Do psoas muscle area and volume correlate with postoperative complications in patients undergoing rectal cancer resection?

Accepted Manuscript Do psoas muscle area and volume correlate with postoperative complications in patients undergoing rectal cancer resection? Aaron L. Womer, Justin T. Brady, Kevin Kalisz, Nilam D. Patel, Raj M. Paspulati, Harry L. Reynolds, Timothy M. Pawlik, Scott R. Steele PII:

S0002-9610(17)30976-5

DOI:

10.1016/j.amjsurg.2017.10.052

Reference:

AJS 12631

To appear in:

The American Journal of Surgery

Received Date: 7 July 2017 Revised Date:

11 October 2017

Accepted Date: 13 October 2017

Please cite this article as: Womer AL, Brady JT, Kalisz K, Patel ND, Paspulati RM, Reynolds HL, Pawlik TM, Steele SR, Do psoas muscle area and volume correlate with postoperative complications in patients undergoing rectal cancer resection?, The American Journal of Surgery (2017), doi: 10.1016/ j.amjsurg.2017.10.052. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Title: Do Psoas Muscle Area and Volume Correlate with Postoperative Complications in Patients Undergoing Rectal Cancer Resection?

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Authors: Aaron L. Womer, BS1 Justin T. Brady, MD1 Kevin Kalisz, MD2 Nilam D. Patel, BS1 Raj M. Paspulati, MD2 Harry L. Reynolds, MD1 Timothy M. Pawlik, MD3 Scott R. Steele, MD1,4

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Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, Ohio, USA Department of Radiology, University Hospitals Cleveland Medical Center, Cleveland, Ohio, USA 3 Department of Surgery, Ohio State University Medical Center, Columbus, Ohio, USA 4 Department of Colorectal Surgery, Cleveland Clinic, Cleveland, Ohio, USA

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Corresponding Author for Review Process: Justin T. Brady, MD General Surgery Resident Department of Surgery University Hospitals Cleveland Medical Center 11100 Euclid Avenue Cleveland, OH 44106 Phone: (858) 204-9489 Email: Justin.Brady @uhhospitals.org

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Corresponding Author for Publication: Scott R. Steele, MD Chairman, Department of Colorectal Surgery Professor of Surgery Cleveland Clinic 9500 Euclid Avenue Cleveland, OH 44195 Phone: (216) 316-5452 E-mail: [email protected]

The manuscript has been seen and approved by all authors and the material is previously unpublished. This manuscript has been presented at the Midwest Surgical Association/Central Surgical Association Annual Meeting, Chicago, IL, August 1st, 2017. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Abstract Background: Increasingly, patients with multiple co-morbidities undergo surgery for rectal

sarcopenia, were associated with postoperative morbidity.

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cancer. We aimed to evaluate if decreased psoas muscle area and volume, as measures for

Methods: Retrospective review of patients undergoing rectal cancer resection at a tertiary

medical center (2007–2015). Variables included demographics, co-morbidities, preoperative

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psoas muscle area and volume, and postoperative complications.

Results: Among 180 patients (58% male, mean age 62.7 years), 44% experienced complications

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(n=79), of which 38% (n=30) were major complications. Malnourished patients had smaller height-adjusted total psoas area than non-malnourished patients (6.4 vs. 9.5 cm2/m2, p=0.004). Among patients with imaging obtained within 90 days of surgery, major morbidity was associated with smaller total psoas area (6.7 vs. 10.5 cm2/m2, p=0.04) and total psoas volume

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(26.7 vs. 42.2 cm3/m2, p=0.04) compared to those with minor complications. Conclusion: Preoperative cross-sectional imaging may help surgeons anticipate postoperative

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complications following rectal cancer surgery.

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Introduction As an increasing population of patients with multiple co-morbidities undergoes major abdominal surgery, colorectal surgeons are faced with the challenge of identifying patients

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preoperatively who are at higher risk of developing postoperative complications in order to

determine if targeted interventions are possible and for risk stratification.[1] Operative risk in these patients is related to their decreased physiologic reserve, an idea which is embodied by the

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concept of frailty. Frailty is an age-related state with decreased physiologic reserve affecting

morbidities as well as functional status.[2]

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multiple body systems.[2] Tools for the assessment of frailty are based on preoperative co-

Despite the utility of frailty assessments in predicting poor postoperative outcomes, many researchers have sought to develop means of measuring physiologic reserve that are more objective and less cumbersome. One such measure is sarcopenia, defined as loss of muscle

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mass, which is quantified using preoperative cross-sectional (CT) imaging.[3–5] Research has shown that for patients with gastrointestinal malignancy, sarcopenia was a better predictor of 1year mortality than subjective frailty indices.[4] Measurements of psoas muscle, including total

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psoas area (TPA) and total psoas volume (TPV), have been used as markers of sarcopenia in surgery literature. Among patient undergoing major intra-abdominal resection, reduced TPV has

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been associated with longer length-of-stay, increased cost of hospitalization, increased morbidity, and decreased long-term survival.[6,7] Unfortunately patients with underlying malignancy may also have nutritional deficits or wasting. However, to date there have been no studies investigating the clinical relevance of sarcopenia specifically to the surgical treatment of rectal cancer patients or the ability to predict morbidity in this population.

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Considering that preoperative cross-sectional imaging is routinely obtained for rectal cancer patients, it would be advantageous for surgeons to extract all possible information pertaining to patients’ operative risk from those imaging studies. Demonstrating the association

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of reduced psoas muscle area and volume on preoperative CT scans with postoperative outcomes could provide groundwork for integrating sarcopenia-associated risk into preoperative planning in the surgical treatment of rectal cancer patients. The aim of this study is to evaluate the

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relationship between psoas muscle measures on preoperative CT scans and postoperative

outcomes among patients undergoing attempted curative surgical resection of rectal cancer. We

following rectal cancer surgery. Methods

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hypothesized that smaller preoperative TPA and TPV are associated with increased morbidity

After obtaining Institutional Review Board approval, we performed a retrospective

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review of all patients undergoing rectal cancer resection at University Hospitals Cleveland Medical Center (UHCMC) from 2007 to 2015. Patients were included in the study if they were at least 18 years of age and had preoperative CT imaging available for review. Patients

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undergoing palliative resection or with incomplete medical records were excluded. Variables collected included demographics, co-morbidities, tumor staging, radiologic data, neoadjuvant

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therapy, postoperative complications, and readmissions. Postoperative complications were categorized using the Clavien-Dindo classification system (Minor: 1-2; Major: 3-5). Patients were categorized as malnourished if they had a serum albumin level of less than 3.0 g/dL or reported >10% weight loss prior to diagnosis. Data were collected and maintained using a HIPAA-compliant REDCap database.

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All images were analyzed by a single observer within the Department of Radiology at UHCMC. Measurements were performed on either diagnostic CT scans of the abdomen and pelvis with or without intravenous contrast or on non-contrast low-dose CT examinations

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obtained during Positron Emission Tomography (PET)/CT studies. All low-dose PET/CT studies were deemed of sufficient quality to determine psoas muscle outlines for purposes of crosssectional area measurement.

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Psoas cross-sectional areas were measured in a semi-automated fashion as previously described by Amini et al.[6] This was accomplished by outlining the psoas muscle cross-sections

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at three levels, as follows: the superior-most measurement at the level of the superior endplate of the L3 vertebral body with the middle and inferior psoas levels located at either 2.0 cm (equating to 4 contiguous slices if 5 mm slice thickness was available) or 2.1 cm (equating to 7 contiguous slices if 3 mm slice thickness was available) increments inferior to the initial measurement. Total

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psoas cross sectional area (TPA) at a given level was calculated as the mean of the three summed cross sectional areas of left and right psoas muscles. Total psoas volume (TPV) was calculated by multiplying a patient’s TPA by the vertical distance over the psoas slices (cm). Both TPA

Statistical Analysis

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and TPV values were normalized for patient height (m2).

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Continuous variables were summarized as means with standard deviations (SD), or

medians with interquartile ranges (IQR). Categorical values were summarized as frequencies with percentages. The Wilcoxon rank-sum test was used to compare median values. P-values less than 0.05 were considered to be statistically significant. Statistical analysis was performed using Stata/SE 14.2 (StataCorp, College Station, TX).

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Results A total of 180 patients met study criteria and were included in the analysis, of whom 178 had height data available. Overall, the mean patient age was 62.7 years and over half (58%) were

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male (Table I). There were 133 (73.9%) patients who underwent low anterior resection and 47 (26.1%) who underwent abdominoperineal resection. Half of patients were smokers and over half had cardiovascular disease (58%). A minority of patients were malnourished (4%). Median

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time from CT scan to surgery was 78 days (29.5-126.5 days). Standard CT imaging was done in 136 patients, and the remaining 44 received PET/CT. Imaging was performed prior to

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neoadjuvant therapy in 85 (47.2%) patients, post-neoadjuvant therapy in 70 (38.9%) patients and the remaining 25 (13.9%) patients did not receive neoadjuvant therapy. Overall, the median TPA was 15.7 cm2 (11.5-20.3). Median TPV overall was 62.6 cm3 (46.0-82.4). When adjusting for height, median TPA was 9.3 cm2/m2 (7.1-12.1) and median TPV was 62.6 cm3/m2 (46.0-

Malnourished patients

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82.4).

There were 8 malnourished patients, and 172 non-malnourished patients in the study

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population. Among malnourished patients, the median TPA normalized for height of 6.4 cm2/m2 (4.6-7.8 cm2/m2) was significantly lower than among non-malnourished patients, 9.5 cm2/m2

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(7.4-12.4 cm2/m2, p=0.004).

Postoperative complications A total of 79 patients (44%) experienced a postoperative complication. When comparing

patients who experienced postoperative complications and those who did not, there was no statistically significant difference in height-normalized TPA (9.6 cm2/m2, 6.6-11.2 vs 9.2 cm2/m2, 7.4-12.4) or height-normalized TPV (38.6 cm3/m2, 26.4-45.8 vs 37.1 cm3/m2, 29.5-49.7;

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p=0.5, Table II). There was no difference in complication rates by overall clinical or pathologic disease stage (P>0.1). Complication rates were similar between groups based upon procedure

Major vs. Minor Postoperative Complications

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performed (P>0.2).

During the study period, 30 patients (17%) experienced major complications and 49 patients (27%) experienced minor complications. Median TPA was smaller among those who

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experienced major complications (13.2 cm2, 10.4-18.1) compared to minor complications, (17.9 cm2, 12.3-20.0, p=0.05; Table II). However, there was no significant difference between groups

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when TPA was normalized for height (p=0.1). Median TPV was significantly lower among those who experienced major complications (52.8 cm3, 41.4-72.5) compared to those who suffered minor complications (71.7 cm3, 49.3-87.3, p=0.04). When normalized for height, TPV was not significantly different among those who experienced major and minor postoperative

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complications (p=0.1).

Subset analysis of surgery within 90 days of CT scan A subset analysis was performed using patients who underwent surgical resection within

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90 days of cross-sectional imaging (n=96). Of the 90-day subset population, 71.9% had undergone neoadjuvant chemotherapy and 69.8% had undergone neoadjuvant radiation. CT

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scans used for evaluation were performed post-neoadjuvant therapy in 67.7% (n=65) of patients, pre-neoadjuvant in 8.3% (n=8) of patients and 24% (n=23) of patient underwent no neoadjuvant therapy. Among this group, 15 patients (16%) experienced major complications, and 34 patients (35%) experienced minor complications. Patients with major complications had a TPA (11.3 cm2, 9.1-17.1) and height-adjusted TPA (6.7 cm2/m2, 6.0-9.8) which were smaller than TPA (18.4 cm2, 13.7-22.7, p=0.01), and height-adjusted TPA (10.5 cm2/m2, 8.2-12.9, p=0.04) of

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patients who had minor complications. Likewise, patients with major complications had TPV (45.3 cm3, 36.3-68.4) smaller than patients with minor complications (73.8 cm3, 54.9-90.6, p=0.01). Height-adjusted TPV among those with major complications (26.7 cm3/m2, 23.9-39.1)

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was smaller than that of patients with minor complications (42.2 cm3/m2, 32.7-51.8, p=0.04). Discussion

The aim of this study was to evaluate if there was a difference in radiologic psoas muscle

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measurements between patients who did or did not have postoperative complications following curative rectal cancer resection. We found that malnourished rectal cancer patients had smaller

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TPA compared to patients with normal nutritional status. Of patients who underwent surgery within 90 days of imaging, those who experienced major postoperative complications had smaller TPA and TPV on preoperative imaging than those who suffered minor complications. We are not aware of prior studies correlating psoas muscle measurements and postoperative

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complications specific to rectal cancer surgery patients.

Psoas muscle measurements, as markers of sarcopenia, have been shown to be associated with postoperative complications in other fields of surgery. Amini et al. showed that pancreatic

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cancer patients with TPV in the lowest sex-specific quartile had an increased rate of all complications, as well as higher rate of severe complications.[6] Similarly, Gani et al.

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demonstrated that TPV in the lowest sex-specific quartile was associated with a higher rate of complications among patients undergoing any major abdominal resection.[7] The results of the present study corroborate this previous literature which correlated smaller TPA and TPV to more severe postoperative complications in rectal cancer patients. A previous analysis of those undergoing pancreas, hepatobiliary, and colorectal resections showed that low TPV was associated with approximately $14,000 increase in total hospital cost, as well as nearly five-fold

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risk of mortality.[7] Considering the financial and safety risks of sarcopenia in the operating room (OR), it behooves surgeons to consider the presence of sarcopenia in colorectal cancer patients. The ability to identify patients at high risk of severe postoperative complications may

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lead way to future interventions to mitigate surgical risk and reduce the financial burden of complications.

In the field of colorectal surgery, psoas cross-sectional area and psoas muscle density

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have been used as markers of sarcopenia. Psoas density has been shown to be associated with increased complication rates, as well as disease-free survival.[8] Jones et al showed that

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estimated psoas area, similar to TPA, below cutoff values for cachexia, conferred increased risk of experiencing major postoperative complications.[9] The results of this study corroborate with the tendency towards smaller psoas area and volume among patients who experience postoperative morbidity. Our study suggests this association is pertinent among those

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undergoing curative rectal cancer surgery.

Major morbidity was associated with TPA and TPV among patients who received surgery within 90 days of diagnostic imaging, however, this association was not present among all

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patients, independent of time from imaging to surgery. No similar time-sensitivity of the relationship between sarcopenia and postoperative outcomes could be found in other colorectal

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sarcopenia literature.[3,8,10–12] Previous studies of TPA and TPV had restricted their data to those who received surgery within 30 and 90-days of abdominal imaging.[6,7] For this reason, we consider the 90-day subset analysis to be consistent with other sarcopenia research. We hypothesize that with increased time between diagnostic imaging and surgery (>90 days), some patients may have had a change in muscle mass status not accurately reflected by their preoperative imaging. Patients with longer time between diagnostic imaging and surgery may

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experience physiologic changes which alter the functional compromise suggested by their diagnostic imaging. Larger studies may be able to show how the interval between diagnostic imaging and surgery affects the association between radiologic sarcopenia and postoperative

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outcomes.

We acknowledge that there are certain limitations to the present study. This was a

retrospective review which has inherent limitations in the available information documented in

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the medical record. This was a single center study with a smaller sample size of 180 patients, including 8 with malnutrition; thus we are limited to the generalizability of the outcomes to other

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sites and we are underpowered to detect smaller difference between groups. Not all patients were imaged within 90 days of surgery which also decreased our sample size. To increase sample size, we used imaging data consisting of diagnostic pelvic CT as well as low-dose PET/CT scans. The quality of low-dose PET/CT scans were determined to be of satisfactory quality by the

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reviewing radiologist for accurate psoas measurement, but this could be a potential source for differences in measurement. We were limited to one measure of nutrition (serum albumin) that was routinely assessed in patients, of which there are other measures (i.e., visceral fat measures

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and immune status) that would be helpful in future research. Despite these limitations, the difference in psoas areas between patients with major versus minor postoperative complications

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suggests that sarcopenia is an important marker associated with serious postoperative morbidity and that surgeons may be able use this information to improve pre-surgical optimization. Conclusion

Patients who had major complications had significantly smaller TPA and TPV, suggestive

of sarcopenia, compared to patients with minor complications. Similar signs of sarcopenia are also found in patients with malnutrition, compared to non-malnourished patients. There is more

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information to be gained from preoperative imaging than merely rectal cancer staging. Further investigation is needed in order to better understand the relationship between sarcopenia and

Acknowledgements

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postoperative outcomes in rectal cancer patients.

We would like to acknowledge Ms. Allison Weaver for her work on the rectal cancer database. For hosting the REDCap database, we would like to acknowledge grant support from the Clinical

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and Translational Science Collaborative (CTSC, 4UL1TR000439).

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Frailty Index in Predicting 1-Year Mortality among 1,326 Patients Undergoing Gastrointestinal Surgery for a Malignant Indication. J. Am. Coll. Surg. 2016;222:397– 407e2.

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Prado CM, Lieffers JR, McCargar LJ, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal

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tracts: a population-based study. Lancet Oncol. 2008;9:629–635. Amini N, Spolverato G, Gupta R, et al. Impact Total Psoas Volume on Short- and LongTerm Outcomes in Patients Undergoing Curative Resection for Pancreatic

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Gani F, Buettner S, Margonis GA, et al. Sarcopenia predicts costs among patients

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Adenocarcinoma: a New Tool to Assess Sarcopenia. J. Gastrointest. Surg. 2015;19:1593–

undergoing major abdominal operations. Surgery 2016;160:1–10. 8.

Sabel MS, Terjimanian M, Conlon ASC, et al. Analytic Morphometric Assessment of Patients Undergoing Colectomy for Colon Cancer. J. Surg. Oncol. 2013;108:169–175. Jones KI, Doleman B, Scott S, Lund JN, Williams JP. Simple psoas cross-sectional area

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measurement is a quick and easy method to assess sarcopenia and predicts major surgical complications. Color. Dis. 2015;17:O20–O26. Lieffers JR, Bathe OF, Fassbender K, Winget M, Baracos VE. Sarcopenia is associated

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with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br. J. Cancer 2012;107:931–936.

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Huang DD, Wang SL, Zhuang CL, et al. Sarcopenia, as defined by low muscle mass, strength and physical performance, predicts complications after surgery for colorectal cancer. Color. Dis. 2015;17:O256–O264.

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Reisinger KW, Jeroen LA, van Vugt A, et al. Functional Compromise Reflected by

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Sarcopenia, Frailty, and Nutritional Depletion Predicts Adverse Postoperative Outcome After Colorectal Cancer Surgery. Ann. Surg. 2014;261(2), 345-352. Table I. Patient Characteristics

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All Patients (n=180) Age, mean (SD) 62.7 (13.5) Male gender, n (%) 105 (58.3) Comorbidities, n (%) Diabetes 33 (18.3) Smoking 91 (50.6) COPD 10 (5.6) Cardiovascular Disease 104 (57.8) Malnutrition 8 (4.4) Days from CT imaging to surgery, mean 81.2 (53.9) Median Days from CT imaging to surgery, median (IQR) 78 (29.5-126.5) Overall Clinical Stage (n, %) I 15 (8.4) II 46 (25.7) III 71 (39.7) IV 24 (13.4) Unknown 23 (12.9) Overall Pathological Stage (n, %) 0 21 (11.7) I 47 (26.1) II 55 (30.6) III 33 (18.3) IV 24 (13.3) Procedure performed (n, %) Low Anterior Resection 133 (73.9) Abdominoperineal Resection 47 (26.1) Overall complications (n, %) 79 (43.9) Major complications 30 (16.7) Minor complications 49 (27.2) CT Type (n, %) Regular CT 136 (75.6) PET/CT 44 (24.4) Psoas Measurements Median in cm2 (IQR) 15.7 (11.5-20.3) Median normalized to height, in cm2/m2 (IQR) 9.3 (7.1-12.1) Total Psoas Volume Median, in cm3 (IQR) 62.6 (46.0-82.4) Median normalized to height, in cm3/m2 (IQR) 62.6 (46.0-82.4) Note: SD is Standard Deviation, CT is Computed Tomography, IQR is Interquartile Range

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Table II. Psoas Measurement Comparisons

15.8 (11.9-21.2)

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6.4 (4.6-7.8)

9.5 (7.4-12.4)

Any Postoperative Complication (n=79) 15.8 (10.9-19.6)

No postoperative complications (n=101) 15.4 (12.3-20.9)

9.6 (6.6-11.2)

9.2 (7.4-12.4)

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63.2 (43.8-81.2)

62.3 (49.3-83.5)

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11.3 (7.5-14.2)

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38.6 (26.4-45.8)

37.1 (29.5-49.7)

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Major complication (n=30, n=28 for height normalized) 13.2 (10.4-18.1)

Minor complication (n=49)

P-value

17.9 (12.3-20.0)

0.05

7.7 (6.1-10.9)

10.2 (7.4-11.7)

0.1

52.8 (41.4-72.5) 30.9 (24.3-43.7)

71.7 (49.3-87.3) 41.3 (29.7-49.2)

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Major complication (n=15) (n=13 for height normalized) 11.3 (9.1-17.1)

Minor complication (n=34)

P-value

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TPA Median in cm2 (IQR) TPA Median cm2/m2 (IQR) TPV Median cm3 (IQR) TPV Median cm3/m2 (IQR) CT within 90 days of surgery (n=96 total)

P-value

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TPA Median in cm2 (IQR) TPA Median cm2/m2 (IQR) TPV Median in cm3 (IQR) TPV Median cm3/m2 (IQR)

Not Malnourished (n=172)

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Malnourished TPA Median in cm2 (IQR) TPA Median cm2/m2 (IQR)

Malnourished (n=8)

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TPA Median in cm2 18.4 (13.7-22.7) 0.01 (IQR) TPA Median cm2/m2 6.7 (6.0-9.8) 10.5 (8.2-12.9) 0.04 (IQR) TPV Median cm3 (IQR) 45.3 (36.3-68.4) 73.8 (54.9-90.6) 0.01 3 2 TPV Median cm /m 26.7 (23.9-39.1) 42.2 (32.7-51.8) 0.04 (IQR) Note: IQR is Interquartile Range, CT is Computed Tomography, TPA is Total Psoas Area, TPV is Total Psoas Volume

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