Risk factors analysis for percutaneous endoscopic gastrostomy in patients with oral cancer: a retrospective study

Introduction

Oral cancer refers to malignant tumors occurring in the oral cavity and adjacent anatomical structures, accounting for approximately 2.9% of all malignant tumors. It includes various types such as lip cancer, oral pharyngeal cancer, cheek cancer, gingival cancer, tongue cancer, and floor of mouth cancer (1). As a significant component of head and neck cancers, about 90% of oral cancer cases are squamous cell carcinoma (SCC) (2). In China, the incidence of oral cancer is approximately 3.35 per 100,000 individuals, with a mortality rate of 1.56 per 100,000 individuals, showing a noticeable upward trend (3).

Currently, the comprehensive treatment approach for oral cancer mainly involves surgery combined with radiotherapy and chemotherapy. However, surgical procedures and postoperative radiotherapy or chemotherapy often result in damage to the anatomical structures and functions of the maxillofacial region, leading to dysphagia in patients and increasing the risk of malnutrition, thereby affecting the effectiveness of tumor treatment and patient’s survival rates (4). Percutaneous endoscopic gastrostomy (PEG) has been proven effective in avoiding tissue damage in the surgical area, preventing aspiration pneumonia, and reducing the incidence of malnutrition (5-8). Previous studies have recommended PEG treatment for patients requiring long-term (over 1 month) enteral nutrition support (9,10). However, a study (11) has shown that some oral cancer patients who undergo PEG placement do not actually use the PEG tube for enteral nutrition during the postoperative treatment period, or the usage is inadequate. This situation exposes patients to unnecessary risks associated with PEG surgery and complications, leading to increased financial burdens. Therefore, further clarification of the specific indications for PEG treatment in postoperative oral cancer patients and refinement of the criteria for PEG placement are clinically necessary. This study aimed to analyze the relevant clinical characteristics of oral cancer surgical patients undergoing PEG through a case-control study, laying the foundation for elucidating the indications for PEG placement. We present this article in accordance with the STROBE reporting checklist (available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-1880/rc).

Methods

Study design

A retrospective analysis was conducted on the clinical data of oral cancer patients who underwent PEG at the Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine from July 2020 to June 2021. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (No. SH9H-2022-T337-2), and individual consent for this retrospective analysis was waived. Inclusion criteria were as follows: (I) oral cancer surgical patients who underwent PEG placement for the first time at the Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine. Histologically confirmed diagnosis of oral SCC; (II) age ≥18 years; and (III) consciousness without communication barriers. Exclusion criteria were: (I) patients who underwent organ transplantation or had concurrent malignancies in other sites; (II) oral cancer recurrence after treatment; (III) patients with oral cancer distant metastasis ineligible for surgery; (IV) patients unable to cooperate; and (V) severe chronic debilitating diseases such as severe heart, lung, liver, kidney diseases, or cachexia due to tumors.

Since PEG tubes were typically removed after at least 1 month post-procedure, patients with an actual duration of PEG tube usage exceeding 1 month were included in the case group, while patients with either no usage of the PEG tube or an actual usage duration equal to or less than 1 month were included in the control group. Clinical data of both groups were compared and analyzed.

For a detailed study design flow, refer to Figure 1. A total of 246 oral cancer patients who underwent PEG at the Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine from July 2020 to June 2021 were collected. Among them, 142 cases were excluded due to the exclusion criteria. Finally, 104 patients who underwent both oral cancer surgery and PEG placement were included in the study.

Figure 1 Flow chart of the study design. PEG, percutaneous endoscopic gastrostomy.

PEG procedure

The patient is positioned in the left lateral decubitus position. An electronic gastroscope (GIF-290; Olympus, Tokyo, Japan) is inserted orally through the pharynx into the esophagus. The stomach is adequately inflated with air, and the endoscope is positioned on the anterior wall of the middle and lower part of the stomach. After the patient is turned to a supine position, the brightest spot on the abdominal wall illuminated by the endoscope’s light source is selected. The operator applies pressure with their finger to ensure close contact between the gastric wall and the abdominal wall. Under endoscopic guidance, the puncture point with the best abdominal wall compression effect is selected. The skin at the intended puncture point is disinfected with iodine, and local anesthesia is administered with lidocaine injection. A PEG puncture kit (PEG-24-PULL-I-S; Cook Medical, Bloomington, IN, USA) is used. A surgical blade cuts the abdominal wall skin approximately 1 cm. Under the monitoring of the gastroscope, the puncture needle of the guiding sheath is inserted through the skin into the gastric cavity. The puncture needle is withdrawn, leaving the sheath in place. A guide wire is inserted into the sheath, and then a biopsy forceps channel of the endoscope is used to grasp the guide wire. With the endoscope withdrawn from the body, the gastrostomy tube is connected to the guide wire outside the body and pulled out through the puncture point on the abdominal wall. The gastrostomy tube is then externally fixed and tightened, completing the gastrostomy. Refer to Figure 2 for specific details of the procedure.

Figure 2 PEG procedure. (A) Under the monitoring of the gastroscope, the puncture needle of the guiding sheath is inserted into the gastric cavity. (B) The puncture needle is withdrawn, leaving the sheath and a guide wire is inserted into the sheath. Then a biopsy forceps channel of the endoscope is used to grasp the guide wire. (C) The gastrostomy tube is connected to the guide wire outside the body and pulled out through the puncture point on the abdominal wall. (D) The gastrostomy tube is externally fixed and tightened. PEG, percutaneous endoscopic gastrostomy.

Clinical data collection

Clinical data of patients were retrieved and recorded from the outpatient and inpatient electronic medical record systems. Registration information was cross-checked for accuracy. The collected registration information mainly included: (I) general patient information: age, gender, contact information, smoking history, alcohol consumption history, history of hypertension, history of diabetes; (II) oral cancer data: location of oral cancer, whether neoadjuvant chemotherapy was performed, surgical procedures (including whether tracheostomy, neck lymph node dissection, reconstructive surgery, tongue/pharyngeal resection, and mandibular injury were performed), pathological tumor-node-metastasis (TNM) staging of oral cancer, postoperative radiotherapy and chemotherapy; (III) information about PEG insertion time, PEG removal time, etc.; and (IV) telephone follow-up data on the actual usage of PEG and postoperative complications.

Statistical analysis

Statistical analysis was performed using SPSS 26.0 software. Continuous data were expressed as mean ± standard deviation; categorical and ordinal data were expressed as ratios or percentages. Univariate analysis was conducted using independent sample t-tests or Chi-squared tests. Factors with statistical differences were selected for binary logistic regression analysis. Receiver operating characteristic (ROC) curves were plotted, and sensitivity, specificity, Youden’s index, and other indicators were calculated. The significance level was set at α=0.05, and P<0.05 was considered statistically significant.

Results

General characteristics of oral cancer cases

A total of 246 oral cancer patients who underwent PEG at the Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine from July 2020 to June 2021 were initially collected for the study. Among them, 142 cases were excluded due to the exclusion criteria. Finally, 104 patients who underwent both oral cancer surgery and PEG placement were included in the study. There were 77 male patients and 27 female patients, with a mean age of 59.41±10.91 years. Nine cases (8.65%) underwent PEG placement before surgical intervention, while 95 cases (91.35%) underwent PEG placement after surgery.

According to the duration of PEG usage, there were 86 cases in the case group and 18 cases in the control group. The mean age of patients in the case group was 60.17±10.86 years, with 64 male and 22 female patients. The mean age of patients in the control group was 55.78±11.03 years, with 13 male and 5 female patients. Independent sample t-tests or Chi-squared tests were used to analyze the statistical differences in age and information such as smoking, alcohol consumption, hypertension, and diabetes between the two groups. The results showed no significant differences between the two groups.

Analysis of factors influencing the duration of PEG usage

Statistical analysis revealed that factors such as age, gender, smoking, alcohol consumption, history of diabetes, history of hypertension, neoadjuvant chemotherapy, tracheostomy during surgery, neck lymph node dissection, reconstructive surgery, mandibular injury, and pathological classification had no significant impact on the duration of PEG usage between the case group and the control group. However, factors such as tongue/pharyngeal resection during surgery (P=0.03), postoperative combined radiotherapy and chemotherapy (P=0.002), tumor stage (T stage) 3–4 (P<0.001), and node stage (N stage) 2–3 (P<0.001) significantly influenced the duration of PEG usage, with statistically significant differences. Refer to Table 1 for details.

Establishment of predictive model for relevant risk factors and evaluation of diagnostic efficacy

A binary logistic regression analysis was conducted, incorporating factors such as whether tongue/pharyngeal resection was performed, postoperative combined radiotherapy and chemotherapy, T stage, and N stage into the regression analysis. The results indicated that postoperative combined radiotherapy and chemotherapy [odds ratio (OR) =0.241; 95% confidence interval (CI): 0.067, 0.867], T stage 3–4 (OR =5.501; 95% CI: 1.609, 18.807), and N stage 2–3 (OR =4.628; 95% CI: 1.245, 17.195) were independent influencing factors affecting the actual duration of PEG usage. The predictive regression equation is as follows: Y = −1.425X2 + 1.705X3 + 1.532X4 − 0.274. Refer to Table 2 for details.

The ROC curve analysis was employed to assess the diagnostic performance of the predictive model. The results revealed that the area under the ROC curve (AUC) for the combined predictive model was 0.832 (P<0.001). The sensitivity of the model was determined to be 0.767, while the specificity was 0.778. Additionally, the Youden’s index was calculated to be 0.545. A predictive model with an AUC greater than 0.7 indicates its utility for clinical prediction of the actual effective duration of PEG usage. Refer to Table 3 and Figure 3 for detailed information.

Figure 3 ROC curve for combined predictive model. The red line indicates reference line and the blue line indicates ROC curve. ROC, receiver operating characteristic.

Post-PEG complications

Among 104 patients undergoing PEG, a total of 21 individuals experienced PEG-related complications, all of which occurred in the case group. Specifically, 14 individuals (13.46%) exhibited peristomal skin erythema, breakdown; 1 individual (0.96%) experienced dislodgement of the PEG tube; 4 individuals (3.85%) encountered PEG tube obstruction; 2 individuals (1.92%) suffered PEG tube leakage; and 16 individuals (15.38%) experienced gastrointestinal reactions during use, including refractory diarrhea, constipation, and abdominal discomfort.

Discussion

Swallowing is a coordinated process involving the mouth, throat, and esophagus to deliver food into the body. Treatments such as surgery and radiotherapy for oral cancer can disrupt the anatomy and function related to swallowing, leading to swallowing difficulties and eating disorders in 45–75% of patients (12-15). For oral cancer patients at high nutritional risk, clinicians often resort to nutritional support therapies such as nasogastric tube (NGT) feeding or total parenteral nutrition (TPN). However, for oral cancer patients, alterations in oral anatomy make NGT insertion challenging. Moreover, NGT exacerbates postoperative mucosal bleeding and the risk of tissue infection in the surgical area. Prolonged use of NGT can stimulate local inflammation in the oropharyngeal mucosa, leading to adhesions between the NGT and surrounding tissues, making removal difficult. Long-term NGT use can also cause relaxation of the lower esophageal sphincter, leading to reflux and coughing, and in severe cases, aspiration pneumonia, which can be life-threatening (16-18). TPN, requiring intravenous nutritional support, is prone to trigger septic shock and nutritional imbalances, making it not recommended for long-term use.

Using PEG for enteral nutrition support can effectively prevent damage to the surgical area, reduce the risk of aspiration pneumonia, and decrease the occurrence of malnutrition (5-8). However, whether all oral cancer patients require PEG therapy remains a subject of debate. In this retrospective study, we collected relevant clinical data of oral cancer patients who underwent PEG placement after surgery, and conducted a case-control analysis comparing the clinical characteristics between patients who used PEG for more than 1 month and those who used it for less than 1 month. Our findings revealed that factors such as undergoing tongue/pharynx resection during surgery, receiving adjuvant chemotherapy after surgery, and having advanced T and N stages of oral cancer significantly influenced the utilization of PEG.

The location and extent of surgical resection in oral cancer directly impact the occurrence of postoperative dysphagia (19). For instance, resection of facial skin and muscle tissues during surgeries for cheek and lip cancers can lead to masticatory muscle injury and incomplete mouth closure. Extraction of teeth and resection of the jaw bone during gingival cancer surgeries prevent food from being finely masticated into boluses. Tongue resection in tongue cancer and injury to the lingual branch of the glossopharyngeal nerve affect food perception and bolus transport, leading to prolonged swallowing times. Palatal cancer surgeries that damage the nasopharyngeal passage result in incomplete closure and increase the risk of reflux and coughing. Tongue base and pharyngeal wall involvement in oral-pharyngeal cancer surgeries disrupt bolus transfer and swallowing (20). A study involving 95 cases of tongue resection demonstrated that limited tongue movement and reduced tongue volume lead to inadequate airway closure, increasing the risk of coughing and aspiration pneumonia (21). Another study on partial laryngeal resection in head and neck cancer patients showed that those with damaged epiglottis during surgery had longer swallowing recovery times due to difficulties in lifting and propelling the larynx (22).

Patients with advanced oral cancer often require adjuvant chemotherapy after surgery. Both radiotherapy alone and chemoradiotherapy (concurrent or sequential) can affect swallowing function (23). Swallowing fluoroscopy examinations have revealed deterioration in swallowing function in patients undergoing postoperative radiotherapy for head and neck cancer, possibly related to increased thickness of the posterior pharyngeal wall after radiotherapy. During radiotherapy, damage to soft tissues such as facial skin, oral mucosa, and gums, as well as secretory glands such as salivary glands, and cranial nerves including the glossopharyngeal nerve, vagus nerve, accessory nerve, and hypoglossal nerve, may occur. With the accumulation of radiation dose, serious complications such as muscle atrophy, fibrosis, and radiation-induced osteonecrosis can occur, leading to oral feeding difficulties (24-27).

The T staging of oral cancer is determined based on the size and depth of tumor infiltration and is directly related to the extent of surgical resection and reconstruction. Patients with T3–4 stage tumors are at higher risk of developing long-term feeding difficulties after surgery. The N staging of tumors is determined by the number of lymph node metastases, with N2–3 stage tumors often associated with lymph node metastasis accompanied by external nodal extension (ENE), requiring radical neck lymph node dissection during surgery and postoperative adjuvant radiotherapy to the neck lymph node area. Overall, T and N staging affect the extent of tumor resection, lymph node dissection, reconstruction, and postoperative adjuvant chemoradiotherapy regimens. The higher the T and N stages, the more likely patients are to experience long-term feeding difficulties after surgery (18).

Although many previous studies reported that prophylactic PEG improved nutritional status and quality of life (28,29), further clarification of the specific indications for PEG treatment in oral cancer patients are necessary. This study demonstrates a significant correlation between the use of PEG in patients undergoing oral cancer surgery and factors such as tongue/pharyngeal resection during surgery, adjuvant chemoradiotherapy after surgery, and advanced T and N stages of oral cancer. By using these independent influencing factors to establish a combined predictive model for PEG treatment, a sensitivity of 0.767 and specificity of 0.778 were achieved. This suggests that oral cancer patients with these factors may have a stronger indication for prophylactic PEG placement. Otherwise, the best strategy should be short-term NGT. However, this study has several limitations. Firstly, it is a case-control study, and the collection of clinical data for both groups of patients was obtained retrospectively, introducing potential biases during the follow-up process. Secondly, the sample size was relatively small, and there were shortcomings in the observation indicators, which were not comprehensive enough. Additionally, the study did not compare different specific adjuvant chemotherapy regimens and nutritional status in postoperative patients, leading to certain selection biases and information biases. Therefore, further large-scale prospective studies are needed to validate the results of this study.

Conclusions

This study suggested that oral cancer patients with tongue/pharyngeal resection during surgery, postoperative combined radiotherapy and chemotherapy, and advanced T and N stages of oral cancer may have a stronger indication for prophylactic PEG.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-1880/rc

Data Sharing Statement: Available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-1880/dss

Peer Review File: Available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-1880/prf

Funding: This study was supported by the Xinyi Digestive Disease Research Fund (No. KY-2023-05-01) and the Clinical Research Program of Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (No. JYLJ202224).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-1880/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. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (No. SH9H-2022-T337-2), and individual consent for this retrospective analysis was waived.

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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