Abstract
IMPORTANCE
Quality metrics for patients with laryngeal squamous cell carcinoma (SCC) exist, but whether compliance with these metrics correlates with improved survival is unknown.
OBJECTIVE
To examine whether compliance with proposed quality metrics is associated with improved survival in patients with laryngeal SCC treated with surgery with or without adjuvant therapy.
DESIGN, SETTING, AND PARTICIPANTS
This retrospective cohort study included patients from a tertiary care academic medical center who had previously untreated laryngeal SCC and underwent surgery with or without adjuvant therapy from January 1, 2003, through December 31, 2012. Data analysis was performed from August 4, 2015, through December 13, 2015.
INTERVENTIONS
Surgery with or without adjuvant therapy.
MAIN OUTCOMES AND MEASURES
Compliance with quality metrics from the American Head and Neck Society (AHNS), National Comprehensive Cancer Network (NCCN) guidelines, and institutional metrics with face validity covering pretreatment evaluation, treatment, and posttreatment surveillance was evaluated. The association between compliance with the group of metrics and overall survival (OS), disease-specific survival (DSS), and disease-free survival (DFS) was explored using Cox proportional hazards analysis. The association between compliance with individual metrics and survival was similarly determined.
RESULTS
A total of 243 patients (184 men and 59 women) were included in the study (median age, 62 years; age range, 23–87 years). No association was found between increasing levels of compliance with the AHNS or NCCN metrics and survival. The only AHNS or NCCN metric for which greater compliance correlated with improved survival on multivariable Cox proportional hazards analysis controlling for pT stage, pN stage, extracapsular spread, margin status, and comorbidity was pretreatment multidisciplinary evaluation for patients with stage cT3-4 or cN1-3 disease (OS adjusted hazard ratio [aHR], 0.47; 95% CI, 0.24–0.94; DFS aHR, 0.45; 95% CI, 0.23–0.85). For the institutional metrics, multidisciplinary evaluation for all patients (OS aHR, 0.51; 95% CI, 0.29–0.88; DFS aHR, 0.50, 95% CI, 0.32–0.80) and elective neck dissection yield of 18 lymph nodes or more (DFS aHR, 0.36; 95% CI, 0.14–0.99) were associated with improved survival on multivariable Cox proportional hazards analysis.
CONCLUSIONS AND RELEVANCE
In this cohort of patients with surgically treated laryngeal SCC, multidisciplinary evaluation and elective neck dissection yield of 18 lymph nodes or more are associated with improved survival. Development of better quality metrics is necessary because increased compliance with metrics described by the AHNS and NCCN is not associated with improved survival. Previously described metrics for surgically treated oral cavity cancer are not prognostic for surgically treated laryngeal SCC. Future multi-institutional collaboration will be required to validate these findings, develop better quality metrics, and evaluate whether quality metrics for head and neck cancer are site specific.
Measures of quality are used at individual physician-and hospital-wide levels to determine ratings, accreditation, and reimbursement. However, disagreement remains about how to define and measure quality in a pragmatic and actionable manner,1,2 as well as how current metrics correlate with outcomes that reflect high-quality care.3,4 In 2009, the executive council of the American Head and Neck Society (AHNS) approved a set of quality measures for patients with laryngeal squamous cell carcinoma (SCC).5 These metrics address pretreatment, treatment, and posttreatment surveillance. None of the treatment metrics relate to the quality of the surgery itself. Assessing compliance with these metrics was viewed as one way to measure the quality of care for patients with head and neck cancer.6 However, it is unknown whether increased compliance with the described AHNS metrics is associated with improved survival in patients with laryngeal SCC.
In the 6 years since the AHNS metrics were described, others have attempted to define and measure processes of quality care for laryngeal cancer7,8 and cancer of other head and neck sites.9–14 The published studies7,8 of quality metrics for laryngeal cancer have focused on elderly patients and included patients treated with surgical and nonsurgical approaches. In addition, the metrics were related primarily to surveillance, management of recurrent disease, and end-of-life care and did not find a graded response between increasing levels of compliance and the outcome of interest.7,8
This study uses a cohort of surgically treated patients with laryngeal SCC to (1) determine compliance with quality metrics described by the AHNS, National Comprehensive Cancer Network (NCCN) guidelines, and institutional metrics with face validity, (2) identify individual quality metrics associated with improved survival, and (3) measure the association between compliance and survival.
Methods
Patients and Methods
A retrospective review of patients 18 years or older who underwent primary surgical treatment for a laryngeal SCC at Washington University School of Medicine from January 1, 2003, through December 31, 2012, was performed. Data analysis was performed from August 4, 2015, through December 13, 2015. Inclusion criteria for the study were (1) previously untreated primary laryngeal SCC, (2) SCC histologic findings, (3) no history of head and neck cancer, (4) definitive surgical-based management, and (5) a minimum 12-month follow-up (or death). Two hundred ninety-one patients met the study inclusion criteria. Forty-eight patients were excluded because of insufficient documentation to assess compliance with the quality metrics, leaving a cohort of 243 patients. Seven surgeons treated these patients along with other members of the multidisciplinary head and neck cancer team. This study was approved by the Washington University School of Medicine Institutional Review Board. A waiver of informed consent was granted. Data were deidentified after abstraction was performed.
The medical records were reviewed for demographic data and clinical variables, including comorbidity as measured prospectively by the Adult Comorbidity Evaluation 27 index (ACE-27),15 surgical and adjuvant treatment details, pathologic variables, surveillance, patterns of recurrence, and death.
Selection of Quality Metrics
The 3 sets of quality metrics assessed in the study are listed in Table 1. Quality metrics were chosen from the 2009 AHNS quality metrics and the 2014 NCCN Guidelines for Head and Neck Cancers.16 Additional potential quality metrics with face validity were developed in a multidisciplinary fashion at our institution as previously described.12
Table 1.
Quality Metrics
| Evaluation | Quality Metric | Eligibility Criterion |
|---|---|---|
| AHNS Quality Metrics | ||
| Pretreatment evaluation | ||
| 1 | Complete head and neck examination | All patients |
| 2 | Laryngeal examination | All patients |
| 3 | Biopsy | All patients |
| 4 | Radiologic studies of primary | Stage cT2-4 |
| 5 | Radiologic imaging of the head and neck | Stage cT2-4 glottic, all supraglottic |
| 6 | Chest imaging | Stage cT2-4 glottic, all supraglottic |
| 7 | Documentation of TNM staging | All patients |
| 8 | Tobacco cessation counseling | Current smokers |
| 9 | Prelaryngectomy counseling | Undergoing total laryngectomy |
| Treatment related | ||
| 10 | Multidisciplinary evaluation through consultation or tumor board | Stage cT3-4 or cN1-3 |
| 11 | Referral for adjuvant radiation | Stage pT3-4 or pN2-3 |
| 12 | Referral for adjuvant chemoradiation | ECS or positive margins |
| Posttreatment surveillance | ||
| 13 | Regular follow-up | All patients |
| 14 | Thyroid function tests ≤12 mo after radiotherapy | Received adjuvant radiotherapy and alive at 12 mo |
| NCCN Guidelines | ||
| Pretreatment evaluation | ||
| 1 | Complete head and neck examination | All patients |
| 2 | Biopsy | All patients |
| 3 | Radiologic studies of primary and neck | Stage cT2-4 glottic, all supraglottic |
| 4 | Examination with patient under anesthesia with endoscopy | All patients |
| 5 | Tobacco cessation counseling | Current smokers |
| Treatment related | ||
| 6 | Referral for adjuvant radiation | Stage pT3-4 or pN2-3 |
| 7 | Referral for adjuvant chemoradiation | ECS or positive margins |
| 8 | Start of adjuvant therapy ≤6 wk postoperatively | Receiving adjuvant therapy |
| Posttreatment surveillance | ||
| 9 | Regular follow up at NCCN intervals | All patientsa |
| 10 | Posttreatment imaging ≤6 mo after therapy completion | Stage pT3-4 or pN2-3, no clinical suspicion of recurrence, and alive at 6 mo |
| 11 | Thyroid function tests ≤12 mo after radiotherapy | Received adjuvant radiotherapy and alive at 12 mo |
| Additional Institutional Quality Metrics With Face Validity | ||
| Pretreatment evaluation | ||
| 1 | Time from referral to clinic visit ≤14 d | All patientsa |
| 2 | Internal pathologist review of outside biopsy | Pathologist from outside hospital |
| 3 | Pulmonary function tests | Stage cT2-4 and partial laryngeal surgery |
| 4 | Pretreatment dental evaluation | Dentulous and stage cT3-4 or cN1-3 |
| 5 | Multidisciplinary evaluation through consultation or tumor board | All patients |
| Treatment related | ||
| 6 | Time from clinic to definitive surgery ≤21 d | All patients |
| 7 | Initial negative-margin resection | All patients |
| 8 | Elective neck dissection with ≥18 lymph nodes | Stage cN0 undergoing neck dissection |
| 9 | pTNM stage documented | All patients |
| 10 | Margin status documented | All patients |
| 11 | No unplanned surgery ≤14 d | All patients |
| 12 | No unplanned 30-d readmission | All patients |
| Posttreatment surveillance | ||
| 13 | Multidisciplinary follow-up | Received multimodality therapya |
Abbreviations: AHNS, American Head and Neck Society; ECS, extracapsular spread; NCCN, National Comprehensive Cancer Network.
Patients for whom data were missing for this metric were scored as not evaluable
Definitions of Variables and Eligibility
Table 1 lists the eligibility criteria for the quality metrics. For the AHNS metrics, specific indications for assessment of regional nodal basins for metastatic lymphadenopathy and assessment for systemic disease were not specified; thus, the eligibility criteria of all supraglottic cancer and stage cT2-4 glottic cancers were chosen by the study authors. For tobacco cessation counseling, current smoker was defined as having smoked within the month before consultation. All patients were required to have follow-up with their head and neck surgeon for at least 12 months to be included in the study; therefore, for the metric of regular follow-up visits, the metric was defined as consistent multidisciplinary follow-up without a specified interval. Only patients who received multidisciplinary therapy were eligible for the metric.
For the NCCN guidelines, metrics that were recommended as clinically indicated (eg, chest imaging as clinically indicated) were not evaluated because of the lack of objective data to determine clinical necessity. Guidelines described as consider (eg, consider positron emission tomography–computed tomography for stage III or IV disease) were not grouped with the NCCN guidelines given the optional nature of performance. The NCCN guidelines for glottic cancer indicate that complete workup is not indicated for Tis and T1 disease without indicating which parts of the workup are not indicated. For the purposes of this study, patients with stage cT1 glottic carcinoma were exempted from the metric for radiologic studies of the head and neck. For surveillance, the metric was assessed based on recommended follow-up by the surgeon, not actual clinic dates. The head and neck surgeon was scored as compliant only if he or she met each of the subportions of the metric during the entire surveillance period (eg, every 1–3 months for 12 months, then every 2–6 months for months 13–24, and so on).
For the additional metrics with face validity, pretreatment dental evaluation consisted of documentation of a dental referral before, or dental extractions during, the index hospitalization. Elective neck dissection lymph node yield was calculated on the ipsilateral side. If bilateral elective neck dissections were performed, the lymph node count from both sides was averaged.17 Initial negative-margin resection status was based on permanent section margins, regardless of frozen section status in the operating room. Unplanned surgery within 14 days did not include planned staged neck dissections or dental extractions but included additional resection for positive margins. We defined a 30-day unplanned readmission as an admission to any service in the hospital within 30 days of discharge that was unexpected.18 For thyroid function testing, if a patient was dead less than 12 months after completing radiotherapy, the metric was not evaluable. For surveillance imaging, if imaging was prompted by clinical suspicion of recurrence or the patient was dead less than 6 months after the completion of therapy, the metric was not evaluable.
Outcome Measures
The outcome measures included compliance rates with quality metrics and measures of survival (overall survival [OS], disease-specific survival [DSS], and disease-free survival [DFS]). For each patient, a compliance score for the group of metrics was calculated based on the opportunity model used by the Centers for Medicare & Medicaid Services.19 For example, if a patient was eligible for 10 metrics and 6 were performed, the compliance score was 60% (6 of 10).
The OS was calculated from the date of surgery to the date of death from any cause. The DSS was calculated from the date of surgery to the date of death from laryngeal SCC or direct treatment effects. The DFS was calculated from the date of surgery to the date of death or first recurrence. Patients lost to follow-up were censored at the date of last contact with the head and neck surgeon.
AHNS Quality Metrics, NCCN Guidelines, and Survival
To determine the association between compliance with the group of AHNS metrics and survival, compliance scores were calculated for each patient as described above. No patients had less than 40% of the metrics performed. Compliance scores were divided into 3 groups (40%–79%, 80%–99%, and 100%). Estimates of survival were calculated for OS, DSS, and DFS using Kaplan-Meier analysis and compared among the 3 compliance groups using the log rank test. Multivariable Cox proportional hazards analysis was performed for the compliance score, controlling for pT stage, pN stage, extracapsular spread (ECS), final margin status, and overall severity of comorbidity. The pT stage was dichotomized into T1-2 vs T3-4, pN stage was dichotomized into N0-1 vs N2-3, and the ACE-27 comorbidity score was dichotomized to no or mild comorbidities (scores of 0–1) and moderate or severe comorbidities (scores of 2–3). The association between compliance with the overall group of metrics and OS, DSS, and DFS was expressed as an adjusted hazard ratio (aHR) and 95% CI. Log minus log plots were used to test the proportional hazards assumption for variables included in the Cox proportional hazards models. The same method was used to assess the association between compliance with the NCCN guidelines and survival.
Performance of Individual Quality Metrics and Survival
The association between performance of an individual quality metric and OS, DSS, and DFS was investigated. Univariable Cox proportional hazards analysis and multivariable Cox proportional hazards analysis controlling for pT stage, pN stage, ECS, final margin status, and overall severity of comorbidity were used to calculate the association between performance of an individual metric and OS, DSS, and DFS in similar fashion.
Statistical Analysis
Statistical significance was indicated by 2-tailed P ≤ .05. Data analysis was performed using SPSS statistical software, version 22.0 (SPSS Inc).
Results
Oncologic Characteristics
The demographic, oncologic, and treatment details of the patients are presented in the eTable in the Supplement. A total of 243 patients (184 men and 59 women) were included in the study (median age, 62 years; age range, 23–87 years). In all, 138 tumors (56.8%) were located in the glottic larynx. Of the 243 patients, 122 (50.2%) had advanced pathologic T-stage disease, and 54 of 243 (22.2%) had pathologic N2- or N3-stage disease. Eighty-four patients (34.6%) received adjuvant therapy: 49 of 240 (20.4%) received adjuvant radiotherapy without chemotherapy, and 35 of 240 (14.6%) received adjuvant chemo-radiation. The cohort of patients had a median follow-up of 42 months (interquartile range [IQR], 24–68 months). There were 73 total deaths, 46 deaths due to disease, and 31 recurrences. Five-year OS, DSS, and DFS rates were 85% (95% CI, 81%-90%), 86% (95% CI, 81%-91%), and 78% (95% CI, 73%-83%), respectively.
Compliance With Quality Metrics
Compliance with the quality metrics from the AHNS, NCCN guidelines, and additional potential metrics are shown in the eFigure in the Supplement. The median compliance rate was 85% (IQR, 79%-93%) for the 14 AHNS quality metrics and 78% (IQR, 67%-88%) for the 11 NCCN measures. Individual AHNS and NCCN care processes with the lowest compliance were tobacco cessation counseling (22 of 136 [16.2%]) and referral to a speech-language pathologist for prelaryngectomy counseling (14 of 77 [18.2%]). The AHNS and NCCN care processes with the highest compliance were complete head and neck examination, laryngeal examination, biopsy (all 100%), and radiologic studies of the head and neck (163 of 165 [98.8%]). Of the additional institutional metrics, 218 of 243 patients (89.7%) had an initial margin-negative resection, and 215 of 243 (88.5%) had no unplanned 30-day readmission.
Association Between Compliance With AHNS Quality Metrics and Survival
Kaplan-Meier analysis revealed a significantly better OS and DFS and a strong trend toward improved DSS for patients with 100% compliance with the 14 AHNS metrics relative to other compliance levels (log-rank P = .006 for OS, .048 for DFS, and .07 for DSS) (Figure 1, A–C). No significant differences were found between the 80% through 99% group and the 79% or less group across any of the survival metrics. After controlling for pT stage, pN stage, ECS, final margin status, and comorbidity, there was an increased risk of death in the 80% through 99% compliance group compared with the 100% group (OS aHR, 2.2; 95% CI, 1.03–4.7) (Figure 1, D-F). No other significant differences were found in survival among the 100%, 80% through 99%, and 79% or less compliance levels.
Figure 1. Association of Compliance With the American Head and Neck Society (AHNS) Metrics and Survival.
Kaplan-Meier estimates of overall survival (A), disease-specific survival (B), and disease-free survival (C) for different levels of compliance with the AHNS metrics (100% vs 80%–99% vs ≤79%). Comparison of overall survival (D), disease-specific survival (E), and disease-free survival (F) for different levels of compliance with the AHNS metrics after controlling for pT stage, pN stage, extracapsular spread, final margin status, and comorbidity. aHR indicates adjusted hazard ratio.
Association Between Compliance With NCCN Guidelines and Survival
Kaplan-Meier analysis revealed no difference in OS, DSS, or DFS for different levels of compliance with the NCCN guidelines (log-rank P = .05, .19, and .30 for OS, DSS, and DFS, respectively) (Figure 2, A-C). After pT stage, pN stage, ECS, final margin status, and comorbidity were controlled for, no association was found between levels of compliance and survival (Figure 2, D-F).
Figure 2. Association of Compliance With the National Comprehensive Cancer Network (NCCN) Guidelines and Survival.
Kaplan-Meier estimates of overall survival (A), disease-specific survival (B), and disease-free survival (C) for different levels of compliance with the NCCN guidelines (100% vs 80%-99% vs ≤79%). Comparison of overall survival (D), disease-specific survival (E), and disease-free survival (F) for different levels of compliance with the NCCN guidelines after controlling for pT stage, pN stage, extracapsular spread, final margin status, and comorbidity. aHR indicates adjusted hazard ratio.
Association Between Compliance With Individual Quality Metrics and Survival
The association between compliance with individual quality metrics and OS, DSS, and DFS on univariable analysis is given in Table 2. Of the AHNS metrics and NCCN guidelines, only multidisciplinary evaluation through consultation or tumor board for patients with advanced T-stage or nodal disease was associated with improved survival (OS HR, 0.47; 95% CI, 0.25–0.90; DFS HR, 0.51; 95% CI, 0.27–0.94). There were no individual pretreatment or surveillance metrics for which increased compliance was associated with improved survival. For the additional metrics with face validity, a negative-margin resection at the time of initial surgery was associated with improved OS, DSS, and DFS (HR, 0.48; 95% CI, 0.26–0.90; HR, 0.37; 95% CI, 0.18–0.77; and HR, 0.55; 95% CI, 0.31–0.97, respectively), and multidisciplinary evaluation for all patients was associated with improved DFS (HR, 0.59; 95% CI, 0.37–0.92) and a strong trend to improved OS and DSS (HR, 0.61; 95% CI, 0.36–1.03; HR, 0.67; 95% CI, 0.33–1.36, respectively).
Table 2.
Unadjusted Analysis of Individual Quality Metrics and Survival
| Quality Metric | HR (95% CI) | ||
|---|---|---|---|
| OS | DSS | DFS | |
| AHNS Quality Metric | |||
| Pretreatment | |||
| Complete head and neck examination | NAa | NA | NA |
| Laryngeal examination | NA | NA | NA |
| Biopsy | NA | NA | NA |
| Imaging of primary | 0.58 (0.08–4.23) | NA | 0.69 (0.10–4.98) |
| Imaging for regional metastases | 1.00 (0.14–7.20) | NA | 1.20 (0.18–9.30) |
| Chest imaging | 1.33 (0.53–3.32) | 1.72 (0.41–7.12) | 0.68 (0.33–1.42) |
| Documentation of TNM staging | 1.54 (0.70–3.35) | 1.74 (0.62–4.85) | 1.59 (0.80–3.16) |
| Tobacco cessation counseling | 1.07 (0.50–2.27) | 1.20 (0.49–2.91) | 0.77 (0.36–1.61) |
| Prelaryngectomy counseling | 0.75 (0.26–2.15) | 0.64 (0.19–2.18) | 0.53 (0.19–1.50) |
| Multidisciplinary evaluation (cT3–4 or ≥1 LN) | 0.47 (0.25–0.90)b | 0.49 (0.23–1.07) | 0.51 (0.27–0.94)b |
| Treatment | |||
| Referral adjuvant radiation | 2.34 (1.17–4.69) | 3.68 (1.44–9.44) | 1.73 (0.95–3.15) |
| Referral adjuvant chemoradiation | 1.29 (0.59–2.85) | 1.25 (0.53–2.98) | 1.16 (0.57–2.38) |
| Surveillance | |||
| Thyroid function testing | 0.53 (0.26–1.11) | 0.52 (0.23–1.21) | 0.65 (0.33–1.29) |
| Regular follow-up | 1.54 (0.53–4.47) | 1.36 (0.41–4.54) | 1.64 (0.58–4.65) |
| NCCN Guidelines | |||
| Pretreatment | |||
| Complete head and neck examination | NA | NA | NA |
| Biopsy | NA | NA | NA |
| Imaging of primaryand neck | 1.00 (0.14–7.20) | NA | 1.29 (0.18–9.30) |
| Examination with patient under anesthesia | NA | NA | NA |
| Tobacco cessation counseling | 1.07 (0.50–2.27) | 1.20 (0.49–2.91) | 0.77 (0.36–1.6) |
| Treatment | |||
| Referral for adjuvant radiation | 2.34 (1.17–4.69) | 3.68 (1.44–9.44) | 1.73 (0.95–3.15) |
| Referral adjuvant chemoradiation | 1.29 (0.59–2.85) | 1.25 (0.53–2.98) | 1.16 (0.57–2.38) |
| Start of adjuvant therapy ≤6 wk | 0.97 (0.47–1.97) | 0.75 (0.33–1.71) | 1.11 (0.57–2.17) |
| Surveillance | |||
| Thyroid function testing | 0.53 (0.26–1.11) | 0.52 (0.23–1.21) | 0.65 (0.33–1.29) |
| Posttreatment imaging | 1.30 (0.70–2.43) | 1.55 (0.73–3.32) | 1.18 (0.66–2.10) |
| Follow-up (NCCN schedule) | 0.74 (0.45–1.24) | 0.82 (0.44–1.54) | 0.82 (0.54–1.27) |
| Additional Quality Metrics With Face Validity | |||
| Pretreatment | |||
| Referral to clinic visit ≤14 d | 1.67 (0.52–5.42) | 1.34 (0.31–5.74) | 1.86 (0.67–5.14) |
| Review of outside pathologist | 0.66 (0.16–2.80) | 0.72 (0.10–5.48) | 1.04 (0.25–4.28) |
| Pulmonary function tests | 1.81 (0.80–4.07) | 3.50 (0.96–12.8) | 1.20 (0.61–2.33) |
| Pretreatment dentalevaluation | 1.33 (0.57–3.09) | 1.48 (0.62–3.54) | 1.08 (0.49–2.35) |
| Multidisciplinary evaluation (all patients) | 0.61 (0.36–1.03) | 0.67 (0.33–1.36) | 0.59 (0.37–0.92)b |
| Treatment | |||
| Clinic to surgery ≤21 d | 0.81 (0.51–1.29) | 0.85 (0.48–1.52) | 1.00 (0.68–1.48) |
| Initial margin negative resection | 0.48 (0.26–0.90)b | 0.37 (0.18–0.77)b | 0.55 (0.31–0.97)b |
| Elective ND with ≥18 LNs | 0.71 (0.26–1.94) | 1.26 (0.26–6.02) | 0.42 (0.17–1.03) |
| pTNM stage documented | 0.86 (0.48–1.54) | 1.05 (0.47–2.36) | 0.81 (0.49–1.34) |
| Margin status documented | 0.89 (0.55–1.42) | 1.13 (0.61–2.07) | 1.02 (0.68–1.53) |
| No unplanned surgery ≤14 d | 0.82 (0.38–1.79) | 0.86 (0.31–2.41) | 0.66 (0.34–1.28) |
| No unplanned 30-d readmission | 2.07 (0.75–5.67) | 2.78 (0.67–11.5) | 0.99 (051–1.89) |
| Multidisciplinary follow-up | 1.54 (0.53–4.47) | 1.36 (0.41–4.54) | 1.64 (0.58–4.65) |
Abbreviations: AHNS, American Head and Neck Society; DFS, disease-free survival; DSS, disease-specific survival; HR, hazard ratio; LN, lymph node; NA, not applicable; NCCN, National Comprehensive Cancer Network; ND, neck dissection; OS, overall survival.
Metrics for which there were no events in the nonadherence group cannot be evaluated to calculate an HR of survival.
Denotes variables significantly associated with improved survival.
The association between compliance with individual metrics and OS, DSS, and DFS was assessed in an adjusted Cox proportional hazards model that controlled for pT stage, pN stage, ECS, final margin status, and overall severity of comorbidity (Table 3). Multidisciplinary evaluation through consultation or tumor board for patients with advanced T-stage or nodal disease was the only AHNS or NCCN metric for which compliance was associated with improved survival (OS aHR, 0.47; 95% CI, 0.24–0.94; DFS aHR, 0.45; 95% CI, 0.23–0.85). For the additional metrics with face validity, elective neck dissection with 18 lymph nodes or more was associated with improved DFS (aHR, 0.36; 95% CI, 0.14–0.99). Multidisciplinary evaluation for all patients remained associated with improved survival (OS aHR, 0.51; 95% CI, 0.29–0.88; DFS aHR, 0.50; 95% CI, 0.32–0.80).
Table 3.
Adjusted Analysis of Individual Quality Metrics and Survival
| Quality Metric | aHR (95% CI)a | ||
|---|---|---|---|
| OS | DSS | DFS | |
| AHNS Quality Metrics | |||
| Pretreatment | |||
| Complete head and neck examination | NAb | NA | NA |
| Laryngealexamination | NA | NA | NA |
| Biopsy | NA | NA | NA |
| Imaging of primary | 0.64 (0.08-4.97) | NA | 1.04 (0.14-7.88) |
| Imaging for regional metastases | 0.97 (0.13-7.32) | NA | 1.55 (0.21-11.5) |
| Chest imaging | 1.13 (0.44-2.92) | 1.04 (0.25-4.44) | 0.60 (0.28-1.29) |
| Documentation of TNM staging | 1.32 (0.59-2.95) | 1.25 (0.43-3.65) | 1.30 (0.64-2.64) |
| Tobacco cessation counseling | 1.05 (0.48-2.27) | 1.37 (0.55-3.45) | 0.69 (0.33-1.48) |
| Prelaryngectomy counseling | 0.78 (0.26-2.31) | 0.80 (0.22-2.85) | 0.48 (0.17-1.39) |
| Multidisciplinary evaluation (stage cT3-4 or ≥1 LN) | 0.47 (0.24-0.94)c | 0.61 (0.25-1.47) | 0.45 (0.23-0.85)c |
| Treatment | |||
| Referraladjuvant radiation | 1.85 (0.82-4.18) | 2.38 (0.79-7.16) | 1.24 (0.59-2.61) |
| Referraladjuvant chemoradiation | 1.13 (0.50-2.53) | 1.22 (0.50-2.97) | 0.88 (0.41-1.91) |
| Surveillance | |||
| Thyroid function testing | 0.46 (0.21-1.00) | 0.40 (0.16-1.01) | 0.66 (0.31-1.38) |
| Regular follow-up | 1.40 (0.44-4.42) | 1.02 (0.28-3.67) | 1.39 (0.47-4.13) |
| NCCN Guidelines | |||
| Pretreatment | |||
| Complete head and neck examination | NA | NA | NA |
| Biopsy | NA | NA | NA |
| Imaging of primary and neck | 0.97 (0.13-7.32) | NA | 1.55 (0.21-11.5) |
| Examination with patient under anesthesia | NA | NA | NA |
| Tobacco cessation counseling | 1.05 (0.48-2.27) | 1.37 (0.55-3.45) | 0.69 (0.33-1.48) |
| Treatment | |||
| Referralfor adjuvant radiation | 1.85 (0.82-4.18) | 2.38 (0.79-7.16) | 1.24 (0.59-2.61) |
| Referral adjuvant chemoradiation | 1.13 (0.50-2.53) | 1.22 (0.50-2.97) | 0.88 (0.41-1.91) |
| Start of adjuvant therapy ≤6 wk | 0.99 (0.47-2.09) | 0.79 (0.34-1.86) | 1.22 (0.61-2.46) |
| Surveillance | |||
| Thyroid function testing | 0.46 (0.21-1.00) | 0.40 (0.16-1.01) | 0.66 (0.31-1.38) |
| Posttreatment imaging | 0.94 (0.45-1.94) | 0.74 (0.30-1.80) | 0.88 (0.46-1.69) |
| Follow-up (NCCN schedule) | 0.86 (0.51-1.45) | 1.06 (0.54-2.07) | 0.89 (0.57-1.38) |
| Additional Quality Metrics With Face Validity | |||
| Pretreatment | |||
| Referralto clinic visit ≤14 d | 1.72 (0.53-5.65) | 1.52 (0.35-6.71) | 1.83 (0.66-5.10) |
| Review of outside pathologist | 0.97 (0.22-4.38) | 1.07 (0.13-8.96) | 1.20 (0.28-5.18) |
| Pulmonary function tests | 2.15 (0.93-5.01) | 3.97 (0.91-17.5) | 1.48 (0.72-3.03) |
| Pretreatment dental evaluation | 1.10 (0.46-2.66) | 1.25 (0.51-3.10) | 0.87 (0.38-1.9) |
| Multidisciplinary evaluation (all patients) | 0.51 (0.29-0.88)c | 0.54 (0.26-1.14) | 0.50 (0.32-0.80)c |
| Treatment | |||
| Clinic to surgery ≤21 d | 1.01 (0.62-1.64) | 1.10 (0.59-2.04) | 1.14 (0.76-1.72) |
| Initialmargin negative resection | 0.61 (0.32-1.17) | 0.58 (0.27-1.24) | 0.66 (0.36-1.19) |
| Elective NDwith ≥18 LNs | 0.69 (0.22-2.14) | 2.26 (0.35-14.8) | 0.36 (0.14-0.99)c |
| pTNM stage documented | 0.66 (0.36-1.21) | 0.62 (0.26-1.45) | 0.72 (0.43-1.21) |
| Margin status documented | 0.85 (0.53-1.36) | 1.06 (0.57-1.96) | 0.97 (0.64-1.47) |
| No unplanned surgery ≤14 d | 0.98 (0.44-2.18) | 1.19 (0.41-3.41) | 0.65 (0.33-1.27) |
| No unplanned 30-d readmission | 2.30 (0.83-6.38) | 3.20 (0.75-13.6) | 1.11 (0.57-2.18) |
| Multidisciplinary follow-up | 1.40 (0.44-4.42) | 1.02 (0.28-3.67) | 1.39 (0.47-4.13) |
Abbreviations: AHNS, American Head and Neck Society; aHR, adjusted hazard ratio; DFS, disease-free survival; DSS, disease-specific survival; HR, hazard ratio; LN, lymph node; NA, not applicable; NCCN, National Comprehensive Cancer Network; ND, neck dissection; OS, overall survival.
Adjusted for pT stage, pN stage, extracapsular spread, final margin status, and Adult Comorbidity Evaluation 27 index comorbidity score.15 Final margin status was not used to adjust for the metric of initial margin-negative resection.
Metrics for which there were no events in the noncompliance group cannot be evaluated to calculate an aHR of survival.
Denotes variables significantly associated with improved survival after adjustment.
Discussion
In this study that examined the association between compliance with quality metrics and survival in surgically treated patients with laryngeal SCC, we found no consistent correlation between increasing levels of compliance with quality metrics and improved survival. Differences in survival did exist between 100% adherence and a lesser level of compliance for AHNS and NCCN metrics. However, no consistent association was found between compliance levels and survival that recapitulate a dose-response relationship.
Association of Individual Quality Metrics and Improved Survival
One major finding of the study is that the only quality metric consistently related to improved survival was multidisciplinary evaluation via consultation or tumor board presentation. Compliance with this metric was associated with improved survival on unadjusted and adjusted analysis. This association was found in 2 different sets of evaluable patients (denominators): all patients (the evaluable group for the institutional metric) and in patients with advanced T-stage or nodal disease (the evaluable group for the AHNS metric). A prospective study20 on the effect of multidisciplinary tumor board on the treatment of patients with head and neck cancer found a change in diagnosis or treatment in 32 of 120 patients (26.7%) and an escalation or modality shift in care in 17 of 84 patients (20.2%). In other studies,13,21 multidisciplinary tumor board evaluation for patients with locally advanced head and neck cancer was associated with favorable oncologic outcomes,21 and congruence between multidisciplinary treatment planning conference recommendations and actual treatment provided conferred a survival benefit in a heterogeneous cohort of patients with head and neck cancer.13 A prior study12 that evaluated quality metrics for surgically treated oral cavity SCC found no association between multidisciplinary evaluation and survival. Oral cavity SCC is managed almost exclusively with up-front surgery, suggesting that multidisciplinary evaluation may be more beneficial for planning optimal therapy in the setting of 2 or more alternative treatment options, particularly when decision making is complex and multifactorial.
Need for Better Quality Metrics
Another major finding of this study is that there is a need for better quality metrics for surgically treated laryngeal SCC. For the AHNS quality metrics and the NCCN guidelines, increasing levels of compliance were not consistently associated with improved survival on unadjusted or adjusted analysis.
In addition, none of the treatment-related AHNS metrics or the NCCN guidelines are related to the quality of the surgery itself.5,16 Two quality metrics with face validity evaluated in this study that are related to the quality of surgery have promise: elective neck dissection with lymph node yield of 18 or more and negative-margin resection at the time of initial surgery. In oral cavity SCC12,17,22 and a heterogeneous group of cancers of head and neck sites,23 lymph node yield of 18 or more during elective neck dissection was associated with improved survival. In this study, lymph node yield of 18 or more during elective neck dissection was associated with improved DFS on multivariable analysis. A negative-margin resection at the time of initial surgery was associated with improved OS, DSS, and DFS on univariable analysis, and there was a strong trend toward improved survival on the multivariable analysis. Both of these metrics are more closely linked to the quality of the surgery performed and warrant further study as potential quality metrics for surgically treated laryngeal SCC.
Site-Specific Metrics for Head and Neck Cancer?
This study also raises the possibility that quality metrics for head and neck cancer may be site specific. The AHNS used separate metrics for oral cavity and laryngeal SCC.5 Previous work12 at our institution identified that for surgically treated oral cavity SCC, 4 individual quality metrics (elective neck dissection with 18 or more lymph nodes, no unplanned surgery within 14 days, no unplanned 30-day readmissions, and referral for adjuvant therapy if pathologic stage III or IV disease) were associated with improved survival individually and as a group of metrics (clinical care signature). None of these individual metrics were consistently associated with improved survival in patients with surgically treated laryngeal SCC, although elective neck dissection with 18 or more lymph nodes was associated with improved DFS on multivariable analysis. Conversely, multidisciplinary evaluation was consistently and significantly associated with improved survival in patients with surgically treated laryngeal SCC but not in oral cavity cancer. These studies are limited by being small and single-institution retrospective cohort studies. These data serve as hypothesis-generating data that head and neck quality metrics may be site specific. Further multi-institutional collaboration will be required to test this hypothesis.
Limitations
This study has a number of limitations. Its retrospective nature is limited by the accuracy of the medical record. It is a single-institution study, so the generalizability of the results are unknown. The NCCN guidelines evolved throughout the study period, and some patients were treated before the publication of the 2009 AHNS guidelines. It is possible that compliance with some of the metrics assessed in this study are truly associated with improved survival, but this association was not captured because the study was underpowered to detect this association. Future multi-institutional studies with a larger number of patients would be necessary to confirm these findings.
Conclusions
This study identified that the only significant process-related quality metric correlated with improved survival in patients with surgically treated laryngeal SCC is pretreatment multidisciplinary evaluation. Elective neck dissection with lymph node yield of 18 or more and initial negative-margin resection are metrics that warrant further investigation. Increasing levels of compliance with quality metrics described by the AHNS and within the NCCN guidelines are not associated with improved survival. Future multi-institutional collaboration will be required to validate these findings, develop better quality metrics, and evaluate whether quality metrics for head and neck cancer are site specific.
Supplementary Material
Key Points.
Question
Is adherence to quality metrics for patients with laryngeal squamous cell carcinoma associated with improved survival?
Findings
In this cohort study of 243 patients, no association was found between increasing levels of compliance with American Head and Neck Society or National Comprehensive Cancer Network metrics and improved survival. Process metrics associated with improved survival were multidisciplinary evaluation and elective neck dissection yield of 18 lymph nodes or more.
Meaning
When considering survival as an outcome, development of better quality metrics for the treatment of laryngeal cancer appears necessary, although future studies will be required to validate these findings and define meaningful metrics that predict survival or value-based outcomes.
Acknowledgments
Funding/Support: This research was funded in part by the P30 Research Center for Auditory and Vestibular Studies and grant P30DC04665 from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health.
Role of the Funder/Sponsor: The funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
Footnotes
Author Contributions: Drs Graboyes and Nussenbaum had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Graboyes, Kallogjeri, Nussenbaum.
Acquisition, analysis, or interpretation of data: All authors.
Drafting of the manuscript: Graboyes, Nussenbaum. Critical revision of the manuscript for important intellectual content: All authors.
Statistical analysis: Graboyes, Townsend, Kallogjeri, Piccirillo.
Administrative, technical, or material support: Nussenbaum.
Study supervision: Nussenbaum.
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Kallogjeri reported owning stock in and serving as a statistical consultant for PotentiaSystems; however, there is no conflict of interest relevant to the work reported on in the this article. No other disclosures were reported.
Previous Presentation: This study was presented at the American Head & Neck Society Ninth International Conference on Head and Neck Cancer; July 19, 2016; Seattle, Washington.
Disclaimer: Dr Piccirillo is the editor and Dr Kallogjeri is the statistics editor of JAMA Otolaryngology–Head & Neck Surgery. Neither was involved in the editorial evaluation or decision to accept this manuscript for publication.
Additional Contributions: The following additional members of the multidisciplinary head and neck cancer team helped develop the potential quality metrics: Douglas Adkins, MD, Jason Diaz, MD, Hiram Gay, MD, Wade Thorstad, MD, and Tanya Wildes, MD (all with the Washington University School of Medicine).
Contributor Information
Evan M. Graboyes, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St Louis, Missouri.
Melanie E. Townsend, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St Louis, Missouri.
Dorina Kallogjeri, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St Louis, Missouri.
Jay F. Piccirillo, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St Louis, Missouri.
Brian Nussenbaum, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St Louis, Missouri.
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