Comment on: Duodenal diverted sleeve gastrectomy with ileal interposition does not cause biliary salt malabsorption

Abstract

Since the introduction of the biliopancreatic diversion with duodenal switch in the late 1980s [ [1] Marceau P. Biron S. Hould F.S. et al. Duodenal switch improved standard biliopancreatic diversion: a retrospective study. Surg Obes Relat Dis. 2009; 5: 43-47 Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar ], there has been a constant search to retain the efficacy of the original biliopancreatic diversion (BPD) as a weight loss and metabolic procedure, while reducing typical side effects, such as frequent and loose stools, flatus, and protein loss. These side effects are directly related to malabsorption, the consequence of a shorter functional small bowel, as well as reduced bile salt reabsorption. In 1990, a comparison between the jejunoileal bypass and the biliointestinal-Eriksson procedure demonstrated a reduction in the postoperative loss of bile acids and choleretic diarrhea without an effect on weight loss [ [2] Nyhlin H. Brydon G. Danielsson A. Eriksson F. Bile acid malabsorption after intestinal bypass surgery for obesity. A comparison between jejunoileal shunt and biliointestinal bypass. Int J Obes. 1990; 14: 47-55 PubMed Google Scholar ]. Recent studies on irritable bowel syndrome (IBS) and chronic diarrhea have outlined the role of gut peptide fibroblast growth factor 19 (FGF19), a hormone produced by the ileum, which normally provides feedback inhibition of bile acid synthesis [ 3 Camilleri M. Advances in understanding of bile acid diarrhea. Expert Rev Gastroenterol Hepatol. 2014; 8: 49-61 Crossref PubMed Scopus (59) Google Scholar , 4 Walters J.R. Bile acid diarrhea and FGF19: new views on diagnosis, pathogenesis and therapy. Nat Rev Gastroenterol Hepatol. 2014; 11: 426-434 Crossref PubMed Scopus (74) Google Scholar ]. This feedback results in a decrease in the serum level of 7 α-hydroxy-4-cholesten-3-one (C4). Thus, for any reason that reduces bile salt reabsorption by the intestinal mucosa (cholestyramine sequestrants, insufficient reabsorption by the intestine), FGF19 production decreases leading to bile acid synthesis and increased C4 serum levels. This finding might explain the frequent diarrhea observed after malabsorptive procedures, such as BPD, a situation similar to that of irritable bowel syndrome, at least with regard to its symptoms. In IBS, patients identified with increased bile acid excretion in feces also had more fecal fat and borderline increased colonic permeability [ [5] Camilleri M. Busciglio I. Acosta A. et al. Effect of increased bile acid synthesis or fecal excretion in irritable bowel syndrome-diarrhea. Am J Gastroenterol. 2014; 109: 1621-1630 Crossref PubMed Scopus (71) Google Scholar ]. However, although C4 is a surrogate for bile acid synthesis, bile acid diarrhea is identified more effectively with total fecal bile acids than with serum C4. Because the authors hypothesized that the 50-cm terminal ileum is able to reabsorb sufficient bile acids to avoid malabsorption, it is difficult to understand why current malabsorptive procedures, such as the BPD, which features a 100-cm terminal ileum common channel, could also not reabsorb adequately. Indeed, in the study, 2 out of 12 patients exhibited malabsorption, where one of the patients had normal C4 levels; this finding suggests that other phenomena may play a role in leading to malabsorption side effects after a small bowel short-circuit. A recent study [ [6] Carswell K.A. Vincent R.P. Belgaumkar A.P. et al. The effect of bariatric surgery on intestinal absorption and transit time. Obes Surg. 2014; 24: 796-805 Crossref PubMed Scopus (78) Google Scholar ] has shown that fat excretion was increased after biliopancreatic diversion with duodenal switch (BPD-DS) compared to Roux-en-Y gastric bypass (RYGB), as well as purely restrictive procedures and nonoperated obese individuals. In addition, increased intestinal permeability was found after BPD-DS. Moreover, in the same study, no differences were found regarding transit time and the absence of effect on plasma citrulline levels, which suggested that a portion of intestinal adaptation developed over time, not only after RYGB but also after BPD-DS. In addition to IBS, bile acid metabolism is altered in type 2 diabetes mellitus (T2 DM) patients [ [7] Prawitt J. Caron S. Staels B. Bile acid metabolism and the pathogenesis of type 2 diabetes. Curr Diab Rep. 2011; 11: 160-166 Crossref PubMed Scopus (169) Google Scholar ], and the FGF19 pathway has been implicated in the etiology of T2 DM and its remission after RYGB [ 8 Gerhard G.S. Styer A.M. Wood G.C. et al. A role for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care. 2013; 36: 1859-1864 Crossref PubMed Scopus (163) Google Scholar , 9 Stanley S. Buettner C. FGF19: How gut talks to brain to keep your sugar down. Mol Metab. 2013; 3: 3-4 Abstract Full Text Full Text PDF Scopus (5) Google Scholar ]. Serum FGF19 and bile acids are significantly increased after RYGB in diabetic patients with remission of diabetes compared to the preoperative values. The same observation was also found to a lesser extend after RYGB in nondiabetic patients [ [10] De Giorgi S. Campos V. Egli L. et al. Long-term effects of Roux-en-Y gastric bypass on postprandial plasma lipid and bile acids kinetics in female non diabetic subjects: A cross-sectional pilot study. Clin Nutr. 2014; (In Press) PubMed Google Scholar ]. The authors once again have shown that FGF19 plays an important role in T2 DM remission after metabolic surgery and appears to be one of the mechanisms that several, if not, all bariatric procedures utilize. The only malabsorptive procedure in which C4 serum levels were assessed is the biliointestinal bypass, and C4 serum levels were increased compared to adjustable gastric banding [ [11] Benetti A. Del Puppo M. Crosignani A. et al. Cholesterol metabolism after bariatric surgery in grade 3 obesity: differences between malabsorptive and restrictive procedures. Diabetes Care. 2013; 36: 1443-1447 Crossref PubMed Scopus (54) Google Scholar ]. Although a relationship exists between FGF19 and C4 levels, C4 and FGF19 expression was not examined following RYGB and malabsorptive biliointestinal bypass, respectively [ 8 Gerhard G.S. Styer A.M. Wood G.C. et al. A role for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care. 2013; 36: 1859-1864 Crossref PubMed Scopus (163) Google Scholar , 11 Benetti A. Del Puppo M. Crosignani A. et al. Cholesterol metabolism after bariatric surgery in grade 3 obesity: differences between malabsorptive and restrictive procedures. Diabetes Care. 2013; 36: 1443-1447 Crossref PubMed Scopus (54) Google Scholar ]. Moreover, there is no known report on BPD or BPD-DS on FGF19 or C4 levels. Although BPD yields malabsorption, its true mechanism on weight loss and diabetes might not be related to malabsorption but to the hormonal consequences of early stimulation of the terminal ileum and cecum, suggesting the importance of ileal transposition [ 12 Buchwald H. Dorman R.B. Rasmus N.F. Michalek V.N. Landvik N.M. Ikramuddin S. Effects on GLP-1, PYY, and leptin by direct stimulation of terminal ileum and cecum in humans: implications for ileal transposition. Surg Obes Relat Dis. 2014; (In Press) Google Scholar , 13 Santoro S. Castro L.C. Velhote M.C. et al. Sleeve gastrectomy with transit bipartition: a potent intervention for metabolic syndrome and obesity. Ann Surg. 2012; 256: 104-110 Crossref PubMed Scopus (82) Google Scholar ]. Interestingly, ileal interposition with diverted sleeve gastrectomy (II-DSG) studied by Foschi et al. does indicate a small bowel short-circuit unlike the ileal interposition with sleeve gastrectomy (II-SG) [ [14] DePaula A.L. Macedo A.L. Rassi N. Laparoscopic treatment of metabolic syndrome in patients with type 2 diabetes mellitus. Surg Endosc. 2008; 22: 2670-2678 Crossref PubMed Scopus (57) Google Scholar ]. Finally, the authors present a complex procedure somewhere between a RYGB and BPD-DS [ [15] Gagner M. Surgical treatment of nonseverely obese patients with type 2 diabetes mellitus: sleeve gastrectomy with ileal transposition (SGIT) is the same as the neuroendocrine brake (NEB) procedure or ileal interposition associated with sleeve gastrectomy (II-SG), but ileal interposition with diverted sleeve gastrectomy (II-DSG) is the same as duodenal switch. Surg Endosc. 2011; 25: 655-656 Crossref PubMed Scopus (8) Google Scholar ]. However, it is difficult to define the respective roles of the sleeve gastrectomy and ileal interposition clearly because both lead to increased GLP1 secretion [ 16 Yousseif A. Emmanuel J. Karra E. et al. Differential effects of laparoscopic sleeve gastrectomy and laparoscopic gastric bypass on appetite, circulating acyl-ghrelin, peptide YY3-36 and active GLP-1 levels in non-diabetic humans. Obes Surg. 2014; 24: 241-252 Crossref PubMed Scopus (177) Google Scholar , 17 Gaitonde S. Kohli R. Seeley R. The role of the gut hormone GLP-1 in the metabolic improvements caused by ileal transposition. J Surg Res. 2012; 178: 33-39 Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar , 18 Mason E.E. Ileal [correction of ilial] transposition and enteroglucagon/GLP-1 in obesity (and diabetic?) surgery. Obes Surg. 1999; 9: 223-228 Crossref PubMed Scopus (135) Google Scholar , 19 Nausheen S. Shah I.H. Pezeshki A. Sigalet D.L. Chelikani P.K. Effects of sleeve gastrectomy and ileal transposition, alone and in combination, on food intake, body weight, gut hormones, and glucose metabolism in rats. Am J Physiol Endocrinol Metab. 2013; 305: E507-E518 Crossref PubMed Scopus (46) Google Scholar ]. The rationale on which their variable length of interposed ileum is based is consistent with a recent animal study performed by Ramzy [ [20] Ramzy A.R. Nausheen S. Chelikani P.K. Ileal transposition surgery produces ileal length-dependent changes in food intake, body weight, gut hormones and glucose metabolism in rats. Int J Obes (Lond). 2014; 38: 379-387 Crossref PubMed Scopus (30) Google Scholar ], which demonstrates that reduction in food intake and weight gain, increase in lower gut hormones, glycemic improvements, and associated changes in tissue metabolic markers following surgery are dependent on the length of the transposed ileum. In their study, Foschi et al. did not measure the fecal excretion of bile acids and fat, which are typically the sign of malabsorption. Thus, it is impossible to conclude that II-DSG is not a malabsorptive procedure, particularly when considering the small bowel short-circuit and the clinical results reported by the authors. There is most likely no single pathway to explain T2 DM improvement and weight loss maintenance after bariatric surgery. Chronic lipid malabsorption has been demonstrated to be the primary metabolic abnormality explaining the achievement of energy balance in postobese patients after BPD and plays a key role in long-term weight stability [ 21 Tataranni P.A. Mingrone G. Raguso C.A. et al. Twenty-four-hour energy and nutrient balance in weight stable postobese patients after biliopancreatic diversion. Nutrition. 1996; 12: 239-244 Abstract Full Text PDF PubMed Scopus (37) Google Scholar , 22 Scopinaro N. Thirty-five years of biliopancreatic diversion: notes on gastrointestinal physiology to complete the published information useful for a better understanding and clinical use of the operation. Obes Surg. 2012; 22: 427-432 Crossref PubMed Scopus (44) Google Scholar ]. Thus, a comparison between II-DSG and BPD-DS regarding fat malabsorption would be important because II-DSG is an even more complex procedure to perform. Alternatively, II-SG, a less complex procedure without the bowel short-circuit, could provide T2 DM control without any malabsorption but with more questionable weight control over time. Duodenal diverted sleeve gastrectomy with ileal interposition does not cause biliary salt malabsorptionSurgery for Obesity and Related DiseasesVol. 11Issue 2PreviewDuodenal diverted sleeve gastrectomy with ileal interposition (DDSG-II) is a bariatric-metabolic operation designed to treat type 2 diabetes mellitus (T2DM). It is restrictive (SG) but also acts on the small bowel with functional effects. The objective of the present study was to investigate whether or not it is also a malabsorptive operation. Full-Text PDF