. The consumption of carbohydrates7,11,19 and animal protein1212 Hjorth MF, Christensen L, Larsen TM, Roager HM, Krych L, Kot W et al. Pretreatment Prevotella-To-Bacteroides ratio and salivary amylase gene copy number as prognostic markers for dietary weight loss. Am J Clin Nutr 2020; 111: 1079-1086.,1919 Shin JH, Jung S, Kim SA, Kang MS, Kim MS, Joung H et al. Differential effects of typical Korean versus american-style diets on gut microbial composition and metabolic profile in healthy overweight koreans: A randomized crossover trial. Nutrients 2019; 11. doi:10.3390/nu11102450.
https://doi.org/10.3390/nu11102450....
can modify the enterotypes, as well as the type of enterotype can modulate the responses to the diet.

TABLE 2
Enterotype changes and their relationship with habits and food consumption

In relation to the studies that evaluated change of enterotype with the use of probiotics (Table 3), none were able to observe lasting change. In obese individuals with Prevotella enterotype, the probiotics B. breve CBT BR3 and L. plantarum CBT LP3 seem to have a beneficial effect2020 Song EJ, Han K, Lim TJ, Lim S, Chung MJ, Nam MH et al. Effect of probiotics on obesity-related markers per enterotype: a double-blind, placebo-controlled, randomized clinical trial. EPMA J 2020; 11: 31-51..

TABLE 3
Enterotype changes in individuals using some probiotic supplementation

DISCUSSION

According to the findings in the present study, bariatric surgery appears to alter the microbial community. The changes in general occur from the third month on both the RYGB and gastric band techniques88 Dao MC, Belda E, Prifti E, Everard A, Kayser BD, Bouillot JL et al. Akkermansia muciniphila abundance is lower in severe obesity, but its increased level after bariatric surgery is not associated with metabolic health improvement. Am J Physiol Endocrinol Metab 2019; 317: E446-E459.,1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.. There is no consensus on the duration of this change. Few studies1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.,2222 Tremaroli V, Karlsson F, Werling M, Ståhlman M, Kovatcheva-Datchary P, Olbers T et al. Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation. Cell Metab 2015; 22: 228-238. have investigated such changes for more than a year, but one reported that the change produced by the operation is specific to the microbiota and can persist for up to a decade.

In the first three months after bariatric surgery, there was an increase in alpha diversity55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505. and a shift to a healthier metabolism, with an increase in species richness. Genetic richness, on the other hand, seems to increase only one year after the operation1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.. Alpha diversity as it represents the diversity of a habitat or a community of microorganisms and describes the wealth and equality of individuals, can be used as an interesting indirect marker to assess the effectiveness of surgical treatment in terms of restoring the function of intestinal microflora44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373..

After RYGB, there was a reduction in Firmicutes55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505., an increase in Proteobacteria55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505.,1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.,1717 Sánchez-Alcoholado L, Gutiérrez-Repiso C, Gómez-Pérez AM, García-Fuentes E, Tinahones FJ, Moreno-Indias I. Gut microbiota adaptation after weight loss by Roux-en-Y gastric bypass or sleeve gastrectomy bariatric surgeries. Surg Obes Relat Dis 2019; 15: 1888-1895.,2222 Tremaroli V, Karlsson F, Werling M, Ståhlman M, Kovatcheva-Datchary P, Olbers T et al. Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation. Cell Metab 2015; 22: 228-238., Prevotella44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373., Bacteroidetes44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373.,55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505.,2323 Wagner NRF, Zaparolli MR, Rosa M, Cruz R, Eliana M, Schieferdecker M et al. Postoperative Changes in Intestinal Microbiota and Use of Probiotics in Roux-En-Y Gastric Bypass and. Arq Bras Cir Dig 2018; 31: 1-5., Firmicutes44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373., Fusobacteria1414 Ilhan ZE, Dibaise JK, Isern NG, Hoyt DW, Marcus AK, Kang DW et al. Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding. ISME J 2017; 11: 2047-2058.,1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13., Actinobacteria44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373., Kleibsiella pneumoniae, Escherichia col1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13., Gammaproteobacteria1414 Ilhan ZE, Dibaise JK, Isern NG, Hoyt DW, Marcus AK, Kang DW et al. Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding. ISME J 2017; 11: 2047-2058. and A. muciniphila88 Dao MC, Belda E, Prifti E, Everard A, Kayser BD, Bouillot JL et al. Akkermansia muciniphila abundance is lower in severe obesity, but its increased level after bariatric surgery is not associated with metabolic health improvement. Am J Physiol Endocrinol Metab 2019; 317: E446-E459.. The increase in Proteobacteria after RYGB is already well established in the literature and occurs due to changes in environmental, physiological and metabolic conditions1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.. Such changes, as the increase in intestinal oxygen, the growth of facultative anaerobic bacteria44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373.,1414 Ilhan ZE, Dibaise JK, Isern NG, Hoyt DW, Marcus AK, Kang DW et al. Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding. ISME J 2017; 11: 2047-2058. and the increase in pH facilitate the survival of microorganisms sensitive to acid1414 Ilhan ZE, Dibaise JK, Isern NG, Hoyt DW, Marcus AK, Kang DW et al. Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding. ISME J 2017; 11: 2047-2058.,1717 Sánchez-Alcoholado L, Gutiérrez-Repiso C, Gómez-Pérez AM, García-Fuentes E, Tinahones FJ, Moreno-Indias I. Gut microbiota adaptation after weight loss by Roux-en-Y gastric bypass or sleeve gastrectomy bariatric surgeries. Surg Obes Relat Dis 2019; 15: 1888-1895., and promote changes in the microbial composition. Thus, microbial changes after RYGB are more due to intestinal rearrangement than to weight loss1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.. Despite this, the abundance of Proteobacteria is not considered beneficial, due to its pro-inflammatory property2222 Tremaroli V, Karlsson F, Werling M, Ståhlman M, Kovatcheva-Datchary P, Olbers T et al. Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation. Cell Metab 2015; 22: 228-238..

Regarding the exchange of enterotypes, a study with women after bariatric surgery showed changes from the enterotype Bacteroidetes 2 to Bacteroidetes 1, indicating an important characteristic in the improvement of metabolic results11 Aron-Wisnewsky J, Prifti E, Belda E, Ichou F, Kayser BD, Dao MC et al. Major microbiota dysbiosis in severe obesity: Fate after bariatric surgery. Gut 2019; 68: 70-82.. The Prevotella/Bacteroides (P/B) ratio, it remained stable, with a predominance of Bacteroides55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505..

There was a decrease in Proteobacteria in gastric banding techniques and vertical gastrectomy55 Campisciano G, Cason C, Palmisano S, Giuricin M, Rizzardi A, Croce LS et al. Bariatric surgery drives major rearrangements of the intestinal microbiota including the biofilm composition. Front Biosci - Elit 2018; 10: 495-505., besides to maintaining the P/B ratio before and after the operation44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373.. In the study accomplished out with 14 patients post vertical gastrectomy a difference was observed in terms of the microbial population with an increase in Verrumicrobia1717 Sánchez-Alcoholado L, Gutiérrez-Repiso C, Gómez-Pérez AM, García-Fuentes E, Tinahones FJ, Moreno-Indias I. Gut microbiota adaptation after weight loss by Roux-en-Y gastric bypass or sleeve gastrectomy bariatric surgeries. Surg Obes Relat Dis 2019; 15: 1888-1895..

Bariatric surgery, especially BGYR, not only decreases the amount of food eaten, but also changes eating behavior and food preferences1515 Mathes CM, Spector AC. Food selection and taste changes in humans after Roux-en-Y gastric bypass surgery: A direct-measures approach. Physiol Behav 2012; 107: 476-483.. In such a way, the changes occurred in the microbiota of these patients may be related to changes in patterns and food preferences1616 Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med 2016; 8: 1-13.,1717 Sánchez-Alcoholado L, Gutiérrez-Repiso C, Gómez-Pérez AM, García-Fuentes E, Tinahones FJ, Moreno-Indias I. Gut microbiota adaptation after weight loss by Roux-en-Y gastric bypass or sleeve gastrectomy bariatric surgeries. Surg Obes Relat Dis 2019; 15: 1888-1895. as well as related to the situation of hunger induced by the operation and the rapid microbial adaptation to such stress44 Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes 2018; 9: 367-373..

In the general population, the composition of the intestinal microbiome both at the taxonomic and enterotype levels is directly related to the lifestyle and frequency of ingestion of some foods11 Aron-Wisnewsky J, Prifti E, Belda E, Ichou F, Kayser BD, Dao MC et al. Major microbiota dysbiosis in severe obesity: Fate after bariatric surgery. Gut 2019; 68: 70-82.,1313 Hou Q, Zhao F, Liu W, Lv R, Khine WWT, Han J et al. Probiotic-directed modulation of gut microbiota is basal microbiome dependent. Gut Microbes 2020; 00: 1-20.,2121 Tang ZZ, Chen G, Hong Q, Huang S, Smith HM, Shah RD et al. Multi-omic analysis of the microbiome and metabolome in healthy subjects reveals microbiome-dependent relationships between diet and metabolites. Front Genet 2019; 10. doi:10.3389/fgene.2019.00454.
https://doi.org/10.3389/fgene.2019.00454...
,2525 Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh S. Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Bone 2012; 23: 1-7..

In individuals with a high abundance of Prevotella, greater weight loss was observed with a diet rich in fiber, carbohydrates, proteins and whole grains when compared to a diet based on refined grains and low in fibers77 Christensen L, Vuholm S, Roager HM, Nielsen DS, Krych L, Kristensen M et al. Prevotella Abundance Predicts Weight Loss Success in Healthy, Overweight Adults Consuming a Whole-Grain Diet Ad Libitum: A Post Hoc Analysis of a 6-Wk Randomized Controlled Trial. J Nutr 2019; 149: 2174-2181.,1111 Hjorth MF, Blædel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P et al. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes 2019; 43: 149-157.. They also showed greater fiber degradation when compared to subjects with Bacteroidetes enterotype77 Christensen L, Vuholm S, Roager HM, Nielsen DS, Krych L, Kristensen M et al. Prevotella Abundance Predicts Weight Loss Success in Healthy, Overweight Adults Consuming a Whole-Grain Diet Ad Libitum: A Post Hoc Analysis of a 6-Wk Randomized Controlled Trial. J Nutr 2019; 149: 2174-2181., which can be explained by the fact that high production of short-chain fatty acids affects appetite through different brain signaling pathways, which influence secretion of gastrointestinal hormones.

The P/B ratio was proven to be an important biomarker associated to weight loss with diet1111 Hjorth MF, Blædel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P et al. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes 2019; 43: 149-157.. At the same time that the high P/B ratio is associated with a diet rich in resistant starch and fibers77 Christensen L, Vuholm S, Roager HM, Nielsen DS, Krych L, Kristensen M et al. Prevotella Abundance Predicts Weight Loss Success in Healthy, Overweight Adults Consuming a Whole-Grain Diet Ad Libitum: A Post Hoc Analysis of a 6-Wk Randomized Controlled Trial. J Nutr 2019; 149: 2174-2181., the high-fat and low-fiber diet is associated with a low P/B ratio1111 Hjorth MF, Blædel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P et al. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes 2019; 43: 149-157..

The study that compared the consumption of obese patients for four weeks of a typical Korean diet, a typical American diet, and a recommended American diet, demonstrated that each diet significantly changed the structure of the intestinal microbiota and that responses to diets were affected by the individuals’ initial enterotypes1919 Shin JH, Jung S, Kim SA, Kang MS, Kim MS, Joung H et al. Differential effects of typical Korean versus american-style diets on gut microbial composition and metabolic profile in healthy overweight koreans: A randomized crossover trial. Nutrients 2019; 11. doi:10.3390/nu11102450.
https://doi.org/10.3390/nu11102450....
. The traditional Korean diet, composed mainly of high levels of vegetables, whole grains, low levels of animal foods and saturated fat demonstrated a decrease in Bacteroidetes and a significant increase in Firmicutes suggesting that Firmicutes are essential for the dietary metabolism of vegetable polysaccharides1919 Shin JH, Jung S, Kim SA, Kang MS, Kim MS, Joung H et al. Differential effects of typical Korean versus american-style diets on gut microbial composition and metabolic profile in healthy overweight koreans: A randomized crossover trial. Nutrients 2019; 11. doi:10.3390/nu11102450.
https://doi.org/10.3390/nu11102450....
.

The observations made show that changes in microbial communities driven by dietary choices may be dependent on the host’s enterotype. It is then suggested that enterotyping provides plausible evidence to be a useful strategy for the development of personalized nutrition1919 Shin JH, Jung S, Kim SA, Kang MS, Kim MS, Joung H et al. Differential effects of typical Korean versus american-style diets on gut microbial composition and metabolic profile in healthy overweight koreans: A randomized crossover trial. Nutrients 2019; 11. doi:10.3390/nu11102450.
https://doi.org/10.3390/nu11102450....
.

Despite of the existence of research on the influence of diet on enterotypes probiotics have still been examined for the possibility of impacting enterotypes at a similar level. The use of probiotics to modulate the intestinal microbiota and treat gastrointestinal symptoms has been considered an alternative to improve surgical results2424 Wagner NRF, Ramos MRZ, Carlos L de O, Cruz MRR da, Taconeli CA, Filho AJB et al. Effects of Probiotics Supplementation on Gastrointestinal Symptoms and SIBO after Roux-en-Y Gastric Bypass: a Prospective, Randomized, Double-Blind, Placebo-Controlled Trial. Obes Surg 2020 2020; : 1-8..

In Prevotella’s enterotype obese individuals, the probiotics may have a beneficial effect; however, such supplementation has not shown significant differences between groups at the phylum level and microbial family2020 Song EJ, Han K, Lim TJ, Lim S, Chung MJ, Nam MH et al. Effect of probiotics on obesity-related markers per enterotype: a double-blind, placebo-controlled, randomized clinical trial. EPMA J 2020; 11: 31-51..

Apparently the enterotypes, as well as the entire intestinal microbial population, are shaped mainly by the usual diet, that is, by long-term dietary patterns2121 Tang ZZ, Chen G, Hong Q, Huang S, Smith HM, Shah RD et al. Multi-omic analysis of the microbiome and metabolome in healthy subjects reveals microbiome-dependent relationships between diet and metabolites. Front Genet 2019; 10. doi:10.3389/fgene.2019.00454.
https://doi.org/10.3389/fgene.2019.00454...
. Short-term dietary interventions and probiotics appear to cause only transient changes in the microbiota2525 Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh S. Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Bone 2012; 23: 1-7..

There are few studies where food intake has been evaluated along with the use of probiotics and despite being impacting factors no studies have been found that evaluated the association between bariatric surgery, changes in food preferences and the use of probiotics on enterotypes, as well as the literature about the change of enterotypes is limited and not only to other microbial changes.

CONCLUSION

The intestinal microbiota is modified after bariatric surgery, and this change can influence enterotypes, especially in the first three postoperative months. Both the anatomical as functional modification of the intestinal tract resulting from bariatric surgery and the dietary modifications imposed by the operation seem to be responsible for the change of the enterotypes after it. The use of probiotic supplementation in obese patients was not associated with lasting changes in enterotype. It remains to be investigated whether the use of probiotics after bariatric surgery could influence the enterotype.

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  • Financial source:

    none.
  • Central message

    Bariatric surgery and changes in eating habits after surgery influence enterotypes. The use of probiotics wasn’t associated with such changes.
  • Perspective

    Microbial changes occur after bariatric surgery. Enterotypes appear to be shaped by long-term dietary patterns and can modulate how nutrients are metabolized. Enterotyping each patient can be a useful strategy for a better clinical management of obese patients with the development of personalized nutrition.

Publication Dates

  • Publication in this collection
    18 Oct 2021
  • Date of issue
    2021

History

  • Received
    01 Dec 2020
  • Accepted
    11 Mar 2021
Colégio Brasileiro de Cirurgia Digestiva Av. Brigadeiro Luiz Antonio, 278 - 6° - Salas 10 e 11, 01318-901 São Paulo/SP Brasil, Tel.: (11) 3288-8174/3289-0741 - São Paulo - SP - Brazil
E-mail: revistaabcd@gmail.com