Publications by authors named "Jorge D Machicado"

48 Publications

Pain Experience in Pancreatitis: Strong Association of Genetic Risk Loci for Anxiety and PTSD in Patients With Severe, Constant, and Constant-Severe Pain.

Am J Gastroenterol 2021 Jul 8. Epub 2021 Jul 8.

Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

Introduction: Recurrent acute pancreatitis (RAP) and chronic pancreatitis (CP) are progressive inflammatory syndromes with variable features. Pain is the primary feature that contributes to low physical and mental quality of life with a third of patients reporting severe pain. Pain experience is worsened by depression. Here, we tested the hypothesis that genetic risk of the psychiatric conditions of anxiety and post-traumatic stress disorder (PTSD) is associated with pain in CP and RAP + CP subjects.

Methods: The study cohort included phenotyped and genotyped RAP and CP patients from the North American Pancreatitis Study II of European Ancestry. Candidate genetic association studies were based on the absence of pain vs pain that is constant, constant-severe, or severe. Twenty-eight candidate genetic loci for anxiety and PTSD risk were identified in the literature and were the focus of this study.

Results: We identified 24 significant pain-associated single nucleotide polymorphisms within 13 loci across the 3 pain patterns in CP and RAP + CP (P < 0.002). Thirteen anxiety or PTSD genes were within these pain loci indicating nonrandom associations (P < 4.885 × 10-23). CTNND2 was associated with all pain categories and all pancreatitis etiologies. Implicated systems include neuronal signaling (HTR2A, DRD3, NPY, and BDNF), hypothalamic-pituitary-adrenal axis (NR3C1 and FKBP5), and cell-cell interaction (CTNND2 and THBS2).

Discussion: A component of constant and severe pain in patients with RAP and CP is associated with genetic predisposition to anxiety and PTSD. Identification of patients at risk eligible for trials of targeted treatment as a component of a multidisciplinary pain management strategy should be formally evaluated.
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http://dx.doi.org/10.14309/ajg.0000000000001366DOI Listing
July 2021

Mortality in acute pancreatitis with persistent organ failure is determined by the number, type, and sequence of organ systems affected.

United European Gastroenterol J 2021 Mar;9(2):139-149

Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

Background: Persistent organ failure (POF) is the strongest determinant of mortality in acute pancreatitis (AP). There is a paucity of data regarding the impact of different POF attributes on mortality and the role of different characteristics of systemic inflammatory response syndrome (SIRS) in the risk of developing POF.

Objective: We aimed to assess the association of POF dynamic features with mortality and SIRS characteristics with POF.

Methods: We studied 1544 AP subjects prospectively enrolled at 22 international centers (APPRENTICE consortium). First, we estimated the association of onset, duration, and maximal score of SIRS with POF. Then, we evaluated the risk of mortality based on POF onset, duration, number, type, and sequence of organs affected. Analyses were adjusted for potential confounders.

Results: 58% had SIRS, 11% developed POF, and 2.5% died. Early SIRS, persistent SIRS, and maximal SIRS score ≥ 3 were independently associated with higher risk of POF (p < 0.05). Mortality risk in POF was higher with two (33%, odds ratio [OR] = 10.8, 3.3-34.9) and three (48%, OR = 20.2, 5.9-68.6) organs failing, in comparison to single POF (4%). In subjects with multiple POF, mortality was higher when the cardiovascular and respiratory systems failed first or concurrently as compared to when the renal system failed first or concurrently with other organ (p < 0.05). In multivariate regression model, the number and sequence of organs affected in POF were associated with mortality (p < 0.05). Onset and duration of POF had no impact mortality.

Conclusion: In AP patients with POF, the risk of mortality is influenced by the number, type, and sequence of organs affected. These results are useful for future revisions of AP severity classification systems.
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http://dx.doi.org/10.1002/ueg2.12057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8259236PMC
March 2021

Practice patterns and adherence to nutrition guidelines in acute pancreatitis: An international physician survey.

Pancreatology 2021 Apr 14;21(3):642-648. Epub 2021 Jan 14.

Division of Gastroenterology and Hepatology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA. Electronic address:

Background: There is agreement among GI society guidelines for recommending early oral nutrition with non-liquid diet in patients with mild acute pancreatitis (AP). There is less agreement regarding administration of tube feedings (TF) in AP. Data on physicians' adherence to nutrition guidelines and practice variations are limited.

Aims: To report practice patterns in the nutritional management of different severity profiles of AP.

Methods: We conducted an anonymous electronic survey among physician members of the International Association of Pancreatology and the American Pancreatic Association. We assessed nutrition practices based on severity of AP, and asked relevant questions regarding the preferred administration strategies for enteral nutrition. Responses were compared by practice location and subspecialty.

Results: A total of 178 physicians, mostly medical pancreatologists (40.4%) and surgeons (34.8%) from Europe (43.4%) and North America (32%) responded. Overall, only 26.7% initiated oral nutrition in mild AP on day 1, 40.9% waited >48 h, and 57.3% initiated nutrition with liquid diets. Physicians reported frequently using TF in patients with moderately-severe (30-75%, depending on the amount and location of necrosis) and severe AP (75-80%). Two-thirds of physicians preferred initiating TF after 48 h, administering it post-pylorically, and using semi-elemental or polymeric formulas. Median TF duration was 11 days (IQR, 7-21). Significant variations were noted based on geographic location and physician subspecialty for several aspects of nutritional practices in both mild and non-mild AP.

Conclusion: Adherence to oral nutrition guideline recommendations for mild AP is low. There is significant variability in the use of TF in AP. Our study highlights opportunities for improving consistency of nutrition care in AP and identify potential areas for research.
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http://dx.doi.org/10.1016/j.pan.2021.01.001DOI Listing
April 2021

Dynamic changes in the pancreatitis activity scoring system during hospital course in a multicenter, prospective cohort.

J Gastroenterol Hepatol 2021 Sep 18;36(9):2416-2423. Epub 2021 Feb 18.

Division of Gastroenterology, Hepatology, and Nutrition, Ohio State University, Wexner Medical Center, Columbus, Ohio, USA.

Background And Aim: The primary aim was to validate the Pancreatitis Activity Scoring System (PASS) in a multicenter prospectively ascertained acute pancreatitis (AP) cohort. Second, we investigated the association of early PASS trajectories with disease severity and length of hospital stay (LOS).

Methods: Data were prospectively collected through the APPRENTICE consortium (2015-2018). AP severity was categorized based on revised Atlanta classification. Delta PASS (ΔPASS) was calculated by subtracting activity score from baseline value. PASS trajectories were compared between severity subsets. Subsequently, the cohort was subdivided into three LOS subgroups as short (S-LOS): 2-3 days; intermediate (I-LOS): 3-7 days; and long (L-LOS): ≥7 days. The generalized estimating equations model was implemented to compare PASS trajectories.

Results: There were 434 subjects analyzed including 322 (74%) mild, 86 (20%) moderately severe, and 26 (6%) severe AP. Severe AP subjects had the highest activity levels and the slowest rate of decline in activity (P = 0.039). Focusing on mild AP, L-LOS subjects (34%) had 28 points per day slower decline; whereas, S-LOS group (13%) showed 34 points per day sharper decrease compared with I-LOS (53%; P < 0.001). We noticed an outlier subset with a median admission-PASS of 466 compared with 140 in the rest. Morphine equivalent dose constituted 80% of the total PASS in the outliers (median morphine equivalent dose score = 392), compared with only 25% in normal-range subjects (score = 33, P value < 0.001).

Conclusions: This study highlighted that PASS can quantify AP activity. Significant differences in PASS trajectories were found both in revised Atlanta classification severity and LOS groups, which can be harnessed in AP monitoring/management (ClincialTrials.gov number, NCT03075618).
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http://dx.doi.org/10.1111/jgh.15430DOI Listing
September 2021

Post-Acute Pancreatitis Pancreatic Exocrine Insufficiency: Rationale and Methodology of a Prospective, Observational, Multicenter Cohort Study.

Pancreas 2021 02;50(2):147-152

Division of Gastroenterology, Hepatology, & Nutrition, Department of Internal Medicine, Ohio State University, Wexner Medical Center, Columbus, OH.

Objectives: We describe the methodology of Post-Acute Pancreatitis Pancreatic Exocrine Insufficiency (PAPPEI), a prospective, observational, multicenter cohort study. The objectives of PAPPEI are to estimate the incidence rate of post-acute pancreatitis (AP) pancreatic exocrine insufficiency (PEI), define factors that determine the development of post-AP PEI, and evaluate the impact of post-AP PEI on nutritional status and quality of life.

Methods: Enrollment started in June 2017 in 3 expert academic centers in the United States. Data were collected during hospitalization (baseline) at 3 and 12 months after enrollment. Fecal elastase-1 was used to assess PEI. Study questionnaires are completed by patient interview and review of electronic medical records. Blood is obtained to evaluate vitamin deficiencies and nutritional markers.

Results: As of August 2020, 77 subjects have completed the baseline evaluation. The median age was 58 years (interquartile range, 39-67 years), 38% were male, and 90% were white. The etiology of AP was biliary in 39 subjects (51%), and 51 subjects (66%) had mild AP. Three- and 12-month follow-up data have been collected in 29 and 13 subjects, respectively.

Conclusion: The PAPPEI study aims to expand our understanding of post-AP PEI incidence, including its impact on nutritional status and quality of life.
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http://dx.doi.org/10.1097/MPA.0000000000001743DOI Listing
February 2021

High performance in risk stratification of intraductal papillary mucinous neoplasms by confocal laser endomicroscopy image analysis with convolutional neural networks (with video).

Gastrointest Endosc 2021 07 16;94(1):78-87.e2. Epub 2021 Jan 16.

Division of Gastroenterology, Hepatology, and Nutrition, Division of Internal Medicine, The Ohio State University Wexner Medical Center, Columbus, Ohio, USA.

Background And Aims: EUS-guided needle-based confocal laser endomicroscopy (EUS-nCLE) can differentiate high-grade dysplasia/adenocarcinoma (HGD-Ca) in intraductal papillary mucinous neoplasms (IPMNs) but requires manual interpretation. We sought to derive predictive computer-aided diagnosis (CAD) and artificial intelligence (AI) algorithms to facilitate accurate diagnosis and risk stratification of IPMNs.

Methods: A post hoc analysis of a single-center prospective study evaluating EUS-nCLE (2015-2019; INDEX study) was conducted using 15,027 video frames from 35 consecutive patients with histopathologically proven IPMNs (18 with HGD-Ca). We designed 2 CAD-convolutional neural network (CNN) algorithms: (1) a guided segmentation-based model (SBM), where the CNN-AI system was trained to detect and measure papillary epithelial thickness and darkness (indicative of cellular and nuclear stratification), and (2) a reasonably agnostic holistic-based model (HBM) where the CNN-AI system automatically extracted nCLE features for risk stratification. For the detection of HGD-Ca in IPMNs, the diagnostic performance of the CNN-CAD algorithms was compared with that of the American Gastroenterological Association (AGA) and revised Fukuoka guidelines.

Results: Compared with the guidelines, both n-CLE-guided CNN-CAD algorithms yielded higher sensitivity (HBM, 83.3%; SBM, 83.3%; AGA, 55.6%; Fukuoka, 55.6%) and accuracy (SBM, 82.9%; HBM, 85.7%; AGA, 68.6%; Fukuoka, 74.3%) for diagnosing HGD-Ca, with comparable specificity (SBM, 82.4%; HBM, 88.2%; AGA, 82.4%; Fukuoka, 94.1%). Both CNN-CAD algorithms, the guided (SBM) and agnostic (HBM) models, were comparable in risk stratifying IPMNs.

Conclusion: EUS-nCLE-based CNN-CAD algorithms can accurately risk stratify IPMNs. Future multicenter validation studies and AI model improvements could enhance the accuracy and fully automatize the process for real-time interpretation.
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http://dx.doi.org/10.1016/j.gie.2020.12.054DOI Listing
July 2021

Serum IgG4 Subclass Deficiency Defines a Distinct, Commonly Encountered, Severe Inflammatory Bowel Disease Subtype.

Inflamm Bowel Dis 2021 05;27(6):855-863

Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, United States.

Background: Immunoglobulin G subclass 4 (IgG4) is hypothesized to play an immunomodulatory role, downregulating humoral immune responses. The role of this anti-inflammatory molecule in inflammatory bowel disease (IBD) has not been fully characterized. We sought to define alterations in serum IgG4 in patients with IBD and their association with multiyear disease severity.

Methods: We analyzed metadata derived from curated electronic health records from consented patients with IBD prospectively followed at a tertiary center over a 10-year time period. Patients with IBD with IgG4 serum levels available formed the study population. Demographics and multiyear clinical data were collected and analyzed. We stratified patients with IBD with low, normal, or high serum IgG4 levels.

Results: We found IgG4 characterized in 1193 patients with IBD and low IgG4 levels in 233 patients (20%) and elevated IgG4 levels in 61 patients (5%). An IgG4 deficiency did not significantly correlate with other antibody deficiencies. In a multiple Poisson regression analysis, low IgG4 was associated with more years on biologic agents (P = 0.002) and steroids (P = 0.049) and more hospital admissions (P < 0.001), clinic visits (P = 0.010), outpatient antibiotic prescriptions (P < 0.001), and CD-related surgeries (P = 0.011) during the study period after controlling for certain confounders. Elevated IgG4 was only associated with primary sclerosing cholangitis (P = 0.011). A cohort of patients with IgG4-deficient severe IBD received intravenous Ig replacement therapy, which benefited and was continued in 10 out of 11 individuals.

Conclusions: An IgG4 subclass deficiency, distinct from other antibody deficiencies, occurred commonly in a referral IBD population and was associated with multiple markers of disease severity. This is the first association of IgG4 subclass deficiency with an inflammatory disease process. Further work is needed to define the mechanistic role of IgG4 deficiency in this severe IBD subgroup.
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http://dx.doi.org/10.1093/ibd/izaa230DOI Listing
May 2021

The long-term outcomes of patients with immunoglobulin G4-related sclerosing cholangitis: the Mayo Clinic experience.

J Gastroenterol 2020 Nov 8;55(11):1087-1097. Epub 2020 Aug 8.

Division of Gastroenterology and Hepatology, Mayo Clinic College of Medicine, 200 1st St SW, Rochester, MN, 55905, USA.

Background: The long-term outcomes of immunoglobulin G4-related sclerosing cholangitis (IgG4-SC) are not well known.

Methods: The outcomes of patients with IgG4-SC at Mayo Clinic (1999-2018) were compared to an age- and gender-matched (1:1 ratio) group of patients with primary sclerosing cholangitis (PSC).

Results: We identified 89 patients with IgG4-SC; median age at diagnosis was 67 years, 81% were males, and the median follow-up was 5.7 years. Seventy-eight patients received prednisone for induction of remission, and 53 received at least one other immunosuppressive agent for maintenance of remission. Of the IgG4-SC group, 10 died (median time from diagnosis until death was 6.5 years): 2 due to cirrhosis, 3 due to cholangiocarcinoma (CCA), and 5 due to non-hepatobiliary causes. Eleven patients in the PSC group underwent liver transplantation, while none did in the IgG4-SC group. The incidence of a hepatobiliary adverse event (cirrhosis or CCA) was 3.4 times greater in the PSC compared to the IgG4-SC group (events per 1000 person-years: 52.6; 95% CI 38-73; vs. 15.6; 95% CI 7-32). The probability of development of a hepatobiliary adverse event within 10 years was 11% in the IgG4-SC compared to 45% in the PSC group (P = 0.0001). The overall survival tended to be higher in the IgG4-SC compared to the PSC group (10-year: 79% vs. 68%, respectively; P = 0.11).

Conclusions: In a cohort of IgG4-SC patients, 88% of whom were treated with immunosuppressive drugs, the risk of cirrhosis and CCA was significantly lower compared to an age- and gender-matched group with PSC.
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http://dx.doi.org/10.1007/s00535-020-01714-7DOI Listing
November 2020

Radiomics for the Diagnosis and Differentiation of Pancreatic Cystic Lesions.

Diagnostics (Basel) 2020 Jul 21;10(7). Epub 2020 Jul 21.

Division of Gastroenterology, Hepatology and Nutrition, The Ohio State University Wexner Medical Center, Columbus, OH 43210, USA.

Radiomics, also known as quantitative imaging or texture analysis, involves extracting a large number of features traditionally unmeasured in conventional radiological cross-sectional images and converting them into mathematical models. This review describes this approach and its use in the evaluation of pancreatic cystic lesions (PCLs). This discipline has the potential of more accurately assessing, classifying, risk stratifying, and guiding the management of PCLs. Existing studies have provided important insight into the role of radiomics in managing PCLs. Although these studies are limited by the use of retrospective design, single center data, and small sample sizes, radiomic features in combination with clinical data appear to be superior to the current standard of care in differentiating cyst type and in identifying mucinous PCLs with high-grade dysplasia. Combining radiomic features with other novel endoscopic diagnostics, including cyst fluid molecular analysis and confocal endomicroscopy, can potentially optimize the predictive accuracy of these models. There is a need for multicenter prospective studies to elucidate the role of radiomics in the management of PCLs.
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http://dx.doi.org/10.3390/diagnostics10070505DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7399814PMC
July 2020

Constant-severe pain in chronic pancreatitis is associated with genetic loci for major depression in the NAPS2 cohort.

J Gastroenterol 2020 Oct 17;55(10):1000-1009. Epub 2020 Jul 17.

Department of Medicine, University of Pittsburgh, Room 401.4, 3708 Fifth Ave, Pittsburgh, PA, 15213, USA.

Background: Pain is the most debilitating symptom of recurrent acute pancreatitis (RAP) and chronic pancreatitis (CP) and often requires chronic opioids or total pancreatectomy with islet autotransplantation to manage. Pain is a complex experience that can be exacerbated by depression and vice versa. Our aim was to test the hypothesis that depression-associated genes are associated with a constant-severe pain experience in RAP/CP patients.

Study: A retrospective study was done using North American Pancreatitis Study II (NAPS2) genotyped RAP and CP patients with completed case report forms (n = 1,357). Subjects were divided based on pattern of pain and pain severity as constant-severe pain (n = 787) versus not constant-severe pain (n = 570) to conduct a nested genome-wide association study. The association between reported antidepressant medication use and depression gene loci was tested.

Results: Constant-severe pain was reported in 58% (n = 787) of pancreatitis patients. No differences in sex or alcohol consumption were found based on pain severity. Antidepressant use was reported in 28% (n = 223), and they had lower SF-12 mental quality of life (MCS, p < 2.2 × 10). Fifteen loci associated with constant-severe pain (p < 0.00001) were found to be in or near depression-associated genes including ROBO2, CTNND2, SGCZ, CNTN5 and BAIAP2. Three of these genes respond to antidepressant use (SGCZ, ROBO2, and CTNND2).

Conclusion: Depression is a major co-factor in the pain experience. This genetic predisposition to depression may have utility in counseling patients and in instituting early antidepressant therapy for pain management of pancreatitis patients. Prospective randomized trials are warranted.

Clinical Trials Registration: Clinicaltriasl.gov.# NCT01545167.
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http://dx.doi.org/10.1007/s00535-020-01703-wDOI Listing
October 2020

Intravenous fluid resuscitation in the management of acute pancreatitis.

Curr Opin Gastroenterol 2020 09;36(5):409-416

Division of Gastroenterology, Hepatology & Nutrition, The Ohio State University Wexner Medical Center, Columbus, Ohio, USA.

Purpose Of Review: In the absence of proven effective pharmacologic therapy in acute pancreatitis, and given its simplicity, wide availability, and perceived safety, intravenous fluid resuscitation remains the cornerstone in the early treatment of acute pancreatitis. Herein, we will review the rationale of fluid therapy, critically appraise the published literature, and summarize recent studies.

Recent Findings: Several observational studies and small clinical trials have raised concern about the efficacy and safety of aggressive fluid resuscitation. Early aggressive fluid therapy among acute pancreatitis patients with predicted mild severity appears to have the highest benefit, whereas aggressive resuscitation in patients with predicted severe disease might be futile and deleterious. Lactated Ringer's solution is the preferred fluid type based on animal studies, clinical trials, and meta-analyses. There is a wide variation of fluid resuscitation approaches in current guideline recommendations, quality indicators, and worldwide practice patterns.

Summary: There is lack of high-quality data that supports the use of early aggressive fluid resuscitation. Large, well designed, multicenter randomized controlled trials are needed to determine the optimal timing, fluid type, volume, rate, and duration of fluid resuscitation in acute pancreatitis.
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http://dx.doi.org/10.1097/MOG.0000000000000659DOI Listing
September 2020

Pancreatogenic diabetes, acute pancreatitis management, and pancreatic tuberculosis: Appraising the present and setting goals for the future.

United European Gastroenterol J 2020 05;8(4):365-368

Division of Gastroenterology and Hepatology, The Ohio State University Wexner Medical Center, Columbus, Ohio, USA.

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http://dx.doi.org/10.1177/2050640620917017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7226692PMC
May 2020

Prevalence and Associated Factors of Abdominal Pain and Disability at 1-Year Follow-up After an Attack of Acute Pancreatitis.

Pancreas 2019 Nov/Dec;48(10):1348-1353

From the Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, PA.

Objective: The aim of the study was to report the prevalence and predictors of abdominal pain and disability 1 year after an acute pancreatitis (AP) attack.

Methods: Patients were prospectively enrolled between December 2012 and April 2016. Enrolled subjects were contacted at a median of 13 months after enrollment. Multivariable regression models were used to determine factors independently associated with abdominal pain at follow-up.

Results: Response rate was 71% (110/155). Of respondents, median age was 51 years, 58% were female, and 14% had severe AP. At follow-up, 24% of patients reported abdominal pain (65% intermittent, 35% constant), 10% used analgesics regularly, and 6% had regular opioids use. Furthermore, 41% of patients experienced pain-related interference with work or daily activities, and 8% developed disability. On regression analysis, idiopathic etiology (odds ratio [OR], 3.8; 95% confidence interval [CI], 1.1-13.6) persistent organ failure (OR, 3.3; 95% CI, 1.1-7.9), and recurrent AP (OR, 2.9; 95% CI, 1.1-10.6) were independently associated with abdominal pain at follow-up. Disability at follow-up was associated with younger age, current smoking, and intensive care unit admission (all P < 0.05).

Conclusions: Abdominal pain and disability are potential long-term sequelae of AP. Certain pre-existing factors and pancreatitis features are associated with these outcomes at one-year follow-up of AP.
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http://dx.doi.org/10.1097/MPA.0000000000001434DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6839779PMC
September 2020

Stress and a sedentary lifestyle are associated with irritable bowel syndrome in medical students from Peru: a cross-sectional study.

Eur J Gastroenterol Hepatol 2019 Nov;31(11):1322-1327

Facultad de Medicina Alberto Hurtado, Universidad Peruana Cayetano Heredia, Lima, Peru.

Background: Previous studies suggest that medical students may have higher rates of irritable bowel syndrome as compared to the general population. We hypothesized lifestyle characteristics may be associated to irritable bowel syndrome.

Methods: A cross-sectional survey was conducted in 2015 among students in their fourth, fifth, sixth and seven years of a medical school in Peru. Volunteer participants responded to questions pertaining to demographics, surveys including the Rome III criteria and the Self-reported Stress questionnaire. Regression models were performed to establish variables independently associated with irritable bowel syndrome.

Results: Out of 452 students, 346 responded the survey (response rate: 76.5%; female rate: 47%; median age: 22 years). The irritable bowel syndrome prevalence in respondents was 9.5% (95% confidence interval: 6.7%-13.1%). On univariate analysis, being a senior medical student (odds ratio: 2.8; 95% confidence interval: 1.3-5.9; P < 0.01), mental illness (odds ratio: 3.3; 95% confidence interval: 1.6-6.8; P = 0.002), psychiatric medication use (odds ratio: 2.8; 95% confidence interval: 1.4-5.9; P = 0.005), sedentary lifestyle (odds ratio: 4.4; 95% confidence interval: 1.8-11; P = 0.001) and stress (odds ratio: 4.4; 95% confidence interval: 2.1-9.3; P < 0.001) were associated to irritable bowel syndrome. On a multivariate analysis, a sedentary lifestyle (odds ratio: 3.2; 95% confidence interval: 1.25-8.20; P = 0.01) and stress (odds ratio: 3.0; 95% confidence interval: 1.35-6.67; P < 0.01) were independently associated with irritable bowel syndrome.

Conclusion: The prevalence of irritable bowel syndrome in medical students from Peru is slightly lower compared to the global prevalence of irritable bowel syndrome. Stress and a sedentary lifestyle were independent risk factors associated with irritable bowel syndrome. Our study suggests that lifestyle modifications and stress coping techniques could have an impact to reduce the rates of irritable bowel syndrome in medical students.
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http://dx.doi.org/10.1097/MEG.0000000000001479DOI Listing
November 2019

Period prevalence of chronic pancreatitis diagnosis from 2001-2013 in the commercially insured population of the United States.

Pancreatology 2019 Sep 17;19(6):813-818. Epub 2019 Jul 17.

Division of Gastroenterology and Hepatology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA. Electronic address:

Background: Prevalence estimates of chronic pancreatitis (CP) in the US are scarce. We aimed to determine the prevalence of CP in the commercially insured population of the US.

Methods: We analyzed the IQVIA Legacy PharMetrics database to calculate the period prevalence of CP from 2001 to 2013 among individuals with ≥1 year of enrollment. CP was defined as ≥1 healthcare contacts associated with a non-ancillary claim for a primary diagnosis of CP (ICD-9-CM 577.1). Prevalence estimates were age- and sex- adjusted to the 2010 US population. Sensitivity analysis was performed by using more stringent criteria: a) 1 claim of CP + [≥1 claims of acute pancreatitis (AP), CP or pancreatic cyst/pseudocyst]; b) 1 claim of CP + [≥1 claims for AP, CP or pancreatic cyst/pseudocyst in ≥3 months before or after the index CP claim]; c) ≥2 claims for CP; and d) ≥2 claims for CP separated by ≥ 6 months.

Results: Of 48.67 million eligible enrollees, 37,061 received the diagnosis of CP (mean age, 51.2 ± 15.2 years; 49% male). The age- and sex- adjusted period prevalence of CP per 100,000 was 73.4 (95% CI, 72.6-74.1), 98.7 (95% CI, 97.7-99.7) for adults and 8.3 (95% CI, 7.8-8.8) for children. Prevalence of CP was slightly higher in males (sex ratio, 1.05) and highest in the age group of 46-55 years (135/100,000). On sensitivity analysis, the prevalence of CP per 100,000 decreased to 60.2, 39.7, 38.8, and 18.8 with each of the alternative definitions.

Conclusion: Prevalence estimates reported in our study provide an insight into the population burden of CP in the US.
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http://dx.doi.org/10.1016/j.pan.2019.07.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6756969PMC
September 2019

Reply.

Clin Gastroenterol Hepatol 2019 12 17;17(13):2827. Epub 2019 Jun 17.

Division of Gastroenterology and Hepatology, University of Colorado Anschutz Medical Center, Aurora, Colorado.

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http://dx.doi.org/10.1016/j.cgh.2019.06.016DOI Listing
December 2019

Per Oral Pancreatoscopy Identification of Main-duct Intraductal Papillary Mucinous Neoplasms and Concomitant Pancreatic Duct Stones: Not Mutually Exclusive.

Pancreas 2019 07;48(6):792-794

Division of Gastroenterology, Baylor St. Luke's Medical Center, Houston, TX.

Objectives: Per oral pancreatoscopy (POP) assists in the evaluation and treatment of select benign and neoplastic pancreatic disorders including main-duct intraductal papillary mucinous neoplasm (MD-IPMN). Although pancreatic duct stones are classically thought of as pathognomonic for chronic pancreatitis, its co-occurrence with MD-IPMN as identified via POP may help identify an alternative etiology for presumed idiopathic chronic pancreatitis.

Methods: This was a multicenter retrospective case series of patients found to have pancreatic duct stones with concomitant MD-IPMN by POP.

Results: Thirteen patients with presumed idiopathic chronic calcific pancreatitis were found on POP to have both pancreatic duct stones and MD-IPMN. All patients had a dilated pancreatic duct, and most (92.3%) were symptomatic.

Conclusions: Per-oral pancreatoscopy may identify MD-IPMN as an etiology for patients with presumed idiopathic chronic calcific pancreatitis and associated dilated pancreatic duct. Larger prospective studies are needed to validate these findings.
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http://dx.doi.org/10.1097/MPA.0000000000001333DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6582996PMC
July 2019

Pharmacologic management and prevention of acute pancreatitis.

Curr Opin Gastroenterol 2019 09;35(5):460-467

Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania.

Purpose Of Review: The present article will focus in pharmacologic agents that have been studied to improve acute pancreatitis outcomes, and to prevent the disease at different levels.

Recent Findings: Too little and too much early fluid resuscitation can be harmful. The optimal volume, rate, and duration of intravenous fluid therapy is still unknown. Nonopioid analgesics should be the first line of analgesia in patients with acute pancreatitis. A few pharmacologic agents evaluated in acute pancreatitis have resulted in positive pilot trials; however, larger randomized clinical trials (RCTs) are needed before final conclusions. Statin use is associated with lower incidence of acute pancreatitis in the general population and ongoing studies are evaluating its preventive role in acute pancreatitis recurrences. The preventive role of rectal indomethacin in post-endoscopic retrograde cholangiopancreatography pancreatitis is indisputable, with subject selection and timing of administration requiring further investigation.

Summary: There is still no proven effective disease-specific pharmacologic therapy that changes the natural history of acute pancreatitis. New therapeutic targets and pharmacologic agents are in the horizon. Careful refinement in study design is needed when planning future RCTs. There is also a need for drug development aiming at reducing the incidence of the disease and preventing its sequelae.
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http://dx.doi.org/10.1097/MOG.0000000000000563DOI Listing
September 2019

Endoscopic Ultrasound Placement of Preloaded Fiducial Markers Shortens Procedure Time Compared to Back-Loaded Markers.

Clin Gastroenterol Hepatol 2019 12 28;17(13):2749-2758.e2. Epub 2019 Apr 28.

Division of Gastroenterology and Hepatology, University of Colorado Anschutz Medical Center, Aurora, Colorado. Electronic address:

Background & Aims: Fiducial markers are inert radiopaque gold or carbon markers implanted in or near pancreatic tumor to demarcate areas for image-guided radiation therapy. Endoscopic ultrasound (EUS) pre-loaded fiducial needles (PLNs) have been developed to circumvent technical issues associated with traditional back-loaded fiducials (BLNs). We performed a randomized controlled trial to compare procedure times in patients with pancreatic adenocarcinoma undergoing EUS-guided placement of BLNs vs PLNs.

Methods: In a prospective study, 44 patients with pancreatic adenocarcinoma referred for fiducial marker placement at 2 tertiary care centers were assigned to groups that received PLNs (n = 22) or BLNs (n = 22); each group had the same proportion of patients with tumors of different locations (head or neck vs body or tail).The procedure was standardized among all endoscopists and placement of a minimum of 3 markers inside the tumor was defined as technical success. The times for procedure and fiducial placement were recorded, total number of fiducial markers used documented, and grade of procedure difficulty ranked by passing the needle or deploying the fiducials. Other recorded variables included tumor characteristics, fluoroscopy use, and the number of fiducials clearly seen by EUS and fluoroscopy. The primary aim was to compare the duration of EUS-guided fiducial insertion of BLNs vs PLNs.

Results: The median placement time was significantly shorter in the PLN group (9 min) than the BLN group (16 min) (P < .001). However, the 44% reduction in time did not reach pre-specified levels (≥60%). Similar results were found after stratifying by tumor location. Deployment of BLNs was easier than deployment of PLNs (P = .03). There was no significant difference between groups in technical success, number of fiducials placed, EUS or fluoroscopic visualization, or adverse events. During simulation computed tomography and image-guided radiation therapy, there was no difference between groups in visualization of fiducials, migration rate, or accuracy of placement.

Conclusions: In a randomized controlled trial of 44 patients with pancreatic adenocarcinoma, we found EUS-guided placement of PLNs to require less time and produce similar results compared with BLNs. Further refinements in PLN delivery system are needed to increase the ease of deployment. Clinicaltrials.gov no: NCT02332863.
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http://dx.doi.org/10.1016/j.cgh.2019.04.046DOI Listing
December 2019

A Survey of Expert Practice and Attitudes Regarding Advanced Imaging Modalities in Surveillance of Barrett's Esophagus.

Dig Dis Sci 2018 12 3;63(12):3262-3271. Epub 2018 Sep 3.

University of Colorado Anschutz Medical Center, Mail Stop F735, 1635 Aurora Court, Rm 2.031, Aurora, CO, 80045, USA.

Background: Published guidelines do not address what the minimum incremental diagnostic yield (IDY) for detection of dysplasia/cancer is required over the standard Seattle protocol for an advanced imaging modality (AIM) to be implemented in routine surveillance of Barrett's esophagus (BE) patients. We aimed to report expert practice patterns and attitudes, specifically addressing the minimum IDY in the use of AIMs in BE surveillance.

Methods: An international group of BE experts completed an anonymous electronic survey of domains relevant to surveillance practice patterns and use of AIMs. The evaluated AIMs were conventional chromoendoscopy (CC), virtual chromoendoscopy (VC), volumetric laser endomicroscopy (VLE), confocal laser endomicroscopy (CLE), and wide-area transepithelial sampling (WATS). Responses were recorded using five-point balanced Likert items and analyzed as continuous variables.

Results: The survey response rate was 84% (61/73)-41 US and 20 non-US. Experts were most comfortable with and routinely use VC and CC, and least comfortable with and rarely use VLE, CLE, and WATS. Experts rated data from randomized controlled trials (1.4 ± 0.9) and guidelines (2.6 ± 1.2) as the two most influential factors for implementing AIMs in clinical practice. The minimum IDY of AIMs over standard biopsies to be considered of clinical benefit was lowest for VC (15%, IQR 10-29%) and highest for VLE (30%, IQR 20-50%). Compared to US experts, non-US experts reported higher use of CC for BE surveillance (p < 0.001).

Conclusion: These results should inform benchmarks that need to be met for guidelines to recommend the routine use of AIMs in the surveillance of BE patients.
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http://dx.doi.org/10.1007/s10620-018-5257-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6541486PMC
December 2018

Practice Patterns and Utilization of Tube Feedings in Acute Pancreatitis Patients at a Large US Referral Center.

Pancreas 2018 10;47(9):1150-1155

Department of Surgery, University of Pittsburgh Medical Center.

Objectives: Clinical trials on tube feedings (TFs) have not been sufficiently powered to change practice patterns in acute pancreatitis (AP). We aimed to describe the use, duration, and resource utilization of TF in AP patients at an expert US center.

Methods: Of 423 AP patients prospectively enrolled at the University of Pittsburgh Medical Center from 2004 to 2014, 139 (33%) received TF. Data on TF were assessed in 100 (72%) of 139 patients with complete data available.

Results: Patients on TF were more likely to be male, be obese, have alcohol etiology, and have moderately severe (34% vs 19%) or severe AP (62% vs. 3%) (P < 0.05). Tube feedings were started after a median of 5 days (interquartile range, 3-8 days) from admission and were administered for a median of 39 days (interquartile range, 19-58 days). A nasojejunal route (95%) with an oligomeric formula (92%) was the preferred TF strategy. Feeding tube complications led to at least 1 endoscopic tube replacement in 42% of patients and to an unexpected health care visit in 29% of those discharged on TF (16/55 patients).

Conclusions: Tube feedings form an important component in the management of patients with moderately severe and severe AP. Further studies should define the optimal utilization of TF and ways to reduce TF-related complications.
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http://dx.doi.org/10.1097/MPA.0000000000001141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6131057PMC
October 2018

Will Abandoning Fine-Needle Aspiration Increase Diagnostic Yield From Tissues Collected During Endoscopic Ultrasound?

Clin Gastroenterol Hepatol 2018 08 21;16(8):1203-1206. Epub 2018 Apr 21.

Division of Gastroenterology and Hepatology, University of Colorado Anschutz Medical Campus, Aurora, Colorado.

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http://dx.doi.org/10.1016/j.cgh.2018.04.021DOI Listing
August 2018

A population-based evaluation of the natural history of chronic pancreatitis.

Pancreatology 2018 Jan 24;18(1):39-45. Epub 2017 Nov 24.

University of Pittsburgh Medical Center, Pittsburgh, PA, United States. Electronic address:

Background: Based on reports from tertiary care centers, chronic pancreatitis (CP) is considered to be a painful and debilitating disease frequently requiring invasive interventions. Our primary aim was to assess the natural course of CP in a population-based cohort using endoscopic and surgical interventions as surrogates for disease aggressiveness.

Methods: We identified all patients (n = 89, alcoholic [ACP = 46], non-alcoholic [NACP] = 43) with newly diagnosed definite CP from Olmsted County, Minnesota between 1977 and 2006. Patients were followed until death or censoring. Medical records were reviewed at time of diagnosis and during each follow-up. Both lifetime proportions and cumulative incidence since the initial manifestation of CP were estimated and compared. Survival was estimated with Kaplan-Meier methodology.

Results: Median age at CP diagnosis was 56 years (IQR, 48-67) and 56% were male. During median follow-up of 10 years, 68 (76%) experienced pancreatic pain, but only 27 (30%) needed any invasive therapeutic intervention: 23% had endotherapy and 11% had pancreatic surgery. During the clinical course, when compared with NACP, ACP patients had significantly more (all p < 0.05) pain (87 vs. 65%), recurrent acute pancreatitis (44 vs. 23%), pseudocysts (41 vs. 16%), cumulative incidence of exocrine insufficiency (60 vs. 21%), and annual hospitalizations after CP diagnosis (0.79 vs. 0.25). The cumulative risk of diabetes, calcifications, surgery and overall survival was similar in ACP and NACP.

Conclusions: Our study suggests that CP at a population level may have a milder course than that reported from tertiary centers. We confirm that ACP has a more severe phenotype than NACP.
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http://dx.doi.org/10.1016/j.pan.2017.11.012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5794616PMC
January 2018

Peripheral Eosinophilia in Patients With Inflammatory Bowel Disease Defines an Aggressive Disease Phenotype.

Am J Gastroenterol 2017 12 7;112(12):1849-1858. Epub 2017 Nov 7.

Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.

Objectives: Peripheral blood eosinophilia (PBE) in inflammatory bowel disease (IBD) is associated with ulcerative colitis (UC) and active disease. Little data exist on the long-term impact of PBE on disease course. We aimed to investigate the multi-year patterns of PBE and its impact on disease severity in a large IBD cohort.

Methods: We performed a registry analysis of a consented, prospective, natural history IBD cohort at a tertiary center from 2009 to 2014. Demographics, comorbidities, disease activity, healthcare utilization, and time to hospitalization or surgical resection of patients who displayed PBE were compared to patients without PBE.

Results: Of the 2,066 IBD patients, 19.2% developed PBE. PBE was significantly associated with UC (P<0.001), extensive colitis (P<0.001), and shorter disease duration (P=0.03). Over six years, PBE patients had more active disease (Harvey-Bradshaw Index P=0.001; ulcerative colitis activity index P<0.001), concurrent C-reactive protein elevation (P<0.001), healthcare utilization (hospitalization P<0.001, IBD surgery P<0.001), and more aggressive medical therapy (prednisone P<0.001, anti-TNF P<0.001). Patients with PBE had a significantly reduced time to hospitalization in both UC (P<0.001) and Crohn's disease (CD) (P<0.001) and reduced time to colectomy in UC (P=0.003). On multivariable modeling, PBE remained significantly associated with hospitalization and surgery in both CD and UC. New diagnosis of UC with PBE was associated with increased steroid (P=0.007) and anti-TNF (P=0.001) requirement.

Conclusion: This multi-year study of a large IBD cohort suggests that peripheral blood eosinophilia represents a biomarker of a distinct IBD subgroup, with a unique inflammatory signature, and at risk for worse clinical outcomes.
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http://dx.doi.org/10.1038/ajg.2017.402DOI Listing
December 2017

Acute Pancreatitis Has a Long-term Deleterious Effect on Physical Health Related Quality of Life.

Clin Gastroenterol Hepatol 2017 Sep 1;15(9):1435-1443.e2. Epub 2017 Jun 1.

Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania; Division of Gastroenterology, Veterans Affairs Pittsburgh Health System, Pittsburgh, Pennsylvania. Electronic address:

Background & Aims: It is not clear how acute pancreatitis (AP) affects health related quality of life (HRQOL). We aimed to determine the long-term independent effect of AP on physical and mental HRQOL.

Methods: We analyzed data from 91 patients (mean 52 years of age, 54% women) admitted with AP to the University of Pittsburgh Medical Center from 2011 to 2015 who responded to telephone surveys at a median of 14 months after hospital discharge (interquartile range, 12-16 months). Individuals who did not answer the telephone survey were sent a questionnaire by regular mail. Patients answered questions from the 12-Item Short-Form Survey, and answers were used to calculate mental component summary (MCS) and physical component summary (PCS) scores with norm-based scoring (normal ≥50). HRQOL for these subjects was compared with that of age- and sex-matched individuals without pancreatitis (1:2) identified from the North American Pancreatitis Study. We controlled for other covariates using multivariable regression analysis.

Results: At follow-up, individuals with AP had a significantly lower PCS score (46.2 ± 11.8) than did control subjects (51.1 ± 9.5; P < .01), but a similar MCS score. A 4-point reduction of the PCS was attributed to AP after controlling for sociodemographic factors and medical comorbidities. The only pancreatitis-related factor associated with low PCS score was multisystem organ failure. Presence of abdominal pain, analgesic use, disability, and current smoking at the time of follow-up were also associated with lower PCS scores. Etiology of AP, disease severity (by Revised Atlanta classification), use of nutritional support, and performance of pancreatic interventions did not affect HRQOL at follow-up.

Conclusions: In a 14-month follow-up of patients hospitalized with AP, we found a meaningful, independent, and deleterious effect of AP in the physical HRQOL of these patients, compared to individuals without AP. Further research is needed to determine the duration of this impairment and to evaluate the effects of modifying risk factors.
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http://dx.doi.org/10.1016/j.cgh.2017.05.037DOI Listing
September 2017

Perspectives in Colonoscopy Perforation During Gastroenterology Fellowship.

ACG Case Rep J 2017 29;4:e45. Epub 2017 Mar 29.

University of Pittsburgh Pittsburgh, PA Associate Editor ACG Case Reports Journal.

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http://dx.doi.org/10.14309/crj.2017.45DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5371724PMC
March 2017

Epidemiology of Recurrent Acute and Chronic Pancreatitis: Similarities and Differences.

Dig Dis Sci 2017 07 9;62(7):1683-1691. Epub 2017 Mar 9.

Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, 200 Lothrop Street, M-2, C-Wing, Pittsburgh, PA, 15213, USA.

Emerging data in the past few years suggest that acute, recurrent acute (RAP), and chronic pancreatitis (CP) represent a disease continuum. This review discusses the similarities and differences in the epidemiology of RAP and CP. RAP is a high-risk group, comprised of individuals at varying risk of progression. The premise is that RAP is an intermediary stage in the pathogenesis of CP, and a subset of RAP patients during their natural course transition to CP. Although many clinical factors have been identified, accurately predicting the probability of disease course in individual patients remains difficult. Future studies should focus on providing more precise estimates of the risk of disease transition in a cohort of patients, quantification of clinical events during the natural course of disease, and discovery of biomarkers of the different stages of the disease continuum. Availability of clinically relevant endpoints and linked biomarkers will allow more accurate prediction of the natural course of disease over intermediate- or long-term-based characteristics of an individual patient. These endpoints will also provide objective measures for use in clinical trials of interventions that aim to alter the natural course of disease.
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http://dx.doi.org/10.1007/s10620-017-4510-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5478431PMC
July 2017

Quality of Life in Chronic Pancreatitis is Determined by Constant Pain, Disability/Unemployment, Current Smoking, and Associated Co-Morbidities.

Am J Gastroenterol 2017 04 28;112(4):633-642. Epub 2017 Feb 28.

University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.

Objectives: Chronic pancreatitis (CP) has a profound independent effect on quality of life (QOL). Our aim was to identify factors that impact the QOL in CP patients.

Methods: We used data on 1,024 CP patients enrolled in the three NAPS2 studies. Information on demographics, risk factors, co-morbidities, disease phenotype, and treatments was obtained from responses to structured questionnaires. Physical and mental component summary (PCS and MCS, respectively) scores generated using responses to the Short Form-12 (SF-12) survey were used to assess QOL at enrollment. Multivariable linear regression models determined independent predictors of QOL.

Results: Mean PCS and MCS scores were 36.7±11.7 and 42.4±12.2, respectively. Significant (P<0.05) negative impact on PCS scores in multivariable analyses was noted owing to constant mild-moderate pain with episodes of severe pain or constant severe pain (10 points), constant mild-moderate pain (5.2), pain-related disability/unemployment (5.1), current smoking (2.9 points), and medical co-morbidities. Significant (P<0.05) negative impact on MCS scores was related to constant pain irrespective of severity (6.8-6.9 points), current smoking (3.9 points), and pain-related disability/unemployment (2.4 points). In women, disability/unemployment resulted in an additional 3.7 point reduction in MCS score. Final multivariable models explained 27% and 18% of the variance in PCS and MCS scores, respectively. Etiology, disease duration, pancreatic morphology, diabetes, exocrine insufficiency, and prior endotherapy/pancreatic surgery had no significant independent effect on QOL.

Conclusions: Constant pain, pain-related disability/unemployment, current smoking, and concurrent co-morbidities significantly affect the QOL in CP. Further research is needed to identify factors impacting QOL not explained by our analyses.
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http://dx.doi.org/10.1038/ajg.2017.42DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5828017PMC
April 2017

Acute pancreatitis patient registry to examine novel therapies in clinical experience (APPRENTICE): an international, multicenter consortium for the study of acute pancreatitis.

Ann Gastroenterol 2017 1;30(1):106-113. Epub 2016 Dec 1.

Division of Gastroenterology and Hepatology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA (Georgios I. Papachristou, Jorge D. Machicado, Phil J. Greer, Mohannad Dugum, Efstratios Koutroumpakis Amir Gougol).

Background: We have established a multicenter international consortium to better understand the natural history of acute pancreatitis (AP) worldwide and to develop a platform for future randomized clinical trials.

Methods: The AP patient registry to examine novel therapies in clinical experience (APPRENTICE) was formed in July 2014. Detailed web-based questionnaires were then developed to prospectively capture information on demographics, etiology, pancreatitis history, comorbidities, risk factors, severity biomarkers, severity indices, health-care utilization, management strategies, and outcomes of AP patients.

Results: Between November 2015 and September 2016, a total of 20 sites (8 in the United States, 5 in Europe, 3 in South America, 2 in Mexico and 2 in India) prospectively enrolled 509 AP patients. All data were entered into the REDCap (Research Electronic Data Capture) database by participating centers and systematically reviewed by the coordinating site (University of Pittsburgh). The approaches and methodology are described in detail, along with an interim report on the demographic results.

Conclusion: APPRENTICE, an international collaboration of tertiary AP centers throughout the world, has demonstrated the feasibility of building a large, prospective, multicenter patient registry to study AP. Analysis of the collected data may provide a greater understanding of AP and APPRENTICE will serve as a future platform for randomized clinical trials.
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http://dx.doi.org/10.20524/aog.2016.0109DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5198234PMC
December 2016
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