It is well known that obesity has become a major health issue

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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2011;9: Inreased Perioperative Mortality Following Bariatri Surgery Among Patients With Cirrhosis JEFFREY D. MOSKO* and GEOFFREY C. NGUYEN,*, *Division of Gastroenterology, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada; and Division of Gastroenterology and Hepatology, Johns Hopkins Shool of Mediine, Baltimore, Maryland BACKGROUND & AIMS: The prevalene of nonaloholi fatty liver disease and ensuing irrhosis is expeted to inrease as a result of the obesity epidemi. These trends might inrease the number of bariatri surgeries among patients with irrhosis. We sought to assess the impat of irrhosis on perioperative mortality after bariatri proedures. METHODS: Data on patients who underwent bariatri surgery in the United States between 1998 and 2007 were extrated from the Nationwide Inpatient Sample. In-hospital mortality and length of stay were ompared for patients with no irrhosis, ompensated irrhosis, and deompensated irrhosis. RESULTS: Patients without irrhosis had lower mortality rates than those with ompensated and deompensated irrhosis (0.3% vs 0.9% and 16.3%, respetively, P.0002). After adjusting for ovariates, the adjusted odds ratio of mortality among ompensated and deompensated irrhoti patients ompared with nonirrhoti patients was 2.17 (95% onfidene interval, ) and 21.2 (95% onfidene interval, ), respetively. Mortality inreased with volume of surgery among enters; those with more than 100 surgeries per year had the lowest mortality rates, ompared with those with 50 to 100 surgeries per year and fewer than 50 surgeries per year (0.2% vs 0.4% and 0.7%, respetively; P.0001). The average length of stay was longer for patients with deompensated and ompensated irrhosis, ompared with patients without liver disease (6.7 and 4.4 d vs 3.2 d, respetively; P.0001 and P.03). CONCLUSIONS: Bariatri surgery in patients with irrhosis should be performed while liver disease is well ompensated. Patients with irrhosis should undergo surgery at enters that perform large numbers of these proedures. Keywords: Cirrhosis; Gastri Bypass; Mortality; Postoperative Compliations. It is well known that obesity has beome a major health issue worldwide. It is estimated that more than 300 million people are obese by definition (body mass index, 30). 1 In the United States, obesity is an epidemi with more than one-third of the population affeted, and this publi health problem is expeted to only worsen. 2 Obese patients have inreased morbidity and mortality beause it is assoiated with a plethora of health risks, most of whih are ompliations of their metaboli syndrome. Among these ompliations is nonaloholi fatty liver disease (NAFLD). With the inreasing prevalene of morbid obesity, the prevalene of NAFLD subsequently has inreased as well. NAFLD represents a spetrum of histologi liver lesions ranging from simple steatosis to nonaloholi steatohepatitis. The progressive form of nonaloholi steatohepatitis an progress to irrhosis, end-stage liver disease, and hepatoellular arinoma. 3 It is estimated that 20%- to 40% of patients with obesity-related nonaloholi steatohepatitis will progress to irrhosis. 4 Given the urrent epidemiologi trends, we therefore an antiipate a growing population of obese patients with irrhosis. Obesity also has been shown to be assoiated with a greater prevalene of perioperative morbidity and mortality after major surgial proedures. 5 Beause irrhosis also arries higher perioperative risks, 6 patients who are affeted by both obesity and irrhosis are partiularly high-risk surgial andidates. Many transplant enters have addressed this onern by establishing body mass index limits above whih they will no longer onsider andidates suitable for renal, liver, and lung transplantation. 7 Patients above suh thresholds are enouraged to lose weight before they an beome eligible. Although there are many behavioral, medial, and surgial approahes to the treatment of weight loss, bariatri surgery remains the most effetive treatment for morbid obesity. Adams et al, 8 in a large ohort study, showed an overall and ausespeifi derease in mortality of lose to 30%. As a result, the number of bariatri proedures performed in the United States has inreased dramatially. 9 Despite all of these trends, there are few data with respet to the safety and outomes of bariatri surgeries in patients with irrhosis. In this study, we onduted a large-sale, population-based omparison of bariatri surgial outomes in patients with and without irrhosis. We sought to extend previous literature in this area by determining perioperative mortality rates and length of stay in patients with no irrhosis, and ompensated and deompensated irrhosis. Methods Data Soure All data were extrated from the Nationwide Inpatient Sample (NIS) between 1998 and It is the largest all-payer database of national hospital disharges, maintained as part of the Healthare Cost and Utilization Projet by the Ageny for Healthare Researh and Quality. The NIS is a 20% stratified sample of nonfederal, aute-are hospitals in the United States. Eah reord in the NIS inludes a unique identifier, demo- Abbreviations used in this paper: ICD-9-CM, International Classifiation of Diseases, 9th Revision; NAFLD, nonaloholi fatty liver disease; NIS, Nationwide Inpatient Sample by the AGA Institute /$36.00 doi: /j.gh

2 898 MOSKO AND NGUYEN CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 9, No. 10 graphi data (age, sex, and rae), hospital transfer, admission type (emergent, urgent, or eletive), primary and seondary diagnoses (up to 15), primary and seondary proedures (up to 15), expeted primary and seondary insurane payers, total hospital harges, length of stay, and hospital harateristis (region, urban vs rural loation, bed size, teahing ). Study Population We used the Clinial Modifiation of the International Classifiation of Diseases, 9th Revision (ICD-9-CM) proedural odes to identify all patients in the NIS who had undergone bariatri surgery (44.31, 44.38, 44.39, 44.68, 44.95, 44.69, 43.89, 44.93, 44.50, 44.99, 45.90, 45.91, and 45.51) with a onurrent diagnosis for obesity between 1998 and We exluded all subjets with a diagnosis ode for gastri aner ( , 230.x). By using the Baveno IV lassifiation of irrhosis severity in ombination with ICD-9-CM odes, 3 groups of patients were extrated for omparison: (1) patients with no liver disease; (2) patients with ompensated liver disease (without asites or varieal bleeding: Baveno IV stages 1 and 2); and (3) patients with deompensated liver disease (with asites and/or varieal bleeding: Baveno IV stages 3 and 4). Preditor Variables Admissions were ategorized as having no irrhosis, ompensated irrhosis, or deompensated irrhosis. ICD-9-CM diagnosti odes were used to identify patients with irrhosis (see earlier). The designation of deompensated irrhosis required the presene of the diagnosis ode for asites (789.5) and/or varieal bleeding (456.0 or 456.2x). Data on rae and ethniity were derived from hospital administrative data and ategorized as non-hispani white, Afrian Amerian, Hispani, Asian or Paifi Islander, and other. A liver transplant enter was defined as a hospital or medial enter that performed at least 1 liver transplant during the year of the index admission. We dihotomized hospital bariatri proedural volumes as fewer than 50 proedures per year, 50 to 100 proedures per year, and more than 100 proedures per year. Primary outomes were in-hospital mortality and hospital length of stay. Statistial Analysis Data were analyzed using the Stata 10.0 SE software pakage (StataCorp LP, College Station, TX). Analyses ompared groups of patients with no irrhosis, and ompensated and deompensated irrhosis. These analyses took into aount the stratified 2-stage luster design by use of Stata s SVY (survey data) ommands inorporating individual disharge-level weights. Two-way 2 analyses and the Fisher exat test were performed to ompare ategori variables among different raial groups, and unpaired t tests ompared differenes in means of ontinuous variables. Crude mortality was alulated for the no irrhosis, ompensated irrhosis, and deompensated irrhosis groups. P values that were less than.05 were onsidered statistially signifiant. Survey-based multivariate logisti regression analysis was used to determine the assoiation between mortality and the presene of ompensated and deompensated irrhosis, while adjusting for age, sex, omorbidities, health insurane payer, rae/ethniity, proedural volume, hospital liver transplant, and hospital teahing. With respet to rae/ethniity, whih ontains 25% missing data, we retained reords that did not have rae/ethniity information in the analysis by reating an indiator variable for missing data. The survey data analyses took into aount the following: (1) sampling weights refleting the inverse probability of an observation being seleted during the sampling proess; (2) lustering of observations at the hospital level by use of generalized estimating equations; (3) sampling within strata defined by geographi region, rural versus urban loation, hospital transplant, and hospital teahing. We used a similar multivariable linear regression model to determine the assoiation between liver disease and hospital length of stay. Ethial Considerations The analysis of the NIS uses ompletely unidentified data with no risk of loss of onfidentiality, and an expedited review by the Institutional Review Board of the Johns Hopkins Medial Institutions deemed it exempt from further ethial review. Results Based on the sample in the NIS, there were an extrapolated 3888 bariatri proedures among ompensated irrhoti patients and 62 among deompensated irrhoti patients in the United States between 1998 and The demographi data of patients without liver disease and those with ompensated and deompensated liver disease who underwent bariatri surgery are shown in Table 1. Patients undergoing bariatri surgery in the presene of either ompensated or deompensated liver disease were more likely to be older and male relative to those without irrhosis. These patients also were less likely to have private health insurane. Compared with patients without liver disease, those with ompensated liver disease were more likely to have their surgery at a liver transplant enter. Patients with deompensated irrhosis were more likely to have a predominantly restritive type of proedure, and 40% of them underwent surgery at low-volume enters that performed fewer than 50 bariatri proedures a year. Mortality Rates Patients without irrhosis had lower mortality rates than those with ompensated and deompensated irrhosis (0.3% vs 0.9% and 16.3%, respetively; P.0002). The ombined in-hospital mortality rate for all irrhoti patients was 1.2%. Mortality rates improved with inreasing surgial volumes beause enters with more than 100 proedures per year had the lowest mortality rates when ompared with those with 50 to 100 and fewer than 50 proedures per year (0.2% vs 0.4% and 0.7%, respetively; P.0001). In patients with deompensated irrhosis, the in-hospital postoperative mortality rate was 41% at low-volume enters, whereas there were no deaths among deompensated inpatients after bariatri surgery at highvolume enters. Preditors of Mortality The assoiation between preditor variables and inhospital mortality is shown in Table 2. Among patients undergoing bariatri surgery, the assoiation between irrhosis and mortality remained substantial after adjusting for age, sex, omorbidities, health insurane payer, rae/ethniity, proedural volume, hospital transplant, and teahing. Patients with ompensated irrhosis had a more than 2-fold

3 Otober 2011 BARIATRIC SURGERY AND CIRRHOSIS 899 Table 1. Demographis of Cirrhoti and Nonirrhoti Patients Undergoing Bariatri Surgery No irrhosis (n 670,950) Compensated (n 3888) Cirrhosis Deompensated (n 62) Age, y a 53.8 a Mean Charlson a 1.3 a Index b Female sex 82% 71% 53% Rae/ethniity Non-Hispani 77.0% 84% 87% white Afrian 11% 4% Amerian Hispani 8% 10% Asian/Paifi 0.3% 0.3% Islander Other 3% 2% Health insurane Private 78% 67% 55% Mediare 8% 17% 32% Mediaid 6% 7% Self pay 5% 5% Other 3% 4% Geographi region Northeast 28% 21% Midwest 19% 18% South 31% 31% 35% West 22% 30% 48% Hospital loation Urban 96% 97% Rural 4% 3% Hospital size b Small or 37% 38% 52% medium Large 63% 62% 48% Hospital teahing Nonteahing 45% 42% 40% Teahing 55% 58% 60% Liver transplant 14% 20% enter Type of proedure d Malabsorptive 86% 85% 57% a or mixed Predominantly 14% 14% 43% a restritive Low-volume enter ( 50 gastri bypasses/y) 8% 8% 40% a a P.05 ompared with nonirrhoti patients. b Defined by the number of short-term aute-are hospital beds and speifi to the hospital s teahing, and geographi and urban vs rural loation. The total ount in the ell for this demographi variable is 10 and annot be dislosed per Ageny for Healthare Researh and Quality poliy. d Predominantly restritive proedures inluded sleeve gastretomy, vertial banded gastroplasty, laparosopi adjustable gastri banding, and plaement of an intragastri balloon. higher mortality rate (odds ratio, 2.17; 95% onfidene interval, ) than those without irrhosis, whereas those with deompensated irrhosis had a greater than 20-fold higher mortality rate (odds ratio, 21.2; 95% onfidene interval, ). Other fators assoiated with inreased mortality inluded inreasing age, having omorbidities, being insured by Mediare or Mediaid, having surgery at a transplant enter, and being Cauasian (Table 2). In ontrast, female sex and undergoing surgery at a higher-volume enter orresponded with dereased mortality. Hospital Length of Stay The average hospital length of stay was longer in patients with deompensated and ompensated irrhosis ompared with patients without liver disease (6.7 and 4.4 d vs 3.2 d, respetively; P.0001 and P.0273). After adjustment for age, sex, omorbidities, health insurane payer, rae/ethniity, proedural volume, hospital transplant, and teahing, patients with ompensated irrhosis had a 16% longer length of stay (95% onfidene interval, 9% 23% inrease) (Table 3). Disussion Our study was a large population-based, nationally representative study assessing outomes of bariatri surgeries in patients with irrhosis. We have shown that even though both Table 2. Multivariate Analysis of Preditors of In-Hospital Mortality Adjusted odds ratio (95% onfidene interval) P value Liver disease No irrhosis Compensated irrhosis 2.2 ( ).041 Deompensated 21.1 ( ).0001 irrhosis Age, y 1.04 ( ).0001 Mean Charlson Index 1.2 ( ).0001 Female sex 0.4 ( ).0001 Rae/ethniity Non-Hispani white Afrian Amerian 1.9 ( ).001 Hispani white 1.3 ( ).25 Asian/Paifi Islander 1.2 ( ).62 Health insurane Private Mediare 2.6 ( ).0001 Mediaid 3.5 ( ).0001 Self pay 0.6 ( ).157 Other 1.4 ( ).263 Hospital teahing Nonteahing Teahing 1.3 ( ).13 Hospital transplant Nontransplant Transplant 1.5 ( ).001 Hospital surgial volumes per y ( ) ( ).0001

4 900 MOSKO AND NGUYEN CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 9, No. 10 Table 3. Multivariate Analysis of Preditors of In-Hospital Length of Stay Relative hange, % (95% onfidene interval) P value Liver disease No irrhosis Compensated irrhosis 16 (9% 23%).0001 Deompensated 37 ( 26% to 156%).311 irrhosis Age (per y) 0.2 (0.1% 0.2%).0001 Mean Charlson Index 7 (6% 8%).0001 Female sex 2 ( 4% to 1%).062 Rae/ethniity Non-Hispani white Afrian Amerian 4 (0% 8%).021 Hispani 2 ( 7% to 2%).301 Asian/Paifi Islander 13 ( 22% to 3%).010 Health insurane Private Mediare 15 (11% 19%).0001 Mediaid 20 (14% 26%).0001 Self pay 15 ( 19% to 11%).0001 Other 1 ( 7% to 5%).785 Hospital teahing Nonteahing Teahing 4% ( 3% to 10%).262 Hospital transplant Nontransplant Transplant 6% ( 10% to 25%).477 Hospital surgial volumes per y % ( 27% to 17%) % ( 37% to 30%).0001 ompensated and deompensated irrhosis negatively impat postsurgial outomes, the effet was muh more pronouned in the latter group. In addition, we have shown that undergoing bariatri surgery at high-volume enters may ameliorate poor outomes in irrhoti patients. Although there is a definite pauity of studies speifially looking at weight loss surgery in irrhoti patients, there have been studies addressing outomes in bariatri surgery as well as irrhoti patients separately. Overall 30-day mortality rates for bariatri surgial proedures have been reported to be less than 1%. 10 Flum et al 11 reviewed 16,155 Mediare benefiiaries undergoing bariatri proedures. They found higher mortality rates in older patients, males, and for proedures performed in low-volume enters. In our nonirrhoti population, we found an overall in-hospital mortality rate of 0.3%. However, these reflet only in-hospital mortality and not death events that may our after disharge. In keeping with previous literature, we also found that inreasing age, male sex, and low-volume enters were assoiated with inreased mortality. With respet to mortality rates in irrhoti patients, Millwala et al 12 reported mortality rates ranging from 8.3% to 25% for irrhoti patients undergoing various surgial proedures (ompared with 1.1% in nonirrhoti patients). A single-enter study retrospetively reviewed 50 patients with irrhosis undergoing laparosopi surgeries (1 of whih was a Roux-en-Y gastri bypass). They had no deaths and the mean length of stay in the hospital was 3 days. 13 More reently, Takata et al 7 reviewed 8 patients with irrhosis undergoing laparosopi sleeve gastretomy. Although ompliations developed in 2 of 8 patients, no patients died. Finally, Dallal et al 14 performed an analysis of 27 laparosopi Roux-en-Y gastri bypasses and 3 laparosopi sleeve gastretomies in 30 patients with Child Pugh lass A irrhosis. Again, no mortality ourred, yet one-third developed ompliations extending their hospital stay. The in-hospital mortality rate of 0.9% found in the ompensated irrhoti patients in our study likely an be aounted for by the large sample size. No other study enrolled enough patients to assess perioperative mortality adequately. We found that patients with irrhosis had higher mortality rates when ompared with those with no liver disease. Although there is no previous literature with whih to make diret omparisons, these findings are ongruent with previous evidene that patients with liver disease are at inreased surgial risk owing to altered and diffiult to ontrol hemodynamis, asites, and oagulopathies. The lower overall mortality rate assoiated with bariatri surgery relative to other major surgial proedures is most likely owing to the eletive nature of these proedures, whih allows patients to undergo preoperative medial optimization. However, a irrhosis-assoiated mortality rate of 1.2% for an eletive proedure remains linially signifiant. We found that enters with higher volumes of bariatri proedures had lower mortality rates. This finding is in keeping with previous literature. 15 In addition to greater proedural experiene, large-volume enters also may have the resoures to manage potential surgial ompliations. It would seem intuitive that high-risk populations should undergo bariatri surgery at large-volume enters. However, our finding that 40% of deompensated patients underwent bariatri proedures at lowvolume enters raises onerns over suboptimal delivery of are. Interestingly, bariatri surgery performed at a liver transplant enter was assoiated with inreased mortality. This may be owing to treatment seletion bias in whih siker irrhoti patients may be preferentially referred to and undergo surgery in liver transplant enters. Finally, we found that patients with ompensated and deompensated irrhosis stayed in the hospital longer after their bariatri proedures. This was in keeping with previous literature. As previously disussed, patients with liver disease are at an inreased surgial risk attributable to their underlying disease and subsequent altered systemi physiology. These alterations are, in fat, more likely to ontribute to morbidity than mortality, translating into an inreased stay in the hospital. In the aforementioned study by Dallal et al, 14 the early ompliations that ourred inluded anastomoti leak, aute tubular nerosis, prolonged intubation, ileus, and blood transfusion. Compliations speifi to bariatri surgery inlude bleeding, wound infetion, leaks, venous thromboemboli events, and ardiovasular and pulmonary ompliations. As previously disussed, patients with irrhosis, and partiularly deompensated irrhosis, are at a signifiantly inreased risk of all suh ompliations. Our study had several limitations. Our small ohort of deompensated irrhoti patients undergoing bariatri surgeries often prevented omparison between groups. This made it diffiult to determine the magnitude of inreased risk between ompensated and deompensated irrhoti patients. The use of

5 Otober 2011 BARIATRIC SURGERY AND CIRRHOSIS 901 registry data suh as the NIS database prevents the aquisition of the personal identifiers neessary to validate the ICD-9-CM diagnosti odes. However, the use of ICD-9-CM odes to identify irrhosis has been shown to have good negative and positive preditive value in other administrative databases. 16 Moreover, we would not expet any oding errors to be differential with respet to irrhosis. Suh nondifferential mislassifiations usually lead to onservative estimates of assoiation between irrhosis and outomes. An additional limitation of administrative databases is that they lak the linial information with whih to use previously validated measurements of liver disease severity suh as the Child Pugh and the Model for End-Stage Liver Disease soring systems. These disease measures would have allowed for more preise patient lassifiation of severity of liver disease and thus better appliability to individual patient are and surgial risk assessment. Despite these limitations, our analysis had a number of strengths, whih we believe enhanes its linial relevane and makes it an important ontribution to the developing ompilation of literature on this subjet matter. Our study was population-based with outomes that are refletive of aademi and ommunity hospitals throughout the United States, whih inherently enhanes its generalizability. Finally, the relatively large sample size allowed for statistial analysis inluding adjustment for ovariates known to impat surgial risk. Beause bariatri proedures have been shown to have a profound and sustained weight loss in most patients, the number of bariatri proedures is inreasing at an impressive rate. This trend oupled with the emergene of NAFLD and irrhosis assoiated with the obesity epidemi, may lead to an inreasing prevalene of irrhoti patients pursuing bariatri proedures in an effort to improve their risk of obesity-related onsequenes and potentially to qualify for transplantation. The data presented in this study argues for enhaned preoperative assessment before bariatri surgery as well as the onsideration for early intervention for obesity before the progression to ompensated and deompensated irrhosis. Multienter prospetive studies still are needed to haraterize long-term outomes and enable the development of linial preditive models to more preisely identify whih irrhosis patients are not safe to proeed with bariatri surgery and those who would derive benefit. Consequently, suh studies would failitate the development and implementation of strategies to improve bariatri surgery outomes in patients with irrhosis. erenes 1. World Health Organization. Obesity and overweight. Available at: en/. 2. Flegal KM, Carroll MD, Ogden CL, et al. Prevalene and trends in obesity among US adults, JAMA 2002;288: Guajardo-Salinas GE, Hilmy A. Prevalene of nonaloholi fatty liver disease (NAFLD) and utility of FIBROspet II to detet liver fibrosis in morbidly obese Hispano-Amerian patients undergoing gastri bypass. Obes Surg 2009;12: Tihansky DS, Madan AK. Laparosopi Roux-en-Y gastri bypass is safe and feasible after orthotopi liver transplantation. Obes Surg 2005;15: Rafiq N, Younossi ZM. Effets of weight loss on nonaloholi fatty liver disease. Semin Liver Dis 2008;4: Rizvon MK, Chou CL. Surgery in the patient with liver disease. Med Clin North Am 2003;87: Takata MC, Campos GM, Ciovia R, et al. Laparosopi bariatri surgery improves andiday in morbidly obese patients awaiting transplantation. Surg Obes Relat Dis 2008;4: Adams TD, Gress RE, Smith SC, et al. Long-term mortality after gastri bypass surgery. N Engl J Med 2007;357: Helling TS, Helzberg JH, Nahnani JS, et al. Preditors of nonaloholi steatohepatitis in patients undergoing bariatri surgery: when is liver biopsy indiated? Surg Obes Relat Dis 2008;4: Buhwald H, Avidor Y, Braunwald E, et al. Bariatri surgery: a systemati review and meta-analysis. JAMA 2004;292: Flum DR, Salem L, Elrod JA, et al. Early mortality among Mediare benefiiaries undergoing bariatri surgial proedures. JAMA 2005;294: Millwala F, Nguyen GC, Thuluvath PJ. Outomes of patients with irrhosis undergoing non-hepati surgery: risk assessment and management. World J Gastroenterol 2007;13: Cobb WS, Heniford BT, Burns JM, et al. Cirrhosis is not a ontraindiation to laparosopi surgery. Surg Endos 2005;19: Dallal RM, Mattar SG, Lord JL, et al. Results of laparosopi gastri bypass in patients with irrhosis. Obes Surg 2004;14: Hollenbeak CS, Rogers AM, Barrus B, et al. Surgial volume impats bariatri surgery mortality: a ase for enters of exellene. Surgery 2008;144: Kramer JR, Davila JA, Miller ED, et al. The validity of viral hepatitis and hroni liver disease diagnoses in Veterans Affairs administrative databases. Aliment Pharmaol Ther 2008;27: Reprint requests Address requests for reprints to: Geoffrey C. Nguyen, MD, PhD, FRCPC, Mount Sinai Hospital, 600 University Avenue, Suite 437, Toronto, Ontario M5G 1X5, Canada. fax: (416) geoff.nguyen@utoronto.a Conflits of interest The authors dislose no onflits. Funding Supported by a Canadian Institutes for Health Researh, Canadian Assoiation of Gastroenterology, and the Crohn s and Colitis Foundation of Canada New Investigator Award and an AGA Researh Sholar Award (G.C.N.). The sponsors had no role in the oneptualization, design, or interpretation of the study.

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