Abstract
Background/Aim: Postoperative pneumonia is a serious complication of major oesophageal surgery. We aimed to clarify the association between the degree of improvement in oral hygiene by perioperative oral care and postoperative pneumonia in oesophageal cancer patients. Patients and Methods: Oesophageal cancer patients (n=129) who underwent esophagectomy received perioperative oral care. Their oral hygiene was evaluated using the Oral Assessment Guide (OAG). The relationship between perioperative OAG scores and postoperative complications was analysed. Results: The average OAG scores before starting oral care, pre-operation, and post-operation were 11.0±1.7, 9.1±1.5, and 11.2±3.0, respectively (p<0.001). An increase in preoperative OAG scores was independently associated with postoperative pneumonia on multivariate analysis (p=0.027). Conclusion: Preoperative oral care improves oral hygiene in patients undergoing oesophageal cancer surgery. No improvement in oral hygiene despite preoperative oral care was an independent predictor of postoperative pneumonia.
Oesophageal cancer (EC) is the sixth most common cause of cancer-related death worldwide (1). Although the development of various treatment methods, such as surgical techniques, neoadjuvant therapy, adjuvant therapy, and perioperative management have improved the prognosis of patients with EC (2-8), esophagectomy is correlated with high morbidity and mortality rates (9). Postoperative complications adversely affect the outcome after esophagectomy; hence, it is essential to decrease postoperative complications to improve prognosis (10-12). Among postoperative complications, postoperative pneumonia is one of the most frequent and serious complications of major oesophageal surgery. Perioperative oral care has been reported to be useful in preventing postoperative pneumonia (13, 14). However, in these studies, patients who received oral care were compared with those who did not. No studies have analysed the association between oral hygiene and postoperative outcomes among patients who received oral care. Thus, little is known about the association between the degree of improvement in oral hygiene and postoperative pneumonia in EC patients.
The Oral Assessment Guide (OAG), developed by Eilers et al., is an oral health assessment tool widely used by dentists, dental hygienists, and nurses (15, 16). Knöös et al. reported the usefulness of the OAG in patients receiving radiotherapy to the head and neck region (17), and Saito et al. showed the effectiveness of the OAG for evaluating chemotherapy-induced oral mucositis in breast cancer patients (18). A unique feature of the OAG is that is allows the assessment of the degree of oral hygiene using a numerical value.
In this study, we hypothesised that the degree of oral hygiene is associated with the development of postoperative pneumonia in EC patients. To investigate this hypothesis, we examined the relationship between the degree of oral hygiene, as evaluated by the OAG, and the development of postoperative complications.
Patients and Methods
Patients. A total of 129 EC patients who underwent esophagectomy at Gunma University Hospital from February 2010 to March 2018 were investigated in this study. All patients who received perioperative oral care and had adequate medical records were included in the study. Patients with permanent tracheostomy, a history of chemotherapy or radiotherapy, and head and neck cancers were excluded. Staging was performed according to the 7th edition of the tumour-node-metastasis classification of the Union for International Cancer Control (19). This study conformed to the tenets of the Helsinki Declaration and was approved by the Institutional Review Board for Clinical Research at the Gunma University Hospital (Maebashi, Gunma, Japan; approval number: HS2020-006). Patient consent was obtained using the opt-out method.
Postoperative complications. The Clavien-Dindo (C-D) grading system was used to evaluate postoperative complications (20). Pneumonia was defined as the presence of an abnormal shadow on chest radiography or chest computed tomography (CT) along with fever (temperature >38°C) and positive sputum and/or a white blood cell count >12,000/mm3 (21, 22). Anastomotic leakage was defined based on CT or oesophagography findings and/or the characteristics of anastomotic drains (21).
Oral care intervention and OAG scores. Each patient received oral care from a dentist and dental hygienist. Oral care was started when the operation date was determined and continued until discharge from the hospital. Each patient received oral care while in the intensive care unit as well as during intubation. Oral care included examination of the oral cavity, removal of dental calculus (scaling), professional mechanical tooth cleaning, oral mucosa cleaning, and guidance for a self-care technique.
For the evaluation of oral hygiene, the OAG score was used. The OAG score comprises eight categories: voice, swallowing, lips, tongue, saliva, mucous membranes, gingiva, and teeth or dentures (15). Each category is scored from 1 (healthy) to 3 (severe problems). A sum score from the eight categories is calculated, which ranges from 8 (no oral problems) to 24 (severe oral problems). The OAG score was calculated by an oral surgeon, professional dental hygienist, or professional nurse for evaluating oral diseases at three time points: before starting oral care (2-4 weeks before surgery), pre-operation (1-3 days before surgery), and post-operation (1-2 weeks after surgery). We also examined the change in the OAG score in the perioperative period. OAG score change before surgery was defined as (OAG score pre-operation) – (OAG score before starting oral care), while the OAG score change after surgery was defined as (OAG score post-operation) – (OAG score pre-operation).
Statistical analysis. All statistical analyses were performed using the JMP software (SAS Institute Inc., Cary, NC, USA). Comparison of perioperative OAG scores was performed using the Wilcoxon signed-rank test. Correlations between the OAG score or OAG score change and perioperative complications were analysed using the Mann-Whitney U-test. Receiver operating characteristic (ROC) curve analyses were used to evaluate the potential of OAG score change before surgery to discriminate between patients with and without postoperative pneumonia. The sensitivity and specificity were calculated to detect the optimal cut-off value for postoperative pneumonia using ROC curves. Univariate and multivariate analyses were performed with each predictive factor for postoperative pneumonia using logistic regression analysis. The differences between the group showing increases and decreases in the OAG score were analysed using the Fisher’s exact test. A probability value of <0.05 was considered statistically significant.
Results
Patient characteristics and postoperative complications. Patient characteristics are detailed in Table I. A total of 129 patients with EC were enrolled in this study. Perioperative complications of C-D grade ≥III developed in 18 patients (14.0%). Postoperative pneumonia and anastomotic leakage occurred in 4 (3.1%) and 18 (14.0%) patients, respectively.
Patient characteristics.
Relationship between OAG scores at each evaluation point and postoperative complications. Figure 1 shows the perioperative OAG score at each evaluation point. The preoperative OAG score was significantly lower than the OAG score before starting oral care (9.1±1.5 vs. 11.0±1.7, p<0.001). The postoperative OAG score was significantly higher than the preoperative OAG score (11.2±3.0 vs. 9.1±1.5, p<0.001). The correlations between the OAG scores at each evaluation point and postoperative complications are presented in Figure 2. The postoperative OAG scores were significantly higher in the groups with all complications (C-D grade ≥III), pneumonia, and anastomotic leakage than in the groups without complications (C-D grade ≥III), pneumonia, and anastomotic leakage [all complications (C-D grade ≥III): 12.8±3.2 vs. 11.0±2.9, p=0.014; pneumonia: 15.0±3.5 vs. 11.1±2.9, p=0.01; and anastomotic leakage: 13.0±2.9 vs. 10.9±2.9, p=0.006]. As for the OAG score before starting oral care, no significant differences were observed between the corresponding groups [all complications (C-D grade ≥III): 10.9±1.3 vs. 11.0±1.7, p=0.86; pneumonia: 10.0±2.2 vs. 11.0±2.3, p=0.245; and anastomotic leakage: 11.3±1.5 vs. 10.9±1.7, p=0.374]. Similarly, the preoperative OAG scores were not significantly different between the corresponding groups [all complications (C-D grade ≥ III): 9.4±1.6 vs. 9.1±1.5, p=0.426; pneumonia: 10.0±3.4 vs. 9.1±1.4, p=0.242; and anastomotic leakage: 9.7±2.0 vs. 9.0±1.4, p=0.102].
Comparison of the perioperative Oral Assessment Guide (OAG) score in oesophageal cancer patients.
Comparison of the perioperative Oral Assessment Guide (OAG) score according to all complications (Clavien-Dindo grade ≥ III), postoperative pneumonia, and anastomotic leakage. A. Comparison of the perioperative OAG score according to all complications (Clavien-Dindo grade ≥III). B. Comparison of the perioperative OAG score according to postoperative pneumonia. C. Comparison of the perioperative OAG score according to anastomotic leakage.
OAG score change and postoperative complications. Table II shows the correlations between OAG score change and postoperative complications. The OAG score change before surgery improved significantly among patients without postoperative pneumonia (0.0±1.6 vs. –1.9±1.6, p=0.024). Furthermore, the OAG score change after surgery significantly increased among patients with all complications (C-D grade ≥III), pneumonia, and anastomotic leakage [all complications (C-D grade ≥III): 3.4±2.7 vs. 1.9±2.6, p=0.02; pneumonia: 5.0±2.9 vs. 2.0±2.6, p=0.026; and anastomotic leakage: 3.3±2.6 vs. 1.9±2.6, p=0.033].
Correlations between Oral Assessment Guide (OAG) score change and postoperative complications.
Comparison of clinical characteristics between the OAG score increase and decrease groups. We next analysed the usefulness of the OAG score change before surgery for estimating postoperative pneumonia. ROC analysis for the OAG score change before surgery revealed that the optimal cut-off value for postoperative pneumonia was 0.0 [area under the curve (AUC), 0.798; p=0.019, sensitivity, 75.0%, specificity, 81.6%; Figure 3]. The patients were divided into the OAG score decrease (representing an improvement in oral hygiene) and OAG score increase (representing no improvement in oral hygiene) groups according to these cut-off points. Patients with no change in the OAG score before surgery were included in the OAG score decrease group. We compared clinical characteristics between the OAG score increase and decrease groups to identify factors affecting oral hygiene. As shown in Table III, the rate of diabetes mellitus in the OAG score increase group was significantly higher than that in the OAG score decrease group (23.1% vs. 7.8%, p=0.025).
Receiver operating characteristic curve analysis for the optimal cut-off value of Oral Assessment Guide (OAG) score change before surgery.
Comparison of clinical characteristics between the patients with and without improvement in Oral Assessment Guide (OAG) score.
Univariate and multivariate analyses with regard to the development of postoperative pneumonia. Univariate analysis performed for identifying factors associated with the development of postoperative pneumonia showed that age >65 years and an increase in OAG score significantly predicted postoperative pneumonia (p=0.045 and p=0.016, respectively) (Table IV). However, an increase in the OAG score was independently associated with postoperative pneumonia on multivariate analysis (p=0.027).
Univariate and multivariate analyses for development of postoperative pneumonia.
Discussion
In this study, we demonstrated that perioperative oral care improved oral hygiene, and postoperative OAG scores were associated with the development of postoperative complications in EC patients. In addition, we showed that no improvement in the OAG score before surgery was an independent predictor of postoperative pneumonia. Moreover, a higher number of patients with diabetes mellitus were observed in the OAG increase group.
Several studies have shown that perioperative oral care decreases the incidence of postoperative pneumonia after EC surgery (13, 14). However, all previous studies compared the rate of postoperative pneumonia between patients who did and did not receive preoperative oral care. We quantified the degree of oral hygiene using the OAG score and demonstrated that a change in the OAG score before surgery may predict the development of postoperative pneumonia in patients who received preoperative oral care. To the best of our knowledge, this is the first study to reveal the association between the degree of improvement in oral hygiene and postoperative pneumonia. Since 2012, oral care has been covered by the Japanese medical insurance system. We believe that it is important to discuss the necessity of oral care as well as the quality of oral healthcare management. The OAG score may be of great help for evaluating the effect of oral care.
Previous studies have reported the correlation between postoperative pneumonia after oesophageal surgery and various factors, such as regular smoking, decreased pulmonary function, lack of oral care, old age, greater surgical stress (operation time, blood loss), and worsened general conditions (performance status and complications) (23-27). We hypothesised that a high preoperative OAG score would be associated with a risk of postoperative pneumonia before starting this study. However, unexpectedly, there was no significant difference in the preoperative OAG score between groups with and without postoperative pneumonia. Interestingly, we found that an increase in the OAG score before surgery was an independent predictor of postoperative pneumonia. We suggest that the patients included in the OAG score decrease group (i.e. those who maintained oral hygiene) before surgery could maintain appropriate oral conditions in the perioperative period by themselves. In most cases, dentists or dental hygienists cannot perform oral care for patients every day; hence, oral self-care has a great influence on the patients’ oral hygiene. In fact, the postoperative OAG score in the OAG score decrease group tended to remain lower than that in the OAG score increase group before surgery (11.0±2.9 vs. 12.1±3.4, p=0.089). Therefore, improvement in the OAG score before surgery may partly reflect the patients’ ability to maintain oral hygiene in the perioperative period.
In contrast, there was a significant relationship between the postoperative OAG score and the development of postoperative complications. In this study, we evaluated the postoperative OAG score at 1-2 weeks after surgery, but postoperative complications (including pneumonia and anastomotic leakage) occurred at various times. This indicates that the timing of OAG scoring (before or after the occurrence of postoperative complications) varied in each case. Therefore, further investigation is needed on whether a postoperative increase in the OAG score can be a meaningful predictor of postoperative complications.
In this study, we demonstrated that the OAG score increase group included a higher number of patients with diabetes mellitus than the OAG score decrease group. Several studies have reported that diabetes patients have significantly worse oral hygiene and a more severe form of periodontal disease than people without diabetes (28, 29). Based on the current results, it is suggested that diabetes mellitus may be a factor associated with resistance to oral care. Patients with EC and diabetes mellitus who underwent oesophageal surgery in our hospital were provided with treatment for maintaining glycaemic control by diabetes specialists. Further research is required to ascertain the improvement in oral hygiene among diabetes patients whose conditions did not improve despite appropriate glycaemic control.
This study has several limitations. First, there was a selection bias as this was a retrospective, single-institution study with a relatively small sample size. Second, this study did not include patients who received neoadjuvant chemotherapy and/or radiotherapy. In Japan, neoadjuvant chemotherapy prior to surgery is considered the standard treatment for locally advanced (Stage II/III) EC (30). Moreover, salvage surgery after definitive chemoradiotherapy is widely performed for patients with residual or recurrent EC (31). Chemotherapy and radiotherapy cause mucositis and poor oral hygiene (32, 33). Further studies are warranted to determine whether the OAG score predicts postoperative complications in patients with EC who received chemotherapy and/or radiotherapy.
In conclusion, we demonstrated that the perioperative OAG score was correlated with postoperative complications in patients with EC. In addition, absence of an improvement in the OAG score before surgery was an independent predictor for postoperative pneumonia. Finally, diabetes mellitus might be a factor associated with resistance to oral care. These observations indicate that the evaluation of oral hygiene using the OAG score is useful for providing precise perioperative oral care to prevent postoperative pneumonia.
Footnotes
Authors’ Contributions
K. Kuriyama and M. Sohda designed the study and wrote the initial draft of the manuscript. M. Sohda, S. Yokoo, K. Shirabe and H. Saeki contributed to data analysis and interpretation and assisted in the preparation of the manuscript. K. Kuriyama, T. Watanabe, H. Saito, T. Yoshida, K. Hara, M. Sakai, M. Kim, T. Asami and H. Kuwano contributed to data collection and interpretation, critically reviewed the manuscript. All Authors read and approved the final manuscript.
Conflicts of Interest
The Authors have no related conflicts of interest to declare.
- Received January 24, 2021.
- Revision received February 2, 2021.
- Accepted February 4, 2021.
- Copyright © 2021 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.
