Access to this full-text is provided by Wiley.
Content available from Laryngoscope Investigative Otolaryngology
This content is subject to copyright. Terms and conditions apply.
REVIEW
An equity-based narrative review of barriers to timely
postoperative radiation therapy for patients with head
and neck squamous cell carcinoma
Elizabeth A. Noyes BS
1
| Ciersten A. Burks MD
2
| Andrew R. Larson MD
2
|
Daniel G. Deschler MD
2
1
Harvard Medical School, Boston,
Massachusetts, USA
2
Department of Otolaryngology–Head and
Neck Surgery, Massachusetts Eye and Ear,
Harvard Medical School, Boston,
Massachusetts, USA
Correspondence
Elizabeth A. Noyes, BS, Harvard Medical
School, 25 Shattuck St., Boston, MA 02215.
Email: elizabeth_noyes@hms.harvard.edu
Abstract
Objectives: The majority of patients with head and neck squamous cell carcinoma
(HNSCC) do not commence postoperative radiation treatment (PORT) within the rec-
ommended 6 weeks. We explore how delayed PORT affects survival outcomes, what
factors are associated with delayed PORT initiation, and what interventions exist to
reduce delays in PORT initiation.
Methods: We conducted a PubMed search to identify articles discussing timely
PORT for HNSCC. We performed a narrative review to assess survival outcomes of
delayed PORT as well as social determinants of health (SDOH) and clinical factors
associated with delayed PORT, using the PROGRESS-Plus health equity framework
to guide our analysis. We reviewed interventions designed to reduce delays in PORT.
Results: Delayed PORT is associated with reduced overall survival. Delays in PORT
disproportionately burden patients of racial/ethnic minority backgrounds, Medicaid
or no insurance, low socioeconomic status, limited access to care, more com-
orbidities, presentation at advanced stages, and those who experience postoperative
complications. Delays in PORT initiation tend to occur during transitions in head and
neck cancer care. Delays in PORT may be reduced by interventions that identify
patients who are most likely to experience delayed PORT, support patients according
to their specific needs and barriers to care, and streamline care and referral
processes.
Conclusions: Both SDOH and clinical factors are associated with delays in timely
PORT. Structural change is needed to reduce health disparities and promote equita-
ble access to care for all. When planning care, providers must consider not only bio-
logical factors but also SDOH to maximize care outcomes.
KEYWORDS
adjunctive radiation, head and neck cancer, health disparities, squamous cell carcinoma,
treatment delay
Received: 14 August 2021 Revised: 15 October 2021 Accepted: 25 October 2021
DOI: 10.1002/lio2.692
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2021 The Authors. Laryngoscope Investigative Otolaryngology published by Wiley Periodicals LLC on behalf of The Triological Society.
1358 Laryngoscope Investigative Otolaryngology. 2021;6:1358–1366.wileyonlinelibrary.com/journal/lio2
1|INTRODUCTION
Postoperative radiation treatment (PORT) is an important adjunct to
improve survival outcomes after surgery for head and neck squamous
cell carcinoma (HNSCC).
1
Current National Comprehensive Cancer
Network (NCCN) guidelines recommend initiating PORT within
6 weeks of surgery, yet the majority of HNSCC patients do not com-
mence PORT within this time frame, a trend that has worsened over
time.
2-4
Disparities in timely PORT initiation may contribute to dispar-
ities in overall survival outcomes among HNSCC patients.
5
Timely PORT is significantly impacted by clinical factors as well as
social determinants of health (SDOH), social and demographic factors
such as socioeconomic status (SES), race and ethnicity, insurance, and
geographic location that impact the development of illness, access to
care, and health outcomes.
2,3,6
Inequity and disadvantage in SDOH
have immense potential to cause harm.
7-10
Given the prevalence of
delays in PORT initiation beyond the recommended 6 weeks, we
explore how delayed PORT affects survival outcomes, what factors
are associated with delayed PORT initiation, and what interventions
exist to reduce delays in PORT initiation.
We employ the PROGRESS-Plus health equity framework to
guide our narrative review of the SDOH that impact the timeliness of
PORT initiation and assessment of interventions to improve timely
delivery of PORT.
11
PROGRESS-Plus is an acronym of factors demon-
strated to stratify health opportunity and outcomes: place of resi-
dence, race/ethnicity/culture/language, occupation, gender/sex,
religion, education, SES, and social capital, as well as other “Plus”fac-
tors, which include personal characteristics associated with discrimi-
nation such as disability, personal relationships such as having
smoking parents, and time-dependent relationships such as postoper-
ative course.
11
This equity-based narrative review method allows us
to explicitly consider and describe the SDOH and clinical factors that
may impact delays in PORT.
2|METHODS
We conducted a PubMed literature search including terms for radio-
therapy, delay, and squamous cell carcinoma of the head and neck
which yielded 179 results. These articles and those in their reference
lists were reviewed and included if they were full-length papers pub-
lished in English in the year 2006 or later in a peer-reviewed journal
in the United States which describe the time interval between sur-
gery and adjuvant PORT. Review of these papers led to the emer-
gence of three thematic questions to address: how does delayed
PORT affect outcomes; what factors are associated with delayed
PORT; and what interventions exist to reduce delays in PORT initia-
tion. Our narrative review was guided by the PROGRESS-Plus health
equity framework to respond to these thematic questions and
describe the impact of equity-related factors and SDOH on timely
PORT.
11
We conducted additional analysis of clinical and care pro-
cess factors that emerged from our review as factors that may affect
timely PORT.
3|RESULTS
3.1 |How does delayed PORT affect outcomes?
The present NCCN guideline recommendation to initiate PORT within
6 weeks of surgery is based on a 1979 study at Memorial Sloan Ket-
tering Cancer Center that found greater rates of locoregional recur-
rence among 22 head and neck cancer patients who started radiation
treatment more than 7 weeks after surgery.
3,12
This was affirmed by
subsequent retrospective studies and a meta-analysis that demon-
strated significantly higher locoregional recurrence rates when PORT
initiation was delayed beyond 6 weeks.
3,13-15
In a recent systematic review of survival outcomes of delayed
PORT initiation, four of five studies found a significant association
between delayed PORT initiation and overall survival, and an even
greater association with recurrence-free survival.
5,16-19
The study that
did not find a significant association between delay and overall sur-
vival used study cohort quartiles to define delayed PORT as greater
than 64 days.
20
Another study found PORT delay beyond 50 days to
be associated with worse overall survival among 25 216 patients with
nonmetastatic HNSCC.
3
These studies show that starting PORT
within 6 weeks or less of surgery is associated with improved survival
even with intensity-modulated radiation therapy and concurrent sys-
temic therapy.
19
Delays in PORT initiation account for the majority of
delays in radiation treatment package time, the interval from surgery
to completion of radiation treatment, which is associated with signifi-
cantly decreased overall survival.
21,22
Increasing the delay time in PORT initiation is associated with
even worse survival outcomes. Among 41 291 patients with HNSCC,
increasing delays beyond 7 weeks were associated with progressive
survival decrements.
19
Another study of 15 064 patients with HNSCC
demonstrated that each subsequent day that PORT was delayed
beyond 40 postoperative days led to increased mortality risk up to
70 postoperative days.
23
3.2 |What factors are associated with
delayed PORT?
Here, we report on the association of delayed PORT with each of the
PROGRESS-Plus factors except religion, as we did not find reports of
associations with PORT delay. We consider insurance status alongside
occupation as these are commonly associated. We then explore addi-
tional clinical and care process factors that emerged from the litera-
ture as being associated with timely PORT, including clinical American
Joint Committee on Cancer (AJCC) stage, comorbidities, postopera-
tive course, treating facility, and complex care processes (Table 1).
3.2.1 | Place of residence
Patients who resided closer to the treatment facility where they
received radiation therapy demonstrated greater rates of timely
NOYES ET AL.1359
PORT.
2
This may be mediated by geographic distance as well as socio-
economic disadvantage, as areas characterized by lower education
and income demonstrate a lower density of health care providers and
reduced access to high-quality health care.
11,24
Residing 20 miles
away from the treatment facility was associated with delayed PORT.
2
Patients often face challenges presenting for care due to travel dis-
tance and costs, inability to take time off work, family care obligations,
and not having family or caregivers able to transport them.
25
Infra-
structure to alleviate travel burden and promote equitable distribution
of care and providers may improve outcomes among geographically
marginalized patients.
11
3.2.2 | Race/ethnicity/culture/language
The relationship between race/ethnicity and radiation treatment delay
is complex and is a manifestation of systemic racism experienced by
people of color.
7-9
Black and Asian race and Hispanic ethnicity were
independent risk factors for delayed PORT compared to White
patients and also demonstrate an association with SDOH correlated
with delayed radiation treatment and access to care, including being
un- or underinsured, lower SES, lower education, delayed stage at pre-
sentation, and having medical comorbidities.
2,3,26-31
These racial and
ethnic disparities in timely PORT contribute to lower survival out-
comes among people of color.
32
African American patients had a significantly lower rate of pre-
operative radiation consultations than White patients, which may
contribute to delayed PORT.
26
Patients of color are more likely to
have Medicaid or no insurance, which limits timely access to radia-
tion treatment.
26,33
Black patients are more likely to reside in
under-resourced neighborhoods with lower education and lower
income, which can limit access to health care and PORT.
7,24
Having
a primary language other than English can further inhibit access to
and navigation through health care services.
34
Patients of color are
more likely to get care from low-volume providers, which is associ-
ated with higher rates of postoperative complications and delayed
PORT.
35
There are numerous known barriers to timely presentation among
people of color. Compared to White patients, patients of color show
lower health literacy and less widespread knowledge of warning signs
of cancer and thus may be less likely to present for timely evalua-
tion.
36-38
Black patients especially are more hesitant to present for
care due to historical and ongoing racism and distrust of the medical
system.
39-43
Patients of color have less access to regular preventative
care and less contact with the medical system to discuss concerning
symptoms in a timely manner.
27,30,35
Black patients are overall less
likely to be screened for head and neck cancer than White patients,
thus delaying their diagnosis.
28,29
Delayed presentation and diagnosis
increases the likelihood of presenting with more advanced stages of
cancer and is associated with delayed PORT.
2,3,28,29
TABLE 1 Equity-based factors associated with delayed postoperative radiation treatment (PORT) among head and neck squamous cell
carcinoma (HNSCC) patients, based on the PROGRESS-Plus health equity framework
PROGRESS-Plus
11
Factors associated with delayed PORT:
Place of residence •Residing further from facility (>20 miles) and experiencing barriers to travel
2,25
Race/ethnicity/culture/
language
•Black race, Asian race, Hispanic ethnicity
Patients of color are more likely to have lower socioeconomic status (SES), reduced access to care, and
present with more advanced stage cancer
2,3,26-31
Occupation/insurance status •Medicaid/Medicare, health maintenance organization, or no insurance
2,3
People who are under- or unemployed have limited access to health insurance
50
People of color and of lower SES are more likely to be under- or unemployed and have Medicaid or no
insurance
26,33,46-49
Gender/sex •There is not enough evidence to declare a relationship between gender/sex and delayed PORT
2,3
Education •Lower levels of education
2,3,31,48,54
•Most patients are unaware of the 6-week guideline and clinical consequences of delaying radiation treatment
25
SES •Lower household income
2,3
•Lower income patients experience reduced access to care
27,36
Advanced clinical stage at
presentation
•Higher clinical or pathologic American Joint Committee on Cancer Stage IV HNSCC
2,3
Patients of color, lower SES, Medicaid/no insurance, geographic disadvantage, decreased health literacy, and
decreased overall access to care demonstrate increased stage at diagnosis
27-29,31,36,48,51,59
Comorbidities and clinical
characteristics
•Having one or more comorbidities
3
•Oral cavity cancer compared to other primary cancer sites
66
Postoperative course •Increased postoperative length of stay and 30-day unplanned readmissions
2,3
Treating facility •There is not enough evidence to declare a relationship between treatment at academic centers and delayed
PORT
2,3,66
Complex care processes •Delay at any point in the care process: lack of preoperative radiation consultation, pathology reports beyond 7
postoperative days, PORT referral beyond 10 days of surgery, and PORT consultation beyond 10 days of
referral
26
•Receiving surgery and PORT at different facilities
2,3
1360 NOYES ET AL.
Overall, these differences suggest that care is accessed, adminis-
tered, and performed differently at both the patient and systemic level
for Black patients compared to White patients, which contributes to
racial differences in timely PORT.
3.2.3 | Occupation/insurance status
Patients without insurance or with Medicaid or Medicare experienced
greater odds of delayed PORT compared to those with private insur-
ance.
2,3
Health maintenance organization (HMO) patients also demon-
strate higher rates of delayed PORT.
44
Delays related to insurance are multifaceted and are impacted by
enrollment barriers, restrictive referral systems, and decreased physi-
cian participation. HNSCC patients engage in inherently multi-
disciplinary and complex care, often encompassing multiple facilities
and providers to complete imaging studies, surgery, and pre- and
postoperative care visits as well as coordination of varying providers
including primary care physicians, speech therapists, dentists, nutri-
tionists, surgical oncologists, radiation oncologists, and medical oncol-
ogists. Each facility and provider may have different insurance
guidelines, creating potential for delayed transitions of care. HMO
patients in particular face restrictive networks and often need pre-
authorization for each referral and transition in care, creating potential
for delays.
45
Access to health insurance is unequal and intersects with other
SDOH including race/ethnicity and SES.
30,46
Patients without insur-
ance or with Medicaid are more likely to be people of color and of
lower SES, whereas patients with private insurance are more likely to
be White, younger, and of higher SES.
26,33,46-49
For patients under
65, employment-based insurance is the main source, which puts
patients who are unemployed at risk of limited access to health insur-
ance.
50
Directly associated with structural racism, Black, Indigenous
people, and people of color are more likely to be unemployed or have
lower wage employment where insurance may be unavailable or
unaffordable.
30,33
Finally, patients with private insurance have better
access to the highest quality of health care, as private insurance reim-
burses physicians and hospitals at greater rates than Medicare/Medic-
aid.
49
3.2.4 | Gender/sex
Although one study found male patients were more likely to experi-
ence delayed PORT compared to female patients, another study
reported the opposite finding.
2,3
HNSCC is significantly more preva-
lent in male patients, which may affect these findings.
2,24,36,51
Male
patients are more likely to experience postoperative complications
that are associated with PORT delay and demonstrate worse overall
survival compared to female patients.
52
Although there is not enough
evidence to declare a relationship between gender/sex and delayed
PORT, Mazul et al. found that although female patients with HNSCC
had greater overall survival than males, Black female patients had
significantly worse survival rates than White and Hispanic male
patients.
53
This interaction would be interesting to study in rates of
delayed PORT.
3.2.5 | Education
Patients with lower levels of education were more likely to experience
delayed PORT beyond 6 weeks compared to patients with a higher
level of education.
2,3
Education is a key SDOH and driver of health
equity. Higher levels of education are associated with greater SES,
employment rates, and insurance enrollment, which are associated
with timely PORT.
2,3,31,48,54
Education is a driver of health literacy,
which promotes positive health-seeking behaviors and successful
interaction with the health care system and providers.
48,55
Knowledge of the importance of timely PORT significantly
affected timeliness of radiation. In interviews of 27 HNSCC patients
undergoing surgery and PORT, almost all patients were unaware of
the 6-week guideline and the clinical consequences of delaying radia-
tion treatment.
25
Providers noted that patients were frequently
exhausted from long days at health care facilities visiting multiple pro-
viders and undergoing imaging and testing and therefore may not
absorb all the information that is given to them.
25
Concerted efforts
are needed to increase health literacy and provide proactive health
education, particularly for underserved and minority patients.
3.2.6 | Socioeconomic status
Lower median household income was associated with greater likelihood
of delayed PORT, whereas higher incomes are associated with timely
PORT.
2,3
SES is a powerful determinant that acts through many agents
to affect health outcomes and access to care, including housing, nutri-
tion, education, economic opportunity, living environment, and insur-
ance.
48
Lower SES is a risk factor for receiving lower quality health
care.
48
Those residing in low-income areas face lower numbers of care
facilities and providers, particularly specialists.
27,36
Travel burden and
inability to take time off work is a significant socioeconomic barrier and
reason for treatment delay.
25
Patients who are un- or underemployed
may lack benefits such as health insurance, paid sick leave, and disabil-
ity insurance, which may worsen their financial status and make it more
difficult to attend medical appointments in a timely manner.
33,56,57
3.2.7 | Advanced clinical stage at presentation
Patients who presented with a higher clinical or pathological AJCC
Stage IV HNSCC demonstrated greater odds of delayed PORT com-
pared to those who presented with AJCC Stage I and Stage III can-
cers.
2,3
Patients who present with more advanced stage head and
neck cancer require more aggressive surgical treatment, often require
more complex reconstruction, face more postoperative complications,
and have longer stays in the hospital, which further delay radiation
NOYES ET AL.1361
treatment.
27,51,58
Patients of color, lower SES, Medicaid or no insur-
ance, geographic disadvantage, decreased health literacy, and
decreased overall access to care exemplify SDOH that intersect to
impact increased stage at diagnosis and subsequent delayed
PORT.
27-29,31,36,48,51,59
Lower SES is associated with less health-
seeking behavior, health care utilization, and lower health literacy,
making socioeconomically disadvantaged patients less likely to pre-
sent for timely evaluation.
48
Psychosocial influences such as medical
mistrust are associated with lower rates of screening and delays in
presenting for care.
39-42
Patients of lower SES are overall less likely to
be screened than their higher SES counterparts.
27,36
3.2.8 | Comorbidities and clinical characteristics
Patients with one or more comorbidities were less likely to receive
timely PORT than those without comorbidities.
3
Comorbidities are
associated with lower quality care, including decreased likelihood of
receiving NCCN guideline-concordant care.
60,61
Increasing com-
orbidities in HNSCC patients are associated with increased postopera-
tive complications and longer duration of hospitalization, which are
associated with delayed PORT.
3,61,62
Comorbidities affect the timeliness
of diagnosis and the choice of adjuvant treatment offered, which also
delay PORT.
26,61
Comorbidities are present in patients inequitably, as
Black patients and patients of lower SES are more likely to have medical
comorbidities than White patients and those of higher SES.
30,63-65
Patients with oral cavity cancer were more likely to experience
PORT delays than those with primary tumor site of the oropharynx,
hypopharynx, or larynx.
66
Patients with oral cavity cancer often face
more complex reconstructions, such as with fibular flaps, and thus are
correlated with longer postoperative stays and complications that
contribute to delays in radiation.
2,3,67
3.2.9 | Postoperative course
Increasing postoperative length of stay (LOS) beyond 4 days was
associated with significantly increased odds of delayed PORT, particu-
larly beyond 15 days.
2,3
Having 30-day unplanned readmissions was
associated with delays in PORT.
2
These measures are considered
quality metrics in head and neck cancer care due to their relation to
survival.
62
Postsurgical sequelae including delayed wound healing and
other clinical complications can delay discharge or lead to readmission,
often leading to delayed radiation referrals and missed appoint-
ments.
68
Surgical complications may require time for healing before
radiation treatment.
68
3.2.10 | Treating facility
Many studies found that surgery or radiation at an academic medical
center compared to a nonacademic center was associated with del-
ayed PORT initiation.
2,3,66
Another study found that delays were
more common at a nonacademic center.
69
Academic medical centers
tend to care for more complex patients and may serve as a proxy for
patient complexity contributing to delayed PORT and higher rates of
postoperative complications and longer hospital LOS.
2,3,70,71
There is
not enough evidence to suggest a relationship between treatment at
academic centers and delayed PORT, and this would be an interesting
area for future study.
3.2.11 | Complex care processes
The complex and multidisciplinary nature of head and neck cancer care,
often involving multiple appointments, procedures, providers, and facili-
ties over a long period of time, compounds the potential for delays in
care. Timeliness at all points in the care process was found to be impor-
tant for timely PORT.
26
Having a preoperative radiotherapy consulta-
tion was associated with timely PORT.
26
Patients whose pathology
reports returned within 7 postoperative days and those who received a
PORT referral within 10 days of surgery and PORT consultation within
10 days of PORT referral were more likely to receive timely PORT.
26
Delays were most common in initial primary care referral to surgeons
and initiation of radiation treatment after surgery.
44
Patients who received their surgery and PORT at different facili-
ties were more likely to experience delayed PORT.
2,3
During transi-
tions in care, it may be unclear to patients and providers who are
directing the next steps in care. Insufficient coordination and commu-
nication during care transitions can delay PORT referrals and consul-
tations and prolong the start of radiation treatment.
25
Surgical and
radiation oncologists may not have the same familiarity of the rec-
ommended timeline and particular consequences of delaying radiation
treatment for head and neck cancer patients and furthermore may not
communicate important and relevant information during care transi-
tions, such as what treatment patients received and what treatment is
necessary.
25
Providers face cumbersome patient handoffs, having to
reconcile differing electronic health records or fax over hundreds of
pages of records, leading to further delays in care.
25
On the other
hand, receiving PORT at the same center can facilitate timely care due
to improved communication and accessibility of medical records.
26
Delayed dental evaluations and extractions were strongly associ-
ated with delayed PORT.
68,72
Patients receiving radiation to the head
and neck require dental evaluation and imaging and may need extrac-
tions before receiving radiation treatment to reduce the risk of
osteoradionecrosis.
68,72,73
Patients' preferred or local dentists may be
unfamiliar with the specific needs for these patients in the context of
their treatment.
25
Furthermore, dental care can be challenging to
coordinate in a timely manner and may depend upon insurance and
access to care, and significant out-of-pocket costs from the patient.
74
3.2.12 | Summary
Delays starting PORT disproportionately burden people of color, those
with Medicaid or no insurance, those of low SES, and those with overall
1362 NOYES ET AL.
less access to care. Care is accessed and performed differently at both
the patient and systemic levels according to patients' characteristics,
which contributes to disparities in timely PORT. Delays are more com-
mon among patients with more comorbidities, advanced stage of dis-
ease, those who experience postoperative complications, and at
transitions of care. These complex factors intersect to produce condi-
tions that predictably predispose certain patients to delayed PORT.
3.3 |What interventions exist to reduce delays in
PORT initiation?
Many of the delays in PORT are related to deeply rooted systemic ineq-
uities that must be targeted on a large scale. Recognizing that systemic
change occurs slowly, patients need timely PORT care immediately;
therefore, local interventions that mitigate avoidable delays, streamline
care, and support patients through their treatment may help improve
the timeliness of PORT. Some factors associated with delayed PORT
are modifiable and may be targeted directly by interventions, such as a
patient's insurance status and transitions in care. Others are non-modi-
fiable, such as a patient's race/ethnicity, though interventions may tar-
get mediating factors such as access to care. We surveyed the
literature for interventions aimed at reducing delays in PORT.
Methods to identify patients at a high risk for delay can help
direct resources and interventions to those with the greatest need.
Levy et al. developed validated nomograms to generate estimates of
PORT initiation delay personalized to each patient, incorporating
race/ethnicity, insurance, tumor site, and facility type (academic or
nonacademic).
66
They developed two nomograms: one based on pre-
operative factors including clinical stage and comorbidity and one
based on postoperative factors including LOS and care fragmenta-
tion.
66
Shew et al. used machine learning to predict delays beyond
50 days in adjuvant radiation after surgery for HNSCC, based on
patient and care process factors, most importantly treating facility and
urban vs rural patient demographic.
75
The Stanford Head and Neck Cancer Oncology Program con-
ducted an institutional quality improvement project to reduce delays
in PORT initiation.
72
From chart reviews of 56 patients with oral cav-
ity carcinoma patients who underwent surgery and radiation, the team
identified three key drivers of PORT delay: delayed dental extractions,
delayed radiation oncology initial consult, and poor patient engage-
ment. They developed 12 interventions to address these drivers of
delay. All patients with oral cavity cancer received a preoperative Pan-
orex scan and attended a formal dental consultation if needed. Any
necessary dental extractions were performed pre- or intraoperatively.
Consultations with radiation oncology occurred earlier in the care
pathway, as soon as the need for adjuvant treatment was identified. If
pathology reports were the deciding factor to consult radiation oncol-
ogy, a 10-day postoperative reminder was sent via the electronic
medical record (EMR) to the surgical oncologist. To increase patient
engagement, the team developed a Clinical Visit Summary, a checklist
to outline the important elements and timelines of the patient's indi-
vidual care pathway. Compared to 62% of patients receiving timely
PORT before the intervention, 73% achieved timely PORT afterward,
and avoidable delays were decreased from 24% to 9%.
72
Another quality improvement project developed by Graboyes
et al. called Navigation for Disparities and Untimely Radiation thErapy
(NDURE) centers on social workers as dedicated patient navigators
who met with patients for three in-person sessions to support them
through their treatment.
76
The intervention focused on patient educa-
tion, including a personalized risk estimate of PORT delay and discus-
sion of expectations for PORT.
66,76
They developed a personalized
PORT care plan to keep in the EMR for each patient with a barrier
reduction plan to address their particular barriers. The patient naviga-
tor scheduled all appointments and tracked referrals and appointment
completion, and patients were provided with travel assistance.
NDURE was tested in 15 patients with HNSCC undergoing surgery
and PORT in a single-arm clinical trial and resulted in timely PORT for
86% of patients overall and 100% of Black patients.
76
Developing ways to predict the risk of delay is an important step
to understand who is at risk and focus resources and attention on
those at risk. Targeted interventions such as NDURE demonstrate
high rates of timely PORT when specifically attending to access to
care and providing support and resources through transitions in care.
4|CONCLUSION
HNSCC patient outcomes are heavily dependent on their ability to
access care, including PORT, in a timely manner. PORT delays are
more apparent in transitions in care and in complex and advanced-
stage patients and present inequitably along common fault lines of
race/ethnicity, SES, and insurance status, likely contributing signifi-
cantly to disparities in overall survival of HNSCC patients. These dis-
parities mandate continued need for structural change to reduce
health disparities and promote equitable access to care for all, with
particular focus on underserved and minority patients. When planning
care, providers must consider not only biological factors but also
SDOH to maximize care outcomes. Delays in PORT may be reduced
by interventions to identify patients who are most likely to experience
delayed PORT, provide support according to their specific needs and
barriers to care, and streamline overall care and referral processes.
CONFLICTS OF INTEREST
The authors declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article.
ORCID
Elizabeth A. Noyes https://orcid.org/0000-0003-4656-4269
Ciersten A. Burks https://orcid.org/0000-0002-9377-5715
BIBLIOGRAPHY
1. Harris BN, Pipkorn P, Nguyen KNB, et al. Association of Adjuvant Radi-
ation Therapy with survival in patients with advanced cutaneous squa-
mous cell carcinoma of the head and neck. JAMA Otolaryngol Head
Neck Surg. 2019;145(2):153-158. doi:10.1001/jamaoto.2018.3650
NOYES ET AL.1363
2. Graboyes EM, Garrett-Mayer E, Sharma AK, Lentsch EJ, Day TA.
Adherence to National Comprehensive Cancer Network guidelines
for time to initiation of postoperative radiation therapy for patients
with head and neck cancer. Cancer. 2017;123(14):2651-2660. doi:10.
1002/cncr.30651
3. Harris JP, Chen M, Orosco RK, Sirjani D, Divi V, Hara W. Association
of survival with shorter time to radiation therapy after surgery for US
patients with head and neck cancer. JAMA Otolaryngol Head Neck
Surg. 2018;144(4):349-359. doi:10.1001/jamaoto.2017.3406
4. National Comprehensive Cancer Network. NCCN Clinical Practice
Guidelines in Oncology: Head and Neck Cancers. Vol 3; 2021. https://
www.nccn.org/professionals/physician_gls/pdf/head-and-neck.pdf
5. Graboyes EM, Kompelli AR, Neskey DM, et al. Association of Treat-
ment Delays with survival for patients with head and neck cancer: a
systematic review. JAMA Otolaryngol Head Neck Surg. 2019;145(2):
166-177. doi:10.1001/jamaoto.2018.2716
6. Bergmark RW, Sedaghat AR. Disparities in health in the
United States: an overview of the social determinants of health for
otolaryngologists. Laryngoscope Investig Otolaryngol. 2017;2(4):187-
193. doi:10.1002/lio2.81
7. Bailey ZD, Feldman JM, Bassett MT. How structural racism works —
racist policies as a root cause of U.S. racial health inequities. N. Engl.
J. Med. 2021;384(8):768-773. doi:10.1056/nejmms2025396
8. Hardeman RR, Medina EM, Boyd RW. Stolen breaths. N Engl J Med.
2020;383(3):197-199. doi:10.1056/NEJMp2021072
9. Lee BX. Structural Violence. Violence: an Interdisciplinary Approach to
Causes, Consequences, and Cures. 1st ed. Oxford, UK: John Wiley &
Sons, Inc; 2019:123-142.
10. Farmer PE, Nizeye B, Stulac S, Keshavjee S. Structural violence and
clinical medicine. PLoS Med. 2006;3(10):1686-1691. doi:10.1371/
journal.pmed.0030449
11. O'Neill J, Tabish H, Welch V, et al. Applying an equity lens to inter-
ventions: using PROGRESS ensures consideration of socially stratify-
ing factors to illuminate inequities in health. J Clin Epidemiol. 2014;
67(1):56-64. doi:10.1016/j.jclinepi.2013.08.005
12. Vikram B. Importance of the time interval between surgery and post-
operative radiation therapy in the combined management of head &
neck cancer. Int J Radiat Oncol Biol Phys. 1979;5(10):1837-1840. doi:
10.1016/0360-3016(79)90568-6
13. Vikram B, Strong EW, Shah JP, Spiro R. Failure in the neck following
multimodality treatment for advanced head and neck cancer. Head
Neck Surg. 1984;6(3):724-729. doi:10.1002/hed.2890060304
14. Mantravadi RVP, Haas RE, Liebner EJ, Skolnik EM, Applebaum EL.
Postoperative radiotherapy for persistent tumor at the surgical mar-
gin in head and neck cancers. Laryngoscope. 1983;93(10):1337-1340.
doi:10.1002/lary.1983.93.10.1337
15. Huang J, Barbera L, Brouwers M, Browman G, Mackillop WJ. Does
delay in starting treatment affect the outcomes of radiotherapy? A
systematic review. J Clin Oncol. 2003;21(3):555-563. doi:10.1200/
JCO.2003.04.171
16. Tam M, Wu SP, Gerber NK, et al. The impact of adjuvant
chemoradiotherapy timing on survival of head and neck cancers.
Laryngoscope. 2018;128(10):2326-2332. doi:10.1002/lary.27152
17. Chen MM, Harris JP, Orosco RK, Sirjani D, Hara W, Divi V. Associa-
tion of Time between surgery and adjuvant therapy with survival in
Oral cavity cancer. Otolaryngol Head Neck Surg. 2018;158(6):1051-
1056. doi:10.1177/0194599817751679
18. Cramer JD, Speedy SE, Ferris RL, Rademaker AW, Patel UA,
Samant S. National evaluation of multidisciplinary quality metrics for
head and neck cancer. Cancer. 2017;123(22):4372-4381. doi:10.
1002/cncr.30902
19. Graboyes EM, Garrett-Mayer E, Ellis MA, et al. Effect of time to initia-
tion of postoperative radiation therapy on survival in surgically man-
aged head and neck cancer. Cancer. 2017;123(24):4841-4850. doi:10.
1002/cncr.30939
20. Fujiwara RJT, Judson BL, Yarbrough WG, Husain Z, Mehra S. Treat-
ment delays in oral cavity squamous cell carcinoma and association
with survival. Head Neck. 2017;39(4):639-646. doi:10.1002/hed.24608
21. Daniels CP, Bressel M, Corry J, et al. Treatment package time in node-
positive cutaneous head and neck squamous cell carcinoma. Pract
Radiat Oncol. 2019;10(1):29-35. doi:10.1016/j.prro.2019.09.009
22. Goel AN, Frangos MI, Raghavan G, et al. The impact of treatment
package time on survival in surgically managed head and neck cancer
in the United States. Oral Oncol. 2019;88:39-48. doi:10.1016/j.
oraloncology.2018.11.021
23. Ho AS, Kim S, Tighiouart M, et al. Quantitative survival impact of com-
posite treatment delays in head and neck cancer. Cancer. 2018;
124(15):3154-3162. http://www.ncbi.nlm.nih.gov/pubmed/29742280
24. Gourin CG, Podolsky RH. Racial disparities in patients with head and
neck squamous cell carcinoma. Laryngoscope. 2006;116(7):1093-
1106. doi:10.1097/01.mlg.0000224939.61503.83
25. Graboyes EM, Halbert CH, Li H, et al. Barriers to the delivery of
timely, guideline-adherent adjuvant therapy among patients with
head and neck cancer. JCO Oncol Pract. 2020;16(12):e1417-e1432.
doi:10.1200/op.20.00271
26. Janz TA, Kim J, Hill EG, et al. Association of care processes with
timely, equitable postoperative radiotherapy in patients with surgi-
cally treated head and neck squamous cell carcinoma. JAMA
Otolaryngol Head Neck Surg. 2018;144(12):1105-1114. http://www.
ncbi.nlm.nih.gov/pubmed/30347012
27. Rereddy SK, Jordan DR, Moore CE. Dying to be screened: exploring
the unequal burden of head and neck cancer in health provider
shortage areas. J Cancer Educ. 2015;30(3):490-496. doi:10.1007/
s13187-014-0755-2
28. Ling H, Gadalla S, Israel E, et al. Oral cancer exams among cigarette
smokers in Maryland. Cancer Detect Prev. 2006;30(6):499-506. doi:
10.1016/j.cdp.2006.10.005
29. Dodd VJ, Watson JM, Choi Y, Tomar SL, Logan HL. Oral cancer in
African Americans: addressing health disparities. Am J Health Behav.
2006;32(6):684-692. doi:10.5555/ajhb.2008.32.6.684
30. Yearby R. Racial disparities in health status and access to healthcare:
the continuation of inequality in the United States due to stru-
ctural racism. Am J Econ Sociol.2018;77(3–4):1113-1152. doi:10.1111/
ajes.12230
31. Zajacova A, Lawrence EM. The relationship between education and
health: reducing disparities through a contextual approach. Annu Rev
Public Health. 2018;39(3):273-289. doi:10.1146/annurev-publhealth-
031816-044628
32. Guttmann DM, Kobie J, Grover S, et al. National disparities in treat-
ment package time for resected locally advanced head and neck can-
cer and impact on overall survival. Head Neck. 2018;40(6):1147-
1155. doi:10.1002/hed.25091
33. Lillie-Blanton M, Hoffman C. The role of health insurance coverage in
reducing racial/ethnic disparities in health care. Health Aff. 2005;
24(2):398-408. doi:10.1377/hlthaff.24.2.398
34. Pearson WS, Ahluwalia IB, Ford ES, Mokdad AH. Language prefer-
ence as a predictor of access to and use of healthcare services among
Hispanics in the United States. Ethn Dis. 2008;18(1):93-97. http://
www.ncbi.nlm.nih.gov/pubmed/18447107
35. Bulatao RA, Anderson NB. Understanding racial and ethnic differences
in health in late life: a research. Washington (DC): National Academies
Press; 2004.
36. Goodwin WJ, Thomas GR, Parker DF, et al. Unequal burden of head
and neck cancer in the United States. Head Neck. 2008;30(3):358-
371. doi:10.1002/hed.20710
37. Berkman ND, Sheridan SL, Donahue KE, et al. Health literacy inter-
ventions and outcomes: an updated systematic review. Evidence
report/technology Assessment no. 199. Evid Rep Technol Assess
(Full Rep). 2011;(199):1-941. http://www.ncbi.nlm.nih.gov/pubmed/
23126607
1364 NOYES ET AL.
38. Villagra VG, Bhuva B, Coman E, Smith DO, Fifield J. Health insurance
literacy: disparities by race, ethnicity, and language preference.
Am J Manag Care. 2019;25(3):E71-E75.
39. Adegbembo AO, Frcd C, Tomar SL, Logan HL. Perception of racism
explains the difference between Blacks' and Whites' level of
healthcare trust. Ethn Dis. 2006;16(4):792-798.
40. Adams LB, Richmond J, Corbie-Smith G, Powell W. Medical mistrust
and colorectal cancer screening among African Americans. J Community
Health. 2017;42(5):1044-1061. doi:10.1007/s10900-017-0339-2
41. Powell W, Richmond J, Mohottige D, Yen I, Joslyn A, Corbie-Smith G.
Medical mistrust, racism, and delays in preventive health screening
among African-American men. Behav Med. 2019;45(2):102-117. doi:
10.1080/08964289.2019.1585327
42. Jaiswal J, Halkitis PN. Towards a more inclusive and dynamic under-
standing of medical mistrust informed by science. Behav Med. 2017;
45(2):79-85. doi:10.1080/08964289.2019.1619511
43. Johnson RL, Saha S, Arbelaez JJ, Beach MC, Cooper LA. Racial and
ethnic differences in patient perceptions of bias and cultural compe-
tence in health care. J Gen Intern Med. 2004;19(2):101-110. doi:10.
1111/j.1525-1497.2004.30262.x
44. Itamura K, Kokot N, Sinha U, Swanson M. Association of insurance
type with time course of care in head and neck cancer management.
Laryngoscope. 2020;130(11):E587-E592. doi:10.1002/lary.28423
45. Chernew ME, Wodchis WP, Scanlon DP, McLaughlin CG. Overlap in
HMO physician networks. Health Aff. 2004;23(2):91-101. doi:10.
1377/hlthaff.23.2.91
46. Young GJ, Cohen BB. The process and outcome of hospital care for
Medicaid versus privately insured hospital patients. Inquiry. 1992;
29(3):366-371. http://www.ncbi.nlm.nih.gov/pubmed/1398905
47. Kirby JB, Kaneda T. Coverage using a life table approach *. Demogra-
phy. 2010;47(4):1035-1051.
48. Fiscella K, Franks P, Gold MR, Clancy CM. Inequality in quality:
addressing socioeconomic, racial, and ethnic disparities in health care.
JAMA Otolaryngol Head Neck Surg. 2000;283(19):2579. doi:10.1001/
jama.283.19.2579
49. Akinyemiju T, Sakhuja S, Vin-Raviv N. Racial and socio-economic dis-
parities in breast cancer hospitalization outcomes by insurance status.
Cancer Epidemiol. 2016;43:63-69. doi:10.1016/j.canep.2016.06.011
50. Yabroff KR, Dowling EC, Guy GP, et al. Financial hardship associated
with cancer in the United States: findings from a population-based
sample of adult cancer survivors. J Clin Oncol. 2016;34(3):259-267.
doi:10.1200/JCO.2015.62.0468
51. Osazuwa-Peters N, Christopher KM, Hussaini AS, Behera A,
Walker RJ, Varvares MA. Predictors of stage at presentation and out-
comes of head and neck cancers in a university hospital setting. Head
Neck. 2016;38(S1):E1826-E1832. doi:10.1002/hed.24327
52. Shepherd SJ, Creber N, Mansour K, Wiesenfeld D, Iseli TA, Amott D.
Relationship between age, comorbidities and complications in head
and neck cancer patients undergoing curative surgery. ANZ J Surg.
2020;90(5):851-855. doi:10.1111/ans.15611
53. Mazul AL, Naik AN, Zhan KY, et al. Gender and race interact to influ-
ence survival disparities in head and neck cancer. Oral Oncol. 2021;
112:105093. doi:10.1016/j.oraloncology.2020.105093
54. Hahn RA, Truman BI. Education improves public health and promotes
health equity. Int J Health Serv. 2015;45(4):657-678. doi:10.
1177/0020731415585986
55. Stormacq C, van den Broucke S, Wosinski J. Does health literacy mediate
the relationship between socioeconomic status and health disparities?
Health Promot Int. 2019;34(5):E1-E17. doi:10.1093/heapro/day062
56. Carroll WR, Kohler CL, Carter VL, Hannon L, Skipper JB,
Rosenthal EL. Barriers to early detection and treatment of head and
neck squamous cell carcinoma in African American men. Head Neck.
2009;31(12):1557-1562. doi:10.1002/hed.21125
57. Tangka FKL, Subramanian S, Jones M, et al. Insurance coverage,
employment status, and financial well-being of Young women
diagnosed with breast cancer. Cancer Epidemiol., Biomarkers Prev.
2020;29(3):616-624. doi:10.1158/1055-9965.EPI-19-0352
58. de Melo GM, de Cássia Braga Ribeiro K, Kowalshi LP, Deheinzelin D.
Risk factors for postoperative complications in oral cancer and their
prognostic implications. Arch Otolaryngol Head Neck Surg. 2001;
127(7):828-833.
59. Panth N, Simpson MC, Sethi RKV, Varvares MA, Osazuwa-Peters N.
Insurance status, stage of presentation, and survival among female
patients with head and neck cancer. Laryngoscope. 2020;130(2):385-
391. doi:10.1002/lary.27929
60. Chen MM, Roman SA, Yarbrough WG, Burtness BA, Sosa JA,
Judson BL. Trends and variations in the use of adjuvant therapy for
patients with head and neck cancer. Cancer. 2014;120(21):3353-
3360. doi:10.1002/cncr.28870
61. Sinha P, Kallogjeri D, Piccirillo JF. Assessment of comorbidities in sur-
gical oncology outcomes. J Surg Oncol. 2014;110(5):629-635. doi:10.
1002/jso.23723
62. Weber RS, Lewis CM, Eastman SD, et al. Quality and performance
indicators in an academic Department of Head and Neck Surgery.
Arch Otolaryngol Head Neck Surg. 2010;136(12):1212-1218. doi:10.
1001/archoto.2010.215
63. Tammemagi CM, Nerenz D, Neslund-Dudas C, Feldkamp C,
Nathanson D. Comorbidity and survival disparities among black and
white patients with breast cancer. JAMA. 2005;294(14):1765-1772.
doi:10.1001/jama.294.14.1765
64. Pathirana TI, Jackson CA. Socioeconomic status and multimorbidity: a
systematic review and meta-analysis. Aust N Z J Public Health. 2018;
42(2):186-194. doi:10.1111/1753-6405.12762
65. de CB RK, Kowalski LP, do RDDO LM. Perioperative complications, com-
orbidities, and survival in oral or oropharyngeal cancer. Arch Otolaryngol
Head Neck Surg. 2003;129(2):219-228. doi:10.1001/archotol.129.2.219
66. Levy DA, Li H, Sterba KR, et al. Development and validation of Nomo-
grams for predicting delayed postoperative radiotherapy initiation in
head and neck squamous cell carcinoma. JAMA Otolaryngol Head Neck
Surg. 2020;146(5):455-464. doi:10.1001/jamaoto.2020.0222
67. Lahtinen S, Koivunen P, Ala-Kokko T, et al. Complications and outcome
after free flap surgery for cancer of the head and neck. Br J Oral Maxil-
lofac Surg. 2018;56(8):684-691. doi:10.1016/j.bjoms.2018.07.009
68. Strohl MP, Chen JP, Ha PK, Seth R, Yom SS, Heaton CM. Can early
dental extractions reduce delays in postoperative radiation for
patients with advanced Oral cavity carcinoma? J Oral Maxillofac Surg.
2019;77(11):2215-2220. doi:10.1016/j.joms.2019.05.007
69. George JR, Yom SS, Wang SJ. Combined modality treatment out-
comes for head and neck cancer: comparison of postoperative radia-
tion therapy at academic vs nonacademic medical centers. JAMA
Otolaryngol Head Neck Surg. 2013;139(11):1118-1126. doi:10.1001/
jamaoto.2013.4539
70. Burke L, Khullar D, John Orav E, Zheng J, Frakt A, Jha AK. Do aca-
demic medical centers disproportionately benefit the sickest patients?
Health Aff. 2018;37(6):864-872. doi:10.1377/hlthaff.2017.1250
71. George JR, Yom SS, Wang SJ. Improved outcomes in adjuvant radiother-
apy for oral cavity carcinoma at an academic center: a matched-pair
analysis. Laryngoscope. 2014;124(7):1603-1608. doi:10.1002/lary.24552
72. Divi V, Chen MM, Hara W, et al. Reducing the time from surgery to
adjuvant radiation therapy: an institutional quality improvement pro-
ject. Otolaryngol Head Neck Surg. 2018;159(1):158-165. doi:10.
1177/0194599818768254
73. Wang T-H, Liu C-J, Chao T-F, Chen T-J, Hu Y-W. Risk factors for and
the role of dental extractions in osteoradionecrosis of the jaws: a
national-based cohort study. Head Neck. 2017;39(7):1313-1321. doi:
10.1002/hed.24761
74. Okunseri C, Bajorunaite R, Abena A, Self K, Iacopino AM, Flores G.
Racial/ethnic disparities in the acceptance of Medicaid patients in
dental practices. J Public Health Dent. 2008;68(3):149-153. doi:10.
1111/j.1752-7325.2007.00079.x
NOYES ET AL.1365
75. Shew M, New J, Bur AM. Machine learning to predict delays in adjuvant
radiation following surgery for head and neck cancer. Otolaryngol Head
Neck Surg. 2019;160(6):1058-1064. doi:10.1177/0194599818823200
76. Graboyes EM, Sterba KR, Li H, et al. Development and evaluation of a
navigation-based, multilevel intervention to improve the delivery of
timely, guideline-adherent adjuvant therapy for patients with head
and neck cancer. JCO Oncol Pract. 2021;17(10):e1512-e1523. doi:10.
1200/op.20.00943
How to cite this article: Noyes EA, Burks CA, Larson AR,
Deschler DG. An equity-based narrative review of barriers to
timely postoperative radiation therapy for patients with head
and neck squamous cell carcinoma. Laryngoscope Investigative
Otolaryngology. 2021;6(6):1358-1366. doi:10.1002/lio2.692
1366 NOYES ET AL.
Available via license: CC BY-NC-ND
Content may be subject to copyright.