Research ArticleClinical Studies

Visceral Adipose Tissue and Skeletal Muscle Index Distribution Predicts Severe Pancreatic Fistula Development After Pancreaticoduodenectomy

HIROAKI YAMANE, TOMOYUKI ABE, HIRONOBU AMANO, KEIJI HANADA, TOMOYUKI MINAMI, TSUYOSHI KOBAYASHI, TOSHIKATSU FUKUDA, SHUJI YONEHARA, MASAHIRO NAKAHARA, HIDEKI OHDAN and TOSHIO NORIYUKI
Anticancer Research February 2018, 38 (2) 1061-1066;

Abstract

Background/Aim: In this study, we investigated the effect of body composition on pancreatic fistula (PF) development after pancreaticoduodenectomy (PD). Materials and Methods: All consecutive patients with pancreatic and extrahepatic biliary malignancy following PD who were treated between 2006 and 2016 were enrolled. Results: PF developed in 30.3% of cases (30/99 patients), including a grade B PF in 25.3% of cases (25/99 patients) and a grade C PF in 5.1% of cases (5/99 patients). Univariate analysis identified that body mass index ≥25 kg/m2, visceral adipose tissue area (VATA)/skeletal muscle index (SMI) ≥2.0, pancreatic duct diameter ≤3 mm, and drain amylase concentration (Amy) on postoperative day (POD) 1 ≥5000 U/L were significantly associated with PF (grade B, C) after PD. Multivariate analysis indicated that VATA/SMI ≥2.0 (p=0.009), pancreatic duct diameter ≤3 mm (p=0.003), and drain Amy on POD1 ≥5000 U/L (p=0.032) were independent risk factors for PF. Conclusion: Elevated VATA/SMI was the only preoperative key factor for PF after PD.

Pancreas head malignancies and extrahepatic biliary duct have dismal prognoses, even after curative resection, and often require pancreaticoduodenectomy (PD). Improvements in surgical techniques and perioperative management have dramatically reduced the rates of morbidity and mortality after PD, which are reported as 15.3-44.2% and 0.6-4.3%, respectively (1-4).

However, these results are still dismal among patients undergoing gastrointestinal surgery. Pancreatic fistula (PF) development is among the most concerning of PD complications as it can result in massive bleeding following the formation of pseudo-aneurysm ruptures and refractory abdominal abscesses. A 2005 International Study Group on Pancreatic Fistula (ISGPF) defined PF (5) and documented its occurrence as being approximately 17.9%-30.2% (2, 6-8).

Recently, sarcopenia, which is defined as a decreased amount of skeletal muscle, was shown to adversely affect prognosis after surgical resection in various cancer types (9-12). Kaido et al. reported that patients with sarcopenia were susceptible to postoperative infectious complications compared with non-sarcopenia patients among liver transplant recipients (12). Previous studies have demonstrated that anthropomorphic factors negatively affect postoperative complications (13, 14). However, the mechanism by which anthropomorphic factors influence postoperative outcomes after PD and the development of PF remain unclear. We created a new evaluation system by combining visceral adipose tissue area (VATA) and skeletal muscle index (SMI) imbalance, and used this system to identify patients with severe obesity and sarcopenia. The definition of sarcopenia and obesity differs among countries; thus, a new VATA/SMI evaluation system could be used to standardize these assessments.

To date, several variables, including postoperative drain amylase (Amy), main pancreatic duct diameter, remnant pancreas volume, pancreatic texture, and malnutrition status, were reported to be risk factors for PF development after PD (2, 3, 8, 15). In this study, we identified the clinicopathological variables, including anthropomorphic factors, evaluated using preoperative computed tomography (CT), that are associated with PF development.

Materials and Methods

Patients. Patients who underwent PD between 2006 and 2016 were identified from the Onomichi General Hospital Department of Surgery, retrospectively. We included patients who developed pancreatic ductal adenocarcinoma, adenocarcinoma of the papilla, extrahepatic cholangiocarcinoma, and intraductal papillary-mucinous carcinoma. The study was approved by the local Institutional Review Board and written informed consent was obtained from all patients (OJH-201642).

Preoperative CT analysis of anthropomorphic composition. Eight weeks prior to operation, all patients underwent a preoperative non-enhanced and enhanced multidetector CT (DISCOVERY CT750 HD; GE Healthcare, Waukesha, WI, USA and Sensation 16; Siemens, Forchheim, Germany, respectively) with a section thickness of 2.5-5 mm. The CT images at the third lumbar vertebra (L3) were analysed using Advantage Workshop 4.5 (GE Healthcare, Waukesha, WI, USA) and Virtual Place Fujin (AZE Ltd., Tokyo, Japan) (11). Body composition assessment included VATA, subcutaneous adipose tissue area (SATA), and skeletal muscle area. CT analysis was performed by trained investigators (H.Y. and T.A.), who were blinded to patient characteristics and clinical outcomes. Tissue Hounsfield unit (HU) thresholds were employed as follows: -29 to 150 HU for skeletal muscle area, -190 to -30 for SATA, and -150 to -50 for VATA (16). Skeletal muscle area was defined at the L3 level and included the psoas major and minor, paraspinal muscles, and abdominal wall muscles. Skeletal muscle area was normalized for height in meters squared (m2) to create the SMI. In our study, a VATA/SMI ≥2.0 was defined as high and a VATA/SMI <2.0 was defined as low.

Definition of sarcopenia and pancreatic fistula. Sarcopenia was defined as a SMI <43 cm2/m2 with a BMI <25 kg/m2 for males, a SMI <53 cm2/m2 with a BMI ≥25 kg/m2 for males and a SMI <41 cm2/m2 for females (17). PF development was defined using the ISGPF (5). In this study, our definition of PF development as grades B and C was according to the ISGPF.

Ethical approval. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Statistical analysis. Continuous variables were reported at the median and were analysed using the non-parametric Mann-Whitney U-test. Categorical variables were compared using the Fisher's exact test. The logistic regression analysis was performed to determine the associations between clinicopathologic factors and development of PF. Statistically significant variables on univariate analysis were entered into a multivariate logistic analysis. Differences between the results of comparative tests were considered significant according to a two-sided p-value of <0.05. Cut-off values for significant variables were employed according to the receiver operating characteristic curve. Calculations were performed using SPSS software (version 22; IBM Corp., Armonk, NY, USA).

Results

The overall mortality and morbidity rates in the 99 patients were 1.0% (1/99 patients) and 36.4% (36/99 patients), respectively. PF developed in 30.3% of cases (30/99 patients), including a grade B PF in 25.3% of cases (25/99 patients) and a grade C PF in 5.1% of cases (5/99 patients). Nighty-nine patients who underwent PD were divided into two groups: the PF (N=30, 30.3%) and non-PF (N=69, 69.7%) groups. Patient demographics and univariate analyses are shown in Table I.

Risk factors for PF after PD. Univariate analysis indicated that obese patients (i.e., BMI ≥25 kg/m2; p=0.032) and patients with a high-VATA/SMI (p=0.002), pancreatic duct diameter ≤3 mm (p<0.001) and drain Amy concentration ≥5000 U/L on POD1 (p=0.002) were significantly at a higher risk of developing PF. Multivariate analyses identified that high-VATA/SMI (hazard ratio [HR], 5.353; 95% confidence interval [CI]=1.534-18.680; p=0.009), pancreatic duct diameter ≤3 mm (HR=6.580; 95%CI=1.906-22.717; p=0.003) and drain Amy concentration ≥5000 U/L on POD1 (HR=4.910; 95%CI=1.144-21.065; p=0.032) were the independent risk factors for PF (Table II).

Comparison of the characteristics between patients subdivided according to VATA/SMI. Clinicopathological variables for low- and high-VATA/SMI groups are shown in Table III. Patients with a high-VATA/SMI were more likely to be male (p=0.001), have a higher BMI (p<0.001), exhibit hypertension (p=0.003), smoke more regularly (p=0.013), and abuse alcohol (p=0.001) more often than did patients with a low-VATA/SMI. The SMI level was equivalent between high- and low-VATA/SMI patients, whereas VATA was significantly higher in high-VATA/SMI patients (p<0.001). SATA was much higher in high-VATA/SMI patients (p<0.001). A longer operation time (p=0.002) and increased intraoperative bleeding (p=0.002) were seen in high-VATA/SMI patients. Notably, the postoperative complications were strongly associated with a high-VATA/SMI rather than a low-VATA/SMI (p=0.001). PF development occurred in 14.9% (7/47 patients) of patients with a low-VATA/SMI and in 44.2% (23/52 patients) of patients with a high-VATA/SMI (p=0.002).

Discussion

In this study, we identified that a high-VATA/SMI, pancreatic duct ≤3 mm and drain Amy concentration ≥5,000 U/L on POD1 were independently associated with PF development after PD. Previously, the VATA, soft pancreas, pancreatic duct ≤3 mm, and an abnormal drain Amy concentration have been reported as risk factors for PF development after PD (5, 6, 10, 15, 18). The ability to predict PF occurrence by evaluating clinicopathological features in the clinical setting is beneficial to patients. Several studies have reported that sarcopenia is related to postoperative complications (12). In our study, sarcopenia by itself was not significantly related to PF due to the high proportion of older participants. In contrast, Kirihara et al. reported that a greater VATA and less skeletal muscle were associated with PF after PD (2). Using the VATA/SMI evaluation, severe obesity and sarcopenia are extracted rather than a simple assessment of VATA and SMI. The VATA/SMI is simple and easy to calculate as well as provides insight into how to approach nutrition in patients following surgery and provide an early rehabilitation program in patients with a high-VATA/SMI. Patients with a high-VATA/SMI were susceptible to postoperative complications in our study. These findings emphasize the importance of the assessment and potential treatment of a high-VATA/SMI or an imbalance of visceral adipose and skeletal muscle in patients with hepatobiliary cancer who are scheduled for potentially curative surgery.

View this table:
Table I.

Univariate analysis of risk factors for pancreatic fistula development in patients who underwent pancreaticoduodenectomy.

More abundant visceral adipose tissue was detected, while more intraoperative bleeding and longer operation time were reported (19, 20). In agreement with these observations, groups with elevated VATA/SMI levels were associated with massive intraoperative bleeding and longer operative time compared with groups with low-VATA/SMI. The loss of skeletal muscle along with increased adipose tissue promotes the production of pro-inflammatory adipokines, such as leptin, tumour necrosis factor-α, interleukin (IL)-1, and IL-6 (21, 22). These data suggest that higher amount of visceral adipose tissue would not only interfere with surgical recovery by promoting the excessive production of pro-inflammatory cytokines, but also suppress the immune system. However, Goujoux et al. reported that there were no correlations with postoperative complications and body composition, as indicated by BMI and VATA (23). Further investigations of this underlying mechanism are necessary.

View this table:
Table II.

Multivariate logistic analysis of risk factors for pancreatic fistula development in patients who underwent pancreaticoduodenectomy.

View this table:
Table III.

Comparison of clinicopathological variables between patients with low and high visceral adipose tissue area/skeletal muscle index.

Pancreatic duct diameter is a well-documented risk factor for PF development after PD (3, 24, 25). Pratt et al. reported that a smaller pancreatic duct is an increased risk factor for PF development (26). Additionally, soft pancreatic tissue is a well-known risk factor for PF development and is likely due to the fragility of the parenchyma and a narrow main pancreatic duct given the difficulty in suturing following PF development after PD (8). Pancreatic duct and texture were frequently observed to influence preoperative pancreatitis due to tumor obstruction, which resulted in the widening of the pancreatic duct and hardening of its texture. This suggests that preoperative assessment with endoscopic ultrasonography-elastography also provides important information for selecting surgical intervention (27). Evaluating the combined VATA/SMI ratio and pancreatic fibrosis by EUS-elastography is important to predict PF after PD.

Some reports have proposed that the high drain Amy concentration is not related with PF occurrence (28, 29). Conversely, many reports have shown that the Amy value in drainage was important for predicting PF development after PD (6, 15, 30). In our study, drain Amy concentration ≥5000 U/L on POD1 was an independent risk factor for PF development. Kawai et al. reported that intraoperative bleeding >1000 ml, a soft pancreas, and drain Amy on POD1 >4000 U/L are significant predictive factors for PF development (6). Meanwhile, Molinari et al. reported that the drain Amy on POD1 ≥5000 U/L was the only significant factor for PF development (15). Indeed, while the pancreatic diameter and postoperative drain Amy level are important risk factors for PF development after PD, no measure can be assessed preoperatively. Preoperative measures would help to identify patients who are at a high-risk for PF development. Patients can then act to enhance their nutrition and level of activity in preparation for their operation.

This study has some limitations. We included patients not only with pancreatic duct adenocarcinoma, but also with extrahepatic biliary malignancies. Therefore, we could not provide long-term outcomes. In addition, this is a retrospective non-randomized study from a single institution with a relatively small number of patients.

In conclusion, the preoperative evaluation of muscle and adipose volume was effective in predicting PF development after PD. This assessment would be useful in determining individual surgical procedures and provide perioperative management. We suggest that managing the level of visceral adipose tissue or skeletal muscle will help prevent PF development.

Acknowledgements

This manuscript has not been published and is not under consideration for publication elsewhere.

Footnotes

  • Conflicts of Interest

    The Authors declare no conflicts of interest.

  • Received November 19, 2017.
  • Revision received December 4, 2017.
  • Accepted December 5, 2017.

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Visceral Adipose Tissue and Skeletal Muscle Index Distribution Predicts Severe Pancreatic Fistula Development After Pancreaticoduodenectomy
HIROAKI YAMANE, TOMOYUKI ABE, HIRONOBU AMANO, KEIJI HANADA, TOMOYUKI MINAMI, TSUYOSHI KOBAYASHI, TOSHIKATSU FUKUDA, SHUJI YONEHARA, MASAHIRO NAKAHARA, HIDEKI OHDAN, TOSHIO NORIYUKI
Anticancer Research Feb 2018, 38 (2) 1061-1066;
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