Meeting Quality Metrics in Oral Squamous Cell Carcinoma Surgery: A Single-Center Experience

Patient-centered quality metrics have been proposed to evaluate and optimize hospital processes, aiming to improve patient outcomes. Furthermore, they can be used to objectively rate and compare the ability of health care providers to meet the needs of their patients. In patients with advanced resectable oral squamous cell carcinoma, optimal surgical treatment of the neck and timely initiation of both surgical and adjuvant therapy, when indicated, are crucial for recurrence-free and overall survival. This retrospective analysis included 160 patients who received primary resection of oral squamous cell carcinoma and concurrent neck dissection.It aimed to investigate how well quality metrics were met during a 6-year period in the department of oral and maxillofacial surgery at a university hospital. 93.1% of patients were seen in the specialist's office within 21 days after referral. Resection was classified as R0 in 94.4%. A lymph node yield >= 18 was achieved in 82.5%. The lymph node ratio was <= 6% in 43.3% of nodal-positive necks. Readmission and unplanned revision surgery were rare (6.9%). Adjuvant radiotherapy was started <= 6 weeks after surgery in 45.3%, and the indication was in accordance with international guidelines in all cases.
 
Quality metrics are an effective tool for planning process optimization in a hospital. Moreover, nodal quality metrics such as lymph node yield and lymph node ratio could, after validation, complement existing and well-established prognostic parameters for patient-specific adaptation of adjuvant treatment plans.

Accepted for publication: November 29, 2022

Published online: December 15, 2022

The final edited and typeset version will appear in the future.

Introduction

Oral Squamous Cell Carcinoma (OSCC) is a common malignancy. Despite guideline-compliant therapy in specialized centers and by an experienced interdisciplinary team, the prognosis is often poor. Treatment quality can be objectively described by various indicators. Such quality metrics can relate, for example, to treatment outcomes or costs. Patient-centered quality metrics in OSCC surgery usually focus on patient survival and satisfaction.

Recurrence- and progression-free survival in OSCC can be improved by early, well-planned treatment with clear resection margins (R0) and optimal surgical treatment of the neck (neck dissection). Survival is known to be significantly affected by cervical lymph node involvement. The quality of the neck dissection can be measured by the number of cervical lymph nodes harvested (lymph node yield, LNY). A lymph node yield of 18 or more and a maximum of 6% metastatic lymph nodes (lymph node ratio, LNR) is considered by many authors to be a quality standard of prognostic significance (EBRAHIMI ET AL. 2014, DIVI ET AL. 2016, MALLEN-ST. CLAIR 2017, JUDSON 2018). The overall quality of surgical treatment can be estimated by the frequency of unplanned repeat hospitalizations within 14 days and repeat surgeries within 30 days after primary surgery (APPACHI ET AL. 2019). Interdisciplinary collaboration and general patient management can be measured by whether the indication for adjuvant radiotherapy in patients with locally advanced disease was correctly made according to the National Comprehensive Cancer Network (NCCN) guidelines, and whether radiotherapy was initiated within 6 weeks of surgery. The efficiency of in-hospital processes can be assessed, for example, by the time between patient referral and surgery.

The purpose of this study was to evaluate how well our department met the above quality metrics to better understand the feasibility and overall value of analyzing quality metrics in head and neck cancer surgery.

Materials and methods

For this retrospective analysis, the clinical information system of the University Hospital Zurich, Department of Oral and Maxillofacial Surgery, was searched for patients aged 18 years or older who had undergone primary resection of an OSCC and concurrent neck-dissection with or without free flap reconstruction between January 2013 and December 2018.

Patients with a synchronous malignancy, prior oral cavity cancer surgery, or an incomplete dataset were excluded from further analysis, as were patients treated with sentinel neck dissection only. Data through January 2021 were included.

All patients were operated on by experienced surgeons according to the standards of our department, which is certified by the German cancer society ("Deutsche Krebsgesellschaft" DKG). Data on age, gender, malignancy, surgery, and follow-up were obtained from patient charts and surgical reports.

Statistical analyses were performed with SPSS (version 26; IBM Corp., Armonk, NY, USA) and included descriptive statistics.

All patients have signed an informed consent form for further use of their medical data. The relevant ethics committee approved the conduct of this study (KEK Zürich, approval no.: 2019-01852). This study fulfills the criteria of the Declaration of Helsinki.

Results

Patient data
160 patients (95 men, 65 women) met the inclusion criteria, as is shown in figure 1. Their mean age at diagnosis was 64.6 years (range, 26 to 92 years; median, 65 years).

Smoking and alcohol consumption were prevalent: 105 patients drank alcohol regularly (65.6%), and 118 patients were smokers (73.8%).

OSCC was most frequently found on the tongue with 65 cases (40.6%), followed by the floor of mouth (32 patients, 20%), mandibular gingiva (28 patients, 17.5%), maxillary gingiva (13 patients, 8.1%), and retromolar region (11 patients, 6.9%). Multifocal carcinoma was found in two cases.

107 patients had advanced disease at the time of diagnosis (66.9%). The distribution of pT, pN, and UICC cancer stages is shown in Tables I-III.

Surgery
124 patients (77.5%) were treated with a free-flap reconstruction, most commonly with a radial forearm flap (76 patients), fibula flap (26 patients), or anterolateral thigh flap (17 patients). In 5 cases, other flaps (scapula, latissimus dorsi, and sural flap) were used. The remaining patients were eligible for direct defect closure.

69 patients underwent unilateral supraomohyoid neck dissection of levels I-III (43.1%). Unilateral neck dissection of levels I-IV was performed in 59 cases (36.9%), and that of levels I-V in 11 cases (6.9%). In the remaining 21 patients, various combinations of levels were dissected on one or both sides.

Quality Metrics
Most patients were referred by dentists, followed by general practitioners and otorhinolaryngologists. All but 23 patients were seen within 14 days of referral (85.6%), and another 12 within three weeks. Of the remaining 11 patients, 5 initially refused treatment or presented to another physician beforehand, and 3 had difficulty being brought to our department because they lived in a nursing home. For the remaining 3 patients, the reasons for the delay are unknown. On average, surgery took place 20 days after the first consultation in our office (median, 20 days; range, 6-34 days). When comparing patients with and without free flap reconstruction, there was no statistically significant difference in the timing of surgery, although a tendency toward later surgery was noted when extensive planning for fibula flap reconstruction was required.

Clear resection margins (R0) were achieved in 151 patients (94.4%). 9 resections were classified as R1; there were no R2 resections. A lymph node yield of 18 or more was achieved in 132 patients (82.5%), with a mean of 29 lymph nodes harvested (median, 27; range, 9-82). Lymph node metastases were found in 76 patients (47.5%) with a mean of 3.3 positive lymph nodes (median, 2). Occult metastases were found in 29 of the 100 patients with a clinically nodal-negative neck (cN0). On the other hand, 13 patients with a cN+ neck had no lymph node metastases on histopathologic examination and were downstaged to a pN0 neck. Extra-nodal extension (ENE) was detected in 29 patients. Among the 76 patients with positive lymph nodes, the mean lymph node ratio was 11.5% (mean, 7.4%; range, 2.1-88.9%). A lymph node ratio of 6% or less was obtained in 33 patients (43.4%). For a tabular overview, see Table IV.

The length of hospital stay averaged 17.4 days (median, 15 days; range, 4-53 days).

Unplanned readmission within 14 days of discharge was required in 11 cases (6.9%). Unplanned repeat surgery within 30 days of primary surgery was performed in 17 patients. Of these, 11 required surgery under general anesthesia (6.9%): 9 patients required follow-up resection due to an R1 resection margin, and 2 cases required revision of the free flap.  The remaining minor unplanned surgeries were due to wound dehiscence or fistula, surgical closure of a tracheostomy, or evacuation of a post-surgical hematoma.

The indication for adjuvant therapy was correctly made according to the NCCN guidelines in all cases. In 8 cases, adjuvant therapy was not started at the patient's request, although it was formally indicated. 75 patients received adjuvant radiotherapy. It was started at a mean of 7.25 weeks after surgery (median, 7.07 weeks; range, 2.18-11.85 weeks). In 34 patients (45.3%), radiotherapy was started within 6 weeks after surgery.

Discussion

In a competitive environment and when treating patients with potentially life-limiting diagnoses, all health care providers must strive for excellence. One means of assuring quality is an independent certification, for example by the German cancer society ("Deutsche Krebsgesellschaft" DKG). To be certified, centers must meet strict criteria (Deutsche Krebsgesellschaft 2010). This ensures compliance with expert guidelines such as the "S3-Leitlinie" (Leitlinienprogramm Onkologie 2021), which are developed after central multinational evaluation of cancer data (e.g., DÖSAK tumor registry).

Quality metrics have been defined to facilitate the evaluation, comparison, and improvement of a surgical center's treatment processes according to international guidelines. Adherence to quality metrics is associated with improved patient outcomes (GRABOYES ET AL. 2016, LIU ET AL. 2021). Overall, the nodal and process-related quality metrics were well met in our department. Patients were seen shortly after referral, and surgery was performed promptly. Surgical outcomes can be described as excellent, with high R0 resection rates and low complication rates, especially considering flap failures.  Evaluation of the quality metrics was feasible as all necessary parameters are documented in the standard medical records. At this time, comparison with other centers is difficult, because to the authors' knowledge, no other center has openly published its current data on adherence to quality metrics.

The underlying high-quality database with comprehensive and complete data makes the results of our study meaningful. A limitation might be found in the inherent selection bias. In our university hospital, patients with advanced disease and therefore more complex treatment plans are disproportionally common. The exclusion of patients with sentinel neck dissection in this study may have further contributed to this problem. The high rate of patients with advanced lymph node involvement (stages pN2b and higher) may explain why the LNR of <= 6% was achieved rather rarely. Since the lymph node yield is limited to some degree, the more lymph nodes affected, the higher the lymph node ratio is bound to be.

Although the recommended interval between surgery and adjuvant radiotherapy is 6 weeks, radiotherapy was started later in most of our patients. Except for a few rare cases in which delays due to repeated interdisciplinary tumor board meetings or holidays may have played a role, radiotherapy was deliberately postponed. A careful patient-specific benefit-risk analysis is critical when planning any adjuvant therapy. Delayed general recovery after major surgery, wound dehiscence, infection, or the need for prolonged outpatient rehabilitation warrant postponement of radiotherapy. Ultimately, patient-specific treatment planning must be a key objective. Thorough and honest patient information and preparation, involvement of patients and their families in decision-making, and optimal interdisciplinary collaboration can help optimize treatment processes and shorten treatment time.

In addition to quality assessment, some quality metrics may also have prognostic value for patient outcomes (REINISCH ET AL. 2014, HINGSAMMER ET AL. 2019, SHEPPARD ET AL. 2021). The current literature is inconclusive regarding the suitability of lymph node yield and lymph node ratio as prognostic factors (JABER ET AL. 2014, DE KORT ET AL. 2019, HUANG ET AL. 2019). Because both LNY and LNR are influenced by many variables, it is advisable to use these parameters in addition to the well-established predictive values for an even more specific risk assessment for each patient (MARRES ET AL. 2014, LIM ET AL. 2017). A follow-up analysis of this extensive dataset, analyzing LNY and LNR as a function of neck dissection type, cancer type, and patient and tumor characteristics, will shed light on this aspect. Evaluation of complication and recurrence rates, as well as survival analyses per subgroups, will provide further helpful insights and will reveal whether adherence to the quality metrics improves patient outcomes as measured by recurrence-free or overall survival. This may contribute to the future use of LNY and LNR as risk stratification tools for individualized treatment plan adjustment in patients with OSCC.
We encourage other cancer centers to also assess their adherence to the above quality metrics in order to collect and evaluate comprehensive data, aiming to further improve quality of care in the best interest of their patients.

Acknowledgements
The authors sincerely thank Dr. Christelle Fongaufier for the French translation of the extended abstract.

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