Impact of occlusal support on postoperative complications in patients with colorectal cancer resections

Introduction

A reduction in the number of remaining teeth in frail patients contributes to a series of processes that deteriorate oral functions, including masticatory disorders, frailty, and a decline in physical and mental functions (1). Patients with masticatory disorders tend to consume fewer side dishes, which are more challenging to chew than main meals, resulting in nutritional deficiencies, particularly inadequate protein intake (2). However, this condition is reversible (1), as dietary counseling and cooking guidance from a dietitian can address protein intake deficiencies by adapting meals to the patient’s chewing ability alongside timely dental treatment (2,3).

In cases of masticatory dysfunction, the loss of the periodontal ligament significantly decreases grip strength, leg extension ability, and total body muscle mass, common issues among older individuals living alone (4). Additionally, many older patients without family support struggle to implement the cooking methods provided by dietitians.

Meanwhile, in patients undergoing surgery for gastrointestinal cancer, a preoperative reduction of the number of remaining teeth can lead to postoperative complications, resulting in longer hospital stays and higher medical costs (5,6). In addition, some evidence suggests that a decrease in molar occlusal surface area has a greater impact on medical costs than a reduction in the number of remaining teeth (6).

Infectious complications are more common in colorectal cancer than in other gastrointestinal cancers, and it is especially important to consider risk factors because of their prognostic impact (7). Since the postoperative course of gastrointestinal cancer varies by organ, it is also important to identify organ-specific risk factors.

In this study, we aimed to investigate the relationship between occlusal support range, dietary habits during hospitalization and postoperative outcomes in subjects aged 65 years and older, in line with previous studies on oral status (8), and to determine whether reduced occlusal support range is a factor influencing postoperative infectious complications. We present this article in accordance with the STROBE reporting checklist (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2024-1013/rc).

Methods

Patients

This retrospective case control study enrolled 179 older patients aged ≥65 years diagnosed with colorectal cancer who underwent colorectal surgery at Tokyo Women’s Medical University Adachi Medical Center between January 2017 and December 2021. The exclusion criteria were: (I) patients who underwent emergency surgery, and (II) those with incomplete data. Of these 179 patients, 10 patients who underwent emergency surgery were excluded due to insufficient data, leaving 169 patients (102 men and 67 women) for analysis. Table 1 presents a summary of the demographic and clinical characteristics of the patients. This study was conducted in compliance with the principles of the Declaration of Helsinki and its subsequent amendments, also the ethical guidelines of Tokyo Women’s Medical University. The Ethics Committee of Tokyo Women’s Medical University approved the study protocol before the collection and analysis of patient data (approval No. 4150). The requirement for informed consent was waived due to the retrospective nature, and a notice on a website gave patients the option to opt out of the study at any time.

Parameters of oral conditions

A dentist evaluated each patient’s teeth and jawbone through oral cavity examination and panoramic radiographs of the whole jaw before surgery. The number of functioning teeth was defined as the number of present teeth, excluding third molars and teeth with retained roots due to advanced caries. Occlusal support was classified according to the Eichner index (EI) into three groups: Group A, for patients with all four occlusal support zones in the upper and lower jaws, including the left and right molar and premolar regions; Group B, for patients with one to three occlusal support areas in the premolars, molars, or anterior teeth; and Group C, for patients with no occlusal support in either jaw.

The timing of dental visit was decided by the surgeon’s judgement and the patient’s agreement after the patient had consented to the surgery, but in many cases, they were carried out within a month of the date of admission. Perioperative oral management before cancer surgery has been included in the Japanese health insurance system since 2012 to reduce postoperative complications. At our hospital, we dentists examine and take panoramic radiographs of all colon cancer patients undergoing surgery except for emergency surgery patients. The dentist and dental hygienist performed mechanical tooth cleaning and dental calculus removal, and preoperatively extracted teeth that could not be saved and temporarily fixed loose teeth, creating an oral environment that facilitates perioperative oral care.

Parameters of patient characteristics

We analyzed clinicopathological factors associated with EI, including: sex (male/female), age (≥80/<80 years), living with someone (yes/no), performance status (0/1), diabetes mellitus (yes/no), heart disease (yes/no), pulmonary dysfunction (yes/no), body mass index (BMI) (≥25.0/<25.0 kg/m²), modified Glasgow prognostic score (mGPS) (score 0,1/score 2) (9), prognostic nutrition index (PNI) (>40/ ≤40) (10), psoas muscle index (PMI) (cm²/m²) (low/high) (11), location (colon/rectum), approach (laparotomy/laparoscopy), stage (I–III/IV), Lymph node metastasis (N0/≥N1), depth of tumor invasion (≥T3/<T3), blood loss (≥107/<107 mL), operation time (≥263/<263 min), and colostomy (yes/no).

Height and weight were measured, and BMI was calculated by nurses on admission, the day before surgery, and at discharge. Median blood loss was 125 (range, 0–1,147) mL, with a cut-off value of 107 mL at the 75th percentile. Median operative time was 203 (range, 112–566) min, with a 75th percentile cutoff of 263 min. Pulmonary dysfunction was defined as having less than 80% percent vital capacity (%VC) or less than 70% of forced expiratory volume in one second (FEV1.0%).

Blood samples were collected at admission. mGPS was scored as follows: score 2, CRP >1.0 mg/dL and albumin <3.5 g/dL; score 1, CRP>1.0 mg/dL; and score 0, CRP ≤1.0 mg/dL and albumin ≥3.5 g/dL (9). PNI was calculated using the following formula: serum albumin level (g/dL) ×10+total lymphocyte count (per mm³) × 0.005 (10). The PMI cutoff values for sarcopenia were 6.36 cm²/m² for men and 3.92 cm²/m² for women (11).

Assessment of diet form in the hospital and at home

The dietitian, speech-language-hearing therapist, and nurse worked together to determine the diet based on the EI and advised the attending physician on the day of admission for all patients. The dietitian interviewed each patient and their family to record dietary patterns at home, including main meal type (porridge/rice) and side dish type (chopped/not chopped). The dietitian also provided dietary counseling based on the patient’s EI classification. During hospitalization, the dietitian, speech-language pathologist, and nurses confirmed the patients’ dietary patterns. Side dishes that were below 3 cm in length were defined as “chopped”.

Postoperative complications

A team of doctors conducted postoperative surveillance. Complications classified as Grade II or higher, according to the Clavien-Dindo classification, were included in the analysis of incidence rates. Surgical site infections (SSI) were diagnosed following the National Nosocomial Infection Surveillance (NNIS) System standards, as outlined by the Centers for Disease Control and Prevention.

The surgeons examined the wound sites daily and documented their findings in the patients’ medical records. Computed tomography (CT) scans were used to diagnose anastomotic leakage. A group of doctors monitored the patients until 30 days after surgery. The data were then reviewed and summarised by the authors.

Assessment of nutritional adequacy after surgery

Nutritional intake was calculated as the protein intake (g/kg) and nutrient sufficiency ratio (%) in relation to the energy requirement (kcal) for each main meal and side dish after the completion of intravenous infusion. The daily energy requirement (kcal/day) was defined as ideal body weight (kg) × 30 kcal. The nutrient sufficiency ratio (%) was calculated based on dietary intake from the end of infusion to discharge, using the departmental standard for postoperative colon cancer patients (soft vegetarian diet), with 48.9% of the energy derived from main meals and 51.1% from side dishes. The following equations were used to calculate the energy sufficiency ratios.

Staple food nutrient sufficiency ratio: main food energy intake (kcal/day)/[energy requirement (kcal/day) × 0.489] × 100%

Nutrient sufficiency ratio of side dishes: energy intake of side dishes (kcal/day)/[energy requirement (kcal/day) × 0.511] × 100%

Parameters of postoperative outcome

The following postoperative outcomes were assessed: the day diet was initiated, the day of intravenous infusion completion, the number of days after infusion completion, length of postoperative hospital stay (days), postoperative weight loss (%), incidence of all postoperative complications, incidence of postoperative infectious complications, and incidence of SSI. Postoperative weight loss was calculated as (discharge weight − preoperative weight)/preoperative weight × 100%.

Predictive factors for postoperative infectious complications

The following factors were selected as adjustment factors to determine whether EI (A/B), EI (A/C), and EI (B/C) were factors influencing postoperative infectious complications: sex (male/female), age (≥80/<80 years), performance status (0/1), diabetes mellitus (yes/no), heart disease (yes/no), pulmonary dysfunction (yes/no), BMI (≥25.0/<25.0), mGPS (score 0,1/score 2), PNI (>40/≤40), PMI (cm²/m²) (low/high), location (colon/rectum), approach (laparotomy/laparoscopy), stage (I–III/IV), lymph node metastasis (N0/≥N1), depth of tumor invasion (≥T3/<T3), blood loss (≥107/<107 mL), operation time (≥263/<263 min), and colostomy (yes/no).

The preoperative preparation methods

The preoperative preparation methods were taking 2,000 mL of Niflec@ on the day before surgery for rectum cancer patients and taking 100 g of Magcorol P@ on the day before surgery for colon cancer patients.

The method of wound closure

The method of wound closure for all of the patients was same technique we performed wound lavage with physiological saline through syringe pressure and applied the see-through film dressing with absorbent pad cut into mesh shape.

Statistical analysis

Statistical analyses were performed using JMP®15 software (SAS Institute Inc., Cary, NC, USA). Fisher’s exact test was used to analyze patient characteristics by EI category (A, B, and C). The Kruskal-Wallis test was applied to compare the number of teeth and postoperative outcomes across EI classifications, and the Steel-Dwass test was applied if significant differences were found. We used Bowker’s test to assess changes in dietary patterns from home to hospital. Fisher’s exact test was used to compare the incidence of postoperative complications by EI category, and the Cochran-Armitage trend test was applied when significant differences were observed. Logistic regression analysis was used to evaluate the relationship between EI and postoperative infectious complications. Statistical significance was set at P<0.05 for all tests.

Results

Demographic and clinical characteristics of patients by EI (Table 2)

According to the Eichner classification, there were 57, 55, and 57 patients in groups A, B, and C, respectively. The number of teeth decreased as the EI classification declined. In total, 9 patients (15.8%) in group A, 15 patients (27.3%) in group B, and 31 patients (54.4%) in group C had not worn dentures, despite the dentist’s recommendation. However, no significant differences were found regarding diabetes mellitus, pulmonary dysfunction, BMI, cancer location, surgical approach, stage, lymph node metastasis, tumor depth of tumor invasion, blood loss, or operating time across the EI groups. Significant differences were observed among the three groups in these variables, including sex, age, cohabitation status, performance status, heart disease, mGPS, PNI, PMI, colostomy, number of teeth, and denture use.

Dietary patterns in the hospital compared to the home according to EI classification (Table 3)

No patients in group A and only 3 patients (5.5%) in group B consumed porridge at home. There was no significant change in hospital, with only 1 patient (1.8%) in group A and 5 patients (9.1%) in group B consuming porridge as their main meal. However, in group C the number of patients consuming porridge increased significantly from 7 (12.3%) at home to 31 (54.4%) in the hospital (P<0.05). The number of patients consuming chopped side dishes also significantly increased across all groups during hospitalization. In group A, 14 patients (24.6%) consumed chopped side dishes in the hospital, compared to just 1 patient (1.8%) at home. In group B, the number increased from 2 patients (3.6%) at home to 17 patients (30.9%) in the hospital, and in group C, it increased from 19 patients (33.3%) at home to 49 patients (86.0%) in the hospital (P<0.05).

Association of EI with surgery-related factors (Table 4)

Postoperative dietary nutrient sufficiency rates for staple meals in groups A, B, and C were 41.4% (14.4–63.1%), 37.2% (14.6–58.5%), and 36.0% (8.6–63.2%), respectively. For main meals, the rates were 50.7% (17.6–83.8%), 48.0% (24.4–71.5%), and 47.6% (10.5–77.2%). There were no significant differences in these values between groups. Protein intake per body weight was 1.1 g (0.4–1.7 g) in group A, 1.0 g (0.5–1.5 g) in group B, and 1.0 g (0.5–1.5 g) in group C, without significant differences. The median time to initiate a postoperative diet was 4 days (4–9 days) in group A, 4 days (4–25 days) in group B, and 5 days (4–11 days) in group C. The median time to complete infusion was 6 days (6–20 days) in group A, 6 days (6–25 days) in group B, and 15 days (6–130 days) in group C, with significant differences (P<0.001). The median duration of hospital stay following infusion was 6 days (2–15 days) in group A, 7 days (3–14 days) in group B, and 8 days (4–38 days) in group C (P<0.01). The total postoperative hospital stay was significantly prolonged as occlusal support decreased: 11 days (7–22 days) in group A, 13 days (8–32 days) in group B, and 25 days (9–139 days) in group C (P<0.01). Postoperative weight loss was 3.1% (+3.6% to 6.6%), 3.8% (+1.4% to 8.8%), and 5.4% (0 to 9.8%) in groups A, B, and C, respectively, with weight loss significantly increasing as occlusal support decreased (P<0.01). Postoperative complications included 30 total complications, 19 infectious complications, 16 cases of SSI, 4 pulmonary complications, 4 urinary tract infections, 2 cases of enteritis, 1 drain infection, 1 retrograde drain infection, 1 catheter infection, 1 case of atelectasis, 7 cases of ileus, and 3 cases of delirium (Table 5).

The incidence of total postoperative complications was 1 patient (1.8%) in group A, 9 patients (16.4%) in group B, and 20 patients (35.1%) in group C. Infectious complications occurred in 1 patient (1.8%) in group A, 3 patients (5.5%) in group B, and 15 patients (26.3%) in group C. SSIs occurred in 1 patient (1.8%) in group A, 4 patients (7.3%) in group B, and 14 patients (24.6%) in group C. All complications, including infectious complications and SSIs, were significantly associated with the EI classification (P<0.01).

Impact of EI on the development of postoperative infectious complications (Table 6)

Univariate analysis revealed significant relationships between postoperative infectious complications and EI (A/C) and EI (B/C), with odds ratios (ORs) of 20.0 [95% confidence interval (CI): 3.82–368.63] and 6.19 (95% CI: 1.89–28.01), respectively. Other significant factors included mGPS OR 8.32 (95% CI: 3.03–25.34), PNI OR 5.77 (95% CI: 2.08–18.70), PMI OR 14.92 (95% CI: 2.96–271.84), Stage OR 3.87 (1.22–11.33), Lymph node metastasis OR 2.99 (95% CI: 1.12–8.91), blood loss OR 6.56 (95% CI: 2.43–18.52), and colostomy OR 5.31 (95% CI: 1.63–16.26). Multivariate analysis of these factors showed EI (A/C) OR of 13.05 (95% CI: 1.18–143.86), EI (B/C) OR 9.86 (95% CI: 1.55–62.94), mGPS OR 4.50 (95% CI: 1.05–19.28), and blood loss OR 6.38 (95% CI: 1.58–25.81) as independent predictors of postoperative infectious complications.

Discussion

In the present study, providing a diet tailored to patients with reduced occlusal support maintained their postoperative nutritional intake at levels comparable to those with good occlusal support. However, the postoperative recovery was poorer in patients with preoperatively reduced occlusal support, suggesting that EI may serve as a predictor of postoperative infectious complications.

Chewing ability declines if the occlusal support area is reduced, particularly when fewer bicuspids and molars remain. This is regardless of the relative total number of teeth (2-4). Prior research has linked occlusal support in molars to several factors, including the number of remaining teeth (3), glucose release (3), self-rated masticatory ability (4), and maximum occlusal force (3). The EI, used in this study, is a common measure for evaluating occlusal support in molars by assessing the contact between opposing teeth across four areas: the left and right molars and left and right bicuspids (3,4,12).

Patients aged 65 and older who underwent surgery for colorectal cancer were classified almost equally into three groups based on EI. A previous study in institutions with older patients showed that group A constituted approximately one-fifth of groups B and C (3). However, because the present study included older patients fit enough to undergo surgery, the proportion of patients in group A was relatively higher.

In addition, the fact that more than half of the patients in group C did not have dentures may indicate an association between low occlusal support and living alone. We also hypothesize that patients with gastrointestinal cancer often lose weight between cancer diagnosis and surgery, which often makes it difficult for them to fit dentures.

We also compared the types of meals consumed at home and in the hospital based on EI classification. In groups A and B, most patients chose rice as their staple food, both at home and in the hospital. However, in group C, porridge—a softer, more chewable option—was more frequently chosen in the hospital. This highlights the need for nutritional counseling on how patients can easily prepare porridge at home and how to use porridge delivery services. Regarding side dishes, all groups chose more appropriate meal forms in the hospital compared to home. Modifying meal forms for institutionalized older patients can improve protein intake (13), serum albumin levels (14), and body weight (15). In the present study, the provision of meals tailored to occlusal support likely contributed to the similar nutritional intake observed across all groups, regardless of occlusal function. Ensuring adequate nutrition during hospitalisation is critical, as inadequate nutrition during hospitalisation can affect a patient’s health for up to a year after surgery. Multidisciplinary efforts should be made to ensure that patients receive appropriate side dishes and adequate protein (13-15).

Despite this, patients with poor occlusal support experienced poorer postoperative outcomes. No prior studies have explored the association between reduced preoperative occlusal support and postoperative complications in patients with gastrointestinal cancer. Saito et al. (5) found that older gastrointestinal cancer patients with fewer remaining teeth had poor oral hygiene preoperatively, which deteriorated postoperatively, leading to reduced oral intake due to impaired chewing and swallowing. The presence of complications also prolonged hospital stays and increased medical costs. Previous studies (2,13) have stated that patients with a poor oral status have an increased frequency of missed meals, a decreased total energy intake, a loss of diversity in dietary intake, a decreased intake of meat and seafood as protein sources, and low preoperative serum albumin levels and PNI values (16). Because it takes a long time for the occlusal support area to decrease, it is likely that those patients were malnourished before their cancer diagnosis, which contributed to their poorer postoperative outcomes.

Finally, the relationship between EI and the development of postoperative infectious complications was examined, identifying EI (A/C, B/C) as a predictive factor. A significant cause of reduced occlusal surface area is the deterioration of oral health due to periodontal disease, which has been associated with the development of postoperative infectious complications (17). Enterococcus faecalis, the most common pathogen in SSI and a frequent cause of infectious complications in colorectal cancer, is also commonly found in the oral cavities of patients with refractory periodontitis or infected root canals (18).

Other organisms associated with SSI, such as Pseudomonas aeruginosa, Escherichia coli, Staphylococcus aureus, and Candida albicans, are opportunistic pathogens that are often present in the oral cavities of patients with chronic periodontal inflammation (19). It has been suggested that endotoxins, inflammatory cytokines, and other chemical mediators can be transferred from oral biofilms into the bloodstream, impacting the entire body (17). This transfer can occur through several mechanisms: (I) direct migration to the trachea and gastrointestinal tract, (II) hematogenous and lymphatic migration from local areas, and (III) systemic circulation of endotoxins and inflammatory cytokines affecting distant organs, (IV) changes in intestinal flora and compromised intestinal barrier function following ingestion of pathogenic oral bacteria (17). Therefore, we hypothesized that postoperative infectious complications would be more prevalent in patients with poor EI.

Oral frailty is defined as “a set of phenomena in which various oral conditions (e.g., number of teeth, oral hygiene, and oral function) deteriorate with age, along with reduced interest in oral health and physical and mental resilience. Poor oral health has also been reported to increase mortality in cancer patients (20). This leads to increased vulnerability of the oral cavity, eating dysfunction, and ultimately physical and mental decline contributing to frailty” (1). However, this process is reversible (1).

The oral cavity plays a critical role in nutrient intake, and there is a well-established link between oral problems causing malnutrition and malnutrition exacerbating oral problems. During the perioperative period of gastrointestinal cancer, oral health is a crucial factor, as it not only influences the quantity of nutrition intake but also contributes to gastrointestinal symptoms due to inadequate mastication. To ensure sufficient nutritional intake during the perioperative period and reduce the risk of undernutrition, ongoing nutritional assessments and counseling, combined with dental care, should begin from the first outpatient visit. However, many patients with declining EI live alone and may struggle to prepare meals without assistance. Therefore, medical nutrition therapy should take this into account and address these issues.

The limitations of this study are as follows: First, it was a retrospective study conducted at a single institution. Second, no comparison could be made with patients whose dietitian did not determine the diet form based on the EI classification. Third, the presence or absence of dentures could not be accounted for in this assessment, as many patients did not wear dentures before surgery due to improper fit. Previous research has shown that absolute chewing ability declines and may not improve even with dentures (3,6,21). Furthermore, once denture use is interrupted, it may become a permanent pattern of non-use (19). In the future, dentists should adjust dentures at the time of cancer diagnosis. Fourth, this study could not evaluate the relationship between postoperative infectious complications and the presence of periodontal disease or the effectiveness of oral care interventions. Previous studies suggest that these may have a significant impact on postoperative infectious complications in colorectal cancer (22). CDC guidelines for SSI prevention indicate that preoperative infectious lesions in distant sites are a risk factor for SSI and that these lesions should be treated preoperatively (23). The most effective interventions should be evaluated in future randomized controlled trials.

Conclusions

The postoperative nutritional intake of patients with reduced occlusal support was comparable to that of patients with good occlusal support when an appropriate diet was provided. However, the postoperative course was poor in patients with preoperative reduced occlusal support, suggesting that EI may be an indicator of postoperative infectious complications in colorectal cancer surgery patients aged 65 and older.

Acknowledgments

We would like to express our heartfelt gratitude to Dr. Hiroshi Fukuda, Dr. Miyuki Furuya, Dr. Gen Kato from the clinical epidemiology seminar at Juntendo University for their guidance on the significance of the Eichner index at the commencement of this study. Their expertise, which greatly contributed to the improvement of this paper, was indispensable for its completion.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2024-1013/rc

Data Sharing Statement: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2024-1013/dss

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2024-1013/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2024-1013/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in compliance with the principles of the Declaration of Helsinki and its subsequent amendments, also the ethical guidelines of Tokyo Women’s Medical University. The Ethics Committee of Tokyo Women’s Medical University approved the study protocol before the collection and analysis of patient data (approval No. 4150). The requirement for informed consent was waived due to the retrospective nature, and a notice on a website gave patients the option to opt out of the study at any time.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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