Skip to main content

Advertisement

SpringerLink
Log in

Modulation of the Gut Microbiota and Serum Biomarkers After Laparoscopic Sleeve Gastrectomy: a 1-Year Follow-Up Study

  • Original Contributions
  • Published:
Obesity Surgery Aims and scope Submit manuscript

Abstract

Purpose

Bariatric surgery is a treatment option for those affected by severe obesity. This study investigated changes in gut microbiota and serum biomarkers after laparoscopic sleeve gastrectomy (LSG).

Materials and Methods

A total of 126 patients with morbid obesity who underwent LSG were enrolled in this study. Routine biochemical tests, hormonal (insulin and glucagon), and cytokine levels (IL-6, IL-1β, TNF-α, IL-10, and TGF–β 1) were measured, in addition, real-time PCR (quantitative PCR, qPCR) quantitated gut microbiota. All the parameters were measured pre-operatively, 3, and 12 months post-surgery (F0, F3, and F12, respectively).

Results

At F3, the level of FBS, HbA1c, HOMA-IR, triglyceride, cholesterol, LDL, BUN, creatinine, urea, SGOT, SGPT, IL-1β, IL-6, IFNγ, insulin, glucagon, the abundance of Prevotella and Bacteroides fragilis group, as well as the concentration of Firmicutes spp. showed significant decrease (P < 0.01), and HDL level, Akkermansia muciniphila and Roseburia spp. abundance, and Bacteroidetes and Bifidobacterium spp. concentration showed significant increase (P < 0.0001). The observed pattern continued or remained stable at F12 for all of these variables. IL-10 and TGF-β1 remained unchanged until F3 and showed a significant drop at F12. At F3, Clostridium cluster IV increased significantly and remained at that level afterward. Moreover, concentration of Phylum Actinobacteria showed an initial drop at F3 and a later increase at F12 (P < 0.0001).

Conclusion

LSG is associated with a significant improvement in serum biomarkers, as well as significant changes in fecal microbiota. Future systems biology analyses would shed more light on the underlying interactions of these parameters, and could help in developing novel diagnostic and therapeutic strategies for obesity management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability

All data generated or analyzed in this study are included in the present article.

References

  1. Chooi YC, Ding C, Magkos F. The epidemiology of obesity. Metabolism. 2019;92:6–10.

    Article  CAS  Google Scholar 

  2. Sivamaruthi BS, Kesika P, Suganthy N, et al. A review on role of microbiome in obesity and antiobesity properties of probiotic supplements. Biomed Res Int. 2019;2019:1–20.

    Article  Google Scholar 

  3. Organization WH. Obesity and overweight. Fact sheet no. 311. Updated January 2015. World Health Organization [Cited: 2015 November 20] Available from: http://www.who.int/mediacentre/factsheets/fs311/en 2015.

  4. Hruby A, Hu FB. The epidemiology of obesity: a big picture. Pharmacoeconomics. 2015;33(7):673–89.

    Article  Google Scholar 

  5. Hady HR, Olszewska M, Czerniawski M, Groth D, Diemieszczyk I, Pawluszewicz P, Kretowski A, Ladny JR, Dadan J. Different surgical approaches in laparoscopic sleeve gastrectomy and their influence on metabolic syndrome: a retrospective study. Medicine. 2018;97(4).

  6. Tabasi M, Ashrafian F, Khezerloo JK, et al. Changes in gut microbiota and hormones after bariatric surgery: a bench-to-bedside review. Obes Surg. 2019;29(5):1663–74.

    Article  Google Scholar 

  7. Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends in Endocrinology & Metabolism. 2015;26(9):493–501.

    Article  CAS  Google Scholar 

  8. Rajoka MSR, Shi J, Mehwish HM, et al. Interaction between diet composition and gut microbiota and its impact on gastrointestinal tract health. Food Sci Human Wellness. 2017;6(3):121–30.

    Article  Google Scholar 

  9. Graessler J, Qin Y, Zhong H, et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. The pharmacogenomics journal. 2013;13(6):514–22.

    Article  CAS  Google Scholar 

  10. Magouliotis DE, Tasiopoulou VS, Sioka E, et al. Impact of bariatric surgery on metabolic and gut microbiota profile: a systematic review and meta-analysis. Obes Surg. 2017;27(5):1345–57.

    Article  Google Scholar 

  11. Hasan N, Yang H. Factors affecting the composition of the gut microbiota, and its modulation. PeerJ. 2019;7:e7502.

    Article  Google Scholar 

  12. Owen-Smith A, Kipping R, Donovan J, et al. A NICE example? Variation in provision of bariatric surgery in England. Bmj. 2013;346:f2453.

    Article  Google Scholar 

  13. Bergström A, Licht TR, Wilcks A, et al. Introducing GUt low-density array (GULDA)–a validated approach for qPCR-based intestinal microbial community analysis. FEMS Microbiol Lett. 2012;337(1):38–47.

    Article  Google Scholar 

  14. Matsuki T, Watanabe K, Fujimoto J, et al. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70(12):7220–8.

    Article  CAS  Google Scholar 

  15. Hermann-Bank ML, Skovgaard K, Stockmarr A, et al. The gut microbiota assay: a high-throughput qPCR approach combinable with next generation sequencing to study gut microbial diversity. BMC Genomics. 2013;14(1):788.

    Article  Google Scholar 

  16. Koliada A, Syzenko G, Moseiko V, et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17(1):120.

    Article  Google Scholar 

  17. Queipo-Ortuño MI, Seoane LM, Murri M, et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One. 2013;8(5):e65465.

    Article  Google Scholar 

  18. Schelbert KB. Comorbidities of obesity. Prim Care. 2009;36(2):271–85.

    Article  Google Scholar 

  19. Webber J. The comorbidities of obesity. Practical Diabetes International. 2001;18(8):293–6.

    Article  Google Scholar 

  20. Ruiz-Tovar J, Oller I, Priego P, et al. Short-and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23(7):861–6.

    Article  Google Scholar 

  21. Mihmanli M, Isil RG, Isil CT, et al. Effects of laparoscopic sleeve gastrectomy on parathyroid hormone, vitamin D, calcium, phosphorus, and albumin levels. Obes Surg. 2017;27(12):3149–55.

    Article  Google Scholar 

  22. Anhê FF, Varin TV, Schertzer JD, et al. The gut microbiota as a mediator of metabolic benefits after bariatric surgery. Can J Diabetes. 2017;41(4):439–47.

    Article  Google Scholar 

  23. Johnson EL, Heaver SL, Walters WA, et al. Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes. J Mol Med. 2017;95(1):1–8.

    Article  CAS  Google Scholar 

  24. Reyed M. The role of bifidobacteria in health. Res J Med Med Sci. 2007;2(1):14–24.

    Google Scholar 

  25. Schneeberger M, Everard A, Gómez-Valadés AG, et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5:16643.

    Article  CAS  Google Scholar 

  26. Tamanai-Shacoori Z, Smida I, Bousarghin L, et al. Roseburia spp.: a marker of health? Future Microbiol. 2017;12(2):157–70.

    Article  CAS  Google Scholar 

  27. Koliada A, Syzenko G, Moseiko V, et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17(1):1–6.

    Article  Google Scholar 

  28. Miranda VP, dos Santos Amorim PR, Bastos RR, de Faria ER, de Castro Moreira ME, do Carmo Castro Franceschini S, do Carmo Gouveia Peluzio M, de Luces Fortes Ferreira CL, Priore SE. Abundance of gut microbiota, concentration of short-Chain fatty acids, and inflammatory markers associated with elevated body fat, overweight, and obesity in female adolescents. Mediators of Inflammation. 2019.

Download references

Acknowledgments

This article was part of the project conducted by Mohsen Tabasi to fulfill the requirement for a Ph.D. degree. We would like to express our gratitude to the Pasteur Institute of Iran and Legal Medicine Research Center for providing financial support. We also would like to express our appreciation to Dr. Nader Shahrokhi, Dr. Sara Ahmadi Badi, Mr. Milad Kheirvari, Mr. Mohammad Reza Yazdannasab, and staff in Shariati Hospital of Tehran, Iran for their technical assistance.

Funding

This project was financially supported by the Pasteur Institute of Iran (grant no. TP-9567).

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Pasteur Institute of Iran, Pasteur Ave., Tehran, 13164, Iran

    Mohsen Tabasi & Saeid Bouzari

  2. Legal Medicine Research Center, Legal Medicine Organization, Tehran, Iran

    Mohsen Tabasi

  3. Department of Epidemiology and Biostatistics, Research Centre for Emerging and Reemerging Infectious Diseases, Pasteur Institute of Iran, Tehran, Iran

    Sana Eybpoosh

  4. Department of Mycobacteriology and Pulmonary Research, Microbiology Research Center, Pasteur Institute of Iran, Tehran, Iran

    Seyed Davar Siadat

  5. Department of Surgery, Tehran University of Medical Sciences, Tehran, Iran

    Fezzeh Elyasinia

  6. Obesity and Eating Habits Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, 5th Floor, Shariati Hospital, North Kargar Ave, Tehran, 1411413137, Iran

    Ahmadreza Soroush

  7. Department of Molecular Biology, Pasteur Institute of Iran (IPI), Pasteur Ave., Tehran, 1316943551, Iran

    Saeid Bouzari

Authors
  1. Mohsen Tabasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sana Eybpoosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seyed Davar Siadat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fezzeh Elyasinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ahmadreza Soroush
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Saeid Bouzari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MT and SE design the study and data analysis. SDS and FE data: collecting and writing paper. ARS and SB: conceptualization, investigation, formal analysis, writing-review and editing. All co-authors commented on the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Ahmadreza Soroush or Saeid Bouzari.

Ethics declarations

Ethics Approval and Consent to Participate

This study was conducted in accordance with the principles of the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All the participants were thoroughly informed about the study and procedures before signing consent forms. Participants were assured of anonymity and confidentiality. The Research Ethics Committee of the Pasteur Institute of Iran, Tehran, approved this study (IR.PII. REC.1397.029).

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tabasi, M., Eybpoosh, S., Siadat, S.D. et al. Modulation of the Gut Microbiota and Serum Biomarkers After Laparoscopic Sleeve Gastrectomy: a 1-Year Follow-Up Study. OBES SURG 31, 1949–1956 (2021). https://doi.org/10.1007/s11695-020-05139-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11695-020-05139-2

Keywords

Search

Navigation