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. 2023 Sep 3;37(5):2253–2259. doi: 10.21873/invivo.13327

Influence of the Oral Health Assessment Tool Score on Survival of Patients With Esophageal Cancer

HIROSHI TAMAGAWA 1,#, AYAKO TAMAGAWA 1,#, TORU AOYAMA 1, ITARU HASHIMOTO 1, YUKIO MAEZAWA 1, KENTARO HARA 1, AYA KATO 1, NATSUMI KAMIYA 1, KAZUKI OTANI 1, MASAKATSU NUMATA 1, KEISUKE KAZAMA 1, JYUNYA MORITA 1, MIE TANABE 1, SHIZUNE ONUMA 1, HARUHIKO CHO 1, SHO SAWAZAKI 1, TAKASHI OHSHIMA 2, NORIO YUKAWA 1, KENJI MITSUDO 3, AYA SAITO 1, YASUSHI RINO 1
PMCID: PMC10500491  PMID: 37652503

Abstract

Background/Aim

We investigated the influence of the preoperative Oral Health Assessment Tool (OHAT) score on the outcomes of patients with esophageal cancer after curative surgery.

Patients and Methods

This study included 90 patients with esophageal cancer who underwent curative surgery and who were screened with the OHAT between 2008 and 2021. The OHAT consists of eight categories with three possible scores. The risk factors for 5-year overall survival (OS) and recurrence-free survival (RFS) were identified.

Results

Patients were divided into healthy (n=42) and unhealthy (n=48) groups. The OHAT score was identified as a significant risk factor for postoperative pneumonia (11.9% vs. 43.8%, p=0.001) and postoperative hospital stay (20.5 days vs. 50.1 days, p=0.042). The 5-year OS rate after surgery was 71.2% in the healthy group and 43.2% in the unhealthy group, which was a significant difference (p=0.015). A multivariate analysis showed that a high OHAT score was a significant independent factor for 5-year OS (p=0.034).

Conclusion

The OHAT score was a useful prognostic marker in patients who underwent curative surgery for esophageal cancer. To improve the oncological outcomes of patients with esophageal cancer, it is necessary to carefully plan perioperative oral/dental care using the OHAT score.

Keywords: Oral Health Assessment Tool, esophageal cancer, longterm survival

With an estimated 604,000 new cases in 2020, esophageal cancer is the eighth most common type of cancer, with 544,000 deaths per year reported worldwide (1). Radical esophagectomy with regional lymph node dissection is indispensable in the curative treatment of localized esophageal cancer (2,3). However, even after curative treatment, more than half of patients experience recurrence, and the prognosis is poor. In addition, complications after esophagectomy are sometimes fatal (4,5). Among postoperative complications, some studies have shown that the development of postoperative pneumonia increased the risk of recurrence and reduced overall survival in esophageal cancer (6,7). Therefore, it is important to predict the occurrence of postoperative complications, such as pneumonia, before surgery and to identify reliable predictive factors for patients.

In recent years, awareness of oral care has increased in medical and nursing care settings after reports of the preventive effects of oral care on aspiration pneumonia in elderly patients requiring nursing care. In patients with esophageal cancer, perioperative professional oral care was reported to decrease the incidence of pneumonia and reintubation rates, decrease wound suture failure, shorten ICU stay and time to oral intake, and even shorten hospital stay (8-10). In addition, professional oral care during radiotherapy for head and neck cancer has been reported to be useful in preventing or reducing complications, such as oral mucositis, improving the treatment completion rate, and maintaining patient quality of life (11). Based on these reports, oral care is now recognized as an important supportive therapy in cancer treatment. However, few methods are available for assessing the risk factors for postoperative pneumonia after esophagectomy (12-16). The Oral Health Assessment Tool (OHAT) was developed for use by nondental professionals, such as nurses, personal care attendants, and allied health or medical professionals. Despite the accumulating evidence regarding oral health and postoperative pneumonia, little information exists on the possible influence of oral health on cancer survival. The aim of this study was to determine whether the OHAT can be used to identify patient survival after esophagectomy for esophageal cancer.

Patients and Methods

Patient data. The inclusion criteria in this retrospective study of selected patients who underwent radical esophageal cancer resection at Yokohama City University between 2008 and 2021 were as follows: 1) histologically proven primary esophageal squamous cell carcinoma or adenocarcinoma, 2) clinical stage IB-III assessed using the Union for International Cancer Control (UICC) Tumor, Lymph node and Metastasis Classification, 7th Edition, and 3) complete resection of esophageal cancer (R0).

Surgical procedure. Subtotal esophagectomy via right thoracotomy and reconstruction with a gastric tube is the standard procedure. Two-field lymph node dissection was performed for middle to lower thoracic tumors, while three-field dissection was applied for upper tumors.

OHAT. The OHAT consists of eight items (‘lips’, ‘tongue’, ‘gums and mucosa’, ‘saliva’, ‘remaining teeth’, ‘dentures’, ‘oral cleaning’, and ‘toothache’) classified into three score levels (0: healthy, 1: somewhat poor, and 2: unhealthy) (17). Scores for each item have clearly defined observation criteria. In the case of a score of 1 or 2, it is recommended that the patient visit to a dental specialist, especially for the marked items. In this study, four items (gingiva and mucosa, remaining teeth, dentures, and oral cleaning) that could be determined form the retrospective clinical data of the subject patients were scored, and the total score (maximum of 8 points) was evaluated and studied (Table I).

Table I. Oral health assessment tool.

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Evaluations and statistical analyses. The significance of the difference between the OHAT score and clinicopathological findings was determined using the chi-squared test. Overall survival (OS) and recurrence-free survival (RFS) curves were generated by the Kaplan-Meier method. Univariate and multivariate analyses were performed using a Cox proportional hazards model. p-Values of <0.05 were considered to indicate statistical significance. The SPSS software program (v27.0 J Win; IBM SPSS, Armonk, NY, USA) was used for all statistical analyses. This study was approved by the Institutional Review Board of Yokohama City University.

Results

Patient characteristics. A total of 169 patients underwent esophagectomy for esophageal cancer between October 2008 and September 2021, and preoperatively, this study included 90 patients screened with the OHAT. The patients’ ages ranged from 43 to 81 years (median: 67 years); 69 patients were male, and 21 were female. The median follow-up period was 72.5 months (13.9-125.2 months). Patients were classified into the OHAT score ≤2 group (OHAT-low group), and 48 patients were classified into the OHAT score ≥3 group (OHAT-high group). The patient characteristics and factors related to the OHAT score are summarized in Table II. There were significant differences in the pathological T factor and lymph node dissection between the two groups. In the OHAT-high group, progress in the depth of invasion and three-field lymph node dissection were less frequent. In terms of smoking status, more patients in the OHAT-high group had a smoking habit, although this difference was not statistically significant (78.6% vs. 93.8%).

Table II. Comparison between oral health assessment tool (OHAT) score and clinicopathological factors.

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BMI: Body mass index; ASA-PS; American Society of Anesthesiologists Physical Status. Statistically significant p-values are shown in bold.

Short-term outcome. Table III summarizes the short-term outcomes of the two groups. Comparing the OHAT-high group and OHAT-low group, the length of hospital stay was significantly longer in the OHAT-high group, and more patients tended to receive postoperative tracheostomy, although this difference was not statistically significant (4.8% vs. 16.7%). Although the total incidence of postoperative complications did not differ between the two groups, the incidence of postoperative pneumonia was significantly higher in the OHAT-high group. The incidence of grade ≥3 severe pneumonia was also higher in the OHAT-high group, the difference was not statistically significant (11.9 vs. 18.8%).

Table III. Relationship between oral health assessment tool (OHAT) score and short-term outcomes.

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Statistically significant p-values are shown in bold.

Survival analyses. The OS rate at 5 years after surgery was 43.2% in the OHAT-high group and 71.2% in the OHAT-low group, which amounted to a significant difference (p=0.015). The OS curves are shown in Figure 1. Univariate analyses for OS showed that oral health status, as scored by the OHAT, was a significant prognostic factor, as were lymph node metastasis, tumor invasion, and pathological stage. The OHAT score and grade ≥3 postoperative pneumonia were selected for the final model to be analyzed by a multivariate analysis (Table IV).

Figure 1. Comparison of the overall survival of patients in the OHAT 0-2 and OHAT 3- groups.

Figure 1

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Table IV. Uni- and multivariate Cox proportional hazards analysis of clinicopathological factors for 5-year overall survival.

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ASA-PS: American Society of Anesthesiologists Physical Status; OHTA; Oral Health Assessment Tool. Statistically significant p-values are shown in bold.

The RFS curves are shown in Figure 2. The RFS rate at 5 years after surgery was 28.3% in the OHAT-high group and 39.8% in the OHAT-low group, which did not amount to a significant difference (p=0.245).

Figure 2. Comparison of the recurrence-free survival of patients in the OHAT 0-2 and OHAT 3- groups.

Figure 2

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Discussion

There have been several reports about the relationship between periodontitis and the clinical outcome in human cancers. Fusobacterium species, part of the normal flora in the human oral cavity, vagina, and gastrointestinal mucosa, are pathogens in periodontal diseases (17) and are associated with a poor prognosis in colorectal cancer (18,19) and pancreatic cancer (20). In esophageal cancer, Yamaura et al. reported that F. nucleatum in esophageal cancer tissues was associated with shorter survival, suggesting a potential role as a prognostic biomarker (21). Douglas et al. reported that the oral cleaning status and cancer prognosis are foundational to the prognosis of head and neck cancer (11). However, no report has shown a correlation between the oral cleaning status and the long-term prognosis of malignant diseases using a simple tool to assess the oral cleaning status. The present study explored whether the OHAT score is a risk factor for long-term survival after esophagectomy for esophageal cancer. We found a significant association with a strong correlation between poor oral health indicators and survival. This result led to three possible interpretations: 1) poor oral health directly affects cancer progression by affecting the development of the tumor or the associated host immune response, 2) oral health conditions are associated with postoperative aspiration pneumonia, or 3) oral health is a marker of overall wellness.

First, several mechanisms have previously been shown to underlie the influence of the oral hygiene status on morbidity and survival in malignant diseases. These include altered immune responses to tumors and changes in the local environment of the tumor. Periodontitis, resulting from poor oral hygiene and the associated inflammatory response (22), can affect the local inflammation and immune response of tumors (23-25). This demonstrates the importance of periodontal disease treatment (26). The association between intestinal bacteria and systemic health is closely related to the network of microbiota and immune responses, and disruption of immune homeostasis can have a major impact on various diseases, including cancer development (27-29). In fact, there are scattered reports that commensal bacteria, such as enterotoxigenic Bacteriodes fragiles, Peptostreptococcus anaerobius, and Escherichia coli are involved in the development of colon cancer (30-32).

Second, the association between the complication rate of postoperative pneumonia and the oral cleaning status may have influenced the prognosis. Postoperative pneumonia can lead to additional pain, prolonged hospital stays, and respiratory failure. These adverse events might lead to early recurrence and/or death. In a previous article showing a significant relationship between the OHAT score and pneumonia, Saensom et al. (33) prospectively evaluated the association between oral health score and ventilator-associated pneumonia (VAP) in 162 patients treated with ventilator management. The results showed that the OHAT score and plaque index were significantly correlated with the development of VAP in both univariate and multivariate analyses. This report also suggested that poor oral cleanliness, as measured by the OHAT score, proved to be a significant independent risk factor for the development of postoperative pneumonia in patients with primary esophageal cancer who underwent radical esophagectomy. In addition, a report presented the relationship between the occurrence of postoperative pneumonia and long-term survival in patients who underwent surgical treatment for esophageal cancer. Kataoka et al. (8) evaluated the impact of infectious complications such as postoperative pneumonia and suture failure on postoperative survival of clinical stage II/III esophageal cancer patients treated by preoperative chemotherapy using data from a randomized controlled trial (JCOG 9907). According to the study, postoperative pneumonia was observed in 30% of patients, and OS was significantly worse than that in patients without postoperative pneumonia (9).

Third, maintaining a good oral cleaning status may be a marker of good survival in all diseases. A retrospective cohort study of 31,694 elderly Japanese subjects examined the oral care status, along with age, sex, education level, smoking, alcohol consumption, and medical history, and found that tooth brushing and regular dental visits were associated with good survival (10). Several similar results regarding an association between tooth loss and total mortality have also been reported (34-37). As a mechanism, it has been suggested that the assessment of oral health, such as tooth loss, may reflect the nutritional status, smoking, cognitive decline, quality of life, and other quality of life issues (such as social isolation, disability, withdrawal, and neglect) that affect mortality (38). In all of these possibilities, the results of this study suggest that improved oral hygiene may contribute to the prognosis of esophageal cancer surgery cases.

The present study is associated with some potential limitations. First, it was a retrospective single-center study with a relatively small sample size, and a large-scale prospective validation study is needed. Second, there was a time bias in this study, and surgical procedures, postoperative chemotherapy, and perioperative care might have been confounding factors during this period. Finally, the analyses of all studies, including the present study, were limited to East Asian cohorts.

In conclusion, poor oral hygiene, as defined by the OHAT score, was a significant risk factor for OS in patients undergoing radical esophageal cancer surgery. The findings of the present study suggest the importance of preoperative oral assessment using the OHAT score and appropriate dental treatment to improve the condition of patients with esophageal cancer.

Conflicts of Interest

The Authors have no conflicts of interest to declare in relation to this study.

Authors’ Contributions

HT, AT, TA, and IH made substantial contributions to the concept and design. TA, YM, KH, AK, NK, KO, MN, KK, JM, MI, HC, SS, TO, and SO made substantial HT, AT, NY, KM, AS, YR and TA contributions to the acquisition of data and the analysis and interpretation of the data. HT, AT, and TA were involved in drafting the article or revising it critically for important intellectual content. HT, AT, and TA gave their final approval of the version to be published.

References

  • 1.Sung H, Ferlay J, Siegel R, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/CAAC.21660. [DOI] [PubMed] [Google Scholar]
  • 2.Lordick F, Mariette C, Haustermans K, Obermannová R, Arnold D, on behalf of the ESMO Guidelines Committee Esophageal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27:v50–v57. doi: 10.1093/ANNONC/MDW329. [DOI] [PubMed] [Google Scholar]
  • 3.Mayanagi S, Irino T, Kawakubo H, Kitagawa Y. Neoadjuvant treatment strategy for locally advanced thoracic esophageal cancer. Ann Gastroenterol Surg. 2019;3(3):269–275. doi: 10.1002/AGS3.12243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Fransen L, Luyer M. Effects of improving outcomes after esophagectomy on the short- and long-term: a review of literature. J Thorac Dis. 2019;11(S5):S845–S850. doi: 10.21037/JTD.2018.12.09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Mantziari S, Hübner M, Demartines N, Schäfer M. Impact of preoperative risk factors on morbidity after esophagectomy: is there room for improvement. World J Surg. 2014;38(11):2882–2890. doi: 10.1007/S00268-014-2686-9. [DOI] [PubMed] [Google Scholar]
  • 6.Tamagawa A, Aoyama T, Tamagawa H, Ju M, Komori K, Maezawa Y, Kano K, Kazama K, Murakawa M, Atsumi Y, Sawazaki S, Hara K, Numata M, Sato T, Yukawa N, Masuda M, Rino Y. Influence of postoperative pneumonia on esophageal cancer survival and recurrence. Anticancer Res. 2019;39(5):2671–2678. doi: 10.21873/ANTICANRES.13392. [DOI] [PubMed] [Google Scholar]
  • 7.Kataoka K, Takeuchi H, Mizusawa J, Igaki H, Ozawa S, Abe T, Nakamura K, Kato K, Ando N, Kitagawa Y. Prognostic impact of postoperative morbidity after esophagectomy for esophageal cancer. Ann Surg. 2017;265(6):1152–1157. doi: 10.1097/SLA.0000000000001828. [DOI] [PubMed] [Google Scholar]
  • 8.Kataoka K, Takeuchi H, Mizusawa J, Igaki H, Ozawa S, Abe T, Nakamura K, Kato K, Ando N, Kitagawa Y. Prognostic impact of postoperative morbidity after esophagectomy for esophageal cancer. Ann Surg. 2017;265(6):1152–1157. doi: 10.1097/SLA.0000000000001828. [DOI] [PubMed] [Google Scholar]
  • 9.Tamagawa A, Aoyama T, Tamagawa H, Ju M, Komori K, Maezawa Y, Kano K, Kazama K, Murakawa M, Atsumi Y, Sawazaki S, Hara K, Numata M, Sato T, Yukawa N, Masuda M, Rino Y. Influence of postoperative pneumonia on esophageal cancer survival and recurrence. Anticancer Res. 2019;39(5):2671–2678. doi: 10.21873/ANTICANRES.13392. [DOI] [PubMed] [Google Scholar]
  • 10.Hayasaka K, Tomata Y, Aida J, Watanabe T, Kakizaki M, Tsuji I. Tooth loss and mortality in elderly Japanese adults: effect of oral care. J Am Geriatr Soc. 2013;61(5):815–820. doi: 10.1111/jgs.12225. [DOI] [PubMed] [Google Scholar]
  • 11.Farquhar D, Divaris K, Mazul A, Weissler M, Zevallos J, Olshan A. Poor oral health affects survival in head and neck cancer. Oral Oncol. 2017;73:111–117. doi: 10.1016/J.ORALONCOLOGY.2017.08.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Zingg U, Smithers B, Gotley D, Smith G, Aly A, Clough A, Esterman A, Jamieson G, Watson D. Factors associated with postoperative pulmonary morbidity after esophagectomy for cancer. Ann Surg Oncol. 2011;18(5):1460–1468. doi: 10.1245/S10434-010-1474-5. [DOI] [PubMed] [Google Scholar]
  • 13.Blencowe N, Strong S, McNair A, Brookes S, Crosby T, Griffin S, Blazeby J. Reporting of short-term clinical outcomes after esophagectomy. Ann Surg. 2012;255(4):658–666. doi: 10.1097/SLA.0B013E3182480A6A. [DOI] [PubMed] [Google Scholar]
  • 14.Atkins BZ, D’Amico TA. Respiratory complications after esophagectomy. Thorac Surg Clin. 2006;16:35–48. doi: 10.1016/J.THORSURG.2006.01.007. [DOI] [PubMed] [Google Scholar]
  • 15.Ferguson M, Celauro A, Prachand V. Prediction of major pulmonary complications after esophagectomy. Ann Thorac Surg. 2011;91(5):1494–1501. doi: 10.1016/J.ATHORACSUR.2010.12.036. [DOI] [PubMed] [Google Scholar]
  • 16.Reinersman J, Allen M, Deschamps C, Ferguson M, Nichols F, Shen K, Wigle D, Cassivi S. External validation of the Ferguson pulmonary risk score for predicting major pulmonary complications after oesophagectomy. Eur J Cardiothorac Surg. 2016;49(1):333–338. doi: 10.1093/EJCTS/EZV021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Griffen A, Beall C, Campbell J, Firestone N, Kumar P, Yang Z, Podar M, Leys E. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 2012;6(6):1176–1185. doi: 10.1038/ISMEJ.2011.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, Bruha J, Neary P, Dezeeuw N, Tommasino M, Jenab M, Prehn J, Hughes D. Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis. 2014;33(8):1381–1390. doi: 10.1007/S10096-014-2081-3. [DOI] [PubMed] [Google Scholar]
  • 19.Mima K, Nishihara R, Qian Z, Cao Y, Sukawa Y, Nowak J, Yang J, Dou R, Masugi Y, Song M, Kostic A, Giannakis M, Bullman S, Milner D, Baba H, Giovannucci E, Garraway L, Freeman G, Dranoff G, Garrett W, Huttenhower C, Meyerson M, Meyerhardt J, Chan A, Fuchs C, Ogino S. Fusobacterium nucleatumin colorectal carcinoma tissue and patient prognosis. Gut. 2016;65(12):1973–1980. doi: 10.1136/GUTJNL-2015-310101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Mitsuhashi K, Nosho K, Sukawa Y, Matsunaga Y, Ito M, Kurihara H, Kanno S, Igarashi H, Naito T, Adachi Y, Tachibana M, Tanuma T, Maguchi H, Shinohara T, Hasegawa T, Imamura M, Kimura Y, Hirata K, Maruyama R, Suzuki H, Imai K, Yamamoto H, Shinomura Y. Association of Fusobacterium species in pancreatic cancer tissues with molecular features and prognosis. Oncotarget. 2015;6(9):7209–7220. doi: 10.18632/ONCOTARGET.3109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Yamamura K, Baba Y, Nakagawa S, Mima K, Miyake K, Nakamura K, Sawayama H, Kinoshita K, Ishimoto T, Iwatsuki M, Sakamoto Y, Yamashita Y, Yoshida N, Watanabe M, Baba H. Human microbiome Fusobacterium Nucleatum in esophageal cancer tissue is associated with prognosis. Clin Cancer Res. 2016;22(22):5574–5581. doi: 10.1158/1078-0432.CCR-16-1786. [DOI] [PubMed] [Google Scholar]
  • 22.Pihlstrom B, Michalowicz B, Johnson N. Periodontal diseases. Lancet. 2005;366(9499):1809–1820. doi: 10.1016/S0140-6736(05)67728-8. [DOI] [PubMed] [Google Scholar]
  • 23.You Z, Cushman M, Jenny N, Howard G. Tooth loss, systemic inflammation, and prevalent stroke among participants in the reasons for geographic and racial difference in stroke (REGARDS) study. Atherosclerosis. 2009;203(2):615–619. doi: 10.1016/J.ATHEROSCLEROSIS.2008.07.037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Loos B. Systemic markers of inflammation in periodontitis. J Periodontol. 2005;76(11-s):2106–2115. doi: 10.1902/JOP.2005.76.11-S.2106. [DOI] [PubMed] [Google Scholar]
  • 25.Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44. doi: 10.1038/NRI3785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Tonetti M, D’Aiuto F, Nibali L, Donald A, Storry C, Parkar M, Suvan J, Hingorani A, Vallance P, Deanfield J. Treatment of periodontitis and endothelial function. N Engl J Med. 2007;356(9):911–920. doi: 10.1056/nejmoa063186. [DOI] [PubMed] [Google Scholar]
  • 27.Blumberg R, Powrie F. Microbiota, disease, and back to health: a metastable journey. Sci Transl Med. 2012;4(137):137rv7. doi: 10.1126/SCITRANSLMED.3004184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Erdman S, Poutahidis T. Gut bacteria and cancer. Biochim Biophys Acta. 2015;1856(1):86–90. doi: 10.1016/J.BBCAN.2015.05.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Erdman S, Rao V, Olipitz W, Taylor C, Jackson E, Levkovich T, Lee C, Horwitz B, Fox J, Ge Z, Poutahidis T. Unifying roles for regulatory T cells and inflammation in cancer. Int J Cancer. 2010;126(7):1651–65. doi: 10.1002/IJC.24923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Tsoi H, Chu E, Zhang X, Sheng J, Nakatsu G, Ng S, Chan A, Chan F, Sung J, Yu J. Peptostreptococcus anaerobius induces intracellular cholesterol biosynthesis in colon cells to induce proliferation and causes dysplasia in mice. Gastroenterology. 2017;152(6):1419–1433.e5. doi: 10.1053/J.GASTRO.2017.01.009. [DOI] [PubMed] [Google Scholar]
  • 31.Thiele Orberg E, Fan H, Tam A, Dejea C, Destefano Shields C, Wu S, Chung L, Finard B, Wu X, Fathi P, Ganguly S, Fu J, Pardoll D, Sears C, Housseau F. The myeloid immune signature of enterotoxigenic Bacteroides fragilis-induced murine colon tumorigenesis. Mucosal Immunol. 2017;10(2):421–433. doi: 10.1038/MI.2016.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Zhang S, Fu J, Dogan B, Scherl E, Simpson K. 5-Aminosalicylic acid downregulates the growth and virulence of Escherichia coli associated with IBD and colorectal cancer, and upregulates host anti-inflammatory activity. J Antibiot (Tokyo) 2018;71(11):950–961. doi: 10.1038/S41429-018-0081-8. [DOI] [PubMed] [Google Scholar]
  • 33.Saensom D, Merchant A, Wara-Aswapati N, Ruaisungnoen W, Pitiphat W. Oral health and ventilator-associated pneumonia among critically ill patients: a prospective study. Oral Dis. 2016;22(7):709–714. doi: 10.1111/ODI.12535. [DOI] [PubMed] [Google Scholar]
  • 34.Adolph M, Darnaud C, Thomas F, Pannier B, Danchin N, Batty G, Bouchard P. Oral health in relation to all-cause mortality: the IPC cohort study. Sci Rep. 2017;7(1):44604. doi: 10.1038/SREP44604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Tu Y, Galobardes B, Smith G, McCarron P, Jeffreys M, Gilthorpe M. Associations between tooth loss and mortality patterns in the Glasgow Alumni Cohort. Heart. 2007;93(9):1098–1103. doi: 10.1136/HRT.2006.097410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Hu H, Lee Y, Lin S, Chou Y, Chung D, Huang N, Chou Y, Wu C. Association between tooth loss, body mass index, and all-cause mortality among elderly patients in Taiwan. Medicine (Baltimore) 2015;94(39):e1543. doi: 10.1097/MD.0000000000001543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Holm-Pedersen P, Schultz-Larsen K, Christiansen N, Avlund K. Tooth loss and subsequent disability and mortality in old age. J Am Geriatr Soc. 2008;56(3):429–435. doi: 10.1111/J.1532-5415.2007.01602.X. [DOI] [PubMed] [Google Scholar]
  • 38.Friedman P, Lamster I. Tooth loss as a predictor of shortened longevity: exploring the hypothesis. Periodontol 2000. 2016;72(1):142–152. doi: 10.1111/PRD.12128. [DOI] [PubMed] [Google Scholar]

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