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Effect of perioperative oral care on prevention of postoperative pneumonia associated with esophageal cancer surgery

Effect of perioperative oral care on prevention of postoperative pneumonia associated with... The aim of this study was to investigate the effectiveness of oral care in prevention of postoperative pneumonia associated with esophageal cancer surgery. Postoperative pneumonia is a severe adverse event associated with esophageal cancer surgery. It is thought to be caused by aspiration of oropharyngeal fluid containing pathogens. However, the relationship between oral health status and postoperative pneumonia has not been well investigated. This study included 539 patients with esophageal cancer undergoing surgery at 1 of 7 university hospitals. While 306 patients received perioperative oral care, 233 did not. Various clinical factors as well as occurrence of postoperative pneumonia were retrospectively evaluated. Propensity-score matching was performed to minimize selection biases associated with comparison of retrospective data between the oral care and control groups. Factors related to postoperative pneumonia were analyzed by logistic regression analysis. Of the original 539 patients, 103 (19.1%) experienced postoperative pneumonia. The results of multivariate analysis of the 420 propensity score-matched patients revealed longer operation time, postoperative dysphagia, and lack of oral care intervention to be significantly correlated with postoperative pneumonia. The present findings demonstrate that perioperative oral care can reduce the risk of postoperative pneumonia in patients undergoing esophageal cancer surgery. Abbreviations: BMI = body mass index, CI = confidence interval, CRP = C-reactive protein, FEV = forced expiratory volume, OR = odds ratio, PMTC = professional mechanical tooth cleaning. Keywords: esophageal cancer surgery, oral care, postoperative pneumonia, propensity score Editor: Neil Merrett. 1. Introduction The authors have no conflicts of interest and source of funding. With the development of various treatment methods, including Perioperative Oral Management Center, Nagasaki University Hospital, b perioperative management, prognosis in patients with esophageal Department of Clinical Oral Oncology, Nagasaki University Graduate School of [1] cancer has improved in recent decades. However, some adverse Biomedical Sciences, Nagasaki, Department of Oral and Maxillofacial Surgery, Kobe University Graduate School of Medicine, Kobe, Department of Dentistry events, such as suture insufficiency and cardiovascular and [2] and Oral Surgery, Shinshu University School of Medicine, Matsumoto, respiratory complications, often occur postoperatively. Post- Department of Oral Maxillofacial Surgery, Graduate School of Medical Sciences, operative pneumonia is one of the more frequent and possibly Nagoya City University, Nagoya, Department of Dentistry and Oral Surgery, fatal complications among patients who undergo major Kansai Medical University, Hirakata, Department of Oral and Maxillofacial [3] Surgery, Osaka City University Graduate School of Medicine, Osaka, esophageal surgery. In a study by Ando et al, the rate of Department of Preventive Dentistry, Kagoshima University Graduate School of incidence of respiratory complications was 19.5%, and severity Medical and Dental Sciences, Kagoshima, Japan. of postoperative complications, degree of residual tumor, and Correspondence: Souichi Yanamoto, Department of Clinical Oral Oncology, number of dissected mediastinal nodes were found to be Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, significant prognostic factors among patients who underwent Nagasaki 852-8588, Japan (e-mail: [email protected]). esophageal cancer surgery. The authors also stated that Copyright © 2017 the Author(s). Published by Wolters Kluwer Health, Inc. approximately half the cases of early death after surgery for This is an open access article distributed under the Creative Commons advanced esophageal cancer were caused by pulmonary Attribution License 4.0 (CCBY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. complications. Many authors have reported risk factors for postoperative pneumonia after esophageal resection; factors such Medicine (2017) 96:33(e7436) as old age, pulmonary function, diabetes mellitus, and surgical Received: 24 February 2017 / Received in final form: 11 June 2017 / Accepted: 15 June 2017 stress were found to be related to the frequency of postoperative [4–18] pneumonia, although the relationship between oral health http://dx.doi.org/10.1097/MD.0000000000007436 1 Soutome et al. Medicine (2017) 96:33 Medicine status and postoperative pneumonia was not described in these studies. One of the main causes of postoperative pneumonia is thought to be aspiration of oropharyngeal fluid containing pathogenic [19] [20] microorganisms. Akutsu et al described that tooth brushing by the patients 5 times per day decreased the incidence of postoperative pneumonia in patients undergoing esophagec- [21] tomy with thoracotomy. Hiramatsu et al also reported that preoperative professional oral cleaning and teeth and tongue brushing with deep breathing, breathing exercises, respiratory muscle stretching, proper diet, and cessation of smoking prevented postoperative pneumonia in those who underwent esophageal cancer resection. However, those studies were based on a small number of patients with historical control, and did not analyze other risk factors for postoperative pneumonia. There have been no well-designed studies that show the effects of oral Figure 1. Patients distribution to the oral care and control groups in each health care on prevention of postoperative pneumonia after hospital. esophageal cancer surgery. In a previous retrospective study involving a relatively small number of patients, we, too, have reported that perioperative oral care might reduce the risk of [22] floss, followed by gargling 3 times per day. PMTC was performed postoperative pneumonia after esophageal resection. The [23] by the method reported by Axelsson and Lindhe, including purpose of this study is to investigate the effectiveness of polishing using rubber cup, brush, and rubber tip with polishing perioperative oral care in prevention of postoperative pneumonia paste containing fluoride. Edenturous patients received only by multicenter retrospective analysis of a large number of patients cleaning of the tongue and denture, and instruction to gargling. using propensity score matching analysis. All patients received final oral cleaning by a dentist or dental hygienist the day before surgery. After surgery, patients of both 2. Methods groups were asked to perform frequent (every 3–6hours) gargling with water during the daytime. 2.1. Study design This study was a multicenter, case–control study with propensity 2.4. Variables score matching analysis. The objective variable was occurrence of postoperative pneumo- nia. Pneumonia was diagnosed by the presence of fever, elevated 2.2. Patients white blood cell and C-reactive protein (CRP) levels, and pulmonary infiltrates requiring antibiotic therapy, according to Between 2011 and 2015, 569 patients with esophageal cancer [2,4,11] the criteria reported by several investigators. On the basis underwent surgery, excluding endoscopic mucosal resection or [2–16] of previous literature, predictor variables were defined as submucosal dissection, at 1 of 7 university hospitals, including patient factors: age, sex, body mass index (BMI), smoking and those of Nagasaki University, Kobe University, Kagoshima drinking habits, diabetes mellitus, hypertension, preoperative University, Kansai Medical University, Nagoya City University, serum creatinine and albumin concentrations, and forced Shinshu University, and Osaka City University. Among them, 30 expiratory volume (FEV) 1%; tumor factors: site and stage; patients with inadequate medical records were excluded, and the treatment factors: operation method (open thoracic esophagec- remaining 539 patients were included in the study. The included tomy or thoracoscopy-assisted esophagectomy), operation time, patients were divided into 2 groups: an oral care group (n=306) blood loss, and neoadjuvant chemotherapy; postoperative and a control group (n=233 patients). In Japan, the Medical dysphagia; and oral care intervention. Patients who had not Insurance System established coverage for perioperative oral care smoked for a year or longer were classified as not having a in 2012. Patients in the control group had undergone surgery smoking habit. Tumors were categorized as being located in the before the start of perioperative oral care in each hospital, while upper, middle, or lower esophagus. Tumor stage was classified those in the oral care group had undergone surgery after the said according to the criteria proposed by the Japan Esophageal period. Since the time of introduction of oral care depending on the [24] Society. Postoperative dysphagia was defined on the basis of hospital, the rate of patients who received oral care differs (Fig. 1). medical records as choking when the patient started a paste diet after surgery, aspiration during swallowing (observed through videofluoroscopic examination), or continued tube feeding at the 2.3. Oral care intervention time of discharge. Each patient in the oral care group received oral care from a Further, duration of hospitalization and death within 30 days dentist and dental hygienist. Oral care was started from the time of hospitalization were compared between the oral care and the decision for hospitalization was made. It included oral health control groups. instruction, removal of dental calculus (scaling), professional mechanical tooth cleaning (PMTC), removal of tongue coating 2.5. Statistical analysis with a toothbrush, cleaning denture, and extraction of teeth with severe periodontitis showing pain, pus discharge, mobility, or Statistical analyses were performed using the SPSS software marked alveolar bone loss by X-ray examination. Patients were (version 24.0; Japan IBM Co., Tokyo, Japan). First, the instructed to clean teeth by toothbrush, interdental brush, dental correlation between each variable and postoperative pneumonia 2 Soutome et al. Medicine (2017) 96:33 www.md-journal.com in all 539 patients was analyzed by x test and 1-way analysis of Table 2 variance, followed by multivariate logistic regression analysis. Results of univariate analysis of variables associated with post- Differences in mean duration of hospitalization and mortality operative pneumonia among the original 539 patients. rate between the oral care and control groups were analyzed by Postoperative Postoperative Student’s t test and Fisher’s exact test, respectively. Variable pneumonia (-) pneumonia (+) P Next, propensity score analysis was performed to minimize Age, y 65.4± 8.29 66.6± 8.18 .090 selection biases associated with retrospective data analysis Sex between the 2 groups. For each patient, a propensity score for male 362 (79.9%) 91 (20.1%) .231 oral care intervention was calculated by logistic regression female 74 (86.0%) 12 (14.0%) analysis of all predictive variables. The propensity score matched Body mass index 21.0± 3.22 21.0± 2.92 .787 groups (oral care vs control) were then evaluated by logistic Smoking habit regression analysis for identifying factors associated with the - 173 (86.9%) 26 (13.1%) .006 development of postoperative pneumonia. In all analyses, + 263 (77.4%) 77 (22.6%) Drinking habit 2-tailed P values<0.05 were considered statistically significant. - 116 (87.2%) 17 (12.8%) .032 + 320 (78.8%) 86 (21.2%) 2.6. Ethics Diabetes - 396 (81.6%) 89 (18.4%) .201 The study design was approved by the institutional review boards + 40 (74.1%) 14 (25.9%) of all participating hospitals. We published research plan and Hypertension guaranteed opt-out opportunity by the homepage of each hospital. - 270 (79.9%) 68 (20.1%) .497 + 166 (82.6%) 35 (17.4%) Serum creatinine concentration, mg/dL 0.88± 0.537 0.88± 0.238 .936 3. Results Serum albumin concentration, g/dL 3.58± 0.804 3.60± 0.812 .834 Obstructive pulmonary disorder Background variables of the original 539 patients in the oral - 310 (81.4%) 71 (18.6%) .718 care and control groups before propensity score matching + 126 (79.7%) 32 (20.3%) are summarized in Table 1. The tumor stage, frequency of Tumor site (upper esophagus) thoracoscopy-assisted esophagectomy, and operation time in the Upper 50 (74.6%) 17 (25.4%) .184 oral care group were greater than those in the control group. Middle/lower 386 (81.8%) 86 (18.2%) Of the original 539 patients, 103 (19.1%) experienced Stage postoperative pneumonia, and 3 of 306 patients (0.980%) in Stages 1–2 167 (84.8%) 30 (15.2%) .089 the oral care group and 3 of 233 patients (1.29%) in the control Stages 3–4 269 (78.7%) 73 (21.3%) group died from complications within 30 days after surgery Operation method (P=1.00). There was no significant difference in average Thoracoscopy-assisted 330 (81.9%) 73 (18.1%) .315 duration of hospitalization between the oral care (45.2 days) Open thoracic 106 (77.9%) 30 (22.1%) Operation time, min 573± 174 645± 140 .002 and control (42.3 days) groups (P=.577). Upon univariate Blood loss, g 504± 537 582± 555 .189 analysis, smoking and drinking habits, operation time, postop- Neoadjuvant chemotherapy erative dysphagia, and oral care intervention were found to be - 157 (81.3%) 36 (18.7%) .909 + 279 (80.6%) 67 (19.4%) Postoperative dysphagia Table 1 - 353 (90.5%) 37 (9.5%) .000 Comparison of variables between the oral care and control groups + 83 (55.7%) 66 (44.3%) comprising the original 539 patients. Oral care intervention Before matching - 174 (74.7%) 59 (25.3%) .002 Oral care Control group + 262 (85.6%) 44 (14.4%) Propensity score variable group n= 306 n= 233 P Values are expressed as mean± standard deviation or number (%). P< .05. Age, y 65.7± 8.40 65.7± 8.19 .799 Sex (male) 251 (82.0%) 202 (86.7%) .143 significantly related to postoperative pneumonia (Table 2). Of Body mass index 21.1± 3.20 20.9± 3.10 .455 Smoking habit 196 (64.1%) 144 (61.8%) .592 these variables, operation time, postoperative dysphagia, and oral Drinking habit 229 (74.8%) 177 (76.0%) .763 care intervention were found to be significantly correlated with Diabetes 29 (9.48%) 25 (10.7%) .631 postoperative pneumonia by multivariate analysis (Table 3). Hypertension 114 (37.3%) 87 (37.3%) .984 Propensity scores were calculated for all patients by logistic Serum creatinine concentration, mg/dL 0.92± 0.625 0.83± 0.227 .055 regression analysis of all 17 variables associated with oral care Serum albumin concentration, g/dL 3.63± 0.781 3.53± 0.833 .148 intervention. The concordance index (c index) was 0.650—which Obstructive pulmonary disorder 90 (29.4%) 68 (29.2%) .954 indicated a strong ability to differentiate between patients with and Tumor site (upper esophagus) 41 (13.4%) 26 (11.2%) .435 without oral care—and the Hosmer–Lemeshow statistic was Stage 3–4 208 (68.0%) 134 (57.5%) .012 insignificant (P=.363), indicating good calibration. Propensity Open thoracic esophagectomy 63 (20.6%) 73 (31.3%) .004 Operation time, min 625± 153 571± 152 .000 scores—which reflected the probability that a patient would receive Blood loss, g 506± 489 536± 603 .526 oral care intervention—ranged from 0.2704 to 0.9941 in the oral Neoadjuvant chemotherapy 200 (65.4%) 146 (62.7%) .517 care group and 0.1456 to 0.9117 in the control group. Postoperative dysphagia 76 (24.8%) 73 (31.3%) .095 Propensity score analysis resulted in 420 patients (210 in each group) being matched (Table 4). The results of univariate analysis Values are expressed as mean± standard deviation or number (%). P< .05. of the propensity score matched groups revealed old age, smoking 3 Soutome et al. Medicine (2017) 96:33 Medicine Table 3 Table 5 Results of multivariate analysis of variables associated with Results of univariate analysis of variables associated with post- postoperative pneumonia among the original 539 patients. operative pneumonia in 420 propensity score matched patients. Variable P Odds ratio 95% CI Postoperative Postoperative Variable pneumonia (-) pneumonia (+) P Smoking habit .139 1.527 0.871–2.679 Drinking habit .689 1.140 0.599–2.168 Age, y 65.0± 8.63 68.0± 8.01 .028 Operation time .000 1.003 1.001–1.005 Sex Postoperative dysphagia .000 7.862 4.805–12.864 Male 290 (80.8%) 69 (19.2%) .724 Oral care intervention .001 0.438 0.266–0.721 Female 51 (83.6%) 10 (16.4%) Body mass index 21.2± 2.93 21.1± 2.74 .694 CI= confidence interval. Smoking habit P< .05. - 139 (86.9%) 21 (13.1%) .021 + 202 (77.7%) 58 (22.3%) Drinking habit Table 4 - 88 (88.9%) 11 (11.1%) .027 Comparison of variables between the oral care and control groups + 253 (78.8%) 68 (21.2%) comprising 420 propensity score matched patients. Diabetes After matching - 307 (81.9%) 68 (18.1%) .315 Oral care Control + 34 (75.6%) 11 (24.4%) Propensity score variable group n= 210 group n= 210 P Hypertension - 208 (79.7%) 53 (20.3%) .368 Age, y 66.0± 8.60 66.0± 8.53 .834 + 133 (83.6%) 26 (16.4%) Sex (male) 180 (85.7%) 179 (85.2%) 1.000 Serum creatinine concentration, mg/dL 0.84± 0.224 0.88± 0.215 .166 Body mass index 21.2± 2.79 21.1± 3.00 .641 Serum albumin concentration, g/dL 3.60± 0.804 3.71± 0.732 .273 Smoking habit 135 (64.3%) 125 (59.5%) .366 Obstructive pulmonary disorder Drinking habit 161 (76.7%) 160 (76.2%) 1.000 - 243 (81.3%) 56 (18.7%) 1.000 Diabetes 21 (10.0%) 24 (11.4%) .753 + 98 (81.0%) 23 (19.0%) Hypertension 79 (37.6%) 80 (38.1%) 1.000 Tumor site (upper esophagus) Serum creatinine concentration, mg/dL 0.85± 0.222 0.85± 0.224 .977 upper 34 (75.6%) 11 (24.4%) .315 Serum albumin concentration, g/dL 3.66± 0.714 3.57± 0.860 .261 middle/lower 307 (81.9%) 68 (18.1%) Obstructive pulmonary disorder 60 (28.6%) 61 (29.0%) 1.000 Stage Tumor site (upper esophagus) 20 (9.52%) 25 (11.9%) .528 Stages 1–2 148 (85.5%) 25 (14.5%) .058 Stages 3–4 124 (59.0%) 123 (58.6%) 1.000 Stages 3–4 193 (78.1%) 54 (21.9%) Open thoracic esophagectomy 57 (27.1%) 53 (25.2%) .739 Operation method Operation time, min 581± 137 587± 135 .652 Thoracoscopy-assisted 255 (82.3%) 55 (17.7%) .394 Blood loss, g 539± 625 512± 484 .626 Open thoracic 86 (78.2%) 24 (21.8%) Neoadjuvant chemotherapy 132 (62.9%) 132 (62.9%) 1.000 Operation time, min 573± 134 631± 140 .001 Postoperative dysphagia 62 (29.5%) 60 (28.6%) .914 Blood loss, g 521± 578 546± 471 .722 Neoadjuvant chemotherapy Values are expressed as mean± standard deviation or number (%). - 128 (82.1%) 28 (17.9%) .797 + 213 (80.7%) 51 (19.3%) and drinking habits, longer operation time, postoperative Postoperative dysphagia dysphagia, and lack of oral care intervention to be correlated - 271 (90.9%) 27 (9.1%) .000 with development of postoperative pneumonia (Table 5). Table 6 + 70 (57.4%) 52 (42.6%) presents the results of multivariate analysis, which revealed 3 Oral care intervention significant factors associated with postoperative pneumonia: - 158 (75.2%) 52 (24.8%) .003 operation time [P=.011; odds ratio (OR), 1.003; 95% confidence + 183 (87.1%) 27 (12.9%) interval (95% CI), 1.001–1.005); postoperative dysphagia Values are expressed as mean± standard deviation or number (%). (P=.000; OR, 7.195; 95% CI, 4.084–12.68), and oral care P< .05. intervention (P=.001; OR, 0.365; 95% CI, 0.204–0.653). Dental clearance before major esophageal surgeries is required nowadays, although there have been no studies with high 4. Discussion evidence level that showed the effect of oral health care on the Postoperative pneumonia frequently develops after esophagec- prevention of pneumonia after esophageal cancer surgery. tomy. It is associated with prolonged hospitalization, higher Guideline for Diagnosis and Treatment of Esophageal Cancer [2] [25] medical costs, and substantial operative mortality. Previous by The Japan Esophageal Society recommended oral care studies have reported incidence rates of postoperative pneumonia before surgery to reduce rate of postoperative pneumonia, while [26] after esophageal surgery as ranging from 7.4% to 50%; in in the revised version of 2017, the description of oral care was addition, various factors, including regular smoking, decreased deleted because of the lack of evidence supporting the efficacy of pulmonary function, diabetes mellitus, old age, greater surgical oral care on the prevention of postoperative pneumonia. stress (operation time, blood loss, and thoracotomy), and general In the present study, 539 patients from 7 hospitals were conditions (performance status and complications) have been enrolled, and propensity score analysis was performed to reduce [4–18] reported to be correlated with this complication. The selection biases associated with retrospective data analysis. The relatively high incidence of postoperative pneumonia despite the incidence rate of postoperative pneumonia after esophageal recent advances in surgical procedures and antibiotic therapy cancer surgery in the present study (19.1%) corresponded to that [4–18] indicates the need for new preventive measures. reported in previous studies. There was no difference in 4 Soutome et al. Medicine (2017) 96:33 www.md-journal.com [3] Ando N, Ozawa S, Kitagawa Y, et al. Improvement in the results of Table 6 surgical treatment of advanced squamous esophageal carcinoma during Results of multivariate analysis of variables associated with 15 consecutive years. Ann Surg 2000;232:225–32. postoperative pneumonia in 420 propensity score matched [4] Ferguson MK, Durkin AE. Preoperative prediction of the risk of pulmonary complications after esophagectomy for cancer. J Thorac patients. Cardiovasc Surg 2002;123:661–9. Variable P Odds ratio 95% CI [5] Avendano CE, Flume PA, Silvestri GA, et al. Pulmonary complications after esophagectomy. Ann Thorac Surg 2002;73:922–6. Age .031 1.040 1.004–1.077 [6] Fang W, Kato H, Tachimori Y, et al. Analysis of pulmonary Smoking habit .208 1.513 0.794–2.883 complications after three-field lymph node dissection for esophageal Drinking habit .364 1.425 0.664–3.058 cancer. Ann Thorac Surg 2003;76:903–8. Stages 3–4 .404 1.286 0.712–2.323 [7] Law S, Wong K, Kwok K, et al. Predictive factors for postoperative Operation time .011 1.003 1.001–1.005 ∗ pulmonary complications and mortality after esophagectomy for cancer. Postoperative dysphagia .000 7.195 4.084–12.675 Ann Surg 2004;240:791–800. Oral care intervention .001 0.365 0.204–0.653 [8] Kinugasa S, Tachibana M, Yoshimura H, et al. Postoperative pulmonary complications are associated with worse short- and long-term outcomes CI= confidence interval. after extended esophagectomy. J Surg Oncol 2004;88:71–7. P< .05. [9] Jiao WJ, Wang TY, Gong M, et al. Pulmonary complications in patients with chronic obstructive pulmonary disease following transthoracic duration of hospitalization between the oral care and control esophagectomy. World J Gastroenterol 2006;12:2505–9. groups, which might be attributable to the fact that duration of [10] Nakamura M, Iwahashi M, Nakamori M, et al. An analysis of the factors hospitalization was affected by other factors, such as adjuvant contributing to a reduction in the incidence of pulmonary complications following an esophagectomy for esophageal cancer. Langenbecks Arch radiotherapy or chemotherapy. Upon multivariate analysis of the Surg 2008;393:127–33. original 539 patients, longer operation time, postoperative [11] Dhungel B, Diggs BS, Hunter JG, et al. Patient and peri-operative dysphagia, and lack of oral care intervention were found to be predictors of morbidity and mortality after esophagectomy: American significantly associated with development of postoperative College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP), 2005-2008. J Gastrointest Surg 2010;14:1492–501. pneumonia, with postoperative dysphagia exhibiting the stron- [12] Zingg U, Smithers BM, Gotley DC, et al. Factors associated with gest correlation with occurrence of pneumonia. postoperative pulmonary morbidity after esophagectomy for cancer. In a statistical analysis of observational data, propensity score Ann Surg Oncol 2011;18:1460–8. matching is a technique that attempts to estimate the effect of a [13] Ferguson MK, Celauro AD, Prachand V. Prediction of major pulmonary treatment, policy, or other intervention by accounting for the complications after esophagectomy. Ann Thorac Surg 2011;91: [27] 1494–500. covariates that predict the receipt of treatment. Propensity [14] Paul DJ, Jamieson GG, Watson DI, et al. Perioperative risk analysis for score matching reduces bias due to confounding variables, which acute respiratory distress syndrome after elective oesophagectomy. ANZ is commonly observed in the estimation of treatment effect by J Surg 2011;81:700–6. mere comparison of outcomes among units with and without [15] Shiozaki A, Fujiwara H, Okamura H, et al. Risk factors for postoperative respiratory complications following esophageal cancer resection. Oncol treatment. In the present study, logistic regression analysis of the Lett 2012;3:907–12. 420 propensity score matched patients revealed old age, longer [16] Sunpaweravong S, Ruangsin S, Laohawiriyakamol S, et al. Prediction of operation time, postoperative dysphagia, and lack of oral care major postoperative complications and survival for locally advanced intervention to be significantly associated with occurrence of esophageal carcinoma patients. Asian J Surg 2012;35:104–9. postoperative pneumonia. To the best of our knowledge, this is [17] Bakhos CT, Fabian T, Oyasiji TO, et al. Impact of the surgical technique on pulmonary morbidity after esophagectomy. Ann Thorac Surg the first study demonstrating the effectiveness of perioperative 2012;93:221–6. oral care in prevention of postoperative pneumonia after [18] Yoshida N, Watanabe M, Baba Y, et al. Risk factors for pulmonary esophagectomy with a high evidence level. Further, we believe complications after esophagectomy for esophageal cancer. Surg Today that our study has generalizability and applicability because the 2014;44:526–32. [19] Akutsu Y, Matsubara H, Okazumi S, et al. 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Because oral care has been covered by the 2014;42:385–8. Japanese medical insurance system since 2012, and most Japanese [22] Soutome S, Yanamoto S, Funahara M, et al. Preventive effect on post- operative pneumonia of oral health care among patients who undergo patients now receive oral care before surgery, it would be esophageal resection: a multi-center retrospective study. Surg Infect challenging to conduct a randomized controlled trial regarding the (Larchmt) 2016;17:479–84. preventive effect of oral care. We are planning another multicenter [23] Axelsson P, Lindhe J. Effect of fluoride on gingivitis and dental caries in a prospective observational study to address these issues. preventive program based on plaque control. Community Dent Oral Epidemiol 1975;3:156–60. [24] Japan Esophageal SocietyJapanese classification of esophageal cancer, References tenth edition: part I. Esophagus 2009;6:1–25. [1] Nafteux P, Depypere L, Van Veer H, et al. 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Effect of perioperative oral care on prevention of postoperative pneumonia associated with esophageal cancer surgery

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Copyright © 2017 the Author(s). Published by Wolters Kluwer Health, Inc.
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Abstract

The aim of this study was to investigate the effectiveness of oral care in prevention of postoperative pneumonia associated with esophageal cancer surgery. Postoperative pneumonia is a severe adverse event associated with esophageal cancer surgery. It is thought to be caused by aspiration of oropharyngeal fluid containing pathogens. However, the relationship between oral health status and postoperative pneumonia has not been well investigated. This study included 539 patients with esophageal cancer undergoing surgery at 1 of 7 university hospitals. While 306 patients received perioperative oral care, 233 did not. Various clinical factors as well as occurrence of postoperative pneumonia were retrospectively evaluated. Propensity-score matching was performed to minimize selection biases associated with comparison of retrospective data between the oral care and control groups. Factors related to postoperative pneumonia were analyzed by logistic regression analysis. Of the original 539 patients, 103 (19.1%) experienced postoperative pneumonia. The results of multivariate analysis of the 420 propensity score-matched patients revealed longer operation time, postoperative dysphagia, and lack of oral care intervention to be significantly correlated with postoperative pneumonia. The present findings demonstrate that perioperative oral care can reduce the risk of postoperative pneumonia in patients undergoing esophageal cancer surgery. Abbreviations: BMI = body mass index, CI = confidence interval, CRP = C-reactive protein, FEV = forced expiratory volume, OR = odds ratio, PMTC = professional mechanical tooth cleaning. Keywords: esophageal cancer surgery, oral care, postoperative pneumonia, propensity score Editor: Neil Merrett. 1. Introduction The authors have no conflicts of interest and source of funding. With the development of various treatment methods, including Perioperative Oral Management Center, Nagasaki University Hospital, b perioperative management, prognosis in patients with esophageal Department of Clinical Oral Oncology, Nagasaki University Graduate School of [1] cancer has improved in recent decades. However, some adverse Biomedical Sciences, Nagasaki, Department of Oral and Maxillofacial Surgery, Kobe University Graduate School of Medicine, Kobe, Department of Dentistry events, such as suture insufficiency and cardiovascular and [2] and Oral Surgery, Shinshu University School of Medicine, Matsumoto, respiratory complications, often occur postoperatively. Post- Department of Oral Maxillofacial Surgery, Graduate School of Medical Sciences, operative pneumonia is one of the more frequent and possibly Nagoya City University, Nagoya, Department of Dentistry and Oral Surgery, fatal complications among patients who undergo major Kansai Medical University, Hirakata, Department of Oral and Maxillofacial [3] Surgery, Osaka City University Graduate School of Medicine, Osaka, esophageal surgery. In a study by Ando et al, the rate of Department of Preventive Dentistry, Kagoshima University Graduate School of incidence of respiratory complications was 19.5%, and severity Medical and Dental Sciences, Kagoshima, Japan. of postoperative complications, degree of residual tumor, and Correspondence: Souichi Yanamoto, Department of Clinical Oral Oncology, number of dissected mediastinal nodes were found to be Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, significant prognostic factors among patients who underwent Nagasaki 852-8588, Japan (e-mail: [email protected]). esophageal cancer surgery. The authors also stated that Copyright © 2017 the Author(s). Published by Wolters Kluwer Health, Inc. approximately half the cases of early death after surgery for This is an open access article distributed under the Creative Commons advanced esophageal cancer were caused by pulmonary Attribution License 4.0 (CCBY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. complications. Many authors have reported risk factors for postoperative pneumonia after esophageal resection; factors such Medicine (2017) 96:33(e7436) as old age, pulmonary function, diabetes mellitus, and surgical Received: 24 February 2017 / Received in final form: 11 June 2017 / Accepted: 15 June 2017 stress were found to be related to the frequency of postoperative [4–18] pneumonia, although the relationship between oral health http://dx.doi.org/10.1097/MD.0000000000007436 1 Soutome et al. Medicine (2017) 96:33 Medicine status and postoperative pneumonia was not described in these studies. One of the main causes of postoperative pneumonia is thought to be aspiration of oropharyngeal fluid containing pathogenic [19] [20] microorganisms. Akutsu et al described that tooth brushing by the patients 5 times per day decreased the incidence of postoperative pneumonia in patients undergoing esophagec- [21] tomy with thoracotomy. Hiramatsu et al also reported that preoperative professional oral cleaning and teeth and tongue brushing with deep breathing, breathing exercises, respiratory muscle stretching, proper diet, and cessation of smoking prevented postoperative pneumonia in those who underwent esophageal cancer resection. However, those studies were based on a small number of patients with historical control, and did not analyze other risk factors for postoperative pneumonia. There have been no well-designed studies that show the effects of oral Figure 1. Patients distribution to the oral care and control groups in each health care on prevention of postoperative pneumonia after hospital. esophageal cancer surgery. In a previous retrospective study involving a relatively small number of patients, we, too, have reported that perioperative oral care might reduce the risk of [22] floss, followed by gargling 3 times per day. PMTC was performed postoperative pneumonia after esophageal resection. The [23] by the method reported by Axelsson and Lindhe, including purpose of this study is to investigate the effectiveness of polishing using rubber cup, brush, and rubber tip with polishing perioperative oral care in prevention of postoperative pneumonia paste containing fluoride. Edenturous patients received only by multicenter retrospective analysis of a large number of patients cleaning of the tongue and denture, and instruction to gargling. using propensity score matching analysis. All patients received final oral cleaning by a dentist or dental hygienist the day before surgery. After surgery, patients of both 2. Methods groups were asked to perform frequent (every 3–6hours) gargling with water during the daytime. 2.1. Study design This study was a multicenter, case–control study with propensity 2.4. Variables score matching analysis. The objective variable was occurrence of postoperative pneumo- nia. Pneumonia was diagnosed by the presence of fever, elevated 2.2. Patients white blood cell and C-reactive protein (CRP) levels, and pulmonary infiltrates requiring antibiotic therapy, according to Between 2011 and 2015, 569 patients with esophageal cancer [2,4,11] the criteria reported by several investigators. On the basis underwent surgery, excluding endoscopic mucosal resection or [2–16] of previous literature, predictor variables were defined as submucosal dissection, at 1 of 7 university hospitals, including patient factors: age, sex, body mass index (BMI), smoking and those of Nagasaki University, Kobe University, Kagoshima drinking habits, diabetes mellitus, hypertension, preoperative University, Kansai Medical University, Nagoya City University, serum creatinine and albumin concentrations, and forced Shinshu University, and Osaka City University. Among them, 30 expiratory volume (FEV) 1%; tumor factors: site and stage; patients with inadequate medical records were excluded, and the treatment factors: operation method (open thoracic esophagec- remaining 539 patients were included in the study. The included tomy or thoracoscopy-assisted esophagectomy), operation time, patients were divided into 2 groups: an oral care group (n=306) blood loss, and neoadjuvant chemotherapy; postoperative and a control group (n=233 patients). In Japan, the Medical dysphagia; and oral care intervention. Patients who had not Insurance System established coverage for perioperative oral care smoked for a year or longer were classified as not having a in 2012. Patients in the control group had undergone surgery smoking habit. Tumors were categorized as being located in the before the start of perioperative oral care in each hospital, while upper, middle, or lower esophagus. Tumor stage was classified those in the oral care group had undergone surgery after the said according to the criteria proposed by the Japan Esophageal period. Since the time of introduction of oral care depending on the [24] Society. Postoperative dysphagia was defined on the basis of hospital, the rate of patients who received oral care differs (Fig. 1). medical records as choking when the patient started a paste diet after surgery, aspiration during swallowing (observed through videofluoroscopic examination), or continued tube feeding at the 2.3. Oral care intervention time of discharge. Each patient in the oral care group received oral care from a Further, duration of hospitalization and death within 30 days dentist and dental hygienist. Oral care was started from the time of hospitalization were compared between the oral care and the decision for hospitalization was made. It included oral health control groups. instruction, removal of dental calculus (scaling), professional mechanical tooth cleaning (PMTC), removal of tongue coating 2.5. Statistical analysis with a toothbrush, cleaning denture, and extraction of teeth with severe periodontitis showing pain, pus discharge, mobility, or Statistical analyses were performed using the SPSS software marked alveolar bone loss by X-ray examination. Patients were (version 24.0; Japan IBM Co., Tokyo, Japan). First, the instructed to clean teeth by toothbrush, interdental brush, dental correlation between each variable and postoperative pneumonia 2 Soutome et al. Medicine (2017) 96:33 www.md-journal.com in all 539 patients was analyzed by x test and 1-way analysis of Table 2 variance, followed by multivariate logistic regression analysis. Results of univariate analysis of variables associated with post- Differences in mean duration of hospitalization and mortality operative pneumonia among the original 539 patients. rate between the oral care and control groups were analyzed by Postoperative Postoperative Student’s t test and Fisher’s exact test, respectively. Variable pneumonia (-) pneumonia (+) P Next, propensity score analysis was performed to minimize Age, y 65.4± 8.29 66.6± 8.18 .090 selection biases associated with retrospective data analysis Sex between the 2 groups. For each patient, a propensity score for male 362 (79.9%) 91 (20.1%) .231 oral care intervention was calculated by logistic regression female 74 (86.0%) 12 (14.0%) analysis of all predictive variables. The propensity score matched Body mass index 21.0± 3.22 21.0± 2.92 .787 groups (oral care vs control) were then evaluated by logistic Smoking habit regression analysis for identifying factors associated with the - 173 (86.9%) 26 (13.1%) .006 development of postoperative pneumonia. In all analyses, + 263 (77.4%) 77 (22.6%) Drinking habit 2-tailed P values<0.05 were considered statistically significant. - 116 (87.2%) 17 (12.8%) .032 + 320 (78.8%) 86 (21.2%) 2.6. Ethics Diabetes - 396 (81.6%) 89 (18.4%) .201 The study design was approved by the institutional review boards + 40 (74.1%) 14 (25.9%) of all participating hospitals. We published research plan and Hypertension guaranteed opt-out opportunity by the homepage of each hospital. - 270 (79.9%) 68 (20.1%) .497 + 166 (82.6%) 35 (17.4%) Serum creatinine concentration, mg/dL 0.88± 0.537 0.88± 0.238 .936 3. Results Serum albumin concentration, g/dL 3.58± 0.804 3.60± 0.812 .834 Obstructive pulmonary disorder Background variables of the original 539 patients in the oral - 310 (81.4%) 71 (18.6%) .718 care and control groups before propensity score matching + 126 (79.7%) 32 (20.3%) are summarized in Table 1. The tumor stage, frequency of Tumor site (upper esophagus) thoracoscopy-assisted esophagectomy, and operation time in the Upper 50 (74.6%) 17 (25.4%) .184 oral care group were greater than those in the control group. Middle/lower 386 (81.8%) 86 (18.2%) Of the original 539 patients, 103 (19.1%) experienced Stage postoperative pneumonia, and 3 of 306 patients (0.980%) in Stages 1–2 167 (84.8%) 30 (15.2%) .089 the oral care group and 3 of 233 patients (1.29%) in the control Stages 3–4 269 (78.7%) 73 (21.3%) group died from complications within 30 days after surgery Operation method (P=1.00). There was no significant difference in average Thoracoscopy-assisted 330 (81.9%) 73 (18.1%) .315 duration of hospitalization between the oral care (45.2 days) Open thoracic 106 (77.9%) 30 (22.1%) Operation time, min 573± 174 645± 140 .002 and control (42.3 days) groups (P=.577). Upon univariate Blood loss, g 504± 537 582± 555 .189 analysis, smoking and drinking habits, operation time, postop- Neoadjuvant chemotherapy erative dysphagia, and oral care intervention were found to be - 157 (81.3%) 36 (18.7%) .909 + 279 (80.6%) 67 (19.4%) Postoperative dysphagia Table 1 - 353 (90.5%) 37 (9.5%) .000 Comparison of variables between the oral care and control groups + 83 (55.7%) 66 (44.3%) comprising the original 539 patients. Oral care intervention Before matching - 174 (74.7%) 59 (25.3%) .002 Oral care Control group + 262 (85.6%) 44 (14.4%) Propensity score variable group n= 306 n= 233 P Values are expressed as mean± standard deviation or number (%). P< .05. Age, y 65.7± 8.40 65.7± 8.19 .799 Sex (male) 251 (82.0%) 202 (86.7%) .143 significantly related to postoperative pneumonia (Table 2). Of Body mass index 21.1± 3.20 20.9± 3.10 .455 Smoking habit 196 (64.1%) 144 (61.8%) .592 these variables, operation time, postoperative dysphagia, and oral Drinking habit 229 (74.8%) 177 (76.0%) .763 care intervention were found to be significantly correlated with Diabetes 29 (9.48%) 25 (10.7%) .631 postoperative pneumonia by multivariate analysis (Table 3). Hypertension 114 (37.3%) 87 (37.3%) .984 Propensity scores were calculated for all patients by logistic Serum creatinine concentration, mg/dL 0.92± 0.625 0.83± 0.227 .055 regression analysis of all 17 variables associated with oral care Serum albumin concentration, g/dL 3.63± 0.781 3.53± 0.833 .148 intervention. The concordance index (c index) was 0.650—which Obstructive pulmonary disorder 90 (29.4%) 68 (29.2%) .954 indicated a strong ability to differentiate between patients with and Tumor site (upper esophagus) 41 (13.4%) 26 (11.2%) .435 without oral care—and the Hosmer–Lemeshow statistic was Stage 3–4 208 (68.0%) 134 (57.5%) .012 insignificant (P=.363), indicating good calibration. Propensity Open thoracic esophagectomy 63 (20.6%) 73 (31.3%) .004 Operation time, min 625± 153 571± 152 .000 scores—which reflected the probability that a patient would receive Blood loss, g 506± 489 536± 603 .526 oral care intervention—ranged from 0.2704 to 0.9941 in the oral Neoadjuvant chemotherapy 200 (65.4%) 146 (62.7%) .517 care group and 0.1456 to 0.9117 in the control group. Postoperative dysphagia 76 (24.8%) 73 (31.3%) .095 Propensity score analysis resulted in 420 patients (210 in each group) being matched (Table 4). The results of univariate analysis Values are expressed as mean± standard deviation or number (%). P< .05. of the propensity score matched groups revealed old age, smoking 3 Soutome et al. Medicine (2017) 96:33 Medicine Table 3 Table 5 Results of multivariate analysis of variables associated with Results of univariate analysis of variables associated with post- postoperative pneumonia among the original 539 patients. operative pneumonia in 420 propensity score matched patients. Variable P Odds ratio 95% CI Postoperative Postoperative Variable pneumonia (-) pneumonia (+) P Smoking habit .139 1.527 0.871–2.679 Drinking habit .689 1.140 0.599–2.168 Age, y 65.0± 8.63 68.0± 8.01 .028 Operation time .000 1.003 1.001–1.005 Sex Postoperative dysphagia .000 7.862 4.805–12.864 Male 290 (80.8%) 69 (19.2%) .724 Oral care intervention .001 0.438 0.266–0.721 Female 51 (83.6%) 10 (16.4%) Body mass index 21.2± 2.93 21.1± 2.74 .694 CI= confidence interval. Smoking habit P< .05. - 139 (86.9%) 21 (13.1%) .021 + 202 (77.7%) 58 (22.3%) Drinking habit Table 4 - 88 (88.9%) 11 (11.1%) .027 Comparison of variables between the oral care and control groups + 253 (78.8%) 68 (21.2%) comprising 420 propensity score matched patients. Diabetes After matching - 307 (81.9%) 68 (18.1%) .315 Oral care Control + 34 (75.6%) 11 (24.4%) Propensity score variable group n= 210 group n= 210 P Hypertension - 208 (79.7%) 53 (20.3%) .368 Age, y 66.0± 8.60 66.0± 8.53 .834 + 133 (83.6%) 26 (16.4%) Sex (male) 180 (85.7%) 179 (85.2%) 1.000 Serum creatinine concentration, mg/dL 0.84± 0.224 0.88± 0.215 .166 Body mass index 21.2± 2.79 21.1± 3.00 .641 Serum albumin concentration, g/dL 3.60± 0.804 3.71± 0.732 .273 Smoking habit 135 (64.3%) 125 (59.5%) .366 Obstructive pulmonary disorder Drinking habit 161 (76.7%) 160 (76.2%) 1.000 - 243 (81.3%) 56 (18.7%) 1.000 Diabetes 21 (10.0%) 24 (11.4%) .753 + 98 (81.0%) 23 (19.0%) Hypertension 79 (37.6%) 80 (38.1%) 1.000 Tumor site (upper esophagus) Serum creatinine concentration, mg/dL 0.85± 0.222 0.85± 0.224 .977 upper 34 (75.6%) 11 (24.4%) .315 Serum albumin concentration, g/dL 3.66± 0.714 3.57± 0.860 .261 middle/lower 307 (81.9%) 68 (18.1%) Obstructive pulmonary disorder 60 (28.6%) 61 (29.0%) 1.000 Stage Tumor site (upper esophagus) 20 (9.52%) 25 (11.9%) .528 Stages 1–2 148 (85.5%) 25 (14.5%) .058 Stages 3–4 124 (59.0%) 123 (58.6%) 1.000 Stages 3–4 193 (78.1%) 54 (21.9%) Open thoracic esophagectomy 57 (27.1%) 53 (25.2%) .739 Operation method Operation time, min 581± 137 587± 135 .652 Thoracoscopy-assisted 255 (82.3%) 55 (17.7%) .394 Blood loss, g 539± 625 512± 484 .626 Open thoracic 86 (78.2%) 24 (21.8%) Neoadjuvant chemotherapy 132 (62.9%) 132 (62.9%) 1.000 Operation time, min 573± 134 631± 140 .001 Postoperative dysphagia 62 (29.5%) 60 (28.6%) .914 Blood loss, g 521± 578 546± 471 .722 Neoadjuvant chemotherapy Values are expressed as mean± standard deviation or number (%). - 128 (82.1%) 28 (17.9%) .797 + 213 (80.7%) 51 (19.3%) and drinking habits, longer operation time, postoperative Postoperative dysphagia dysphagia, and lack of oral care intervention to be correlated - 271 (90.9%) 27 (9.1%) .000 with development of postoperative pneumonia (Table 5). Table 6 + 70 (57.4%) 52 (42.6%) presents the results of multivariate analysis, which revealed 3 Oral care intervention significant factors associated with postoperative pneumonia: - 158 (75.2%) 52 (24.8%) .003 operation time [P=.011; odds ratio (OR), 1.003; 95% confidence + 183 (87.1%) 27 (12.9%) interval (95% CI), 1.001–1.005); postoperative dysphagia Values are expressed as mean± standard deviation or number (%). (P=.000; OR, 7.195; 95% CI, 4.084–12.68), and oral care P< .05. intervention (P=.001; OR, 0.365; 95% CI, 0.204–0.653). Dental clearance before major esophageal surgeries is required nowadays, although there have been no studies with high 4. Discussion evidence level that showed the effect of oral health care on the Postoperative pneumonia frequently develops after esophagec- prevention of pneumonia after esophageal cancer surgery. tomy. It is associated with prolonged hospitalization, higher Guideline for Diagnosis and Treatment of Esophageal Cancer [2] [25] medical costs, and substantial operative mortality. Previous by The Japan Esophageal Society recommended oral care studies have reported incidence rates of postoperative pneumonia before surgery to reduce rate of postoperative pneumonia, while [26] after esophageal surgery as ranging from 7.4% to 50%; in in the revised version of 2017, the description of oral care was addition, various factors, including regular smoking, decreased deleted because of the lack of evidence supporting the efficacy of pulmonary function, diabetes mellitus, old age, greater surgical oral care on the prevention of postoperative pneumonia. stress (operation time, blood loss, and thoracotomy), and general In the present study, 539 patients from 7 hospitals were conditions (performance status and complications) have been enrolled, and propensity score analysis was performed to reduce [4–18] reported to be correlated with this complication. The selection biases associated with retrospective data analysis. The relatively high incidence of postoperative pneumonia despite the incidence rate of postoperative pneumonia after esophageal recent advances in surgical procedures and antibiotic therapy cancer surgery in the present study (19.1%) corresponded to that [4–18] indicates the need for new preventive measures. reported in previous studies. There was no difference in 4 Soutome et al. Medicine (2017) 96:33 www.md-journal.com [3] Ando N, Ozawa S, Kitagawa Y, et al. Improvement in the results of Table 6 surgical treatment of advanced squamous esophageal carcinoma during Results of multivariate analysis of variables associated with 15 consecutive years. Ann Surg 2000;232:225–32. postoperative pneumonia in 420 propensity score matched [4] Ferguson MK, Durkin AE. Preoperative prediction of the risk of pulmonary complications after esophagectomy for cancer. J Thorac patients. Cardiovasc Surg 2002;123:661–9. Variable P Odds ratio 95% CI [5] Avendano CE, Flume PA, Silvestri GA, et al. Pulmonary complications after esophagectomy. Ann Thorac Surg 2002;73:922–6. Age .031 1.040 1.004–1.077 [6] Fang W, Kato H, Tachimori Y, et al. Analysis of pulmonary Smoking habit .208 1.513 0.794–2.883 complications after three-field lymph node dissection for esophageal Drinking habit .364 1.425 0.664–3.058 cancer. Ann Thorac Surg 2003;76:903–8. Stages 3–4 .404 1.286 0.712–2.323 [7] Law S, Wong K, Kwok K, et al. Predictive factors for postoperative Operation time .011 1.003 1.001–1.005 ∗ pulmonary complications and mortality after esophagectomy for cancer. Postoperative dysphagia .000 7.195 4.084–12.675 Ann Surg 2004;240:791–800. Oral care intervention .001 0.365 0.204–0.653 [8] Kinugasa S, Tachibana M, Yoshimura H, et al. Postoperative pulmonary complications are associated with worse short- and long-term outcomes CI= confidence interval. after extended esophagectomy. J Surg Oncol 2004;88:71–7. P< .05. [9] Jiao WJ, Wang TY, Gong M, et al. 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