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Measurement of visceral fat on preoperative computed tomography predicts complications after sigmoid colectomy for diverticular disease Rafel Tappouni, M.D.a, Paul Mathew, B.S.b, Tara M. Connelly, M.B., B.Ch., M.Sc.b, Franklyn Luke, M.D.c, Evangelos Messaris, M.D., Ph.D.b,* a

Department of radiology, Wake Forest School of Medicine, One Medical Center Boulevard, WinstonSalem, NC 27157, USA; bDepartment of Surgery, Division of Colon & Rectal Surgery, The Pennsylvania State University, College of Medicine, 500 University Drive, Hershey, PA 17033, USA; cDepartment of radiology, The Pennsylvania State University, College of Medicine, 500 University Drive, Hershey, PA 17033, USA

KEYWORDS: Diverticulitis; Volumetric fat parameters; Visceral fat; Complications; Sigmoidectomy

Abstract BACKGROUND: Visceral and subcutaneous abdominal fat parameters have been associated with worse surgical outcomes in colorectal cancer but have not been investigated in diverticulitis. METHODS: Volumetric fat parameters were measured on preoperative computed tomography scans from 211 diverticulitis patients. Primary outcome was a serious postoperative complication (ClavienDindo grades 2-4). Variables including age, disease duration, American Society of Anesthesiology score, ostomy, immunosuppression, body mass index, and volumetric fat parameters were examined. SPSS was used for statistics. RESULTS: The serious postoperative complication rate was 12.7%. On univariate analysis, several factors including older age (P 5 .0001), ostomy creation (P 5 .02), higher visceral fat (VF, P 5 .01), emergent surgery (P 5 .05), and higher American Society of Anesthesiology score (P 5 .05) were associated with complications. On multivariate regression analysis, only VF was independently associated with complications. CONCLUSIONS: Diverticulitis patients with high VF are more likely to develop complications after sigmoidectomy. VF measurement may potentially be used as a tool to assist in surgical decision making and prediction of outcomes. Ó 2015 Elsevier Inc. All rights reserved.

The authors declare no conflicts of interest. * Corresponding author. Tel.: 11-717-531-5164; fax: 11-717-5310646. E-mail address: [email protected] Manuscript received June 4, 2014; revised manuscript October 11, 2014 0002-9610/$ - see front matter Ó 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2014.10.026

Diverticular disease (DD) is one of the most common colonic disorders in Western societies. The prevalence of DD increases with age and affects over 60% of individuals 50 years or older.1 Presently, the incidence of DD is rising and the mean age of patients with DD is decreasing.2 The majority of patients with DD remain asymptomatic; however, approximately 20% experience symptoms related to diverticulitis such as abdominal pain, pyrexia, diverticular bleeding,

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and/or altered bowel habit.3 Up to 20% of this symptomatic subgroup of patients require surgical intervention.4 Surgery is indicated for recurrent episodes and serious DD complications such abscesses, perforation, bleeding, obstruction, and fistula formation.5 Obesity has been linked to an increased risk of cardiovascular disease, metabolic syndrome, hypertension, diabetes mellitus, and, more recently, diverticulitis and its associated complications.2,6,7 In the United States, as obesity rates rise, a concurrent increase in the number of reported episodes of diverticulitis has been observed.8 Abdominal or ‘‘central’’ obesity is the most prevalent manifestation of obesity and is a marker of dysfunctional adipose tissue.9 Intra-abdominal or visceral fat (VF) has been demonstrated to be a proinflammatory cytokine-producing organ.10 Additionally, increased VF has been demonstrated to be a prognostic marker of surgical outcomes following hepatectomy, gastrectomy, and colectomy for colon cancer.11–14 Several studies have reported an association between various obesity parameters such as body mass index (BMI), waist circumference, waist-to-hip ratio, and VF and the occurrence of DD and its complications.7,15–17 VF, measured using ultrasound, has been shown to be an independent risk factor for both the development of DD18 and diverticulitis-associated complications.17 However, there are no published data evaluating the relationship between VF and postoperative complications in this patient cohort. We hypothesize that (1) increased visceral adiposity correlates with the risk of complications following sigmoidectomy for diverticulitis and (2) quantitative assessment of VF may provide a radiological tool to assist in predicting postoperative outcomes and providing accurate prognoses. The purpose of this study was to examine the relationship between radiologically derived volumetric measurements of VF and complications arising following sigmoidectomy for diverticulitis.

transfer from the picture archiving and communication system to iNtuition for fat analysis because of technical issues. Ultimately, 211 patients in total were included in this study. This was a retrospective study of CT scans performed as part of previous clinical care and as such informed consent was waived. A review of medical records was performed. Patient demographics (sex, smoking history, age at diagnosis, age at sigmoid resection, comorbidities [Charlson comorbidity score],19 perioperative steroid and/or immunosuppressant use, presence of diabetes mellitus, BMI, American Society of Anesthesiology [ASA] score and duration of DD) and operative factors (surgical indication, surgical approach [laparoscopic vs open], and requirement for ostomy creation during sigmoid resection) were recorded. Thirty-day postoperative surgical complications using the Clavien– Dindo score20 and 90-day readmission data were recorded. The Clavien–Dindo Scoring system is a validated, widely used scoring system for the classification of postoperative complications. Clavien–Dindo grades were annotated as follows: Grade I: Any deviation from the expected or normal postoperative course.

Patients and Methods

 Includes wounds opened at the beside for infection and the use of anti-emetics, and/or antipyretics  Excludes surgical, radiological, or endoscopic intervention Grade II: All other pharmacological treatment not included in Grade I.  Includes the use of total parenteral nutrition and blood transfusions Grade III: Surgical, radiological, or endoscopic intervention required. Grade IV: Complication that is a threat to life requiring management in the ICU.  Includes organ dysfunction, major cerebral vascular accident, and so on.

Patient identification In this Internal Review Board approved study, all patients undergoing sigmoid resection for diverticulitis between January 1, 2002 and December 31, 2012 (n 5 288) at Penn State, Milton S. Hershey Medical Center were identified from the institutional Structured Query Language database using International Statistical Classification of Diseases 10 codes for diverticulitis and sigmoid resection. An abdominal computed tomography (CT) scan taken less than 1 month before sigmoid resection was required for inclusion in the study. Of the 288 identified patients, 50 did not have preoperative CT scans (42 had barium enemas, 2 had no radiographical imaging, 6 had images taken .1 month preoperatively), 23 had CT images that were cut-off at 3 or more anatomic levels of study, 1 had hepatomegaly with the liver occupying greater than 50% of the abdominal cavity, and 3 patients’ images would not

CT analysis Abdominal CT images were taken after the administration of contrast in a 16-slice multi dimensional CT scanner (Siemens Medical solutions, Malvern, PA) using 120 kV and 200 mA and a slice thickness of 3 to 8 mm, a matrix of 512 ! 512 and pixel size .585 to .859 mm. TeraRecon iNtuition software (TeraRecon, Foster City, CA) was used to measure fat parameters in a semi-automated manner. The software identifies and highlights subcutaneous fat and VF in blue and green, respectively. The clinician must then ensure that the highlighted area is correct before continuing. A CT range of 2120 to 240 Hounsfield units was used to encompass all fat. Thus, lower tissue density and increased fat content are represented by a smaller number of Hounsfield units.21 For each scan, the lumbar (L) 1 vertebral plane was identified

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on a sagittal image. The view was then switched to the axial plane and 4 measurements were taken at the level of each midvertebral body from L1 to L5. The 4 measurements were as follows: (1) total cross-sectional area of visceral/ intra-abdominal adiposity or ‘‘VF’’ measured in cm2; (2) total cross-sectional area of subcutaneous adiposity or ‘‘subcutaneous fat’’ (SF) measured in cm2; (3) abdominal circumference (AC) measured in cm; and (4) visceral: subcutaneous ratio (VSR, %) as calculated by the iNtuition software using the formula VF/(SF 1 VF). The fat analysis software and measurement of fat parameters are demonstrated in Figs. 1 and 2. The averages of the results taken at the 5 vertebral levels for each of these 4 measurements were then calculated for each patient. This provided a single value at each parameter (SF, VF, AC, VSR) for each patient.

Statistical analysis SPSS (IBM, Armonk, NY) software was used for statistical analysis. The chi-square and the Mann-Whitney tests were used for comparison of the groups’ baseline characteristics (those with postoperative complications and/ or 90-day readmissions versus those without). The Pearson’s test was used for bivariate correlations. Quantitative variables are expressed as mean values 6 standard deviation. All variables that were found to be associated with

Figure 2 Diverticulitis patient with high VF. Axial preoperative CT image taken at the L1 vertebral level of a 65-year-old female with diverticulitis who underwent sigmoidectomy and developed postoperative complications. iNtuition fat analysis software is used to record the abdominal circumference of 108 cm, VF of 329 cm2, SF of 280 cm2 and the visceral: subcutaneous ratio of 54% (calculated using the formula of VF/(SF 1 VF)). These 4 measurements were recorded at each of the 5 vertebral levels from L1 to L5. SF is highlighted in blue. VF is highlighted in green. (For interpretation of the references to color in this Figure, the reader is referred to the web version of this article.)

postoperative complications on univariate analysis with a P value of less than or equal to .05 were then entered into a multivariate regression analysis to determine independent prognosticators of postoperative complications.

Results Univariate analysis

Figure 1 Diverticulitis patient with low VF. Axial preoperative CT image taken at the L1 vertebral level of a 44-year-old female with diverticulitis who underwent sigmoidectomy with no postoperative complications. iNtuition fat analysis software was used to record the abdominal circumference of 92.4 cm, VF of 51.8 cm2, SF of 125 cm2 and the visceral: subcutaneous ratio of 29.2% (calculated using the formula of VF/(SF 1 VF)). These 4 measurements were recorded at each of the 5 vertebral levels from L1 to L5 for each patient. SF is highlighted in blue. VF is highlighted in green. (For interpretation of the references to color in this Figure, the reader is referred to the web version of this article.)

Patient demographics and operative variables. Table 1 lists the demographics of the 211 identified patients. The population was 55.9% (n 5 118) male. A 19.4% (41 of 211) emergent resection rate was demonstrated. The majority of procedures (145 of 211) were performed as open (vs laparoscopic) and 193 were for complicated (abscessing, perforating, or fistulizing) disease. The Clavien–Dindo grade 2 to 4 serious postoperative complication rate was 12.7% with 27 patients experiencing a complication. On univariate analysis (Tables 2 and 3), the complication group contained more current or ex-smokers (P 5 .05), more patients with higher ASA grades (P 5 .05), and more emergent resections (P 5 .05) and ostomy creations (P 5 .02). Mean age at diagnosis of DD was also higher in those with complications (62.88 6 11.29 vs 51.95 6 14.1 years, P 5 .0001). Patients who were older at the time of surgery were more likely to experience a complication (64.26 6 11.88 vs 55.28 6 12.47 years, P 5 .001). There was no difference in disease duration between those who did and did not experience a complication (Table 4).

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4 Table 1 Demographics of the 211 included diverticulitis patients undergoing sigmoid resection Variable

Number (%)

Male sex Smokerdnever: current:former History of diabetes Steroid use ASA 1:2:3:4 Emergent resection Ostomy at resection 30-day readmission Open procedure (vs laparoscopic) Complicated diverticulitis

118 (55.9) 129:30:52 (61.1, 14.2, 24.6) 40 12 14:116:65:16 41 97 13 145

(18.9) (5.7) (6.6, 54.9, 30.8, 9) (19.4) (46) (6.2) (68.7)

193 (91.4)

ASA 5 American Society of Anesthesiologists; complicated diverticulitis 5 abscess, perforation, or fistula.

Fat parameters VF was the only fat parameter demonstrated to be statistically different between the 2 groups (those with and without complications) on univariate analysis. Those with complications had a mean VF content of 209.81 6 111.93 vs 162.08 6 86.07 cm2 in those without complications (P 5 .01). Interestingly, there was no difference in BMI between the groups (28.61 6 4.44 vs 28.77 6 5.11, P 5 .88).

Multivariate analysis The 7 covariates found to be statistically significant with a P value of less than or equal to .05 (smoking, ASA grade, emergent resection, VF, ostomy at resection, age at diagnosis, and age at resection) were entered into the multivariate analysis (Table 4). VF was the only factor found to be independently associated with postoperative complications (P 5 .032). Patients with increased VF (.165 cm2) had an odds ratio of 3.1 for developing complications post sigmoid resection (95% confidence interval 1.1 to 8.5). Table 2

Comments Although prior studies have demonstrated an association between various parameters of obesity such as BMI and waist circumference and the development of DD and complicated diverticulitis,17,18 no study to date has measured visceral and SF on preoperative CT scans as a potential indicator of surgical outcome. Therefore, the aim of this study was to examine the relationship between complications after sigmoidectomy for diverticulitis and volumetric measurements of visceral and subcutaneous abdominal fat. We chose to define serious complications as Clavien–Dindo II to IV as these complications require a form of intervention, either medical or surgical as compared with type I complications, which merely describe a deviation from the expected course. The results from the present univariate analysis are in line with published literature, which has demonstrated an association between surgical complications and smoking history, higher ASA score, ostomy, and old age. Univariate analysis of fat measurement also demonstrated that the only volumetric fat parameter significantly associated postoperative complications in our cohort was VF. On multivariate analysis, increased VF was the only factor found to be associated with an increased risk of postoperative complications. This may be explained by several aspects of obesity and VF, which make it a risk factor for adverse outcomes. In general, obese patients present technical challenges intraoperatively that may contribute to longer operative times and postoperative complications. These include difficulty in intubation and adjustments to typical anesthesia routines and difficulty in visualizing viscera. Additionally, patients with central obesity in particular may have increased tension required when closing wounds as well as increased tension on the anastomosis. VF has been associated with increased diarrheal symptoms and gastrointestinal dysfunction in general population-based studies,22 worse outcomes in studies of general and colorectal surgery,12,13 and increased intestinal permeability and decreased immune response in both murine models and humans.23 Obese animal models

Univariate analysis results for noncontinuous variables

Variable

Without postoperative complications (n 5 184)

With postoperative complications (n 5 27)

P value

Male sex Tobacco usednever:current:former History of diabetes Steroid use ASA 1:2:3:4 Emergent resection Ostomy at resection 30-day readmission Open procedure Complicated diverticulitis

99 (53.8%) 114:29:41 34 (18.4%) 9 (4.9%) 14:106:50:14 32 (17.4%) 79 (42.9%) 10 (5.4%) 122 (66.3%) 168 (91.3%)

19 (70.3%) 16:1:11 6 (22.2%) 3 (11.1%) 0:10:15:2 9 (33.3%) 18 (66.7%) 3 (22.2%) 23 (96.2%) 25 (92.5%)

.10 .05 .59 .17 .05 .05 .02 .25 .15 .82

ASA 5 American Society of Anesthesiologists; complicated diverticulitis 5 abscess, perforation, or fistula. Statistically significant values are in bold type.

R. Tappouni et al. Table 3

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Univariate analysis results for continuous variables

Variable

Without postoperative complications (n 5 184)

With postoperative complications (n 5 27)

P value

Mean age at diagnosis (years, SD) Mean disease durations (years, SD) Mean age at surgery (years, SD) Body mass index Visceral fat (cm2) Subcutaneous fat (cm2) Visceral/subcutaneous fat ratio (%) Abdominal circumference (cm)

51.95 7.49 55.28 28.77 162.08 198 45.26 99.20

62.88 6.82 64.26 28.61 209.81 187.99 50.62 102.08

.0001 .39 .001 .88 .01 .57 .23 .37

± 14.1 6 3.72 ± 12.47 6 5.11 ± 86.07 6 89.05 6 21.05 6 16.11

± 11.29 6 3.52 ± 11.88 6 4.44 ± 111.93 6 66.36 6 11.80 6 11.42

SD 5 standard deviation Statistically significant values are in bold type.

have demonstrated a reduced T-cell response to mitogen stimulation, increased apoptosis of developing T-cell populations, impaired memory T-cell function, decreased natural killer cell numbers, impaired natural killer and dendritic cell function, and lower levels of IL2 when exposed to mitogens leading to an increased susceptibility to Candida albicans, Staphylococcus aureus, and certain viruses.24–29 In obese human subjects, a decrease in overall circulating T cells has been shown by flow cytometry. One study investigating weight loss and T cells has shown that after a weight reduction program subjects showed increased T-cell responsiveness to mitogen exposure.25 These factors in combination likely play a role in the association between increased VF and postoperative complications. Contrary to prior published literature citing an association between high BMI and postoperative complications, our data showed a minimal increase in the mean BMI of the cohort with complications compared with the cohort without complications (28.77 and 28.61, respectively). Generally, VF measurements were higher and subcutaneous measurements were lower in the patient group with complications compared with the group without complications. This led to an increase in the VF/SF ratio in the complication group (50.64% vs 45.26% in the group without complications). Although this difference was not statistically significant, the VF/SF ratio had the lowest P

Table 4

Multivariate analysis

Variable

P value

OR

95% confidence interval

Visceral fat (cm2) Smoking Emergent colectomy ASA Ostomy at resection Age at diagnosis Age at resection

.032 .23 .80 .81 .37 .56 .15

3.1 1.3 1.2 .9 1.6 .96 1.1

1.1 to 8.5 .822 to 2.3 .35 to 3.9 .44 to 1.9 .55 to 4.9 .84 to 1.1 .94 to 1.3

ASA 5 American Society of Anesthesiologists; CI 5 confidence interval; OR 5 odds ratio Statistically significant values are in bold type.

value after VF. It is therefore possible that in a larger study this may establish statistical significance.

Measuring parameters of adiposity Assessment of VF and SF and the VSR can be obtained using abdominal CT images that were obtained before the surgery. Because these CT scans are readily available, no additional testing or risk is incurred by the patient. The calculations of VF and SF and AC and VSR are easily and rapidly obtained in a semi-automated way using commercially available three-dimensional reconstruction software. For assessment of all fat parameters, it is crucial that the operator ensures that the skin and superficial fat are included in the images at multiple levels. The analysis of an individual patient takes less than 5 minutes.

Limitations Limitations of our study include the exclusion of 50 patients with DD undergoing colectomy because of lack of CTs. This was primarily because of the inclusion of patients from the early 2000s, when barium enemas were more commonly used. However, including CT scans were required for the measurement of fat parameters that were key to our study. It is controversial to include emergent patients as they may have increased incidences of postoperative complications. However, this was accounted for in the multivariate analysis and did not prove to be associated with increased complications. This is perhaps because very ill patients with life-threatening disease, who have a high mortality rate, proceed directly to the operating room without undergoing CT. A validated scoring system for complications, the Clavien-Dindo scoring system, was used. Because of the relatively small number of patients with complications, we were only able to correlate fat parameters with the presence of a more severe (grade 2 to 4) complication and not an individual grade or type of complication. Furthermore, the small number of complications may underestimate the effect between the variables that were included in the regression analysis.

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Additionally, 26 patients were excluded because the CT image did not include all their subcutaneous thus preventing accurate measurement. Because most of these patients were obese, it is possible that this has created selection bias by excluding a specific group of patients. In summary, patients with increased visceral abdominal fat are more likely to develop complications after sigmoid resection for diverticulitis. Radiographic VF analysis can be used as a tool in preoperative planning and predicting postoperative morbidity. Although several factors were associated with increased risk of postoperative complications in these patients, VF was the only parameter to retain statistical significance after multivariate analysis.

12. Cecchini S, Cavazzini E, Marchesi F, et al. Computed tomography volumetric fat parameters versus body mass index for predicting short-term outcomes of colon surgery. World J Surg 2011;35: 415–23. 13. Kunisaki C, Makino H, Takagawa R, et al. Predictive factors for surgical complications of laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc 2009;23:2085–93. 14. Tsujinaka S, Konishi F, Kawamura YJ, et al. Visceral obesity predicts surgical outcomes after laparoscopic colectomy for sigmoid colon cancer. Dis Colon Rectum 2008;51:1757–65; discussion, 1765–7. 15. Strate LL, Liu YL, Aldoori WH, et al. Obesity increases the risks of diverticulitis and diverticular bleeding. Gastroenterology 2009;136: 115–122.e1. 16. Dobbins C, Defontgalland D, Duthie G, et al. The relationship of obesity to the complications of diverticular disease. Colorectal Dis 2006;8:37–40. 17. Jeong JH, Lee HL, Kim JO, et al. Correlation between complicated diverticulitis and visceral fat. J Korean Med Sci 2011;26:1339–43. 18. Afonso M. Visceral fat: a key factor in diverticular disease of the colon. J Port Gastrenterol 2012;2:62–5. 19. Charlson ME, Pompei P, Ales KL, et al. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373–83. 20. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–13. 21. Yajima Y, Narui T, Ishii M, et al. Computed tomography in the diagnosis of fatty liver: total lipid content and computed tomography number. Tohoku J Exp Med 1982;136:337–42. 22. Delgado-Aros S, Locke 3rd GR, Camilleri M, et al. Obesity is associated with increased risk of gastrointestinal symptoms: a populationbased study. Am J Gastroenterol 2004;99:1801–6. 23. Brun P, Castagliuolo I, Di Leo V, et al. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 2007; 292:G518–25. 24. Karlsson EA, Beck MA. The burden of obesity on infectious disease. Exp Biol Med (Maywood) 2010;235:1412–24. 25. Tanaka S, Isoda F, Ishihara Y, et al. T lymphopaenia in relation to body mass index and TNF-alpha in human obesity: adequate weight reduction can be corrective. Clin Endocrinol (Oxf) 2001;54:347–54. 26. Nieman DC, Henson DA, Nehlsen-Cannarella SL, et al. Influence of obesity on immune function. J Am Diet Assoc 1999;99:294–9. 27. Nieman DC, Nehlsen-Cannarella SI, Henson DA, et al. Immune response to obesity and moderate weight loss. Int J Obes Relat Metab Disord 1996;20:353–60. 28. O’Rourke RW, Kay T, Scholz MH, et al. Alterations in T-cell subset frequency in peripheral blood in obesity. Obes Surg 2005;15:1463–8. 29. Lynch LA, O’Connell JM, Kwasnik AK, et al. Are natural killer cells protecting the metabolically healthy obese patient? Obesity (Silver Spring) 2009;17:601–5.

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