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Risk Factors for Surgical Site Infection after SoftTissue Sarcoma Resection, Including the Preoperative Geriatric Nutritional Risk Index Hiromi Sasaki 1, Satoshi Nagano 1, Noboru Taniguchi 1 and Takao Setoguchi 2,* Department of Orthopaedic Surgery, Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima 890-8520, Japan; [email protected] (H.S.); [email protected] (S.N.); [email protected] (N.T) 2 Department of Medical Joint Materials, Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima 890-8520, Japan * Correspondence: [email protected]; Tel.: +81-99-275-5381 1

Received: 3 November 2018; Accepted: 29 November 2018; Published: 3 December 2018

Abstract: Malignant soft-tissue sarcoma resection is associated with a relatively high incidence of surgical site infection (SSI). The known risk factors for SSI following soft-tissue sarcoma resection include tumor size and location, prolonged surgery, and massive blood loss. The geriatric nutritional risk index (GNRI) was used as a tool to help predict the occurrence of SSI after major surgery. We investigated the utility of the GNRI as a predictor of SSI following soft-tissue sarcoma resection. We retrospectively reviewed 152 patients who underwent surgical resection of soft-tissue sarcoma in our institute, and found that the incidence of SSI was 18.4% (28/152). The SSI and nonSSI groups significantly differed regarding surgical time, diameter of the skin incision, maximum tumor diameter, instrumentation, presence of an open wound, preoperative chemotherapy, preoperative C-reactive protein concentration, and GNRI. Binomial logistic regression analysis showed that the risk factors for SSI following soft-tissue sarcoma surgery were male sex, larger skin incision diameter, larger maximum tumor diameter, presence of an open wound, and lower GNRI. Our findings indicate that malnutrition is a risk factor for SSI after soft-tissue sarcoma resection, and suggest that appropriate assessment and intervention for malnutrition may reduce the incidence of SSI. Keywords: soft-tissue sarcoma; surgical site infection (SSI); geriatric nutritional risk index (GNRI); malnutrition

1. Introduction Soft-tissue sarcomas are a rare and heterogeneous group of tumors that account for 1% of all adult malignancies, affect almost every site in the body, and retain the full range of malignant behavior [1]. The incidence of surgical site infection (SSI) following tumor resection is high, and is especially high in cases of high-grade sarcoma, such as undifferentiated pleomorphic sarcoma and liposarcoma [2]. Because of its rarity, the risk factors for SSI after soft-tissue sarcoma resection are yet to be well clarified. Patients with cancer reportedly have high rates of malnutrition (40–80%) [3]. The strong correlation between cancer and inflammation is well known [4]. Systemic inflammation in patients with cancer causes an elevation in C-reactive protein (CRP), and decreases in serum albumin and total protein, which reflects malnutrition [5]. Thus, preoperative nutritional intervention is important for patients with cancer [6]. However, malnutrition is often unrecognized because of ineffective screening techniques [7]. Malnutrition in patients with cancer is related to poorer clinical outcome, poor quality of life, and poor prognosis [8]. Malnutrition is also associated with a higher incidence of Nutrients 2018, 10, 1900; doi:10.3390/nu10121900

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SSI, higher incidence of morbidity, and longer duration of hospitalization following major surgery [9]. The geriatric nutritional risk index (GNRI) was generated to evaluate the risk of malnutritionrelated complications in adult patients [10], and is a significant predictor of prognosis in many types of cancer [11–18]. The present study aimed to evaluate the potential risk factors for SSI, including preoperative GNRI, following soft-tissue sarcoma resection [19]. 2. Materials and Methods 2.1. Patient Data We retrospectively examined the records of 152 patients who were treated for soft-tissue sarcoma at the Department of Orthopedic Surgery, Kagoshima University from January 2007 to December 2016. Patients’ clinical characteristics were collected from the medical records, including sex, age, date of surgery, routine preoperative blood-test results, tumor size, tumor location, treatment, and comorbidities. An open wound was defined as a skin defect that remained after tumor resection and required secondary closure via skin grafting. Hypertension was defined in accordance with the World Health Organization/International Society of Hypertension guidelines as a blood pressure greater than 140/90 (grade 1) [20]. The results of preoperative blood tests including whiteblood-cell count, hemoglobin concentration, CRP concentration, total protein, and total cholesterol were extracted to evaluate the preoperative nutritional status. The occurrence of SSI was assessed in accordance with the definition of the Centers for Disease Control and Prevention [21]. Patients for whom some of these data were missing were excluded from the study. 2.2. Geriatric Nutritional Risk Index The GNRI was calculated from the serum albumin concentration and bodyweight using the following formula: GNRI = (1.489 × albumin (g/L)) + (41.7 × (bodyweight/ideal body weight)). The bodyweight/ideal bodyweight value was set to 1 when the patient’s bodyweight exceeded the ideal bodyweight [10]. The ideal bodyweight was defined as a body mass index (BMI) of 22 kg/m2 [12,22]. 2.3. Statistical Analysis Patients were divided into those who developed SSI (SSI group) and those who did not (non-SSI group). Differences in variables between the SSI and non-SSI groups were evaluated using the Student’s t-test, Mann–Whitney U test, and Fisher’s exact test. Correlation coefficients were analyzed via Spearman’s rank correlation coefficient. When the correlation coefficients between variables were >0.6, only one variable with the incidence of SSI, i.e., skin incision, was selected. Multivariable stepwise binomial logistic regression analysis was used to examine the relationships between the incidence of SSI and the assessed variables. Because of the small number of patients and the relatively large number of variables, we applied a stepwise selection method to identify significant variables, as previously described [23]. A p-value /=65 Years With Acute Heart Failure. Am. J. Cardiol. 2016, 118, 550– 555. Moore, J.; Isler, M.; Barry, J.; Mottard, S. Major wound complication risk factors following soft tissue sarcoma resection. Eur. J. Surg. Oncol. 2014, 40, 1671–1676. Whitworth, J.A.; World Health Organization; ISoHWG. 2003 World Health Organization (WHO)/International Society of Hypertension (ISH) statement on management of hypertension. J. Hypertens. 2003, 21, 1983–1992. Mangram, A.J.; Horan, T.C.; Pearson, M.L.; Silver, L.C.; Jarvis, W.R. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am. J. Infect. Control. 1999, 27, 97–132.

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