https://orcid.org/0000-0002-3808-548X
Abstract
This study was designed to assess the glycemic control after sleeve gastrectomy surgeries in overweight and obese patients with T2DM as well as the associated factors that may affect glycemic control in those patients. We conducted a retrospective study based on retrieving the required information from patient's files in Medical Records Departments for type II diabetic overweight and obese patients who underwent laparoscopic sleeve gastrectomy (LSG), in Taif, from January 2017 to December 2019. The follow-up duration for all patient was three-to-six months postoperatively. We found that LSG achieved a significant glycemic control in overweight and obese patients with T2DM. Preoperatively, mean ± SD fasting blood glucose, random blood glucose and hemoglobin A1C were 160.7 ± 65.6 mg/dL, 237.4 ± 66.9 mg/dL and 8.4 ± 1.5%, respectively. Postoperatively, mean ± SD fasting blood glucose, random blood glucose and hemoglobin A1C were 103.4 ± 36 mg/dL, 113.6 ± 15.7 mg/dL and 6.2 ± 0.9% (P < .001, for each). Multivariable logistic regression analysis revealed that increasing age was the most significant independent predictor that affect diabetic control in our study [odds ratio, 1.141, 95% confidence interval (1.015 to 1.282), P = .027)]. We concluded that LSG is a successful treatment option for glycemic control in overweight and obese patients with T2DM especially younger patients usually three-to-six months following surgery.
Introduction
Obesity is defined as abnormal or excessive fat accumulation with the body mass index is equal or more than 30 kg/m2 (Engin Citation2017). Obesity is a major health problem that affects approximately two billion people worldwide. A plenty of complications related to obesity such as, cardiovascular diseases, stroke, cancer, in addition to type 2 diabetes mellitus (T2DM) are well-known. Recently, obesity is dramatically increasing compared to past years in both adults and children. It is more common in Saudi women than Saudi men (Alenazi et al. Citation2015; DeNicola et al. Citation2015). Obesity indirectly influences the country’s economy by increasing the medical costs-related obesity complications and affects worker performance and productivity (Ludwig and Pollack Citation2009; Qasim et al. Citation2018).
T2DM is an alteration in body metabolic function, which affects pancreatic cells causing abnormal blood glucose level (Hu et al. Citation2001; Mokdad et al. Citation2001; van Greevenbroek et al. Citation2013). Diabetes mellitus (DM) is associated with a plenty of complications that appear with long-term of diabetes and high blood glucose level affects body functions and may cause retinopathy, neuropathy, nephropathy and increase susceptibility to infections (Kantharidis et al. Citation2011; Kautzky-Willer et al. Citation2016).
Anti-diabetic medication, dietary control and life style modification showed successful outcomes on some patients with type II diabetes (American Diabetes Association Citation2016). In Saudi Arabia, budget spent on diabetic patients to provide optimal management by medications is getting increased every year. Conventional medication alone does not provide an optimum therapy for glycemic control in diabetic patients especially in obese patients. Bariatric surgery is more effective in glycemic control than medications (Robert et al. Citation2016). Three most performed bariatric procedures are omega-loop gastric bypass, laparoscopic sleeve gastrectomy (LSG), and Roux-en-Y gastric bypass (LRYGB) show variable effects on glycemic control in diabetic patients (Mika et al. Citation2018). Majority of studies proved the utility of bariatric surgeries in glycemic control in type II diabetic patients (Buchwald et al. Citation2009; Mingrone et al. Citation2012; Mingrone et al. Citation2015). Albeit, minor studies showed that bariatric surgeries do not offer a long-lasting surgical cure for type II diabetic patients (DiGiorgi et al. Citation2010; Jurowich et al. Citation2012; Shah and Laferrère Citation2017).
To the authors’ knowledge, no previous studies were conducted in Taif government, Saudi Arabia, addressing the usefulness of bariatric surgeries, more specifically LSG, in glycemic control in type II diabetic patients. To address this knowledge gap, we implemented this study to assess the glycemic control following LSG in overweight and obese patients with T2DM.
Materials and methods
Study design
We conducted a retrospective study based on retrieving the required information from patient's files in Medical Records Departments for type II diabetic overweight and obese patients who underwent LSG in King Abdulaziz Specialist Hospital and Alhada Military Hospital in Taif, Saudi Arabia, from January 2017 to December 2019. A total of 96 patients were included in the study. The eligibility criteria included overweight and obese adult diabetic patients with T2DM who underwent LSG. Exclusion criteria were patients less than 18 years and type 1 diabetes.
Data collection
Collected data included patients’ baseline characteristics [age, sex, body mass index (BMI)], preoperative and postoperative blood glucose indices [fasting blood glucose (FBG), random blood glucose (RBG) and glycosylated hemoglobin (HbA1c) concentrations] and lipid profile [total cholesterol (TC), Triglycerides (TG), high-density lipoprotein cholesterol (HDL-C), Low-density lipoprotein cholesterol (LDL-C)]. In the case of multiple readings, we selected and recorded the most recent one, as well as identified the associated risk factors that may affect glycemic control following LSG. The follow-up duration for all patients ranged from three to six months postoperatively according to available data.
Research sample
We used (G*power 3.1) to compute the attained power (Faul et al. Citation2007). Our work had > 95% power. A post-hoc power calculation was conducted according to the difference between two dependent means (HBA1c values postoperative vs preoperative) at sample size = 96 and type I error threshold (α) ≤ .05.
Primary outcomes
Assessment of glycemic control in type II diabetic overweight and obese patients as short and medium term results following LSG.
Secondary outcomes
Identification of associated factors that may affect glycemic control following LSG.
Statistical analysis
Continuous variables were presented as the mean ±standard deviation (SD) if normally distributed or median(range) if not normally distributed. Shapiro–Wilk test was used to assess the normality of the continuous variables. Categorical variables were presented by the count and percentage. Missed values were replaced by series mean. Paired samples t-test was used to compare the means between two related groups on the same continuous, dependent variable. Wilcoxon Signed-Rank Test is the nonparametric alternative to paired t-test. Binary logistic regression analysis is a multifactorial regression model used with a binary outcome. HBA1c was dichotomized into controlled vs uncontrolled diabetes. All comparisons were two-tailed. P-value < .05 indicates a statistically significant difference. All statistical analyses were performed using IBM SPSS Statistics, version 24 (IBM; Armonk, New York, USA).
Results
Our study included 96 overweight/obese with T2DM patients. Patients aged 27–64 years (mean 44.3, SD 8.6 years). Male to female ratio was 60/36. Body mass index ranged 27.6–77 kg/m2 (mean 44.5, SD 8.1 kg/m2) as demonstrated in Table .
Table 1. Baseline characteristics of the patients underwent LSG.
Regarding glycemic control following bariatric surgery, patients following LSG had highly statistically significant decrease in fasting blood glucose, random blood glucose and HbA1c levels compared to their preoperative levels (P < .001), as shown in Table . In addition, patients after LSG had statistically significant decrease in total cholesterol (P < .001), TG (P < .001) and LDL (P = .042) levels compared to their preoperative levels. No significant change in HDL level was found (P = .84), as shown in Table . Approximately 91.7% (88/96) of patients showed adequate glycemic control following LSG, as shown in Table . A logistic regression was performed to determine the effects of age, gender, and preoperative BMI on the likelihood that patients have uncontrolled DM (HbA1C > 7.5%). The model explained 15.8% (Nagelkerke R2) of the variance in diabetic control and correctly classified 91.7% of cases. Increasing age was significantly associated with an increased likelihood of exhibiting uncontrolled DM (P = .027), as shown in Table .
Table 2. Changes in blood glucose indices following LSG.
Table 3. Changes in lipid profile following LSG.
Table 4. Diabetic control following LSG.
Table 5. Backward logistic regression predicting the likelihood of diabetic control following LSG based on age, gender, and preoperative body mass index.
Discussion
Our results showed that LSG achieved a significant glycemic and lipid control in overweight and obese patients with T2DM, in terms of reduced levels of fasting blood glucose, random blood sugar, and HbA1c as well as total cholesterol, triglycerides and low-density lipoproteins during follow-up duration ranged from three to six months postoperatively.
Bariatric surgery is a promising treatment option mainly in obese patients with T2DM. It is considered as a metabolic surgery owing to its role in metabolic regulation and the subsequent T2DM remission (Koliaki et al. Citation2017). Currently, LSG is considered one of the most common bariatric surgeries all over the world. A limited number of previously reported studies stressed on the early weight-independent effects of LSG in patients with obesity and T2DM, such as glycemic control (Wallenius et al. Citation2018).
In support of our results, a Saudi study by Ahmed and coworkers reported a substantial reduction in HbA1c levels diabetic patients who underwent bariatric surgeries (Ahmed et al. Citation2018). da La Harpe et al. in their matched case–control study showed the success of LRYGB in weight loss and the resultant remission of T2DM obese patients (de La Harpe et al. Citation2020). Wallenius et al. clarified that the effects of LSG on early glycemic control (two days and three weeks) are comparable following LRYGB and LSG in T2DM (Wallenius et al. Citation2018). In support, Cho and coworkers reported in their metaanalysis that remission of T2DM was independent to the degree of excess weight loss in both LSG and LRYGB operations (Cho et al. Citation2015).
In addition, Yamamoto et al. (Citation2016) clarified the postulated underlying mechanisms of bariatric surgeries-induced glycemic control. These mechanisms were the effect of gastrointestinal hormones, intestinal gluconeogenesis, gut motility and actions of bile acids and bacterial flora (Yamamoto et al. Citation2016). In the same vein, Heneghan and colleagues outlined a multitude of benefits of bariatric surgical procedures in reverse metabolic hazards of obesity including weight loss and glycemic control (Heneghan et al. Citation2012).
Kaska and coworkers related the improvement of glucose metabolism in T2DM patients following bariatric surgeries to the interaction between the increased circulating bile acids and both nuclear farnezoid X receptor (FXR) and membrane G-protein-receptor (TGR-5) (Kaska et al. Citation2016).
However, the role of bile acids as a main mechanism in the improvement of glucose metabolism following LSG did not accepted by Steinert et al. study (Citation2013).
Our work revealed that increasing age is the most important predictor of glycemic control following LSG. In corroboration, Jindal et al. stated that younger obese patients have higher chance in T2DM remission more than older patients after LSG. In the current work, patients aged 27–64 years (mean 44.2, SD 3.6 years) (Jindal et al. Citation2020).
On the contrary, Giordano and Victorzon in their systemic review reported that bariatric surgeries have equal benefits and complications regardless the age of patients (Giordano and Victorzon Citation2015). Also, the effects of bariatric surgery in early and adult-onset obese patients are comparable (Kristensson et al. Citation2020). However, shorter diabetes duration, lower fasting glucose before surgery, baseline HbA1c and waist circumference are important correlates for higher remission rates in patients with T2DM (Panunzi et al. Citation2016). The current study showed the significance of LSG in lipid control in obese patients with T2DM. Our results coincided with a study of Kjellmo et al. who reported decreased and normalized triglycerides and low-density lipoprotein cholesterol in morbidly obese patients following bariatric surgery (Kjellmo et al. Citation2018). Hyperlipidemia is a well-documented risk factor for cardiovascular complications (Nelson Citation2013). Sjöström and coworkers conducted a study that showed the reduction of microvascular and macrovascular complications of T2DM following bariatric surgeries (Sjöström et al. Citation2014). Several studies reported comparable results (Friedman et al. Citation2018; Cooiman et al. Citation2019).
The present study had some limitations. First, the incomplete medical records for most of the patients, e.g. duration of diabetes, postoperative body mass index, and surgery-related complications data. Second, the lack of long-term LSG glycemic control outcomes.
Conclusions
LSG is a successful treatment modality for glycemic control as well as lipid control in overweight and obese patients with T2DM especially younger patients. LSG revealed a favorable impact on overweight and obese diabetic patients by remission of T2DM usually three-to-six months following surgery.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Ethical approval
The Institutional Review Board at King Abdulaziz Specialist Hospital (Ethical approval No. 322/HAP-02-T-067, dated 12/01/2020) and Alhada Armed Forces Military Hospital approved the study (Ethical approval No. 2020-449/H-02-T-078, dated 19/02/2020). The need for patient consent was waived. Confidentiality of data was maintained and used only for the purpose of epidemiologic analysis.
Statement on consent
Waiver of consent had been obtained from the research ethics committee.
Data availability statement
The data that support the finding of this study was uploaded to Zenodo data via the link below https://doi.org/10.5281/zenodo.6463260.
References
- Ahmed A, Alanazi W, Ahmed R, AlJohi W, AlBuraikan D, AlRasheed B, ALMuqbil B, Al-Zahrani A, Yousef Z, AL-Jahdali H. 2018. The influences of bariatric surgery on hemoglobin A1C in a sample of obese patients in Saudi Arabia. Diabetes, Metab Syndr Obes Targets Ther. 11:271–276. doi:10.2147/DMSO.S161540.
- Alenazi S, Koura H, Zaki S, Mohamed A. 2015. Prevalence of obesity among male adolescents in Arar Saudi Arabia: future risk of cardiovascular disease. Indian J Community Med. 40:182. doi:10.4103/0970-0218.158864.
- American Diabetes Association. 2016. Obesity management for the treatment of type 2 diabetes. Sec. 6. In standards of medical care in diabetes. Diabetes Care. 39:S47–S51. doi:10.2337/dc16-S009.
- Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, Bantle JP, Sledge I. 2009. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 122:248–256. e5. doi:10.1016/j.amjmed.2008.09.041.
- Cho J-M, Kim HJ, Lo ME, Park S, Szomstein S, Rosenthal RJ. 2015. Effect of sleeve gastrectomy on type 2 diabetes as an alternative treatment modality to Roux-en-Y gastric bypass: systemic review and meta-analysis. Surg Obes Relat Dis. 11:1273–1280. doi:10.1016/j.soard.2015.03.001.
- Cooiman MI, Aarts EO, Janssen IMC, Hazebroek EJ, Berends FJ. 2019. Weight loss, remission of comorbidities, and quality of life after bariatric surgery in young adult patients. Obes Surg. 29:1851–1857. doi:10.1007/s11695-019-03781-z.
- de La Harpe R, Rüeger S, Kutalik Z, Ballabeni P, Suter M, Vionnet N, Laferrère B, Pralong F. 2020. Weight loss directly influences intermediate-term remission of diabetes mellitus after bariatric surgery: a retrospective case-control study. Obes Surg. 30:1332–1338. doi:10.1007/s11695-019-04283-8.
- DeNicola E, Aburizaiza OS, Siddique A, Khwaja H, Carpenter DO. 2015. Obesity and public health in the Kingdom of Saudi Arabia. Rev Environ Health. 30. doi:10.1515/reveh-2015-0008.
- DiGiorgi M, Rosen DJ, Choi JJ, Milone L, Schrope B, Olivero-Rivera L, Restuccia N, Yuen S, Fisk M, Inabnet WB, Bessler M. 2010. Re-emergence of diabetes after gastric bypass in patients with mid- to long-term follow-up. Surg Obes Relat Dis. 6:249–253. doi:10.1016/j.soard.2009.09.019.
- Engin A. 2017. The definition and prevalence of obesity and metabolic syndrome. Adv Exp Med Biol. 960:1–17. doi:10.1007/978-3-319-48382-5_1.
- Faul F, Erdfelder E, Lang A-G, Buchner A. 2007. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 39:175–191. doi:10.3758/bf03193146.
- Friedman AN, Wahed AS, Wang J, Courcoulas AP, Dakin G, Hinojosa MW, Kimmel PL, Mitchell JE, Pomp A, Pories WJ, et al. 2018. Effect of bariatric surgery on CKD risk. J Am Soc Nephrol. 29:1289–1300. doi:10.1681/ASN.2017060707.
- Giordano S, Victorzon M. 2015. Bariatric surgery in elderly patients: asystematic review. Clin Interv Aging. 10:1627–1635. doi:10.2147/CIA.S70313.
- Heneghan HM, Nissen S, Schauer PR. 2012. Gastrointestinal surgery for obesity and diabetes: weight loss and control of hyperglycemia. Curr Atheroscler Rep. 14:579–587. doi:10.1007/s11883-012-0285-5.
- Hu FB, Manson JE, Stampfer MJ, Colditz G, Liu S, Solomon CG, Willett WC. 2001. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med. 345:790–797. doi:10.1056/NEJMoa010492.
- Jindal R, Gupta M, Ahuja A, Nain P, Sharma P, Aggarwal A. 2020. Factors determining diabetic remission after sleeve gastrectomy: a prospective study. Niger J Surg. 26:66–71. doi:10.4103/njs.NJS_9_19.
- Jurowich C, Thalheimer A, Hartmann D, Bender G, Seyfried F, Germer CT, Wichelmann C. 2012. Improvement of type 2 diabetes mellitus (T2DM) after bariatric surgery – who fails in the early postoperative course? Obes Surg. 22:1521–1526. doi:10.1007/s11695-012-0676-2.
- Kantharidis P, Wang B, Carew RM, Lan HY. 2011. Diabetes complications: the microRNA perspective. Diabetes. 60:1832–1837. doi:10.2337/db11-0082.
- Kaska L, Sledzinski T, Chomiczewska A, Dettlaff-Pokora A, Swierczynski J. 2016. Improved glucose metabolism following bariatric surgery is associated with increased circulating bile acid concentrations and remodeling of the gut microbiome. World J Gastroenterol. 22:8698. doi:10.3748/wjg.v22.i39.8698.
- Kautzky-Willer A, Harreiter J, Pacini G. 2016. Sex and gender differences in risk, pathophysiology and complications of type 2 diabetes mellitus. Endocr Rev. 37:278–316. doi:10.1210/er.2015-1137.
- Kjellmo CA, Karlsson H, Nestvold TK, Ljunggren S, Cederbrant K, Marcusson-Ståhl M, Mathisen M, Lappegård KT, Hovland A. 2018. Bariatric surgery improves lipoprotein profile in morbidly obese patients by reducing LDL cholesterol, apoB, and SAA/PON1 ratio, increasing HDL cholesterol, but has no effect on cholesterol efflux capacity. J Clin Lipidol. 12:193–202. doi:10.1016/j.jacl.2017.10.007.
- Koliaki C, Liatis S, le Roux CW, Kokkinos A. 2017. The role of bariatric surgery to treat diabetes: current challenges and perspectives. BMC Endocr Disord. 17:50. doi:10.1186/s12902-017-0202-6.
- Kristensson FM, Andersson-Assarsson JC, Svensson P-A, Carlsson B, Peltonen M, Carlsson LMS. 2020. Effects of bariatric surgery in early- and adult-onset obesity in the prospective controlled Swedish obese subjects study. Diabetes Care. 43:860–866. doi:10.2337/dc19-1909.
- Ludwig DS, Pollack HA. 2009. Obesity and the economy. JAMA. 301:533–535. doi:10.1001/jama.2009.52.
- Mika A, Kaska L, Proczko-Stepaniak M, Chomiczewska A, Swierczynski J, Smolenski RT, Sledzinski T. 2018. Evidence that the length of bile loop determines serum bile acid concentration and glycemic control after bariatric surgery. Obes Surg. 28:3405–3414. doi:10.1007/s11695-018-3314-9.
- Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Leccesi L, Nanni G, Pomp A, Castagneto M, Ghirlanda G, Rubino F. 2012. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 366:1577–1585. doi:10.1056/NEJMoa1200111.
- Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Nanni G, Castagneto M, Bornstein S, Rubino F. 2015. Bariatric–metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet. 386:964–973. doi:10.1016/S0140-6736(15)00075-6.
- Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. 2001. Prevalence of besity, diabetes, and obesity-related health risk factors. JAMA. 289:76–79. doi:10.1001/jama.289.1.76.
- Nelson RH. 2013. Hyperlipidemia as a risk factor for cardiovascular disease. Prim Care Clin Off Pract. 40:195–211. doi:10.1016/j.pop.2012.11.003.
- Panunzi S, Carlsson L, De Gaetano A, Peltonen M, Rice T, Sjöström L, Mingrone G, Dixon JB. 2016. Determinants of diabetes remission and glycemic control after bariatric surgery. Diabetes Care. 39:166–174. doi:10.2337/dc15-0575.
- Qasim A, Turcotte M, de Souza RJ, Samaan MC, Champredon D, Dushoff J, Speakman JR, Meyre D. 2018. On the origin of obesity: identifying the biological, environmental and cultural drivers of genetic risk among human populations. Obes Rev. 19:121–149. doi:10.1111/obr.12625.
- Robert A, Al Dawish M, Braham R, Musallam M, Al Hayek A, Al Kahtany N. 2016. Type 2 diabetes mellitus in Saudi Arabia: major challenges and possible solutions. Curr Diabetes Rev. 13:59–64. doi:10.2174/1573399812666160126142605.
- Shah A, Laferrère B. 2017. Diabetes after bariatric surgery. Can J Diabetes. 41:401–406. doi:10.1016/j.jcjd.2016.12.009.
- Sjöström L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden Å, Bouchard C, Carlsson B, Karason K, Lönroth H, et al. 2014. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA. 311:2297–2304. doi:10.1001/jama.2014.5988.
- Steinert RE, Peterli R, Keller S, Meyer-Gerspach AC, Drewe J, Peters T, Beglinger C. 2013. Bile acids and gut peptide secretion after bariatric surgery: a 1-year prospective randomized pilot trial. Obesity. 21:E660–E668. doi:10.1002/oby.20522.
- van Greevenbroek MMJ, Schalkwijk CG, Stehouwer CDA. 2013. Obesity-associated low-grade inflammation in type 2 diabetes mellitus: causes and consequences. Neth J Med. 71:174–187.
- Wallenius V, Dirinck E, Fändriks L, Maleckas A, le Roux CW, Thorell A. 2018. Glycemic control after sleeve gastrectomy and roux-En-Y gastric bypass in obese subjects with type 2 diabetes mellitus. Obes Surg. 28:1461–1472. doi:10.1007/s11695-017-3061-3.
- Yamamoto H, Kaida S, Yamaguchi T, Murata S, Tani M, Tani T. 2016. Potential mechanisms mediating improved glycemic control after bariatric/metabolic surgery. Surg Today. 46:268–274. doi:10.1007/s00595-015-1134-2.