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Increased Adiposity and Reduced Lean Body Mass in Patients with Short Bowel Syndrome

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Abstract

Background

Few studies have examined the metabolic consequences of short bowel syndrome (SBS) and its effects on body composition in adults. We hypothesized that body composition of SBS patients is altered compared to a normal age-, race-, and sex-matched population, regardless of parenteral nutrition (PN) dependence.

Aim

To compare the body composition of adult patients with SBS to age-, sex-, and race-matched healthy controls.

Methods

Twenty patients with SBS underwent body composition analysis using the GE Lunar iDXA scanner. Patients were age-, sex-, and race-matched to controls from the National Health and Nutrition Examination Survey (1999–2004). Mean differences in body mass index, fat-free mass, fat mass, percent body fat, visceral adipose tissue mass and volume, and bone mineral density were measured. Statistical analysis was performed using SAS 9.4 software.

Results

Fifty-five percent of subjects had a history of PN use, and 30% were current PN users. Mean percent body fat for SBS patients was 35.1% compared to 30.9% for healthy controls (p = 0.043). Fat-free mass was reduced in SBS (p = 0.007). Patients with reduced bone mass had a trend toward significantly more years of PN exposure compared to those with normal bone mass (p = 0.094), and a trend toward older age (p = 0.075).

Conclusions

SBS is associated with increased percent body fat and reduced fat-free mass, suggesting that improved dietary and therapeutic interventions are needed to restore normal metabolic indices and avoid risk of metabolic syndrome in SBS patients.

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Abbreviations

SBS:

Short bowel syndrome

PN:

Parenteral nutrition

NHANES:

National Health and Nutrition Examination Survey

DXA:

Dual-energy X-ray absorptiometry

BIA:

Bioelectric impedance analysis

FFM:

Fat-free mass

FM:

Fat mass

%BF:

% body fat

VFM:

Visceral adipose fat mass

VFV:

Visceral adipose fat volume

BMD:

Bone mineral density

NDSR:

Nutrition data system research

VAT:

Visceral adipose tissue

References

  1. Billiauws L, Maggiori L, Joly F, Panis Y. Medical and surgical management of short bowel syndrome. J Visc Surg. 2018;155:283–291.

    Article  CAS  Google Scholar 

  2. Boutte HJ, Rubin DC. Short bowel syndrome. In: Bardan E, Shaker R, eds. Gastrointestinal Motility Disorders: A Point-of-Care Clinical Guide. Springer; 2018:343–351.

  3. Levin MS, Rubin DC. Intestinal adaptation. In: Langnas AN, Goulet O, Quigley EM, Tappenden KA, eds. Intestinal Failure. Oxford: Blackwell Publishing; 2008:45–56.

    Chapter  Google Scholar 

  4. Wang Y, Iordanov H, Swietlicki EA, et al. Targeted intestinal overexpression of the immediate early gene tis7 in transgenic mice increases triglyceride absorption and adiposity. J Biol Chem. 2005;280:34764–34775.

    Article  CAS  Google Scholar 

  5. Tantemsapya N, Meinzner-Derr J, Erwin CR, Warner BW. Body composition and metabolic changes associated with massive intestinal resection in mice. J Pediatr Surg. 2008;43:14–19.

    Article  Google Scholar 

  6. Barron L, Courtney C, Bao J, et al. Intestinal resection-associated metabolic syndrome. J Pediatr Surg. 2018;53:1142–1147.

    Article  Google Scholar 

  7. Pichler J, Chomtho S, Fewtrell M, Macdonald S, Hill S. Body composition in paediatric intestinal failure patients receiving long-term parenteral nutrition. Arch Dis Child. 2014;99:147–153.

    Article  Google Scholar 

  8. Engelstad HJ, Barron L, Moen J, et al. Remnant small bowel length in pediatric short bowel syndrome and the correlation with intestinal dysbiosis and linear growth. J Am Coll Surg. 2018;227:439–449.

    Article  Google Scholar 

  9. Carlsson E, Bosaeus I, Nordgren S. Body composition in patients with short bowel syndrome: an assessment by bioelectric impedance spectroscopy (BIS) and dual-energy absorptiometry (DXA). Eur J Clin Nutr. 2004;58:853–859.

    Article  CAS  Google Scholar 

  10. Carlsson E, Bosaeus I, Nordgren S. Body composition in patients with an ileostomy and inflammatory bowel disease: validation of bio-electric impedance spectroscopy (BIS). Eur J Clin Nutr. 2002;56:680–686.

    Article  CAS  Google Scholar 

  11. Tjellesen L, Staun M, Nielsen PK. Body composition changes measured by dual-energy X-ray absorptiometry in patients receiving home parenteral nutrition. Scand J Gastroenterol. 1997;32:686–690.

    Article  CAS  Google Scholar 

  12. Skallerup A, Nygaard L, Olesen SS, Kohler M, Vinter-Jensen L, Rasmussen HH. The prevalence of sarcopenia is markedly increased in patients with intestinal failure and associates with several risk factors. Clin Nutr (Edinburgh, Scotland). 2018;37:2029–2035.

    Article  Google Scholar 

  13. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey, 2018. Available at: https://www.cdc.gov/nchs/nhanes/index.htm. Accessed August 6, 2018.

  14. Li CY, Ford ES, Zhao GX, Balluz LS, Giles WH. Estimates of body composition with dual-energy X-ray absorptiometry in adults. Am J Clin Nutr. 2009;90:1457–1465.

    Article  CAS  Google Scholar 

  15. Frivolt K, Hetterich H, Schwerd T, et al. Increase of intra-abdominal adipose tissue in pediatric Crohn disease. J Pediatr Gastroenterol Nutr. 2017;65:633–638.

    Article  CAS  Google Scholar 

  16. Bryant RV, Schultz CG, Ooi S, et al. Visceral adipose tissue is associated with stricturing Crohn’s disease behavior, fecal calprotectin, and quality of life. Inflamm Bowel Dis. 2019;25:592–600.

    Article  Google Scholar 

  17. Marchix J, Goddard G, Helmrath MA. Host-gut microbiota crosstalk in intestinal adaptation. Cell Mol Gastroenterol Hepatol. 2018;6:149–162.

    Article  Google Scholar 

  18. Kliewer KL, Ke JY, Lee HY, et al. Short-term food restriction followed by controlled refeeding promotes gorging behavior, enhances fat deposition, and diminishes insulin sensitivity in mice. J Nutr Biochem. 2015;26:721–728.

    Article  CAS  Google Scholar 

  19. Haas V, Kent D, Kohn MR, et al. Incomplete total body protein recovery in adolescent patients with anorexia nervosa. Am J Clin Nutr. 2018;107:303–312.

    Article  Google Scholar 

  20. El Ghoch M, Calugi S, Lamburghini S, Dalle GR. Anorexia nervosa and body fat distribution: a systematic review. Nutrients. 2014;6:3895–3912.

    Article  Google Scholar 

  21. Mayer L, Walsh BT, Pierson RN, et al. Body fat redistribution after weight gain in women with anorexia nervosa. Am J Clin Nutr. 2005;81:1286–1291.

    Article  CAS  Google Scholar 

  22. Dulloo AG, Jacquet J, Girardier L. Poststarvation hyperphagia and body fat overshooting in humans: a role for feedback signals from lean and fat tissues. Am J Clin Nutr. 1997;65:717–723.

    Article  CAS  Google Scholar 

  23. Shaw K, Gennat H, O’Rourke P, Del Mar C. Exercise for overweight or obesity. Cochrane Database Syst Rev. 2006;4:CD003817.

    Google Scholar 

  24. Ohkawara K, Tanaka S, Miyachi M, Ishikawa-Takata K, Tabata I. A dose-response relation between aerobic exercise and visceral fat reduction: systematic review of clinical trials. Int J Obes. 2005;2007:1786–1797.

    Google Scholar 

  25. Verheggen RJ, Maessen MF, Green DJ, Hermus AR, Hopman MT, Thijssen DH. A systematic review and meta-analysis on the effects of exercise training versus hypocaloric diet: distinct effects on body weight and visceral adipose tissue. Obes Rev. 2016;17:664–690.

    Article  CAS  Google Scholar 

  26. Chin SH, Kahathuduwa CN, Binks M. Physical activity and obesity: what we know and what we need to know. Obes Rev. 2016;17:1226–1244.

    Article  Google Scholar 

  27. Shook RP. Obesity and energy balance: what is the role of physical activity? Expert Rev Endocrinol Metab. 2016;11:511–520.

    Article  CAS  Google Scholar 

  28. Kalaitzakis E, Carlsson E, Josefsson A, Bosaeus I. Quality of life in short-bowel syndrome: impact of fatigue and gastrointestinal symptoms. Scand J Gastroenterol. 2008;43:1057–1065.

    Article  Google Scholar 

  29. Royall D, Greenberg GR, Allard JP, Baker JP, Harrison JE, Jeejeebhoy KN. Critical assessment of body-composition measurements in malnourished subjects with Crohn’s disease: the role of bioelectric impedance analysis. Am J Clin Nutr. 1994;59:325–330.

    Article  CAS  Google Scholar 

  30. Tjellesen L, Nielsen PK, Staun M. Body composition by dual-energy X-ray absorptiometry in patients with Crohn’s disease. Scand J Gastroenterol. 1998;33:956–960.

    Article  CAS  Google Scholar 

  31. Frank AP, de Souza Santos R, Palmer BF, Clegg DJ. Determinants of body fat distribution in humans may provide insight about obesity-related health risks. J Lipid Res. 2018;60:1710–1719.

    Article  Google Scholar 

  32. Zong G, Zhang Z, Yang Q, Wu H, Hu FB, Sun Q. Total and regional adiposity measured by dual-energy X-ray absorptiometry and mortality in NHANES 1999–2006. Obesity (Silver Spring). 2016;24:2414–2421.

    Article  CAS  Google Scholar 

  33. Barreira TV, Staiano AE, Harrington DM, et al. Anthropometric correlates of total body fat, abdominal adiposity, and cardiovascular disease risk factors in a biracial sample of men and women. Mayo Clin Proc. 2012;87:452–460.

    Article  Google Scholar 

  34. Bi X, Seabolt L, Shibao C, et al. DXA-measured visceral adipose tissue predicts impaired glucose tolerance and metabolic syndrome in obese Caucasian and African–American women. Eur J Clin Nutr. 2015;69:329–336.

    Article  CAS  Google Scholar 

  35. Rothney MP, Catapano AL, Xia J, et al. Abdominal visceral fat measurement using dual-energy X-ray: association with cardiometabolic risk factors. Obesity (Silver Spring). 2013;21:1798–1802.

    Article  Google Scholar 

  36. Jeppesen PB, Mortensen PB. The influence of a preserved colon on the absorption of medium chain fat in patients with small bowel resection. Gut. 1998;43:478–483.

    Article  CAS  Google Scholar 

  37. Pironi L, Joly F, Forbes A, et al. Long-term follow-up of patients on home parenteral nutrition in Europe: implications for intestinal transplantation. Gut. 2011;60:17–25.

    Article  Google Scholar 

Download references

Acknowledgments

These studies were supported by NIH NIDDK R01 DK112378 (DCR, NOD, MSL, BWW), NIH NIDDK R01 DK106382 (DCR, MSL), and the Digestive Diseases Research Core Center at Washington University School of Medicine NIDDK P30 DK52574 (NOD, DCR) and the Biobank Core. We thank Kelly Monroe, Latoya Evans, Darren Nix, and Rodney Newberry for their support in the Biobank Core.

Author information

Authors and Affiliations

  1. Division of Gastroenterology, Department of Medicine, Washington University School of Medicine, 660 S. Euclid Avenue, Campus Box 8124, St. Louis, MO, 63110, USA

    Adeeti J. Chiplunker, Marc S. Levin, Nicholas O. Davidson & Deborah C. Rubin

  2. Division of Biostatistics, Washington University School of Medicine, 660 S. Euclid Ave, Campus Box 8067, St. Louis, MO, 63110, USA

    Ling Chen

  3. VA St. Louis Health Care System, 915 N. Grand Blvd, St. Louis, MO, 63106, USA

    Marc S. Levin

  4. Division of Pediatric Surgery, St. Louis Children’s Hospital, One Children’s Place, Suite 6110, St. Louis, MO, 63110, USA

    Brad W. Warner

  5. Department of Developmental Biology, Washington University School of Medicine, 660 S. Euclid Ave, St. Louis, MO, 63110, USA

    Nicholas O. Davidson & Deborah C. Rubin

  6. William B Kountz Professor of Medicine, Division of Gastroenterology, Washington University School of Medicine, 660 S. Euclid Avenue, Campus Box 8124, St. Louis, MO, 63110, USA

    Deborah C. Rubin

Authors
  1. Adeeti J. Chiplunker
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Corresponding author

Correspondence to Deborah C. Rubin.

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Conflict of interest

Research grant funding was utilized in the conduct of the research including study coordinator staff, body composition analysis, and statistical analysis at Washington University School of Medicine. The authors received no financial assistance with regard to manuscript preparation. All authors have no other financial disclosures.

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

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10620_2019_6032_MOESM1_ESM.tif

Supplemental Figure 1: Correlation of duration of disease, length of remaining small bowel, and duration of PN therapy with body composition. Panels A–C: Correlation of the duration of short bowel syndrome with (A) fat mass, (B) fat-free mass, and (C) visceral fat mass. Panels D–F: Correlation of the length of remaining small bowel versus (D) fat mass, (E) fat-free mass, and (F) visceral fat mass. Panels G–I: Correlation of duration of parenteral nutrition and (G) fat mass, (H) fat-free mass, and (I) visceral fat mass. (TIFF 537 kb)

10620_2019_6032_MOESM2_ESM.tif

Supplemental Figure 2: Correlation of dietary composition (total caloric intake and percentage of calories from fat or carbohydrate) with BMI and fat mass. Panels A–B: Correlation of the percent calories obtained from fat with (A) BMI and (B) fat mass. Panels C–D: Correlation of the percent calories obtained from carbohydrates with (C) BMI and (D) fat mass. Panels E–F: Correlation of total caloric intake versus (E) BMI and (F) fat mass. (TIFF 269 kb)

Supplementary material 3 (DOCX 25 kb)

Supplementary material 4 (DOCX 13 kb)

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Chiplunker, A.J., Chen, L., Levin, M.S. et al. Increased Adiposity and Reduced Lean Body Mass in Patients with Short Bowel Syndrome. Dig Dis Sci 65, 3271–3279 (2020). https://doi.org/10.1007/s10620-019-06032-4

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