Positive impact of perioperative oral management on the risk of surgical site infections after abdominal surgery: A multicenter retrospective analysis conducted in Japan

Background: Postoperative surgical site infections (SSI) can be major complications, which can prolong postoperative treatment. Perioperative oral management (POM) was rst covered by Japanese national health insurance system in 2012, and patients that are scheduled to undergo major surgical treatment receive dental and oral management during the perioperative period. Objectives: The purpose of the present study was to investigate the ability of POM to prevent perioperative SSI in patients undergoing abdominal surgery. Methods: The patients’ medical records were retrospectively reviewed, and the effects of POM were investigated in a multicenter analysis involving many cases. Detailed information about SSI was assessed and compared between patients with and without POM in univariate and multivariate analyses. Results: In total, the cases of 2,782 patients (1,750 males 1,032 females) were reviewed. Of these, POM was performed in 778 patients (28.0%). Univariate analyses revealed that diabetes mellitus, Eastern Cooperative Oncology Group (ECOG) performance status, the American Society of Anesthesiologists (ASA) classication, the surgical site, the preoperative Prognostic Nutritional Index score, POM, the extent of surgery, the operation time, and the amount of intraoperative blood loss were signicantly associated with postoperative SSI (Chi-square or Mann-Whitney U-test, p <0.01). The multivariate analysis revealed that POM had signicant preventative effects against postoperative SSI (estimate: -0.245, standard error: 0.080, p <0.01). The surgical site, the ASA classication, and the operation time were also signicant and independent clinical predictors of SSI. Conclusion: This study suggests that POM helps to prevent SSI in patients that undergo abdominal surgery.

Positive impact of perioperative oral management on the risk of surgical site infections after abdominal surgery: A multicenter retrospective analysis conducted in Japan

Introduction
Surgical site infections (SSI) are associated with increased morbidity and mortality. In addition, SSI have an important in uence on the duration of hospitalization and healthcare expenditure, and they also have a negative impact on patients' quality of life [1]. In a report about nosocomial infection surveillance in Japan [2], the incidence of SSI in Japan was estimated to be around 6%. The latter report revealed that SSI occurred most frequently after abdominal surgery (digestive organ surgery), which accounted for 88% of all SSI. SSI remain one of the most common infectious complications after abdominal surgery. Thus, measures to prevent SSI are important [3].
The Surgeon General's report on oral health in America showed that oral functional management can prevent general complications during the perioperative period [4]. In Japan, perioperative oral management (POM) was rst covered by the national health insurance system in 2012, and patients that are scheduled to undergo surgery for cancer, cardiovascular disease, or organ transplantation receive dental and oral functional management during the perioperative period. POM might help to prevent dental-related local and systemic infections in patients that are compromised by invasive surgery. POM has been reported to help prevent postoperative pneumonia, which has been attributed to the aspiration of oral/oropharyngeal pathogens, in some cancer patients 4

Patients And Methods
The present study was conducted by the Japanese Stomatological Society. The medical records of 2,782 patients who were scheduled to undergo abdominal surgery under general anesthesia between April 2016 and March 2017 at 16 university hospitals were examined in this study. The medical records of these patients were retrospectively reviewed, and data concerning the presence or absence of SSI and clinical factors that might in uence the risk of SSI were collected. The presence/absence of SSI was determined based on the documentation in the patients' medical records. The potential predictors of SSI included patient factors (age, sex, smoking habits, diabetes mellitus, severe heart disease, severe pulmonary disease, Eastern Cooperative Oncology Group performance status (ECOG-PS), and the preoperative Prognostic Nutritional Index (PNI)), treatment factors (the risk of general anesthesia, the surgical site, the extent of surgery, the operation time, and the amount of intraoperative blood loss), and the presence/absence of POM. Severe heart disease was de ned as ≥ grade 3 on the New York Heart Association Functional Classi cation [7]. Severe pulmonary disease was de ned as a percentage vital capacity (VC) of < 60% or a percentage forced expiratory volume in one second (%FEV1) of < 50%. The risk of general anesthesia was evaluated with the American Society of Anesthesiologists (ASA) physical status classi cation [8]. The extent of surgery was divided into 3 groups; i.e., into endoscopic surgery or an incision of ≤ 10 cm, laparotomic surgery or an incision of > 10 cm, or laparostomy and thoracotomy. The surgical sites were divided into 10 groups: the stomach/duodenum, the jejunum/ileum/appendix/colon, the rectum, the liver, the gallbladder/biliary tract, the pancreas, the abdominal wall/abdominal hernias, the peritoneum/retroperitoneum/mesentery/retina, the anus/periphery, and the spleen. The PNI was calculated according to the method reported by Onodera et al [9]. PNI scores were classi ed into 50-point groups. Operation times were classi ed into 3-hour groups, and intraoperative blood loss was categorized into 300-ml groups.
POM was generally initiated from the time when the decision to hospitalize the patient was made. POM included oral health instructions; the removal of dental calculi (scaling); professional mechanical tooth cleaning; the removal of tongue coatings with a toothbrush; the cleaning and adjustment of dentures; and the extraction of teeth affected by severe periodontitis that exhibited pain, pus discharge, mobility, or marked alveolar bone loss on an X-ray examination.
The effects of POM on SSI were investigated statistically via univariate analyses (Chi-square test, Mann-Whitney U-test) and multivariate analysis (stepwise logistic regression analysis). Statistical analyses were performed using JMP ver.13 (SAS Institute Inc., North Carolina, USA). P-values of < 0.05 were considered to be signi cant.
The results of the univariate analyses are also summarized in Table 1. The presence of SSI was signi cantly associated with the presence of diabetes mellitus, ECOG-PS, ASA physical status, the surgical site, the preoperative PNI score, the extent of surgery, the operation time, and the amount of intraoperative blood loss. Higher prevalence rates of SSI were associated with diabetes mellitus, higher ECOG-PS scores, higher ASA physical status classes, particular surgical sites, lower preoperative PNI scores, the absence of POM, more invasive surgery, longer operation times, and higher amounts of intraoperative blood loss. Sex, age, severe heart disease, and severe pulmonary disease were not signi cantly associated with the prevalence of SSI.
The results of the stepwise multivariate analysis are summarized in

Discussion
Postoperative SSI are an important marker of surgical quality and are associated with longer hospital stays, higher rates of reoperation and readmission, and increased mortality. Poor survival was observed in patients with various types of cancer who exhibited SSI after surgery. It has also been suggested that SSI are associated with shorter disease-free and overall survival in several types of cancer, such as head and neck cancer, breast cancer, colon cancer, and gastric cancer 2 . Furthermore, Nespoli et al. showed that postoperative infections were associated with a poor 5-year survival rate among colon cancer patients [10]. SSI are one of the most common postoperative morbidities, occurring in 5-40% of patients who undergo colorectal surgery 2 . In addition, it was reported that SSI occur in 7.6% of patients after major abdominal surgery. In the present study, SSI arose in 9.9% of patients, which was compatible with the ndings of previous studies. As SSI occur quite frequently, measures aimed at preventing them are required.
Many investigators have studied the factors that in uence the prevalence of SSI after abdominal surgery. Togo et al. revealed that SSI were signi cantly associated with a long operation time, marked intraoperative blood loss, a high blood transfusion requirement, and bile stulas among liver cancer patients [11]. Mingmei et al. demonstrated that SSI were signi cantly associated with the type of surgery; the surgical procedure (laparoscopic or open); and hospital size; i.e., the number of beds, in patients with colorectal cancer [12]. Fukuda et al. showed that SSI were signi cantly associated with blood transfusions, the use of antidiabetic drugs, the use of steroids, the operation time, the ASA classi cation, the surgical procedure, emergency surgery, and age [13]. In the current study, we retrospectively reviewed the cases of patients who underwent abdominal surgery and tried to identify factors that in uence the prevalence of SSI. As a result, we found that hepatic, biliary, or pancreatic surgery; a poorer ASA physical status; and a longer operation time were signi cantly associated with a higher prevalence of SSI. Most of these risk factors are di cult to control before surgery.
On the other hand, this study revealed that POM interventions had independent, signi cant, and bene cial impacts on the risk of SSI after abdominal surgery. Recently, Nobuhara et al. reported that POM reduced the risk of SSI after surgery for colorectal cancer 4 . Our ndings were compatible with those of the latter study. Other studies have found that preoperative oral care reduced the risk of postoperative pneumonia after surgery for esophageal, lung, or major cancer [14][15][16]. As the aspiration of oral/oropharyngeal uid containing pathogenic microorganisms is considered to be the main cause of postoperative pneumonia, it is logical that controlling oral bacteria reduces the risk of postoperative pneumonia. Similarly, our results suggested that the use of POM might signi cantly reduce the risk of SSI after abdominal surgery.
Gingivitis and periodontal disease provide opportunities for bacterial overgrowth, and the richly vascularized and often ulcerated tissues associated with these diseases are susceptible to bacterial invasion [17]. The bulk of dental plaque, such as bio lm, is composed of microcolonies of oral bacteria [14]. Nobuhara et al. mentioned that the oral cavity is recognized as a signi cant reservoir of pathogenic microorganisms, which can infect multiple organs [5]. Oral bacteria are known to in uence various general diseases, such as pneumonia, cardiovascular disease, cerebrovascular disease, rheumatoid arthritis, preterm or low-weight births, sepsis, carcinogenesis, and non-alcoholic steatohepatitis, and SSI [18,19]. Therefore, achieving quantitative and qualitative control of oral bacteria via oral healthcare is considered to be important for preventing infectious diseases.
The direct transfer of oral bacteria might cause SSI after head and neck or upper digestive tract surgery, as well as postoperative aspiration pneumonia 5 . In addition, the intravascular invasion of odontogenic bacteria, in ammatory cytokines, and/or endotoxins, and their transport to remote organs through blood vessels or lymph ducts might cause SSI at various surgical sites [5]. It is well known that transient bacteremia often occurs after tooth extraction and tooth brushing. The CDC guidelines suggest that preoperative infectious lesions at remote sites are a risk factor for SSI [6]. In 2012, POM started to be covered by the Japanese national health insurance system, and it has since been widely performed in patients that are scheduled to undergo cancer treatment, organ transplantation, cardiovascular surgery, or orthopedic implant surgery. We assessed the changes in the prevalence of oral bacteria detected in blood cultures before and after the introduction of insurance coverage for POM and found that the introduction of insurance coverage for POM had a bene cial effect on the frequency of systemic infections caused by oral bacteria [20].
In addition, we recently found that POM had signi cant positive effects on perioperative serum albumin levels in patients that were treated surgically under general anesthesia (submitted for publication). It has been reported that a decreased serum albumin level is an independent risk factor for severe postoperative complications and a poor prognosis [21]. Some researchers have reported that dental infections and poor oral health are closely related to lower serum albumin levels. POM, including oral care, the removal of chronic dental infections, and prosthodontic treatments, has positive effects on serum albumin levels, which might consequently reduce the risk of SSI after abdominal surgery [21].
One of the major advantages of the present study is that it was the rst to clarify the bene cial effects of POM on the risk of SSI in patients that undergo abdominal surgery, based on a multicenter retrospective study involving a large number of cases. As for the limitations of the present study, the POM criteria and treatment protocols differed from institute to institute because of the study's retrospective nature. In addition, the POM intervention rate was quite low (28.0%). However, there are ethical di culties associated with conducting a prospective randomized control study to evaluate the e cacy of POM because POM has only been covered by the Japanese national health insurance system since 2012, and most Japanese patients now receive POM before undergoing cancer, cardiovascular, or transplant treatment. Furthermore, the protocols for and aims of dental interventions are still subject to debate. The establishment of guidelines for POM in patients that are scheduled to undergo surgery is needed in order to standardize such dental interventions.

Conclusion
This study suggested that POM has signi cant bene cial effects on the risk of SSI in patients that undergo abdominal surgery.