Publications by authors named "Giovanni Casella"

102 Publications

Comment on: Alarmists at the Gates: Esophageal Adenocarcinoma After Sleeve Gastrectomy Is Not Different than with Other Bariatric/Metabolic Surgeries.

Obes Surg 2022 Aug 13. Epub 2022 Aug 13.

Department of Surgical Sciences, Sapienza University of Rome, Viale Regina Elena, 324, 00161, Rome, Italy.

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http://dx.doi.org/10.1007/s11695-022-06241-3DOI Listing
August 2022

Accurate liquid biopsy for the diagnosis of non-alcoholic steatohepatitis and liver fibrosis.

Gut 2022 Jul 12. Epub 2022 Jul 12.

Università Cattolica del Sacro Cuore, Rome, Italy

Objective: Clinical diagnosis and approval of new medications for non-alcoholic steatohepatitis (NASH) require invasive liver biopsies. The aim of our study was to identify non-invasive biomarkers of NASH and/or liver fibrosis.

Design: This multicentre study includes 250 patients (discovery cohort, n=100 subjects (Bariatric Surgery Versus Non-alcoholic Steato-hepatitis - BRAVES trial); validation cohort, n=150 (Liquid Biopsy for NASH and Liver Fibrosis - LIBRA trial)) with histologically proven non-alcoholic fatty liver (NAFL) or NASH with or without fibrosis. Proteomics was performed in monocytes and hepatic stellate cells (HSCs) with iTRAQ-nano- Liquid Chromatography - Mass Spectrometry/Mass Spectrometry (LC-MS/MS), while flow cytometry measured perilipin-2 (PLIN2) and RAB14 in peripheral blood CD14CD16 monocytes. Neural network classifiers were used to predict presence/absence of NASH and NASH stages. Logistic bootstrap-based regression was used to measure the accuracy of predicting liver fibrosis.

Results: The algorithm for NASH using PLIN2 mean florescence intensity (MFI) combined with waist circumference, triglyceride, alanine aminotransferase (ALT) and presence/absence of diabetes as covariates had an accuracy of 93% in the discovery cohort and of 92% in the validation cohort. Sensitivity and specificity were 95% and 90% in the discovery cohort and 88% and 100% in the validation cohort, respectively.The area under the receiver operating characteristic (AUROC) for NAS level prediction ranged from 83.7% (CI 75.6% to 91.8%) in the discovery cohort to 97.8% (CI 95.8% to 99.8%) in the validation cohort.The algorithm including RAB14 MFI, age, waist circumference, high-density lipoprotein cholesterol, plasma glucose and ALT levels as covariates to predict the presence of liver fibrosis yielded an AUROC of 95.9% (CI 87.9% to 100%) in the discovery cohort and 99.3% (CI 98.1% to 100%) in the validation cohort, respectively. Accuracy was 99.25%, sensitivity 100% and specificity 95.8% in the discovery cohort and 97.6%, 99% and 89.6% in the validation cohort. This novel biomarker was superior to currently used FIB4, non-alcoholic fatty liver disease fibrosis score and aspartate aminotransferase (AST)-to-platelet ratio and was comparable to ultrasound two-dimensional shear wave elastography.

Conclusions: The proposed novel liquid biopsy is accurate, sensitive and specific in diagnosing the presence and severity of NASH or liver fibrosis and is more reliable than currently used biomarkers.

Clinical Trials: Discovery multicentre cohort: Bariatric Surgery versus Non-Alcoholic Steatohepatitis, BRAVES, ClinicalTrials.gov identifier: NCT03524365.Validation multicentre cohort: Liquid Biopsy for NASH and Fibrosis, LIBRA, ClinicalTrials.gov identifier: NCT04677101.
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http://dx.doi.org/10.1136/gutjnl-2022-327498DOI Listing
July 2022

Obesity and Psychological Factors Associated with Weight Loss after Bariatric Surgery: A Longitudinal Study.

Nutrients 2022 Jun 28;14(13). Epub 2022 Jun 28.

Department of Experimental Medicine, Sapienza University of Rome, 00161 Rome, Italy.

Bariatric surgery is indicated for treatment of severely obese people and can lead to significant weight loss as well as reduction of comorbidities associated with obesity. The present study aims to investigate the relationship between different psychological factors (e.g., tendency to binge eating, impulsivity, alexithymia), adherence to the nutritional plan, and weight loss after bariatric surgery. Forty-five candidates for bariatric surgery accessing a center for the care of obesity were assessed at T0 (pre-surgery) and T1 (6 months post-surgery) through anthropometric and psychometric measures. Simple linear correlations and linear regressions were conducted to evaluate the relationship between the psychological variables, adherence to nutritional plan, and weight loss 6 months after bariatric surgery. Non-planning impulsivity was the principal factor that succeeded in explaining adherence to the diet plan among all the variables considered. Adherence to the nutritional plan and non-planning impulsivity were considered reliable short-term predictors of weight loss after bariatric surgery. This evidence explains the usefulness of promoting research on psychological predictors of outcome in bariatric surgery. Mid- and long-term weight maintenance and quality of life need to be investigated through further follow-up.
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http://dx.doi.org/10.3390/nu14132690DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9268521PMC
June 2022

Gluten Induces Subtle Histological Changes in Duodenal Mucosa of Patients with Non-Coeliac Gluten Sensitivity: A Multicentre Study.

Nutrients 2022 Jun 15;14(12). Epub 2022 Jun 15.

Department of Pathology and Laboratory Medicine, Mayo Clinic, Rochester, MN 55907, USA.

Histological changes induced by gluten in the duodenal mucosa of patients with non-coeliac gluten sensitivity (NCGS) are poorly defined. To evaluate the structural and inflammatory features of NCGS compared to controls and coeliac disease (CeD) with milder enteropathy (Marsh I-II). Well-oriented biopsies of 262 control cases with normal gastroscopy and histologic findings, 261 CeD, and 175 NCGS biopsies from 9 contributing countries were examined. Villus height (VH, in μm), crypt depth (CrD, in μm), villus-to-crypt ratios (VCR), IELs (intraepithelial lymphocytes/100 enterocytes), and other relevant histological, serologic, and demographic parameters were quantified. The median VH in NCGS was significantly shorter (600, IQR: 400-705) than controls (900, IQR: 667-1112) ( < 0.001). NCGS patients with Marsh I-II had similar VH and VCR to CeD [465 µm (IQR: 390-620) vs. 427 µm (IQR: 348-569, = 0·176)]. The VCR in NCGS with Marsh 0 was lower than controls ( < 0.001). The median IEL in NCGS with Marsh 0 was higher than controls (23.0 vs. 13.7, < 0.001). To distinguish Marsh 0 NCGS from controls, an IEL cut-off of 14 showed 79% sensitivity and 55% specificity. IEL densities in Marsh I-II NCGS and CeD groups were similar. : NCGS duodenal mucosa exhibits distinctive changes consistent with an intestinal response to luminal antigens, even at the Marsh 0 stage of villus architecture.
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http://dx.doi.org/10.3390/nu14122487DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230100PMC
June 2022

Intracholecystic versus Intravenous Indocyanine Green (ICG) Injection for Biliary Anatomy Evaluation by Fluorescent Cholangiography during Laparoscopic Cholecystectomy: A Case-Control Study.

J Clin Med 2022 Jun 17;11(12). Epub 2022 Jun 17.

Department of Surgical Sciences, Sapienza University of Rome, 00161 Rome, Italy.

(1) Background: Fluorescence cholangiography has been proposed as a method for improving the visualization and identification of extrahepatic biliary anatomy in order to possibly reduce injuries and related complications. The most common method of indocyanine green (ICG) administration is the intravenous route, whereas evidence on direct ICG injection into the gallbladder is still quite limited. We aimed to compare the two different methods of ICG administration in terms of the visualization of extrahepatic biliary anatomy during laparoscopic cholecystectomy (LC), analyzing differences in the time of visualization, as well as the efficacy, advantages, and disadvantages of both modalities. (2) Methods: A total of 35 consecutive adult patients affected by acute or chronic gallbladder disease were enrolled in this prospective case-control study. Seventeen patients underwent LC with direct gallbladder ICG injection (IC-ICG) and eighteen subjects received intravenous ICG administration (IV-ICG). (3) Results: The groups were comparable with regard to their demographic and perioperative characteristics. The IV-ICG group had a significantly shorter overall operative time compared to the IC-ICG group ( = 0.017). IV-ICG was better at delineating the duodenum and the common hepatic duct compared to the IC-ICG method ( = 0.009 and = 0.041, respectively). The cystic duct could be delineated pre-dissection in 76.5% and 66.7% of cases in the IC-ICG and IV-ICG group, respectively, and this increased to 88.2% and 83.3% after dissection. The common bile duct could be highlighted in 76.5% and 77.8% of cases in the IC-ICG and IV-ICG group, respectively. Liver fluorescence was present in one case in the IC-ICG group and in all cases after IV-ICG administration (5.8% versus 100%; < 0.0001). (4) Conclusions: The present study demonstrates how ICG-fluorescence cholangiography can be helpful in identifying the extrahepatic biliary anatomy during dissection of Calot's triangle in both administration methods. In comparison with intravenous ICG injection, the intracholecystic ICG route could provide a better signal-to-background ratio by avoiding hepatic fluorescence, thus increasing the bile duct-to-liver contrast.
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http://dx.doi.org/10.3390/jcm11123508DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9224771PMC
June 2022

Sex difference in the safety and efficacy of bariatric procedures: a systematic review and meta-analysis.

Surg Obes Relat Dis 2022 07 20;18(7):983-996. Epub 2022 Apr 20.

Department of Experimental Medicine, Section of Medical Pathophysiology, Food Science and Endocrinology, Sapienza University of Rome, Rome, Italy.

With the prevalence of obesity alarmingly increasing, it is of primary interest to identify those factors predicting the success of anti-obesity therapeutic strategies currently adopted in clinical practice, and in particular, those of bariatric procedures showing the greatest success in terms of weight loss and maintenance in both the short and long term. Given sex-related differences in psychosocial status, hormonal homeostasis, and body fat distribution, it is likely that the response to different weight management strategies differs by sex. The objective was to elucidate the effect of sex on different bariatric procedures' efficacy and safety outcomes. Searches of PubMed, Cochrane, and Embase databases were performed, followed by hand-searching of reference lists from all relevant articles. We included all the studies evaluating the effect of bariatric procedures on body mass index loss (BMIL), and/or percentage excess weight loss (%EWL), and/or percentage excess body mass index loss, and/or percentage of responders, and/or short-/long-term complications and co-morbidity resolution, broken down by sex. Twenty-seven studies with a total of 114,919 patients were included. Men were more likely to achieve greater BMIL, consistent with higher male baseline BMI, and women were 2.87 times more likely to be classified as weight responders (95% confidence interval [CI]: 1.90-4.34), as well as to perform better in terms of %EWL (95% CI: .13-.54). Upon subgroup analysis based on bariatric procedure, women were more likely to be successful in terms of %EWL upon bioenteric intragastric balloon (BIB) placement (.72, 95% CI: .42-1.02). There was no sex difference regarding investigated co-morbidity resolution (hypertension, diabetes, and obstructive sleep apnea syndrome) or occurrence of short-term complications, whereas women were more likely to develop long-term complications, with an odds ratio of 1.97 (95% CI: 1.57-2.49). Sex does not have a clear effect on efficacy outcomes of bariatric procedures. Differentiating by procedure, BIB may be more effective in women, although results are discordant based on the weight loss outcome considered. If the short-term postoperative complication rate is similar across both sexes, long-term complications occur more frequently in women. To clarify the real effect of sex on bariatric procedure-derived health benefits, it is crucial to report sex-stratified results in future studies, as well as evaluate body composition changes that go beyond simple body weight reduction.
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http://dx.doi.org/10.1016/j.soard.2022.03.022DOI Listing
July 2022

Advice of General Practitioner, of Surgeon, of Endocrinologist, and Self-determination: the Italian Road to Bariatric Surgery.

Obes Surg 2022 06 6;32(6):1996-2002. Epub 2022 Apr 6.

IRCCS Humanitas, Rozzano, Milan, Italy.

Purpose: Bariatric surgery (BS) is considered the most efficient treatment for severe obesity. International guidelines recommend multidisciplinary approach to BS (general practitioners, endocrinologists, surgeons, psychologists, or psychiatrists), and access to BS should be the final part of a protocol of treatment of obesity. However, there are indications that general practitioners (GPs) are not fully aware of the possible benefits of BS, that specialty physicians are reluctant to refer their patients to surgeons, and that patients with obesity choose self-management of their own obesity, including internet-based choices. There are no data on the pathways chosen by physicians and patients to undergo BS in the real world in Italy.

Methods: An exploratory exam was performed for 6 months in three pilot regions (Lombardy, Lazio, Campania) in twenty-three tertiary centers for the treatment of morbid obesity, to describe the real pathways to BS in Italy.

Results: Charts of 2686 patients (788 men and 1895 women, 75.5% in the age range 30-59 years) were evaluated by physicians and surgeons of the participating centers. A chronic condition of obesity was evident for the majority of patients, as indicated by duration of obesity, by presence of several associated medical problems, and by frequency of previous dietary attempts to weight loss. The vast majority (75.8%) patients were self-presenting or referred by bariatric surgeons, 24.2% patients referred by GPs and other specialists. Self-presenting patients were younger, more educated, more professional, and more mobile than patients referred by other physicians. Patients above the age of 40 years or with a duration of obesity greater than 10 years had a higher prevalence of all associated medical problems.

Conclusions: The majority of patients referred to a tertiary center for the treatment of morbid obesity have a valid indication for BS. Most patients self-refer to the centers, with a minority referred by a GP or by specialists. Self-presenting patients are younger, more educated, more professional, and more mobile than patients referred by other physicians. Older patients and with a longer duration of obesity are probably representative of the conservative approach to BS, often regarded as the last resort in an endless story.
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http://dx.doi.org/10.1007/s11695-022-06042-8DOI Listing
June 2022

The early reduction of left ventricular mass after sleeve gastrectomy depends on the fall of branched-chain amino acid circulating levels.

EBioMedicine 2022 Feb 4;76:103864. Epub 2022 Feb 4.

Department of Surgical Sciences, Sapienza University of Rome, Viale Regina Elena, 324, Rome, Italy. Electronic address:

Introduction: Body-mass index is a major determinant of left-ventricular-mass (LVM). Bariatric-metabolic surgery (BMS) reduces cardiovascular mortality. Its mechanism of action, however, often encompasses a weight-dependent effect. In this translational study, we aimed at investigating the mechanisms by which BMS leads to LVM reduction and functional improvement.

Methods: Twenty patients (45.2 ± 8.5years) were studied with echocardiography at baseline and at 1,6,12 and 48 months after sleeve-gastrectomy (SG). Ten Wistar rats aged 10-weeks received high-fat diet ad libitum for 10 weeks before and 4 weeks after SG or sham-operation. An oral-glucose-tolerance-test was performed to measure whole-body insulin-sensitivity. Plasma metabolomics was analysed in both human and rodent samples. RNA quantitative Real-Time PCR and western blots were performed in rodent heart biopsies. The best-fitted partial-least-square discriminant-analysis model was used to explore the variable importance in the projection score of all metabolites.

Findings: Echocardiographic LVM (-12%,-23%,-28% and -43% at 1,6,12 and 48 months, respectively) and epicardial fat decreased overtime after SG in humans while insulin-sensitivity improved. In rats, SG significantly reduced LVM and epicardial fat, enhanced ejection-fraction and improved insulin-sensitivity compared to sham-operation. Metabolomics showed a progressive decline of plasma branched-chain amino-acids (BCAA), alanine, lactate, 3-OH-butyrate, acetoacetate, creatine and creatinine levels in both humans and rodents. Hearts of SG rats had a more efficient BCAA, glucose and fatty-acid metabolism and insulin signaling than sham-operation. BCAAs in cardiomyocyte culture-medium stimulated lipogenic gene transcription and reduced mRNA levels of key mitochondrial β-oxidation enzymes promoting lipid droplet accumulation and glycolysis.

Interpretation: After SG a prompt and sustained decrease of the LVM, epicardial fat and insulin resistance was found. Animal and in vitro studies showed that SG improves cardiac BCAA metabolism with consequent amelioration of fat oxidation and insulin signaling translating into decreased intra-myocytic fat accumulation and reduced lipotoxicity.

Funding: This work was supported by the University of Rome Sapienza.
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http://dx.doi.org/10.1016/j.ebiom.2022.103864DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8829082PMC
February 2022

GORD and Barrett's oesophagus after bariatric procedures: multicentre prospective study.

Br J Surg 2021 12;108(12):1498-1505

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

Introduction: Gastro-oesophageal reflux disease (GORD) after bariatric surgery is a debated topic. This study investigated the prevalence of GORD and associated oesophageal complications following bariatric procedures-namely, adjustable gastric banding (AGB), sleeve gastrectomy (SG), Roux-en-Y gastric bypass (RYGB), and one-anastomosis gastric bypass (OAGB).

Methods: This was a prospective multicentre study designed to evaluate the long-term effects of bariatric surgery on GORD. Patients were studied at baseline, at >10 years following AGB, SG, and RYGB, and at >3 years following OAGB (due to the more recent recognition of OAGB as a standard bariatric procedure). Patients were assessed by endoscopy and GORD symptom evaluation.

Results: A total of 241 patients were enrolled. A minimum follow-up of 10 years was completed by 193 patients following AGB (57 patients), SG (95 patients), and RYGB (41 patients), and of >3 years by 48 subjects following OAGB. GORD symptoms increased following AGB and SG (from 14 to 31.6 per cent and from 26.3 to 58.9 per cent, respectively; P < 0.0001), improved following RYGB (from 36.6 to 14.6 per cent; P < 0.0001), and were unchanged following OAGB. The overall prevalence of erosive oesophagitis was greater in the SG group (74.7 per cent) than in the AGB (42.1 per cent), RYGB (22 per cent), and OAGB (22.9 per cent) groups (P < 0.0001). Barrett's oesophagus was found only in patients who had SG (16.8 per cent). Biliary-like gastric stagnation was found in a greater proportion of SG and OAGB patients (79.7 and 69.4 per cent, respectively) than in other treatment groups (P < 0.0001). The prevalence of biliary-type reflux into the oesophagus was higher in patients who underwent SG (74.7 per cent), compared with other treatment groups.

Conclusion: Bariatric surgery leads to gastro-oesophageal complications of variable severity, particularly SG, which can result in a large proportion of patients developing Barrett's oesophagus.
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http://dx.doi.org/10.1093/bjs/znab330DOI Listing
December 2021

Coincidental or Causal? Concurrence of Colorectal Carcinoma with Primary Breast Cancer.

Dig Dis Sci 2022 02 3;67(2):437-444. Epub 2021 Nov 3.

Department of Surgical Sciences, Sapienza University, Rome, Italy.

Multiple primary malignant neoplasms (MPMN) represent the occurrence of a second malignancy in the same patient within 6 months after the detection of first primary (synchronous) tumor, or > 6 months after primary detection (metachronous). We present a case of a patient treated for carcinoma of the breast who developed a metachronous primary malignancy in the colorectal tract. These tumors were histologically different with distinct immune-histochemical parameters. The association between breast and colon cancer is well documented in the literature with several studies reporting the coexistence of common extrinsic and genetic predisposing factors. Although rare, MPMN are becoming more common due to the increased number of elderly cancer survivors, improved diagnosis and enhanced awareness. The association between colorectal and breast cancer should not be dismissed merely as metastasis since there is good precedent for the co-occurrence of these primary tumors.
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http://dx.doi.org/10.1007/s10620-021-07296-5DOI Listing
February 2022

Repercussions of COVID-19-related national lockdown on Emergency Surgery Department: a longitudinal cohort monocentric study.

Minerva Surg 2022 Feb 28;77(1):22-29. Epub 2021 May 28.

Emergency Surgery Department, Sapienza University, Rome, Italy.

Background: COVID-19 lockdown restrictions in conjunction with the pervasive hospital fear endured by the vast majority of the population played a fundamental role in discouraging access to emergency departments (EDs). We aimed at investigating whether and how the COVID-19 outbreak limited the access to ED and affected urgent surgical activities during and immediately after the 2-month pandemic-related national lockdown.

Methods: Data regarding patients who accessed to the surgical ED were retrospectively collected. Analyzed time-periods included: "pre-COVID-19 era," "COVID-19 era" considered as the period of full national lockdown and "post-COVID-19 era" after easing of lockdown measures. Consecutive emergency surgical procedures and ED admissions before, during and after COVID-19-lockdown were retrieved and analyzed.

Results: There was a significant decrease in overall ED admissions and in all-specialty surgical consultations (P<0.01) throughout the outbreak. Once national lockdown was eased, we recorded a subsequent rebound 5-fold rise of emergency surgical procedures compared to COVID-19 group (P=0.011). Time-to-surgery was significantly greater in "COVID-19 era" and "post-COVID-19 era" compared to "pre-COVID-19" group (22.56±4.78, 75.99±15.89 and 16.73±1.76 hours, respectively) (P<0.01). A raised incidence of postoperative complications emerged in the "COVID-19 era" group (37.5%) compared to pre- and post-COVID groups (9.1% and 12.5%, respectively; P<0.001). Mortality rate in the "COVID-19 era" was 31.3% and 7.5% in "post-COVID-19" group (<0.0001).

Conclusions: This study demonstrates the major reduction of emergency surgical procedures and overall, ED admissions caused by COVID-19 pandemic. The raised rate of postoperative complications and mortality might be likely due to the superior severity of surgical conditions observed in the "COVID-19 era" subjects together with a probable deferred pursuit of medical attention.
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http://dx.doi.org/10.23736/S2724-5691.21.08851-1DOI Listing
February 2022

Response to: Sleeve gastrectomy may double the risk of esophageal adenocarcinoma in morbidly obese patients.

Surg Obes Relat Dis 2021 05 13;17(5):1030. Epub 2021 Feb 13.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

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http://dx.doi.org/10.1016/j.soard.2021.02.010DOI Listing
May 2021

Esophageal adenocarcinoma after sleeve gastrectomy: actual or potential threat? Italian series and literature review.

Surg Obes Relat Dis 2021 May 28;17(5):848-854. Epub 2020 Nov 28.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

Background: Sleeve gastrectomy (SG) leads to esophageal mucosal damage in an elevated percentage of cases, configuring a clinical condition of Barrett's esophagus (BE) in a proportion as high as 15-18.8%. BE may rarely evolve into esophageal adenocarcinoma (EAC).

Objectives: To raise awareness of BE as a precancerous lesion which may progress toward malignancy after this popular bariatric procedure.

Setting: Bariatric referral centers, Italy.

Methods: All patients referred to our bariatric center who developed an EAC after SG between 2012 and 2019 were reviewed and consecutively included in this study. The available scientific literature regarding this complication is additionally reviewed.

Results: The 3 male patients comprised in this case series underwent laparoscopic SG between 2012 and 2015 in different bariatric referral centers. Age and body mass index at baseline ranged from 21-54 years and 43.1-75.6 kg/m, respectively. All patients were lost to follow-up early after surgery (3.7 ± 1.4 months), and were diagnosed with EAC at a mean of 27.3 ± 7.6 months after SG. The 4 reported cases in the scientific literature developed an EAC at a mean of 32.5 ± 23 months from SG. Overall, a diagnosis of EAC was made approximately 30.3 ± 17.1 months postoperatively, which seems relatively and worryingly early after surgery.

Conclusion: Although the rate and probability of progression from BE to EAC is still not well defined, assuming that the rising popularity and execution of SG leads to a growth in the BE incidence, then the preoperative identification and stratification of cancer risk factors in this subset of patients is strongly encouraged. Clinical and endoscopic follow-ups are essential to allow for prevention and early diagnosis and for epidemiologic data collection purposes.
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http://dx.doi.org/10.1016/j.soard.2020.11.023DOI Listing
May 2021

Effect of Diet versus Gastric Bypass on Metabolic Function in Diabetes.

N Engl J Med 2020 12;383(24):2392-2393

King's College London, London, United Kingdom

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http://dx.doi.org/10.1056/NEJMc2030030DOI Listing
December 2020

Activities related to inflammatory bowel disease management during and after the coronavirus disease 2019 lockdown in Italy: How to maintain standards of care.

United European Gastroenterol J 2020 12 18;8(10):1228-1235. Epub 2020 Oct 18.

Gastroenterology Unit, Mauriziano Hospital, Turin, Italy.

Background And Aims: Restructuring activities have been necessary during the lockdown phase of the coronavirus disease 2019 (COVID-19) pandemic. Few data are available on the post-lockdown phase in terms of health-care procedures in inflammatory bowel disease (IBD) care, and no data are available specifically from IBD units. We aimed to investigate how IBD management was restructured during the lockdown phase, the impact of the restructuring on standards of care and how Italian IBD units have managed post-lockdown activities.

Methods: A web-based online survey was conducted in two phases (April and June 2020) among the Italian Group for IBD affiliated units within the entire country. We investigated preventive measures, the possibility of continuing scheduled visits/procedures/therapies because of COVID-19 and how units resumed activities in the post-lockdown phase.

Results: Forty-two referral centres participated from all over Italy. During the COVID-19 lockdown, 36% of first visits and 7% of follow-up visits were regularly done, while >70% of follow-up scheduled visits and 5% of first visits were done virtually. About 25% of scheduled endoscopies and bowel ultrasound scans were done. More than 80% of biological therapies were done as scheduled. Compared to the pre-lockdown situation, 95% of centres modified management of outpatient activity, 93% of endoscopies, 59% of gastrointestinal ultrasounds and 33% of biological therapies. Resumption of activities after the lockdown phase may take three to six months to normalize. Virtual clinics, implementation of IBD pathways and facilities seem to be the main factors to improve care in the future.

Conclusion: Italian IBD unit restructuring allowed quality standards of care during the COVID-19 pandemic to be maintained. A return to normal appears to be feasible and achievable relatively quickly. Some approaches, such as virtual clinics and identified IBD pathways, represent a valid starting point to improve IBD care in the post-COVID-19 era.
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http://dx.doi.org/10.1177/2050640620964132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7724532PMC
December 2020

Small intestinal metabolism is central to whole-body insulin resistance.

Gut 2021 06 29;70(6):1098-1109. Epub 2020 Sep 29.

Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy

Objective: To assess the role of jejunum in insulin resistance in humans and in experimental animals.

Design: Twenty-four subjects undergoing biliopancreatic diversion (BPD) or Roux-en-Y gastric bypass (RYGB) were enrolled. Insulin sensitivity was measured at baseline and at 1 week after surgery using oral glucose minimal model.We excluded the jejunum from intestinal continuity in pigs and created a jejunal loop with its vascular and nerve supply intact accessible from two cutaneous stomas, and reconnected the bowel with an end-to-end anastomosis. Glucose stable isotopes were given in the stomach or in the jejunal loop.In vitro studies using primary porcine and human hepatocytes or myoblasts tested the effects of plasma on gluconeogenesis or glucose uptake and insulin signalling.

Results: Whole-body insulin sensitivity (S∙10: 0.54±0.12 before vs 0.82±0.11 after BPD, p=0.024 and 0.41±0.09 before vs 0.65±0.09/pM/min after RYGB, p=not significant) and Glucose Disposition Index increased only after BPD. In pigs, insulin sensitivity was significantly lower when glucose was administered in the jejunal loop than in the stomach (glucose rate of disappearance (R) area under the curve (AUC)/insulin AUC∙10: 1.82±0.31 vs 2.96±0.33 mmol/pM/min, p=0.0017).Metabolomics showed a similar pattern before surgery and during jejunal-loop stimulation, pointing to a higher expression of gluconeogenetic substrates, a metabolic signature of impaired insulin sensitivity.A greater hepatocyte phosphoenolpyruvate-carboxykinase and glucose-6-phosphatase gene expression was elicited with plasma from porcine jejunal loop or before surgery compared with plasma from jejunectomy in pigs or jejunal bypass in humans.Stimulation of myoblasts with plasma from porcine jejunal loop or before surgery reduced glucose uptake, Ser473-Akt phosphorylation and GLUT4 expression compared with plasma obtained during gastric glucose administration after jejunectomy in pigs or after jejunal bypass in humans.

Conclusion: Proximal gut plays a crucial role in controlling insulin sensitivity through a distinctive metabolic signature involving hepatic gluconeogenesis and muscle insulin resistance. Bypassing the jejunum is beneficial in terms of insulin-mediated glucose disposal in obesity.

Trial Registration Number: NCT03111953.
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http://dx.doi.org/10.1136/gutjnl-2020-322073DOI Listing
June 2021

Sleeve gastrectomy and gastroesophageal reflux: a comprehensive endoscopic and pH-manometric prospective study.

Surg Obes Relat Dis 2020 Nov 19;16(11):1629-1637. Epub 2020 Jul 19.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

Background: The impact of sleeve gastrectomy (SG) on gastroesophageal reflux disease (GERD) is still greatly debated. Most of the current evidence available is solely based on symptom evaluation or medication use, while a minority have implemented objective functional measurements.

Objective: To better comprehend the pathophysiological mechanisms involved in the genesis of GERD after SG.

Setting: University Hospital, Italy.

Methods: A total of 21 patients affected by morbid obesity and eligible for SG were prospectively enrolled in the present study. Patients were evaluated by means of endoscopy, high-resolution manometry (HRM), 24-hour pH monitoring, and the Gastroesophageal Reflux Disease Health-Related Quality of Life questionnaire.

Results: Follow-up was completed at least 1 year post operation (mean follow-up, 14.3 ± 2.1 mo) by 19 patients. Body mass index decreased from 41.2 ± .9 to 26.8 ± .8 kg/m (P < .001). Distal contractile integral significantly decreased from 2772.8 ± 399.9 mm Hg/s/cm to 2060.4 ± 338.9 mm Hg/s/cm (P = .01). The 24-hour pH monitoring showed an overall reduction tendency of acid reflux, although this was not statistically significant. All analyzed endoscopic findings withstood substantial pejorative modifications after SG (P < .01). Distal contractile integral values at baseline predicted postoperative Z-line upward migration; HRM, distal latency, and DeMeester score at baseline predicted the development of erosive esophagitis at follow-up, by bootstrap estimates of a logistic regression.

Conclusions: Postoperative GERD-related esophageal sequelae should be carefully considered after SG. Our results demonstrate how acid reflux does not seem to play a relevant role in the pathophysiology of post-SG GERD. Baseline HRM can help stratify the risk of developing erosive esophagitis and Z-line upward migration after SG, while postoperative endoscopic surveillance should be encouraged regardless of the presence or absence of symptoms.
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http://dx.doi.org/10.1016/j.soard.2020.07.013DOI Listing
November 2020

Short-term weight-mediated effects of sleeve gastrectomy on echocardiographic surrogate markers of atherosclerotic vascular disease.

Kardiol Pol 2020 08 25;78(7-8):655-656. Epub 2020 Aug 25.

Department of Surgical Sciences, “Sapienza” University of Rome, Italy

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http://dx.doi.org/10.33963/KP.15560DOI Listing
August 2020

Duodenal-jejunal bypass improves nonalcoholic fatty liver disease independently of weight loss in rodents with diet-induced obesity.

Am J Physiol Gastrointest Liver Physiol 2020 10 19;319(4):G502-G511. Epub 2020 Aug 19.

Fondazione Policlinico Universitario A. Gemelli Istituto di Ricovero e Cura a Carattere Scientifico, Università Cattolica del S. Cuore, Rome, Italy.

Nonalcoholic fatty liver disease (NAFLD) is the most common cause of liver-related mortality. NAFLD is associated with obesity, hepatic fat accumulation, and insulin resistance, all of which contribute to its pathophysiology. Weight-loss is the main therapy for NAFLD, and metabolic surgery is the most effective treatment for morbid obesity and its metabolic comorbidities. Although has been reported that Roux-en-Y gastric bypass can reverse NAFLD, it is unclear whether such effects result from reduced weight, from a lower calorie-intake, or from the direct influence of surgery on mechanisms contributing to NAFLD. We aimed to investigate whether gastrointestinal (GI) bypass surgery could induce direct effects on hepatic fat accumulation and insulin resistance, independently of weight reduction. Twenty Wistar rats on a high-fat diet underwent duodenal-jejunal-bypass (DJB) or sham operation and were pair fed (PF) for 15 wk after surgery to obtain a matched weight. Outcome measures include ectopic fat deposition, expression of genes and proteins involved in fat metabolism, insulin-signaling, and gluconeogenesis in liver and muscle. Despite no differences in body weight and calorie intake, DJB showed lower ectopic fat accumulation, improved peripheral and hepatic insulin sensitivity, and enhanced lipid droplet degradation. In both tissues, DJB increased insulin signaling, whereas hepatic key enzymes involved in gluconeogenesis and de novo lipogenesis were decreased. These findings suggest that DJB can reverse, independently of weight loss, ectopic fat deposition and insulin resistance, two features of NAFLD that share a mutual pathway, in which perilipin-2 (PLIN2) seems to be the main player, supporting further investigation into strategies that target the gut to treat metabolic liver diseases. Our findings suggest that duodenal-jejunal bypass can reverse, independently of weight loss, ectopic fat deposition and insulin resistance, two features of nonalcoholic fatty liver disease that share a mutual pathway, in which perilipin-2 seems to be the main player. Our study supports further investigation into the role of proximal small intestine exclusion in the pathophysiology of nonalcoholic fatty liver disease to uncover less invasive treatments that mimic the effects of metabolic surgery and aims to prevent and treat metabolic liver disease.
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http://dx.doi.org/10.1152/ajpgi.00357.2019DOI Listing
October 2020

The Effect of Sleeve Gastrectomy on Oxidative Stress in Obesity.

Biomedicines 2020 Jun 19;8(6). Epub 2020 Jun 19.

Surgical Sciences Department, "Sapienza" University of Rome, Viale Regina Elena 261, 00161 Roma, Italy.

High concentrations of free radicals are present in the blood of obese patients. Free radicals are associated with endothelial dysfunction, diabetes, and neoplastic transformation, all conditions that are closely related to obesity. The purpose of our study was to determine whether bariatric surgery modifies the production of free radicals in obese patients. In total, 20 patients with morbid obesity, who were candidates for laparoscopic sleeve gastrectomy (SG), and 18 controls were enrolled in the study. Oxidative stress was studied in obese subjects before and after sleeve gastrectomy. The evaluation of oxidative stress was carried out on blood samples using electron paramagnetic resonance, a refined spectroscopic technique used to identify and quantify the major free radicals, such as OH, O, ONOO, and NO. Oxidative stress was higher in subjects with morbid obesity prior to surgery, compared to the controls (CP• 9.9 ± 0.3 µM vs. 5.8 ± 0.2 µM). After SG, values decreased to levels comparable to those of controls (CP• 5.4 ± 0.2 µM). Further analysis identified O as the main free radical responsible for the oxidative stress. Obesity is associated with an increased blood concentration of free radicals. The normalization of free radicals after sleeve gastrectomy highlights another important benefit of this bariatric surgery technique.
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http://dx.doi.org/10.3390/biomedicines8060168DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7344505PMC
June 2020

COVID emergency: an opportunity to increase the interaction between hepatologist and primary care physician.

Minerva Gastroenterol Dietol 2020 Dec 2;66(4):328-330. Epub 2020 Jun 2.

ATS Brianza, Limbiate, Monza-Brianza, Italy.

The outbreak of Coronavirus disease 2019 (COVID-19) worldwide had evidenced the opportunity to increase the interaction between specialist and primary care physician (PCP). COVID 19, started in December 2019 in China, has been considered a public health emergency by the Department of Health and Human Services and, now, it is a pandemic disease with worldwide diffusion. The COVID-19 crisis permits to increase the role of telemedicine as a tool for the delivery of health care services at distance and to slow down the virus diffusion. This technology is cheap and easy to use but it is limited by governmental licensing restrictions, reimbursement barriers, lesser extent of infrastructure and difficulties related to the change. During COVID-19 epidemy, telemedicine is safe, low cost and-permits to treat urgent and routine specialist cases without human proximity and contact which would spread infection, particularly to the elderly and immunocompromised patients. In COVID-19 era, the goal of PCP is to reduce travels and visits in specialized center for liver disease patients. A strict collaboration between specialized hepatologist and PCP is needed.
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http://dx.doi.org/10.23736/S1121-421X.20.02713-0DOI Listing
December 2020

Obesity Surgery and Cancer: What Are the Unanswered Questions?

Front Endocrinol (Lausanne) 2020 15;11:213. Epub 2020 Apr 15.

Division of Diabetes & Nutritional Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.

Obesity has become a global epidemic with a soaring economic encumbrance due to its related morbidity and mortality. Amongst obesity-related conditions, cancer is indeed the most redoubtable. Bariatric surgery has been proven to be the most effective treatment for obesity and its associated metabolic and cardiovascular disorders. However, the understanding of whether and how bariatric surgery determines a reduction in cancer risk is limited. Obesity-related malignancies primarily include colorectal and hormone-sensitive (endometrium, breast, prostate) cancers. Additionally, esophago-gastric tumors are growing to be recognized as a new category mainly associated with post-bariatric surgery outcomes. In fact, certain types of surgical procedures have been described to induce the development and subsequent progression of pre-cancerous esophageal and gastric lesions. This emerging category is of great concern and further research is required to possibly prevent such risks. Published data has generated conflicting results. In fact, while overall cancer risk reduction was reported particularly in women, some authors showed no improvement or even increased cancer incidence. Although various studies have reported beneficial effects of surgery on risk of specific cancer development, fundamental insights into the pathogenesis of obesity-related cancer are indispensable to fully elucidate its mechanisms.
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http://dx.doi.org/10.3389/fendo.2020.00213DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174700PMC
May 2021

Laparoscopic cholecystectomy: which predicting factors of conversion? Two Italian center's studies.

Minerva Chir 2020 Jun 4;75(3):141-152. Epub 2020 Mar 4.

Department of Emergency Surgery, St. Orsola University Hospital, Alma Mater Studiorum, Bologna, Italy.

Background: Laparoscopic cholecystectomy represents the gold standard technique for the treatment of lithiasic gallbladder disease. Although it has many advantages, laparoscopic cholecystectomy is not risk-free and in special situations there is a need for conversion into an open procedure, in order to minimize postoperative complications and to complete the procedure safely. The aim of this study was to identify factors that can predict the conversion to open cholecystectomy.

Methods: We analyzed 1323 patients undergoing laparoscopic cholecystectomy over the last five years at St. Orsola University Hospital-Bologna and Umberto I University Hospital-Rome. Among these, 116 patients (8.7%) were converted into laparotomic cholecystectomy. Clinical, demographic, surgical and pathological data from these patients were included in a prospective database. A univariate analysis was performed followed by a multivariate logistic regression.

Results: On univariate analysis, the factors significantly correlated with conversion to open were the ASA score higher than 3 and the comorbidity, specifically cardiovascular disease, diabetes and chronic renal failure (P<0.001). Patients with a higher mean age had a higher risk of conversion to open (61.9±17.1 vs. 54.1±15.2, P<0.001). Previous abdominal surgery and previous episodes of cholecystitis and/or pancreatitis were not statistically significant factors for conversion. There were four deaths in the group of converted patients and two in the laparoscopic group (P<0.001). Operative morbility was higher in the conversion group (22% versus 8%, P<0.001). Multivariate analysis showed that the factors significantly correlated to conversion were: age <65 years old (P=0.031 OR: 1.6), ASA score 3-4 (P=0.013, OR:1.8), history of ERCP (P=0.16 OR:1.7), emergency procedure (P=0.011, OR:1.7); CRP higher than 0,5 (P<0.001, OR:3.3), acute cholecystitis (P<0.001, OR:1.4). Further multivariate analysis of morbidity, postoperative mortality and home discharge showed that conversion had a significant influence on overall post-operative complications (P=0.011, OR:2.01), while mortality (P=0.143) and discharge at home were less statistically influenced.

Conclusions: Our results show that most of the independent risk factors for conversion cannot be modified by delaying surgery. Many factors reported in the literature did not significantly impact conversion rates in our results.
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http://dx.doi.org/10.23736/S0026-4733.20.08228-0DOI Listing
June 2020

Publisher Correction: New insight into the mechanisms of ectopic fat deposition improvement after bariatric surgery.

Sci Rep 2020 Feb 12;10(1):2786. Epub 2020 Feb 12.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41598-020-58961-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7015884PMC
February 2020

The jejunum is the key factor in insulin resistance.

Surg Obes Relat Dis 2020 Apr 3;16(4):509-519. Epub 2020 Jan 3.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

Background: Biliopancreatic diversion (BPD) is more effective than Roux-en-Y gastric bypass (RYGB) on both insulin resistance and diabetes.

Objectives: Because the major difference between the 2 procedures resides in the length of jejunal bypass, we investigated the role of the jejunum in insulin resistance.

Setting: University hospital in Italy.

Methods: Insulin sensitivity (IS) and secretion were measured before and 4 weeks after RYGB or BPD in 16 patients. A translational study was also conducted in 6 pigs, by isolating a jejunal loop with its vascular and nerve supply (Thiry-Vella loop [TVL]). TVL was doubly stomatized and bowel continuity restored by a side-to-side jejuno-jejunostomy. At baseline and 4 weeks postoperatively a glucose bolus was injected either in the stomach or in the TVL. Whole-body IS and jejunal heat shock proteins (HSPs) were measured. Primary porcine hepatocyte cultures were incubated with plasma or individual HSPs.

Results: Whole-body IS increased from 353.5 ± 26.7 to 442.0 ± 37.4 (P < .05) after RYGB and from 312.4 ± 14.9 to 441.2 ± 15.9 mL/m/min (P < .001) after BPD. Hepatic IS was unchanged after RYGB, while it increased from .3 ± .01 to .4 ± .1 (μM/pM) - 1 (P < .01) after BPD. Total insulin secretion rate remained unchanged after RYGB but decreased (from 58.3 ± 23.6 to 33.1 ± 7.8 nmol/m, P < .05) after BPD. Jejunectomy in pigs enhanced IS (.3 ± .01 versus .2 ± .01 mM/pM, P < .001), while injection of glucose into TVL reduced it (.1 ± .01 versus .3 ± .01 mM/pM, P < .0001). The jejunum secreted HSPs, Hsp70, and GRP78, which impaired insulin signaling in hepatocyte cultures.

Conclusions: This study shows that jejunal bypass in both humans and pigs improves IS. Injection of glucose into the TVL in pigs determines insulin resistance. In response to glucose, the jejunum secretes HSPs that impair insulin signaling.
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http://dx.doi.org/10.1016/j.soard.2019.12.024DOI Listing
April 2020

New insight into the mechanisms of ectopic fat deposition improvement after bariatric surgery.

Sci Rep 2019 11 21;9(1):17315. Epub 2019 Nov 21.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.

Non-alcoholic fatty-liver disease (NAFLD) is frequent in obese patients and represents a major risk factor for the development of diabetes and its complications. Bariatric surgery reverses the hepatic features of NAFLD. However, its mechanism of action remains elusive. We performed a comprehensive analysis of the mechanism leading to the improvement of NAFLD and insulin resistance in both obese rodents and humans following sleeve-gastrectomy (SG). SG improved insulin sensitivity and reduced hepatic and monocyte fat accumulation. Importantly, fat accumulation in monocytes was well comparable to that in hepatocytes, suggesting that Plin2 levels in monocytes might be a non-invasive marker for the diagnosis of NAFLD. Both in vitro and in vivo studies demonstrated an effective metabolic regeneration of liver function and insulin sensitivity. Specifically, SG improved NAFLD significantly by enhancing AMP-activated protein kinase (AMPK) phosphorylation and chaperone-mediated autophagy (CMA) that translate into the removal of Plin2 coating lipid droplets. This led to an increase in lipolysis and specific amelioration of hepatic insulin resistance. Elucidating the mechanism of impaired liver metabolism in obese subjects will help to design new strategies for the prevention and treatment of NAFLD.
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http://dx.doi.org/10.1038/s41598-019-53702-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6872729PMC
November 2019

Late-onset Crohn's disease: a comparison of disease behaviour and therapy with younger adult patients: the Italian Group for the Study of Inflammatory Bowel Disease 'AGED' study.

Eur J Gastroenterol Hepatol 2019 Nov;31(11):1361-1369

Gastroenterology Operative Unit, Azienda Ospedaliera San Camillo-Forlanini, Department of Digestive Diseases, Campus Bio-Medico, University of Rome, Rome.

Background: Disease phenotype and outcome of late-onset Crohn's disease are still poorly defined.

Methods: In this Italian nationwide multicentre retrospective study, patients diagnosed ≥65 years (late-onset) were compared with young adult-onset with 16-39 years and adult-onset Crohn's disease 40-64 years. Data were collected for 3 years following diagnosis.

Results: A total of 631 patients (late-onset 153, adult-onset 161, young adult-onset 317) were included. Colonic disease was more frequent in late-onset (P < 0005), stenosing behaviour was more frequent than in adult-onset (P < 0003), but fistulising disease was uncommon. Surgery rates were not different between the three age groups. Systemic steroids were prescribed more frequently in young adult-onset in the first year, but low bioavailability steroids were used more frequently in late-onset in the first 2 years after diagnosis (P < 0.036, P < 0.041, respectively). The use of immunomodulators and anti-TNF's even in patients with more complicated disease, that is, B2 or B3 behaviour (Montreal classification), remained significantly inferior (P < 0.0001) in late-onset compared to young adult-onset. Age at diagnosis, Charlson comorbidity index, and steroid used in the first year were negatively associated with the use of immunomodulators and biologics. Comorbidities, related medications and hospitalizations were more frequent in late-onset. Polypharmacy was present in 56% of elderly Crohn's disease patients.

Conclusion: Thirty-two percent of late-onset Crohn's disease presented with complicated disease behaviour. Despite a comparable use of steroids and surgery, immunomodulators and biologics were used in a small number of patients.
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http://dx.doi.org/10.1097/MEG.0000000000001546DOI Listing
November 2019

Simulation of gastric bypass effects on glucose metabolism and non-alcoholic fatty liver disease with the Sleeveballoon device.

EBioMedicine 2019 Aug 7;46:452-462. Epub 2019 Aug 7.

Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy. Electronic address:

Background: Gastric bypass surgery is a very effective treatment of obesity and type 2 diabetes. However, very few eligible patients are offered surgery. Some patients also prefer less invasive approaches. We aimed to study the effects of the Sleeveballoon - a new device combining an intragastric balloon with a connecting sleeve, which covers the duodenal and proximal jejunal mucosa - on insulin sensitivity, glycemic control, body weight and body fat distribution.

Methods: We compared the effects of Sleeveballoon, Roux-en-Y Gastric-Bypass (RYGB) and sham-operation in 30 high-fat diet (HFD) fed Wistar rats. Whole body and hepatic insulin sensitivity and insulin signaling were studied. Transthoracic echocardiography was performed using a Vevo 2100 system (FUJIFILM VisualSonics Inc., Canada). Gastric emptying was measured using gastrografin.

Findings: Hepatic (P = .023) and whole-body (P = .011) insulin sensitivity improved in the Sleeveballoon and RYGB groups compared with sham-operated rats. Body weight reduced in both Sleeveballoon and RYGB groups in comparison to the sham-operated group (503.1 ± 8.9 vs. 614.4 ± 20.6 g, P = .006 and 490.0 ± 17.7 vs. 614.4 ± 20.6 g, P = .006, respectively). Ectopic fat deposition was drastically reduced while glycogen content was increased in both liver and skeletal muscle. Gastric emptying (T) was longer (157.7 ± 29.2 min, P = .007) in the Sleeveballoon than in sham-operated rats (97.1 ± 26.3 min), but shorter in RYGB (3.5 ± 1.1 min, P < .0001). Cardiac function was better in Sleeveballoon and RYGB versus sham-operated rats.

Interpretation: The Sleeveballoon reduces peripheral and hepatic insulin resistance, glycaemia, body weight and ectopic fat deposition to a similar level as RYGB, although the contribution of gastric emptying to blood glucose reduction is different.
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http://dx.doi.org/10.1016/j.ebiom.2019.07.069DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6712366PMC
August 2019
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