Abstract
The overwhelming majority of head and neck cancers and related deaths occur in low- and middle-income countries, which have challenges related to burden of disease versus access to care. Yet the additional health care burden of the COVID-19 pandemic has also impacted access to care for patients with head and neck cancer in the United States. This article focuses on challenges and innovation in prioritizing head and neck cancer care in Sub-Saharan Africa, the Indian experience of value-added head and neck cancer care in busy and densely populated regions, and strategies to optimize the management of head and neck cancer in the United States during the COVID-19 pandemic.
Head and neck cancer is primarily a disease of the high-income world, with substantial challenges related to high burden of disease, late presentation, and poor access to care. Low- and middle-income countries account for 67% of head and neck cancer and 82% of head and neck cancer–related deaths.1 Patients in these countries present with advanced disease; in India, two-thirds of patients present with advanced head and neck cancer,2 and in Cape Town, South Africa, approximately 50% of laryngectomees require emergency tracheostomy.3 Only 5% of patients with cancer in Africa and 3% in South Asia have timely access to safe, affordable surgery,4 and, in 2017, only 24 out of 52 African countries had radiotherapy services.5 Less than 4% of people in India suffering from chronic pain from cancer have access to morphine,6 and many African countries do not dispense opioids.
Although the United States provides highly sophisticated cancer care, the additional health care requirements resulting from the COVID-19 pandemic have revealed deficiencies in the health care system and highlighted inequalities to access to care in the United States, including for patients with head and neck cancer.
This article focuses on challenges and innovation in prioritizing head and neck cancer care in Sub-Saharan Africa (Fagan), the Indian experience of value-added head and neck cancer care in busy and densely populated regions (Noronha), and strategies to optimize the management of head and neck cancer in the United States during the COVID-19 pandemic (Graboyes).
CHALLENGES AND INNOVATION IN PRIORITIZING HEAD AND NECK CANCER CARE IN SUB-SAHARAN AFRICA
Sub-Saharan Africa has more than 1 billion people. Yet it has only 19 fellowship-trained head and neck surgeons, and less than 50% of countries have radiation therapy facilities.5 Even where radiation is available, old technology is often used, and treatment delays can approach a year.7 In addition, access to cytology, histopathology, and specialized radiology services are limited, and many patients cannot afford to pay out of pocket for cancer care. Several innovations have been introduced to address these challenges in Sub-Saharan Africa, and are discussed below.
African Head and Neck Surgery Fellowship Training
Two African head and neck fellowship programs have trained 17 head and neck surgeons from 13 African countries. The University of Cape Town has a 1-year hands-on program modeled on North American fellowships. It is funded by Karl Storz Endoscopy and is currently training its 15th fellow. The Pan-African Academy of Christian Surgeons/Johns Hopkins Fellowship is based in Mbingo Baptist Hospital in Cameroon and has a novel outreach fellowship training model with teaching faculty rotating from North American institutions. In an analysis of whether African fellowships have made a sustainable impact on head and neck cancer care in Sub-Saharan Africa, it was reported that all fellows had returned to their countries; all were doing work in public hospitals and hence were involved in transferring surgical skills to trainees; all of those with local radiation therapy services had established head and neck multidisciplinary teams; and there had been a 335% increase in major head and neck surgeries. The authors concluded that high-volume specialized head and neck surgical training was possible in Africa; that training was appropriate in terms of pathology, types of surgery, and affordability; and that the fellowship model made a sustainable change to head and neck practice in Sub-Saharan Africa by populating it with surgeons and teachers of head and neck surgery, by establishing centers of excellence, by building clinical capacity, and by instituting resource-appropriate management.7
African Head and Neck Society
The African Head and Neck Society (https://afhns.org) was established in 2016 by the first 14 African fellowship-trained head and neck surgeons. Its mission is to improve outcomes of patients with diseases of the head and neck in Africa through prevention, clinical excellence, teaching, training, and research and by promoting the highest professional and ethical standards; to coordinate and advance training and education of those engaged in the treatment of patients with diseases of the head and neck in Africa; and to promote friendship and collaboration among those engaged in the treatment of patients with diseases of the head and neck in Africa. It has since held annual conferences and cadaver dissection surgical courses and ultrasound workshops, has published research papers, has served as a link for international otolaryngology and head and neck societies with Africa, runs the African Head and Neck Society Virtual Tumor Board meetings, and has promulgated the African Head and Neck Society Clinical Practice Guidelines for Head and Neck Cancers in Developing Countries and Limited Resource Settings. It is therefore fulfilling a key role in advancing head and neck cancer care and training in Sub-Saharan Africa.
African Head and Neck Society Virtual Tumor Board
With the advent of COVID-19 and development of virtual conferencing software, the African Head and Neck Society introduced a monthly virtual tumor board meeting using Zoom in 2020. It is a free, open-access, multidisciplinary meeting at which interesting clinical cases are presented from around Africa. The second meeting was held in association with the American Academy of Otolaryngology–Head and Neck Surgery. It has attracted more than 150 attendees per meeting and illustrates how virtual conferencing has empowered low- and middle-income countries in terms of knowledge dissemination and networking, and has introduced new opportunities for international collaboration and teaching using virtual platforms.
The African Head and Neck Society Clinical Practice Guidelines for Head and Neck Cancers in Developing Countries and Limited Resource Settings
International head and neck cancer guidelines may be unhelpful, inappropriate, or even harmful when applied in resource-constrained settings, when special investigations, radiotherapy, and complex surgery might not be available or be unaffordable, when management of sequelae of treatment such as hypothyroidism, renal failure, and dysphagia are inadequate, or when cancer surveillance is not possible. The African Head and Neck Society Clinical Practice Guidelines for Head and Neck Cancers (https://afhns.org or https://developingworldheadandneckcancerguidelines.com/) seek to optimize cancer care by tailoring investigations and treatment according to resources available to the individual patient and the treatment center. It reflects the expert opinion of members of the African Head and Neck Society, as well as selected affluent-world surgeons and oncologists. It is directed at local surgeons and oncologists, as well as those undertaking surgical outreach to low- and middle-income countries.
The “Global South” is best qualified to write its own guidelines, as it understands the challenges, constraints, and possibilities of cancer care in limited-resource settings. The promulgation of these guidelines also reflects the Global South’s taking ownership, leadership, and responsibility for head and neck cancer practice in low- and middle-income countries. Guidelines have thus far been released for cancers of the thyroid, salivary glands, oral cavity, oropharynx, hypopharynx, and larynx, with guidelines pending for nasopharynx and the unknown primary. In the initial 22 months, the guidelines have been accessed by more than 8,300 visitors with more than 43,000 page views, with the top 10 countries (listed in order of highest to lowest number of visits) being South Africa, the United States, Kenya, India, Nigeria, the United Kingdom, Turkey, France, Italy, and Uganda.
Open Access Atlas of Otolaryngology, Head and Neck Operative Surgery
Accessing educational and scientific material is key to improving head and neck care in low- and middle-income countries. Yet many trainees, practitioners, and researchers in Sub-Saharan Africa cannot afford textbooks and pay-to-view journals, and the content of modern journals and textbooks is often inappropriate for resource-constrained settings. The Open Access Atlas of Otolaryngology, Head and Neck Operative Surgery (www.entdev.uct.ac.za/guides/open-access-atlas-of-otolaryngology-head-neck-operative-surgery/) is a free, open-access surgical atlas self-published by Johannes J. Fagan in Cape Town, South Africa. More than 100 authors from more than 20 countries have contributed, and volunteers have translated chapters into Portuguese, Spanish, and French. The senior authors are mostly international leaders who volunteered to contribute. It provides detailed descriptions of surgical procedures. It includes surgical cancer procedures no longer performed in high-income countries, such as laryngofissure and hemi-laryngectomy for early laryngeal cancer, that would not be included in modern textbooks. Being in electronic format, chapters are very detailed, with numerous photographs and video clips. The textbook received the Open Education Consortium 2017 Award for Open Education Excellence, a tribute to its contributors (www.oeconsortium.org/projects/open-education-awards-for-excellence/2017-oe-award-winnersoer-categories/).
Head and Neck Cancer Staging
How head and neck cancers are investigated and managed in high-income compared with low- and middle-income countries is increasingly divergent because of technological, financial, and infrastructural differences. Therefore, having a universal staging system is becoming ever more difficult to achieve. Although anatomic site and tumor extent remain central to defining cancer prognosis and staging, the American Joint Committee on Cancer and Union for International Cancer Control have been incorporating an increasing number of nonanatomic prognostic factors into stage groupings. In the eighth edition of the American Joint Committee on Cancer Cancer Staging Manual, p16 status was included in staging of oropharyngeal cancer. Yet, for 16 out of 17 fellowship-trained head and neck surgeons in 13 Sub-Saharan African countries, p16 testing was not routinely available for their patients with oropharyngeal cancer because of unavailability or unaffordability of the laboratory test.8 Another challenge that staging bodies must consider is the diversity of the type and quality of therapeutic interventions in high-income versus low- and middle-income countries that might affect outcomes and prognosis. In 2019, only 24 out of 52 African countries had radiotherapy facilities, and treatment could have been delayed for up to 46 weeks.7 Certain chemotherapy drugs and most targeted agents are also not available to patients in these countries. Such diversity in management might, for instance, invalidate the favorable prognosis for advanced p16+ oropharyngeal cancer reflected in the current staging in such resource-constrained settings. Although the American Joint Committee on Cancer/Union for International Cancer Control should continue to refine staging systems that best reflect prognosis by incorporating non-anatomical factors, anatomically based staging systems must be retained to serve the needs of resource-constrained settings. A model that may be considered is that of a staging system that considers available diagnostic and therapeutic resources, as has been done in the African Head and Neck Society Clinical Treatment Guidelines for Head and Neck Cancer. If the American Joint Committee on Cancer and Union for International Cancer Control do not develop resource-appropriate staging, it would reduce their global relevance and disadvantage most of the world’s patients with cancer. This may be an opportunity for the Global South to promulgate its own resource-appropriate staging guidelines.
CHOOSING WISELY: VALUE-ADDED HEAD AND NECK CANCER CARE IN DENSELY POPULATED AND RESOURCE-CONSTRAINED REGIONS—THE INDIAN EXPERIENCE
Head and neck cancer constitutes between 30% and 40% of cancers in India.9 Oral cavity cancer is the most common cancer in Indian men10; one in every 60 Indians will develop cancer of the oral cavity or pharynx during their lifetime.11 The causative factors for head and neck squamous cell carcinoma in India include smokeless tobacco, smoking, and alcohol; HPV plays a less important etiologic role.9
Curative Setting
Resectable oral cancer
Patients with resectable oral cancer, both localized and locally advanced, are best treated with surgical resection, followed by adjuvant therapy based on various risk factors.12 In most centers in India, micro-vascular free tissue transfer reconstructive surgery is not available, and either primary closure or pedicled flaps are used. Such surgeries can be performed more quickly and more cheaply, thereby facilitating treatment of more patients. The outcomes of patients thus treated match those reported in the global literature, suggesting that even in the absence of a dedicated reconstructive surgical team, good oncologic outcomes are possible.13
Until recently, the management of the N0 neck with early-stage oral cancer was controversial. Options range from elective neck dissection to addressing only the oral primary and performing neck dissection for recurrence.14 In India, watchful waiting is challenging, as patients often travel long distances, and compliance with regular follow-up and radiologic surveillance is poor; this may lead to unsalvageable recurrences. Hence, elective neck dissection is commonly performed. This practice was supported by the N0 trial, which proved that patients with early-stage clinically node-negative oral cancer treated with elective neck dissection had an improved disease-free and overall survival as compared with patients managed with watchful waiting.15
Patients with tumors at high risk of recurrence are treated with adjuvant chemoradiotherapy. The standard of care from the landmark trials was high-dose cisplatin administered at 100 mg/m2 once every 3 weeks during radiation. However, this regimen was difficult to administer in the Indian setting because of patient-related issues (lower body weight, poorer nutrition, and higher toxicity) and logistic (hospitalization and intravenous hydration) and infrastructure issues (challenges with supportive care). Low-dose cisplatin at 30–40 mg/m2 administered once a week during radiation was widely introduced even in the absence of level 1 evidence.16 A subsequent randomized controlled trial comparing high-dose once-every-3-weeks cisplatin to lower-dose once-a-week cisplatin concurrently with radical radiotherapy taught us several important things.17 First, it is possible to administer high-dose cisplatin in the Indian setting, despite the challenges. Second, high-dose cisplatin led to better locoregional control than weekly cisplatin and should therefore continue as the standard of care. However, overall survival (which was not the primary endpoint of the study) was similar between the two cisplatin schedules, suggesting that low-dose weekly cisplatin could possibly be used, with less toxicity, supportive care, and resource utilization, without compromising overall survival. Recent data from Japan suggest that outcomes are similar between the once-a-week and once-every-3-weeks cisplatin schedules when combined with radical radiotherapy.18
Technically unresectable oral cancer
A large proportion of our patients present with bulky, extensive oral cancers, which, although localized, are not easily resectable with negative margins. These include buccal mucosa primaries with edema extending up to the zygoma and tumor extension to the infratemporal fossa, primaries of the anterior two-thirds of the tongue extending to the hyoid or posteriorly to the vallecula, or cancers extensively infiltrating skin. Such patients are usually treated conservatively with radiotherapy or concurrent chemoradiotherapy or palliative chemotherapy and have dismal outcomes, with median survival between 2 and 12 months. Induction chemotherapy in an attempt to downstage a tumor, followed by resection, is an exciting approach.19 In a cohort of 721 patients with technically unresectable oral cancers, we found that with this approach, 43% were able to undergo surgery. The 2-year locoregional control of the entire cohort of patients with technically unresectable oral cancer treated with induction chemotherapy was 21%. Patients who could undergo resection had better outcomes: 2-year locoregional control of 32%, 2-year overall survival of 47%, and a median overall survival of 19.6 months (95% CI, 9.6–25.2) as compared with 15%, 20%, and 8.2 months (95% CI, 7.6–8.6), respectively (p = .0001).20
Oropharyngeal cancer
HPV positivity with oropharyngeal cancer in India is approximately 23%.21 The availability of robotic surgery is limited. The primary treatment is transoral or open resection or definitive radiotherapy or concurrent chemoradiotherapy depending on disease stage.22 Patients with stage II and higher disease benefit from the addition of concurrent cisplatin. In a randomized phase II trial, 40 mg/m2 of cisplatin once a week concurrently with radiotherapy improved oncologic outcomes; the 3-year overall survival and the median overall survival were 62%/not reached versus 42%/27 months (95% CI, 15.2–36.8) in patients treated with concurrent chemoradiotherapy versus radical radiotherapy, respectively.23 This is a feasible approach in the Indian setting.
Treatment intensification can improve outcomes for patients with HPV-negative oropharyngeal cancer, by addition of the EGFR (epidermal growth factor receptor) antibody nimotuzumab to concurrent cisplatin-based chemoradiotherapy.24 A subset analysis of a phase III randomized controlled trial showed that nimotuzumab added to weekly cisplatin-based chemoradiotherapy greatly improved locoregional control and progression-free and overall survival. There was an absolute improvement in the 2-year locoregional control of 19%, with 2-year progression-free survival of 26% and 2-year overall survival of 19%. In this trial, 87% of patients were treated with conventional radiation, further emphasizing that oncologic outcomes are not compromised by forgoing intensity-modulated radiotherapy.25
Hypopharyngeal/laryngeal cancer
A retrospective analysis of 501 patients with locally advanced hypopharyngeal cancer treated with radical radiotherapy or concurrent chemoradiotherapy (30 mg/m2 of cisplatin once a week) reported a 3-year locoregional control rate of 47.1% and 3-year disease-free survival of 40.9%. As radiotherapy machines are widely available and therefore easily accessible to many Indian patients, this is the usual practice in India.26 For patients with locally advanced laryngeal tumors, especially without cartilage involvement, induction chemotherapy can result in laryngeal preservation in up to 70% of patients.27
Precision-based radiotherapy
Both in definitive and adjuvant settings, multiple studies from our institution that used conventional radiotherapy for most patients had similar oncologic outcomes to those reported in international trials.17,25,28 Thus, conventional radiation remains an important option for our patients and permits treatment of patients in remote areas where teletherapy machines exist. In 2019, there were approximately 545 teletherapy machines in India for an estimated population of 1.35 billion.29 However, increasing access to therapy and the ability to treat more patients should not come at the cost of poorer oncologic outcomes. Several randomized clinical trials have reported that conventional three-dimensional conformal radiation led to similar locoregional control and survival compared with intensity-modulated radiation therapy, albeit with an increased risk of xerostomia.30–32
Palliative Setting
Platinum-sensitive disease
Systemic therapy is the standard of care for patients with unresectable recurrent or metastatic disease. Two approaches that have been shown to prolong survival include the addition of cetuximab to intravenous chemotherapy (i.e., the EXTREME regimen), and immunotherapy, either combined with intravenous chemotherapy or as a single agent, based on the tumor PD-L1 expression. Unfortunately, both of these treatment approaches are unaffordable to 97% of the Indian population. Thus, almost all patients are treated with either intravenous chemotherapy or oral metronomic chemotherapy.
Metronomic chemotherapy is chemotherapy that is administered at low doses on a continuous basis, without breaks. Low-cost oral metronomic chemotherapy consisting of 15 mg/m2 of oral methotrexate once a week and 200 mg of celecoxib twice daily is widely used in India in the palliative setting. A retrospective analysis of 340 patients treated with oral metronomic chemotherapy reported a median overall survival of 5.1 months (95% CI, 4.6–5.6).32 A randomized phase II study revealed that an oral metronomic chemotherapy regimen led to a considerable prolongation of median progression-free and overall survival compared with 75 mg/m2 of intravenous cisplatin once in 3 weeks, and with lower toxicities.33 We recently reported the results of our phase III noninferiority trial, in which 422 patients with relapsed, recurrent, or newly diagnosed head and neck squamous cell carcinomas were randomly assigned to oral metronomic chemotherapy or intravenous cisplatin. Patients who received oral metronomic chemotherapy had improvement in oncologic outcomes and quality of life. The median overall survival of patients in the oral metronomic chemotherapy arm was 7.5 months (95% CI, 4.6–12.6) versus 6.2 months (95% CI, 3.2–9.6) for patients who received intravenous cisplatin. There were fewer adverse events for patients who received oral metronomic chemotherapy and an improvement in global health-related quality of life.34
A phase II study of 114 patients with newly diagnosed locally advanced unresectable incurable nonmetastatic disease evaluated palliative radiotherapy (20 Gy in 5 fractions) compared with palliative radiotherapy with 6 mg/m2 of daily cisplatin, with reassessment at 4 weeks and completion of radical chemoradiotherapy (70 Gy of a radiobiologically equivalent dose; 40 mg/m2 of cisplatin once a week added in the chemoradiotherapy arm) for patients who had a partial response. Compared with palliative radiation, patients who received palliative chemoradiotherapy had higher conversion to radical chemoradiotherapy (46.4% vs. 25.5%), prolongation of median survival (10.1 vs. 5.9 months), and improved symptoms and quality of life.35
Platinum-refractory disease
Patients with disease that relapses within 3 to 6 months of receiving cisplatin-based therapy have very poor outcomes. The standard of care is immunotherapy, which is out of reach for 97% to 99% of Indian patients. Most patients therefore receive various regimens of intravenous or oral metronomic chemotherapy. A retrospective analysis of oral metronomic chemotherapy of 100 patients with platinum-refractory oral cancers revealed only limited efficacy, with median overall survival of 3.6 months (95% CI, 2.8–4.4).36 This led us to explore the use of triple oral metronomic chemotherapy (i.e., addition of erlotinib to the double oral regimen of 9 mg/m2 of methotrexate weekly and celecoxib daily). A phase I/II study of 91 patients with platinum-refractory oral cancer showed promising efficacy from the triple oral metronomic chemotherapy regimen; 6-month progression-free survival and 6-month overall survival were 34.5% (95% CI, 23.9–45.3%) and 61.2% (95% CI, 49.2–67.8%), respectively. The median progression-free survival and overall survival were 4.6 months (95% CI, 4.1–5.3) and 7.17 months (95% CI, 5.93–8.10), respectively.37 Although the data are preliminary, this represents an emerging option for our patients with platinum-refractory oral cancers. An outline of the management of oral cancers is provided in Fig. 1.
FIGURE 1.

An Algorithm Outlining the Suggested Management of Oral Cancers, Based on Resectability and Financial Constraint Considerations Abbreviations: +ve, positive; MTHS, months; CHEMO, chemotherapy; RT, radiotherapy; wk, week; +/−, with or without; OMCT, oral metronomic chemotherapy; CPS, combined positive score; EXTREME, cetuximab plus combination chemotherapy; PEMBRO, pembrolizumab; IV, intravenous; BSC, best supportive care.
*Preferred for patients with limited financial resources.
Adjunctive Treatments
The primary expectation of patients treated in the palliative setting is prolongation of life in 41.0%, whereas 58.5% of the patients rate symptom relief as either the primary goal or at least of equal importance.38 Almost 45% of patients experience high distress levels at the start of palliative intent therapy. Counseling by the clinician leads to resolution of distress in 59% of patients; an additional referral to a psychologist leads to resolution of distress in 75%.39 To maximize quality of life for patients, close attention must be paid to various supportive care measures, including analgesia, management of mucositis, dysphagia, nutritional support, and psychological counseling.
DRIVERS OF OUTCOMES AND STRATEGIES TO OPTIMIZE CARE FOR PATIENTS WITH HEAD AND NECK CANCER IN THE UNITED STATES DURING THE COVID-19 PANDEMIC
Responding to the COVID-19 pandemic in the United States necessitated that health systems urgently reallocate health care resources such as hospital beds, ventilators, health care workers, and personal protective equipment toward the management of COVID-19 and away from other clinical activities.40 Concurrently, health systems instituted new infection control measures to minimize transmission of the severe acute respiratory syndrome coronavirus 2, which were of particular relevance to head and neck oncology providers because of the risk of acquiring COVID-19 from aerosols generated during a physical examination or procedure of the upper aerodigestive tract.41 As a result, health systems saw a precipitous decrease in their capacity to care for patients with head and neck cancer and substantial reductions in head and neck cancer–related clinical activity.42,43
Against the backdrop of hitherto unforeseen resource constraints and the potential for viral transmission, novel methods of head and neck cancer service delivery needed to be developed. Frameworks, protocols, and consensus statements from leading academic centers44–49 and professional organizations provided recommendations for head and neck cancer surgical,50 radiation,51,52 and medical oncologic care.53 Although diverse in scope, these recommendations shared a common thread of attempting to develop novel care delivery strategies that recognized the oncologic importance of delivering timely treatment that adheres to evidence-based standards of care amid new capacity limitations. The following sections discuss the role of timely treatment and guideline adherence as drivers of outcomes for patients with head and neck cancer in the United States, examine strategies to optimize head and neck cancer care during the COVID-19 pandemic, and explore the ways in which COVID-19–associated care delivery changes may exacerbate existing disparities in access to care and outcomes for patients with head and neck cancer in the United States.
Drivers of Oncologic Outcomes: Delivery of Timely Head and Neck Cancer Care
Because of the robust and consistent association between treatment delays and worse oncologic outcomes for patients with head and neck cancer,54 strategies to optimize head and neck cancer care delivery in spite of COVID-19 in the United States attempted to ensure timely treatment despite resource constraints and nosocomial infection risks. Across a range of studies, delays in treatment initiation are associated with stage migration,55 higher rates or recurrence,56 and worse overall survival.57 Although precise threshold values for delayed treatment initiation vary,54 a number of studies suggest that mortality increases precipitously for delays beyond 60 days.56,57 The association of treatment delay with survival also varies by stage, with an increased hazard of mortality for stages I/II head and neck cancer relative to stages III/IV.58 Other intervals of timely head and neck cancer care also have a strong and consistent association with recurrence and survival, including initiation of postoperative radiation therapy within 6 weeks of surgery,54,59,60 the duration of radiation therapy,60–62 and treatment package time.63,64 The oncologic impact of treatment delays for patients with head and neck cancer is extensive; the excess hazard conferred by delayed initiation of postoperative radiation therapy or prolonged radiation duration are comparable in magnitude to the mortality risk associated with adverse features such as positive margins or extranodal extension.60
Drivers of Oncologic Outcomes: Delivery of National Comprehensive Cancer Network Guideline-Adherent Treatment
Because of the strong association between the delivery of National Comprehensive Cancer Network guideline-adherent care and oncologic outcomes for patients with head and neck cancer,65,66 novel head and neck cancer care delivery strategies during the COVID-19 pandemic attempted to balance concordance with evidence-based standards with newly limited capacity and viral transmission risk.67 Given the clinical equipoise between surgical and nonsurgical management of certain head and neck subsites/stages, nonsurgical management became the preferred treatment modality. However, adherence to National Comprehensive Cancer Network guidelines to treat oral cavity cancer68,69 and T4a laryngeal cancer70 with a primary surgical approach is associated with improved survival. Other aspects of National Comprehensive Cancer Network guideline-adherent care for patients with surgically treated head and neck cancer that are associated with improved overall survival include negative-margin resection, adjuvant radiation therapy for pT3–4 or N2–3 disease, adjuvant chemoradiation therapy for extranodal extension or positive margins, and initiation of adjuvant therapy within 6 weeks of surgery.59,71,72 Designing new head and neck cancer care delivery systems to reflect these drivers of oncologic outcomes was thus an important consideration in attempts to optimize care delivery during the COVID-19 pandemic.
Drivers of Oncologic Outcomes: Social Determinants of Health
As the COVID-19 pandemic unfolded in the United States, the observed racial/ethnic differences in incidence and outcomes served as a magnifying glass for the stark racial/ethnic disparities in outcomes for patients with head and neck cancer.73 Although the reasons underlying observed racial/ethnic differences in mortality for patients with head and neck cancer are multifactorial, disparities in social determinants of health are major drivers for poor outcomes.73,74 As health systems massively reoriented strategies to deliver timely, guideline-adherent head and neck cancer care, it became imperative to consider how COVID-19–related changes to health care delivery might exacerbate existing racial/ethnic disparities in access to care and worsen oncologic outcomes for racial/ethnic minority patients with head and neck cancer.75
Strategies to Optimize Care: Enhancing Access via Telemedicine
To enhance access to care while minimizing footfall in outpatient clinics, head and neck cancer providers pivoted to direct-to-consumer, telemedicine-based platforms (phone- or video-based) for initial consultations of patients with suspected head and neck cancer and post-treatment follow-up/survivorship care.76 This forward triage strategy allowed for remote assessment and screening of patients with possible head and neck cancer to protect patients, clinicians, and the community from COVID-19. At the start of the pandemic, there was little experience and a lack of data to guide telemedicine-based evaluation for newly diagnosed head and neck cancer.77 Nevertheless, initial reports reflected relatively high uptake of telemedicine-based evaluation and treatment of patients with head and neck cancer,77,78 and it was effective at reducing in-person visits.79 The efficiency of telemedicine can be further enhanced through the use of risk calculators such as the head and neck cancer risk calculator V.2.78 Using patient symptoms to calculate a risk of head and neck cancer, the head and neck cancer risk calculator V.2 allows patients with a low predicted risk of primary or recurrent head and neck cancer to be directly discharged or have in-person appointments deferred, thereby minimizing clinic footfall.78 Despite the publication of practical guides to optimize telemedicine for head and neck cancer,80 challenges remain because of intrinsic limitations of the physical examination, lack of endoscopic evaluation, and inability to perform biopsies.76 In addition, disparities in telemedicine usage for patients with head and neck cancer have been reported, as those who were low-income or on Medicaid or uninsured were more likely to complete a telephone visit in lieu of a video-based visit.81 Nevertheless, it is clear that the COVID-19–inspired shift to telemedicine-based head and neck cancer care delivery will remain in some form long after the COVID-19 pandemic ends.82
Strategies to Optimize Care: Prioritization of Head and Neck Cancer Management
In the setting of an instantaneous and precipitous decrement in resource allocation and capacity, providers and health care systems were forced to make difficult but obligatory decisions regarding prioritization of care for patients with head and neck cancer. Because of the considerable risk of virus transmission during transmucosal aerosol-generating procedures of the upper aerodigestive tract as well as the resource intensity of perioperative care, strategies for prioritizing head and neck cancer management focused particularly on triaging patients for head and neck cancer surgery.44 In general, two triage strategies emerged: (1) general frameworks and (2) prioritization algorithms. General prioritization frameworks were preferred by some because they facilitate case-by-case decision-making and allow for flexibility and the use of clinical judgment,45 whereas others favored prioritization algorithms to minimize the logistical challenges, cognitive burden, and inherent bias associated with case-by-case, framework-based decision-making.83
Numerous frameworks for ethically triaging and prioritizing head and neck cancer care during the COVID-19 pandemic in the United States were developed from leading academic institutions.44–49 These frameworks focused on a number of variables, including the acuity and risk of treatment delay, expected oncologic outcomes, risk of viral transmission during surgery, availability of supportive resources, and safety of health care personnel. To help minimize variability and confusion for providers stemming from the massive number of triage frameworks, an international consensus statement from 35 interprofessional societies was developed to help prioritize surgical care for patients with head and neck cancer. The top five factors to consider for triaging patients with head and neck cancer for surgery (from most to least important) were: (1) risk of cancer progression with delay; (2) COVID-19 status of the patient; (3) oncologic prognosis; (4) availability of operative infrastructure; and (5) effectiveness of and availability of alternative treatment modalities.51
The Surgical Prioritization and Ranking Tool and Navigation Aid for Head and Neck Cancer is a validated, point-based scoring algorithm to prioritize head and neck cancer surgical care based on 15 variables related to the patient, tumor, treatment, resource availability, and wait time factors.83 Surgical Prioritization and Ranking Tool and Navigation Aid for Head and Neck Cancer scores range from −17 to 20, with higher scores representing more urgent prioritization for surgical treatment of head and neck cancer.83 Although the Surgical Prioritization and Ranking Tool and Navigation Aid for Head and Neck Cancer helps prioritize surgical management of head and neck cancer among those diagnosed with head and neck cancer, it does not provide a health care system with guidance for how to prioritize head and neck cancer surgery relative to other surgical procedures. The Medically Necessary, Time-Sensitive scoring system is a surgical scoring system to triage and prioritize surgical cases at the health system level amid the scarce resources of the COVID-19 pandemic, according to 21 variables across three categories (procedure, disease, and patient factors).84 Cumulative Medically Necessary, Time-Sensitive scores range from 21 to 105, with higher scores suggesting poorer perioperative patient outcomes, increased risk of COVID-19 transmission to the health care team, and/or increased hospital resource use.84 Each health system can assign upper and lower thresholds for Medically Necessary, Time-Sensitive scores and adjust them dynamically based on evolving resource availability.
CONCLUSION
The prevalence, etiology, and treatment paradigms for head and neck cancer are variable by region. However, diverse health care delivery systems in Sub-Saharan Africa, India, and the United States (during the COVID-19 pandemic) all face substantial challenges related to high burden of disease, late presentation, and inadequate access to care. Importantly, limitations in capacity and resources constrain head and neck cancer care delivery in all three settings. In Sub-Saharan Africa, the challenges of care delivery are primarily driven by the inadequate number of providers and technology. In India, resource constraints reflect the enormous population and the high incidence of head and neck cancer. During the COVID-19 pandemic in the United States, acute resource reallocation, concurrent with a nosocomial infection risk, resulted in a precipitous decrease in capacity to provide head and neck cancer care.
Although the particular strategies adopted by each health system to deliver head and neck cancer care amid resource constraints are variable, their solutions reflect cross-cutting themes and underlying principles that can facilitate and inform care delivery for patients with head and neck cancer more generally. For example, algorithm-based tools and other objective decision aids were used to prioritize and allocate resources in terms of the type and timing of therapy. In each setting, when it was not feasible to deliver internationally accepted guideline-concordant care based on resource constraints, key stakeholders with knowledge and expertise of the local context adapted guidelines to optimize local fit. Technology-enhanced solutions were also key to improving capacity. Finally, attempts were made in all settings of resource constraint to enhance the multidisciplinary evaluation and treatment of patients with head and neck cancer.
In conclusion, the cross-cutting themes described in this article reflect important strategies for how to make the best of limited resources when caring for patients with head and neck cancer. These initiatives help optimize outcomes for individual patients with head and neck cancer, provide value-driven care at a population-level, and minimize disparities in access and outcomes.
PRACTICAL APPLICATIONS.
There are substantial global and region-specific inequities in head and neck cancer care.
Innovative strategies to prioritize resources and decision trees are presented that optimize and individualize patient care.
The impact of the COVID-19 pandemic on head and neck cancer care and mitigations are discussed.
Footnotes
AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST AND DATA AVAILABILITY STATEMENT
Disclosures provided by the authors and data availability statement (if applicable) are available with this article at DOI https://doi.org/10.1200/EDBK_320923.
REFERENCES
- 1.Patterson RH, Fischman VG, Wasserman I, et al. Global burden of head and neck cancer: economic consequences, health, and the role of surgery. Otolaryngol Head Neck Surg. 2020;162:296–303. [DOI] [PubMed] [Google Scholar]
- 2.Joshi P, Dutta S, Chaturvedi P, et al. Head and neck cancers in developing countries. Rambam Maimonides Med J. 2014;5:e0009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Fagan JJ. Semon Lecture, Royal Society of Medicine: Laryngectomy practice based on personal research. J Laryngol Otol. In press. [DOI] [PubMed] [Google Scholar]
- 4.Alkire BC, Raykar NP, Shrime MG, et al. Global access to surgical care: a modelling study. Lancet Glob Health. 2015;3:e316–e323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Fagan JJ, Zafereo M, Aswani J, et al. Head and neck surgical subspecialty training in Africa: Sustainable models to improve cancer care in developing countries. Head Neck. 2017;39:605–611. [DOI] [PubMed] [Google Scholar]
- 6.Human Rights Watch. Unbearable Pain: India’s Obligation to Ensure Palliative Care. https://www.hrw.org/report/2009/10/28/unbearable-pain/indias-obligation-ensure-palliative-care. October 28, 2009. Accessed March 10, 2021.
- 7.Fagan JJ, Otiti J, Aswani J, et al. African head and neck fellowships: a model for a sustainable impact on head and neck cancer care in developing countries. Head Neck. 2019;41:1824–1829. [DOI] [PubMed] [Google Scholar]
- 8.Fagan JJ, Wetter J, Otiti J, et al. Is AJCC/UICC staging still appropriate for head and neck cancers in developing countries? OTO Open. 2020; 4:2473974X20938313. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Prabhash K, Babu G, Chaturvedi P, et al. Indian clinical practice consensus guidelines for the management of squamous cell carcinoma of head and neck. Indian J Cancer. 2020;57(Suppl):S1–S5. [DOI] [PubMed] [Google Scholar]
- 10.Shetty R, Mathew RT, Vijayakumar M. Incidence and pattern of distribution of cancer in India: a secondary data analysis from six population-based cancer registries. Cancer Res Stat Treat. 2020;3:678–682. [Google Scholar]
- 11.Mathur P, Sathishkumar K, Chaturvedi M, et al. ; ICMR-NCDIR-NCRP Investigator Group. Cancer statistics, 2020: report from National Cancer Registry Programme, India. JCO Glob Oncol. 2020;6:1063–1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Chaturvedi P, Prabhash K, Babu G, et al. Indian clinical practice consensus guidelines for the management of oral cavity cancer. Indian J Cancer. 2020; 57(Suppl):S6–S8. [DOI] [PubMed] [Google Scholar]
- 13.Nair D, Singhvi H, Mair M, et al. Outcomes of surgically treated oral cancer patients at a tertiary cancer center in India. Indian J Cancer. 2017;54:616–620. [DOI] [PubMed] [Google Scholar]
- 14.Kowalski LP, Sanabria A. Elective neck dissection in oral carcinoma: a critical review of the evidence. Acta Otorhinolaryngol Ital. 2007;27:113–117. [PMC free article] [PubMed] [Google Scholar]
- 15.D’Cruz AK, Vaish R, Kapre N, et al. ; Head and Neck Disease Management Group. Elective versus therapeutic neck dissection in node-negative oral cancer. N Engl J Med. 2015;373:521–529. [DOI] [PubMed] [Google Scholar]
- 16.Goyal G, Patil VM, Noronha V, et al. Once-a-week versus once-every-3-weeks cisplatin in patients receiving chemoradiation for locally advanced head-and-neck cancer: a survey of practice in India. Cancer Res Stat Treat. 2018;1:63–67. [Google Scholar]
- 17.Noronha V, Joshi A, Patil VM, et al. Once-a-week versus once-every-3-weeks cisplatin chemoradiation for locally advanced head and neck cancer: a phase III randomized noninferiority trial. J Clin Oncol. 2018;36:1064–1072. [DOI] [PubMed] [Google Scholar]
- 18.Kiyota N, Tahara M, Fujii H, et al. Phase II/III trial of post-operative chemoradiotherapy comparing 3-weekly cisplatin with weekly cisplatin in high-risk patients with squamous cell carcinoma of head and neck (JCOG1008). J Clin Oncol. 2020;38 (15 suppl; abstr 6502). [DOI] [PubMed] [Google Scholar]
- 19.Goel A, Singla A, Prabhash K. Neoadjuvant chemotherapy in oral cancer: current status and future possibilities. Cancer Res Stat Treat. 2020;3:51–59. [Google Scholar]
- 20.Patil VM, Prabhash K, Noronha V, et al. Neoadjuvant chemotherapy followed by surgery in very locally advanced technically unresectable oral cavity cancers. Oral Oncol. 2014;50:1000–1004. [DOI] [PubMed] [Google Scholar]
- 21.Murthy V, Swain M, Teni T, et al. Human papillomavirus/p16 positive head and neck cancer in India: prevalence, clinical impact, and influence of tobacco use. Indian J Cancer. 2016;53:387–393. [DOI] [PubMed] [Google Scholar]
- 22.Prabhash K, Babu G, Chaturvedi P, et al. Indian clinical practice consensus guidelines for the management of oropharyngeal cancer. Indian J Cancer. 2020; 57(Suppl):S12–S15. [DOI] [PubMed] [Google Scholar]
- 23.Sharma A, Mohanti BK, Thakar A, et al. Concomitant chemoradiation versus radical radiotherapy in advanced squamous cell carcinoma of oropharynx and nasopharynx using weekly cisplatin: a phase II randomized trial. Ann Oncol. 2010;21:2272–2277. [DOI] [PubMed] [Google Scholar]
- 24.Noronha V, Patil VM, Joshi A, et al. Nimotuzumab-cisplatin-radiation versus cisplatin-radiation in HPV negative oropharyngeal cancer. Oncotarget. 2020; 11:399–408. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Patil VM, Noronha V, Joshi A, et al. A randomized phase 3 trial comparing nimotuzumab plus cisplatin chemoradiotherapy versus cisplatin chemoradiotherapy alone in locally advanced head and neck cancer. Cancer. 2019;125:3184–3197. [DOI] [PubMed] [Google Scholar]
- 26.Gupta T, Chopra S, Agarwal JP, et al. Squamous cell carcinoma of the hypopharynx: single-institution outcome analysis of a large cohort of patients treated with primary non-surgical approaches. Acta Oncol. 2009;48:541–548. [DOI] [PubMed] [Google Scholar]
- 27.Benson R, Mallick S, Rath GK. Neoadjuvant chemotherapy for larynx preservation: has it lost importance? Indian J Med Paediatr Oncol. 2018;39:227–233. [Google Scholar]
- 28.Laskar SG, Choukar D, Deshpande M, et al. Phase III randomized trial of surgery followed by conventional radiotherapy (5 fr/Wk) (Arm A) vs concurrent chemoradiotherapy (Arm B) vs accelerated radiotherapy (6fr/Wk) (Arm C) in locally advanced, stage III and IV, resectable, squamous cell carcinoma of oral cavity-oral cavity adjuvant therapy (OCAT): final results (NCT00193843). J Clin Oncol. 2016;34 (suppl; abstr 6004). [Google Scholar]
- 29.Munshi A, Ganesh T, Mohanti BK. Radiotherapy in India: history, current scenario and proposed solutions. Indian J Cancer. 2019;56:359–363. [DOI] [PubMed] [Google Scholar]
- 30.Gupta T, Sinha S, Ghosh-Laskar S, et al. Intensity-modulated radiation therapy versus three-dimensional conformal radiotherapy in head and neck squamous cell carcinoma: long-term and mature outcomes of a prospective randomized trial. Radiat Oncol. 2020;15:218. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Ghosh-Laskar S, Yathiraj PH, Dutta D, et al. Prospective randomized controlled trial to compare 3-dimensional conformal radiotherapy to intensity-modulated radiotherapy in head and neck squamous cell carcinoma: long-term results. Head Neck. 2016;38(Suppl 1):E1481–E1487. [DOI] [PubMed] [Google Scholar]
- 32.Patil VM, Noronha V, Joshi A, et al. Retrospective analysis of palliative metronomic chemotherapy in head and neck cancer. Indian J Cancer. 2017;54:25–29. [DOI] [PubMed] [Google Scholar]
- 33.Patil VM, Noronha V, Joshi A, et al. A prospective randomized phase II study comparing metronomic chemotherapy with chemotherapy (single agent cisplatin), in patients with metastatic, relapsed or inoperable squamous cell carcinoma of head and neck. Oral Oncol. 2015;51:279–286. [DOI] [PubMed] [Google Scholar]
- 34.Patil V, Noronha V, Dhumal SB, et al. Low-cost oral metronomic chemotherapy versus intravenous cisplatin in patients with recurrent, metastatic, inoperable head and neck carcinoma: an open-label, parallel-group, non-inferiority, randomised, phase 3 trial. Lancet Glob Health. 2020;8:e1213–e1222. [DOI] [PubMed] [Google Scholar]
- 35.Kumar A, Sharma A, Mohanti BK, et al. A phase 2 randomized study to compare short course palliative radiotherapy with short course concurrent palliative chemotherapy plus radiotherapy in advanced and unresectable head and neck cancer. Radiother Oncol. 2015;117:145–151. [DOI] [PubMed] [Google Scholar]
- 36.Patil VM, Noronha V, Joshi A, et al. Metronomic chemotherapy in platinum-insensitive failures and/or early failures postmultimodality management in oral cancers. Indian J Med Paediatr Oncol. 2015;36:161–165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Patil VM, Noronha V, Joshi A, et al. Phase I/II study of palliative triple metronomic chemotherapy in platinum-refractory/early-failure oral cancer. J Clin Oncol. 2019;37:3032–3041. [DOI] [PubMed] [Google Scholar]
- 38.Patil V, Joshi A, Noronha V, et al. Expectations and preferences for palliative chemotherapy in head and neck cancers patients. Oral Oncol. 2016;63:10–15. [DOI] [PubMed] [Google Scholar]
- 39.Patil V, Noronha V, Joshi A, et al. Distress management in patients with head and neck cancer before start of palliative chemotherapy: a practical approach. J Glob Oncol. 2018;4:1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Emanuel EJ, Persad G, Upshur R, et al. Fair allocation of scarce medical resources in the time of Covid-19. N Engl J Med. 2020;382:2049–2055. [DOI] [PubMed] [Google Scholar]
- 41.Givi B, Schiff BA, Chinn SB, et al. Safety recommendations for evaluation and surgery of the head and neck during the COVID-19 pandemic. JAMA Otolaryngol Head Neck Surg. 2020;146:579–584. [DOI] [PubMed] [Google Scholar]
- 42.Kiong KL, Guo T, Yao CMKL, et al. Changing practice patterns in head and neck oncologic surgery in the early COVID-19 era. Head Neck. 2020;42:1179–1186. [DOI] [PubMed] [Google Scholar]
- 43.Patil VM, Srikanth A, Noronha V, et al. The pattern of care in head-and-neck cancer: comparison between before and during the COVID-19 pandemic. Cancer Res Stat Treat. 2020;3(Suppl S1):7–12. [Google Scholar]
- 44.Topf MC, Shenson JA, Holsinger FC, et al. Framework for prioritizing head and neck surgery during the COVID-19 pandemic. Head Neck. 2020;42:1159–1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Maniakas A, Jozaghi Y, Zafereo ME, et al. ; MD Anderson Head and Neck Surgery Treatment Guidelines Consortium; Consortium members. Head and neck surgical oncology in the time of a pandemic: subsite-specific triage guidelines during the COVID-19 pandemic. Head Neck. 2020;42:1194–1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Ranasinghe V, Mady LJ, Kim S, et al. Major head and neck reconstruction during the COVID-19 pandemic: the University of Pittsburgh approach. Head Neck. 2020;42:1243–1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Weinstein GS, Cohen R, Lin A, et al. Penn Medicine head and neck cancer service line COVID-19 management guidelines. Head Neck. 2020;42:1507–1515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Shuman AG, Campbell BH; AHNS Ethics & Professionalism Service. Ethical framework for head and neck cancer care impacted by COVID-19. Head Neck. 2020;42:1214–1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Patil V, Noronha V, Chaturvedi P, et al. COVID-19 and head and neck cancer treatment. Cancer Res Stat Treat. 2020;3(Suppl S1):15–28. [Google Scholar]
- 50.Mehanna H, Hardman JC, Shenson JA, et al. Recommendations for head and neck surgical oncology practice in a setting of acute severe resource constraint during the COVID-19 pandemic: an international consensus. Lancet Oncol. 2020;21:e350–e359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Thomson DJ, Palma D, Guckenberger M, et al. Practice recommendations for risk-adapted head and neck cancer radiation therapy during the COVID-19 pandemic: an ASTRO-ESTRO consensus statement. Int J Radiat Oncol Biol Phys. 2020;107:618–627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Sinha S, Laskar SG, Mummudi N, et al. Head-and-neck cancer radiotherapy recommendations during the COVID-19 pandemic: adaptations from the Indian subcontinent. Cancer Res Stat Treat. 2020;3:424–426. [Google Scholar]
- 53.European Society of Medical Oncology. ESMO Management and Treatment Adapted Recommendations in the COVID-19 Era: Head and Neck Cancers. https://www.esmo.org/guidelines/cancer-patient-management-during-the-covid-19-pandemic/head-and-neck-cancers-in-the-covid-19-era. Accessed December 30, 2020.
- 54.Graboyes EM, Kompelli AR, Neskey DM, et al. Association of treatment delays with survival for patients with head and neck cancer: a systematic review. JAMA Otolaryngol Head Neck Surg. 2019;145:166–177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Xiao R, Ward MC, Yang K, et al. Increased pathologic upstaging with rising time to treatment initiation for head and neck cancer: a mechanism for increased mortality. Cancer. 2018;124:1400–1414. [DOI] [PubMed] [Google Scholar]
- 56.Liao DZ, Schlecht NF, Rosenblatt G, et al. Association of delayed time to treatment initiation with overall survival and recurrence among patients with head and neck squamous cell carcinoma in an underserved urban population. JAMA Otolaryngol Head Neck Surg. 2019;145:1001–1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Murphy CT, Galloway TJ, Handorf EA, et al. Survival impact of increasing time to treatment initiation for patients with head and neck cancer in the United States. J Clin Oncol. 2016;34:169–178. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Galloway TJ, Kowalski LP, Matos LL, et al. Head and neck surgery recommendations during the COVID-19 pandemic. Lancet Oncol. 2020;21:e416. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Graboyes EM, Garrett-Mayer E, Ellis MA, et al. Effect of time to initiation of postoperative radiation therapy on survival in surgically managed head and neck cancer. Cancer. 2017;123:4841–4850. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60.Ho AS, Kim S, Tighiouart M, et al. Quantitative survival impact of composite treatment delays in head and neck cancer. Cancer. 2018;124:3154–3162. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Mazul AL, Stepan KO, Barrett TF, et al. Duration of radiation therapy is associated with worse survival in head and neck cancer. Oral Oncol. 2020;108:104819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Shaikh T, Handorf EA, Murphy CT, et al. The impact of radiation treatment time on survival in patients with head and neck cancer. Int J Radiat Oncol Biol Phys. 2016;96:967–975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.Tam M, Wu SP, Gerber NK, et al. The impact of adjuvant chemoradiotherapy timing on survival of head and neck cancers. Laryngoscope. 2018;128:2326–2332. [DOI] [PubMed] [Google Scholar]
- 64.Guttmann DM, Kobie J, Grover S, et al. National disparities in treatment package time for resected locally advanced head and neck cancer and impact on overall survival. Head Neck. 2018;40:1147–1155. [DOI] [PubMed] [Google Scholar]
- 65.Gourin CG, Frick KD, Blackford AL, et al. Quality indicators of laryngeal cancer care in the elderly. Laryngoscope. 2014;124:2049–2056. [DOI] [PubMed] [Google Scholar]
- 66.Lewis CM, Nurgalieva Z, Sturgis EM, et al. Improving patient outcomes through multidisciplinary treatment planning conference. Head Neck. 2016;38(Suppl 1): E1820–E1825. [DOI] [PubMed] [Google Scholar]
- 67.Day AT, Sher DJ, Lee RC, et al. Head and neck oncology during the COVID-19 pandemic: reconsidering traditional treatment paradigms in light of new surgical and other multilevel risks. Oral Oncol. 2020;105:104684. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68.Ellis MA, Graboyes EM, Wahlquist AE, et al. Primary surgery vs radiotherapy for early stage oral cavity cancer. Otolaryngol Head Neck Surg. 2018;158:649–659. [DOI] [PubMed] [Google Scholar]
- 69.Spiotto MT, Jefferson G, Wenig B, et al. Differences in survival with surgery and postoperative radiotherapy compared with definitive chemoradiotherapy for oral cavity cancer: a National Cancer Database analysis. JAMA Otolaryngol Head Neck Surg. 2017;143:691–699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70.Grover S, Swisher-McClure S, Mitra N, et al. Total laryngectomy versus larynx preservation for T4a larynx cancer: patterns of care and survival outcomes. Int J Radiat Oncol Biol Phys. 2015;92:594–601. [DOI] [PubMed] [Google Scholar]
- 71.Chen MM, Roman SA, Yarbrough WG, et al. Trends and variations in the use of adjuvant therapy for patients with head and neck cancer. Cancer. 2014; 120:3353–3360. [DOI] [PubMed] [Google Scholar]
- 72.Cramer JD, Speedy SE, Ferris RL, et al. National evaluation of multidisciplinary quality metrics for head and neck cancer. Cancer. 2017;123:4372–4381. [DOI] [PubMed] [Google Scholar]
- 73.Jassal JS, Cramer JD. Explaining racial disparities in surgically treated head and neck cancer. Laryngoscope. In press. [DOI] [PubMed] [Google Scholar]
- 74.Graboyes EM, Ellis MA, Li H, et al. Racial and ethnic disparities in travel for head and neck cancer treatment and the impact of travel distance on survival. Cancer. 2018;124:3181–3191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75.Graboyes E, Cramer J, Balakrishnan K, et al. COVID-19 pandemic and health care disparities in head and neck cancer: scanning the horizon. Head Neck. 2020; 42:1555–1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76.Triantafillou V, Rajasekaran K. A commentary on the challenges of telemedicine for head and neck oncologic patients during COVID-19. Otolaryngol Head Neck Surg. 2020;163:81–82. [DOI] [PubMed] [Google Scholar]
- 77.Kang JJ, Wong RJ, Sherman EJ, et al. The 3 Bs of cancer care amid the COVID-19 pandemic crisis: “be safe, be smart, be kind”- a multidisciplinary approach increasing the use of radiation and embracing telemedicine for head and neck cancer. Cancer. 2020;126:4092–4104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Paleri V, Hardman J, Tikka T, et al. Rapid implementation of an evidence-based remote triaging system for assessment of suspected referrals and patients with head and neck cancer on follow-up after treatment during the COVID-19 pandemic: model for international collaboration. Head Neck. 2020;42:1674–1680. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 79.Kasle DA, Torabi SJ, Savoca EL, et al. Outpatient otolaryngology in the era of COVID-19: a data-driven analysis of practice patterns. Otolaryngol Head Neck Surg. 2020;163:138–144. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Prasad A, Brewster R, Newman JG, et al. Optimizing your telemedicine visit during the COVID-19 pandemic: practice guidelines for patients with head and neck cancer. Head Neck. 2020;42:1317–1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81.Tam S, Wu VF, Williams AM, et al. Disparities in the uptake of telemedicine during the COVID-19 surge in a multidisciplinary head and neck cancer population by patient demographic characteristics and socioeconomic status. JAMA Otolaryngol Head Neck Surg. 2021;147:209–211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82.Khariwala SS, Weinreich HM, McCoul ED, et al. Leveraging COVID-19-inspired changes to advance otolaryngology-here to stay. JAMA Otolaryngol Head Neck Surg. 2020;146:605–607. [DOI] [PubMed] [Google Scholar]
- 83.de Almeida JR, Noel CW, Forner D, et al. Development and validation of a Surgical Prioritization and Ranking Tool and Navigation Aid for Head and Neck Cancer (SPARTAN-HN) in a scarce resource setting: response to the COVID-19 pandemic. Cancer. 2020;126:4895–4904. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Prachand VN, Milner R, Angelos P, et al. Medically necessary, time-sensitive procedures: scoring system to ethically and efficiently manage resource scarcity and provider risk during the COVID-19 pandemic. J Am Coll Surg. 2020;231:281–288. [DOI] [PMC free article] [PubMed] [Google Scholar]
