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

DE-OLIVEIRA, Giúlia Jager Maximowicz; SCHIEFERDECKER, Maria Eliana Madalozzo; CAMPOS, Antonio Carlos L

doi:10.1590/0102-672020210002e1601

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Review Article • ABCD, arq. bras. cir. dig. 34 (02) • 2021 • https://doi.org/10.1590/0102-672020210002e1601 copy

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

Authorship SCIMAGO INSTITUTIONS RANKINGS

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

Authors	Objectives	Population	Main results found
Aron-Wisnewsky, et al., 2019 ¹1 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.	Examine whether the richness of microbial genes get worse in severe obesity and how it relates to worsening comorbidities; and whether the different types of surgery influence microbial characteristics, composition and function.	61 women with severe obesity 41 RYGB and 20 VGB Follow-up before surgery, one, three and 12 months after the procedure	Enterotypes were found in severely obese individuals. A lifestyle and food explain a large part of the microbial composition. There were changes in enterotypes in some patients after surgery (Bacteroidetes 2 to Bacteroidetes 1), such changes occur within 1 year after surgery. The exchange of post-RYGB enterotypes can be an important feature in improving metabolic results
Campisciano et al., 2018 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.	Determine whether bariatric surgery shapes the composition of the intestinal microbiota by influencing the intestinal mucosal biofilm and whether this can lead to a positive and long-lasting result	20 obese patients, 10 VG and 10 RYGB 20 eutrophic patients for control Follow-up before and 3 months after surgery	The amount of Proteobacteria decreased after gastric band surgery and increased after RYGB. An increase in the alpha-diversity pattern was observed after 3 months of surgery as well as the predominance of Bacteroidetes, which can improve the immune response to the host and increase the formation of biofilms and the restoration of the microflora balance. It is suggested that characterizing the microbial communities before surgery can help with clinical management.
Campisciano et al., 2018 ⁴4 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.	Discussion of data on the microbial composition of patients eligible for bariatric surgery considering the first line of treatment in cases of morbid obesity not responsive to diet and / or physical activity	20 obese patients, 10 VG and 10 RYGB 20 eutrophic patients for control Follow-up before and 3 months after surgery	The microbial composition was dominated by Bacteroidetes, Firmicutes and Proteobacteria despite the fact that Actinobacteria was also detected. In RYGB patients there was an increase in Proteobacteria and Prevotella as well as an improvement in the alpha-diversity pattern after 3 months of surgery, an interesting indirect marker to assess the effectiveness of surgical treatment in terms of restoring the function of the intestinal microflora. It was found that microorganisms adapt quickly to the situation of “hunger” induced by surgery
Dao, et al., 2019 ⁸8 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.	Quantify the relative abundance of A. muciniphila before and after 1 year of two types of bariatric surgery in relation to clinical outcomes	65 adult women with severe obesity 21 subjects were followed up before, 1, 3 and 12 months after surgery	The relative abundance of A.muciniphila was lower in severely obese patients when compared to moderate obesity. There was an increase in A. muciniphila after RYGB but not after gastric band. In the enterotype Rumminococcus the A. muciniphila it was significantly increased, in line with its greater richness profile, as well as in the enterotype Bacteroidetes 2, where low levels of A. muciniphila were found. There were no significant changes in the compositions of the enterotypes over time.
Ilhan, et al., 2017 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.	Determine microbial differences after RYGB and gastric band surgery; identify the production of metabolites that distinguish the surgeries; reveal relationships between microbiome and weight loss associated with bariatric surgery.	Follow-up of four groups: after RYGB (24), after VGB (14), healthy and eutrophic (10) and morbidly obese (15).	After RYGB surgery there was an increase in Gammaproteobacteria and Fusobacteria. It is suggested that obesity and surgery (RYGB) change the microbial structure and its functions, reflected by the metabolome and that these changes are due to changes in the anatomy of the GIT. The RYGB group had the highest concentration of butyrate and propionate and was not related to the diet.
Palleja, et al., 2016 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.	Investigate short and long-term changes in the composition of the microbiota and its functioning after intestinal rearrangement induced by RYGB and changes associated with body weight and metabolism	13 individuals with morbid obesity 5 men and 8 women Before, 3 months and 1 year after RYGB	The change to a healthier metabolism occurs in the first 3 months, when there was an increase in species richness after surgery and was maintained for 1 year. Gene richness tends to increase only after 1 year. Changes in the microbiota, in general, occur within 3 months and remain for up to 1 year. These changes may be related to changes in food preferences
Sánchez-Alcoholado, et al., 2019 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.Spain. Methods: We studied 28 patients with severe obesity; 14 underwent a Roux-en-Y gastric bypass (RYGB	Evaluate the short-term evolution of the intestinal microbiome after different bariatric surgery procedures and their functionality and relate it to the resolution of obesity.	28 morbidly obese patients who underwent bariatric surgery using VG or RYGB techniques Data collected before surgery and 3 months after	Just after 3 months of surgery did microbial profiles differ between surgical techniques. After BGYR there was an increase in Proteobacteria and Fusobacteria. It is suggested that pH and bile acid may be the key to the changes produced in the microbiota after bariatric surgery.
Tremaroli, et al., 2015 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.	Identify whether changes in the microbiota previously observed in the short term remain stable over time and whether RYGB and gastric band induced specific changes in the intestinal microbiome.	Three groups of women: 7 after 9 years of RYGB, 7 after 9 years of VGB and 7 with severe obesity (control)	There is a significant difference in the composition of the RYGB microbiota versus obese patients. After RYGB, there was an increase in the abundance of Proteobacteria. The bariatric surgery procedure produces a specific change in the microbiota that persists up to a decade after the surgery, being different from the changes related to dietary interventions for weight loss.

Authors	Objectives	Population	Main results found
Christensen, et al., 2019 ⁷7 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.	Specific effects of enterotypes analyzing individuals in a free consumption, with a diet rich in fiber and whole grains or with moderate consumption of fiber and refined wheat. Investigate whether the Prevotella enterotype is associated with other metabolic and intestinal health markers.	70 healthy and overweight adults. 6 weeks duration	Individuals with a high abundance of Prevotella lost weight with a diet rich in fiber and whole grains when compared to a diet based on refined grains and low in fiber. Among these, those with Bacteroidetes enterotype showed less fiber degradation than the dominant Prevotella subjects. This could explain the metabolic difference in response to a high fiber diet.
Hjorth, et al., 2019 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.	Reanalysis of a 24-week dietary intervention study for potential differences in the response to weight loss between an individual with low P/B ratio, high P/B and undetectable Prevotella.	80 overweight or obese individuals Deficit of 500kcal in the diet, being the composition of the macronutrients: 30% of lipids, 52% of carbohydrates, 18% of protein	Subjects with a low P/B ratio lost less fat and body weight. The 0-Prevotella group lost more weight. Those with a high P/B ratio were more likely to lose body weight when compared to a low P/B ratio specifically on a diet rich in fiber, carbohydrates, proteins and low fat. It was not possible to conclude whether the P/B ratio is related to different effects of the diet or to an unmeasured marker. The P/B ratio has been proven to be an important biomarker associated with weight loss with diet.
Hjorth, et al., 2020 ¹²12 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.	To investigate the interaction between diet, P/B ratio and human salivary amylase gene in weight change, in 26 weeks, as potential pre-treatment markers in personalized nutrition for obesity management	181 participants with increased abdominal circumference One group received a Nordic diet (rich in fiber, whole grains, fruits and vegetables) ad libitum, and the other a controlled diet (Danish diet, similar to the Western diet), for 26 weeks.	The Nordic diet, compared to the Danish diet, had more fiber, whole grains and proteins, less fat and added sugar. Human salivary amylase was not sufficient to predict weight loss between diets. Both participants with a low P/B ratio and those with a high P/B had the same mean of salivary amylase and the enterotypes were not modified. Exclusively among individuals with low salivary amylase and high P/B ratio, they lost more weight with the Nordic diet, while individuals with low P/B ratio lost more weight with the Danish diet.
Shin, et al., 2019 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....	Examine the effects of the standard Korean diet and the Western diet on the intestinal microbiota and metabolic profile of healthy Korean adults.	54 obese or overweight Korean participants, before and after 4 weeks of consumption of 3 different diets Typical Korean diet, typical Western (American) diet, recommended healthy American diet Each diet was administered for 4 weeks, with a 2-week intervals for washout.. All participants received the 3 diets.	The type of diet led to changes in microbial communities in relation to the usual diet. After the Korean diet, there was an increase in Firmicutes, a decrease in Bacteroidetes and an increase in the Firmicutes/Bacteroidetes ratio. Among the individuals, 22 belonged to the Bacteroidetes enterotype, 20 to Prevotella and 12 had a balanced relationship between Bacteroidetes and Prevotella. The Korean diet modified the abundance of the phylum Bacteroidetes and increased Firmicutes due to the high intake of carbohydrates and low animal protein. Diet responses were affected by enterotypes, suggesting that it may be a significant variable that contributes to modulating the microbiota.

Authors	Objectives	Population	Probiotic supplementation	Main results found
Song, et al., 2020 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.	To evaluate whether probiotics with multi strains improve markers related to obesity and to investigate different responses by microbial enterotype of the human intestine.	50 healthy obese 12 weeks of intervention, placebo and probiotic group, data collected every 3 weeks	B. breve CBT BR3 (15 million viable cells) and L. plantarum CBT LP3 (15 million viable cells)	There were no significant differences between groups at the phylum and family level. Anthropometric and biochemical changes were most notable in the Prevotella enterotype. Probiotics may have a beneficial effect on obese individuals with Prevotella enterotype.

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[1] Correspondence: Giúlia Jager Maximowicz de-Oliveira E-mail: giulia_max@hotmail.com; meliana@ufpr.br