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Research

JAMA Otolaryngology–Head & Neck Surgery | Original Investigation

Association of Social-Ecological Factors With Delay in Time to Initiation


of Postoperative Radiation Therapy
A Prospective Cohort Study
Tuleen Sawaf, BS; Celina G. Virgen, MD, MPH; Bryan Renslo, BS; Nathan Farrokhian, MD; Katherine M. Yu, MD;
Shaan N. Somani, MD; Andrés M. Bur, MD; Kiran Kakarala, MD; Yelizaveta Shnayder, MD;
Gregory N. Gan, MD, PhD; Evan M. Graboyes, MD, MPH; Kevin J. Sykes, PhD, MPH

Supplemental content
IMPORTANCE Timely initiation of postoperative radiation therapy (PORT) is associated with
reduced recurrence rates and improved overall survival in patients with head and neck
squamous cell carcinoma (HNSCC). Measurement of the association of social-ecological
variables with PORT delays is lacking.

OBJECTIVE To assess individual and community-level factors associated with PORT delay
among patients with HNSCC.

DESIGN, SETTING, AND PARTICIPANTS This prospective cohort study carried out between
September 2018 and June 2022 included adults with untreated HNSCC who were enrolled in
a prospective registry at a single academic tertiary medical center. Demographic information
and validated self-reported measures of health literacy were obtained at baseline visits.
Clinical data were recorded, and participant addresses were used to calculate the area
deprivation index (ADI), a measure of community-level social vulnerability. Participants
receiving primary surgery and PORT were analyzed. Univariable and multivariable regression
analysis was performed to identify risk factors for PORT delays.

EXPOSURES Surgical treatment and PORT.

MAIN OUTCOMES AND MEASURES The primary outcome was PORT initiation delay (>42 days
from surgery). Risk of PORT initiation delay was evaluated using individual-level
(demographic, health literacy, and clinical data) and community-level information (ADI and
rural-urban continuum codes).

RESULTS Of 171 patients, 104 patients (60.8%) had PORT delays. Mean (SD) age of
participants was 61.0 (11.2) years, 161 were White (94.2%), and 105 were men (61.4%).
Insurance was employer-based or public among 65 (38.5%) and 75 (44.4%) participants,
respectively. Mean (SD) ADI (national percentile) was 60.2 (24.4), and 71 (41.8%) resided in
rural communities. Tumor sites were most commonly oral cavity (123 [71.9%]), with 108
(63.5%) classified as stage 4 at presentation. On multivariable analysis, a model incorporating
individual-level factors with health literacy in addition to community-level factors was most
predictive of PORT delay (AOC= 0.78; R2, 0.18).

CONCLUSIONS AND RELEVANCE This cohort study provides a more comprehensive assessment
of predictors of PORT delays that include health literacy and community-level measures.
Predictive models that incorporate multilevel measures outperform models with Author Affiliations: Department of
individual-level factors alone and may guide precise interventions to decrease PORT delay for Otolaryngology–Head and Neck
Surgery, University of Kansas Medical
at-risk patients with HNSCC.
Center, Kansas City (Sawaf, Virgen,
Renslo, Farrokhian, Yu, Somani, Bur,
Kakarala, Shnayder, Sykes);
Department of Radiation Oncology,
University of Kansas Medical Center,
Kansas City (Gan); Department of
Otolaryngology–Head and Neck
Surgery, Medical University of South
Carolina, Charleston (Graboyes).
Corresponding Author: Tuleen
Sawaf, BS, Department of
Otolaryngology–Head and Neck
Surgery, University of Kansas Medical
JAMA Otolaryngol Head Neck Surg. 2023;149(6):477-484. doi:10.1001/jamaoto.2023.0308 Center, 3901 Rainbow Blvd, Kansas
Published online April 20, 2023. City, KS 66160 (tsawaf@kumc.edu).

(Reprinted) 477
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Research Original Investigation Association of Social-Ecological Factors With Delay in Time to Initiation of Postoperative Radiation Therapy

T
imely initiation of radiation therapy following primary
surgical ablation of head and neck squamous cell car- Key Points
cinoma (HNSCC) is critical to achieving locoregional con-
Question How are individual and community-level factors
trol and improved survival in patients with advanced-stage and associated with risk for postoperative radiation (PORT) delays in
high-risk disease.1,2 Although initiation of postoperative ra- patients with head and neck squamous cell carcinoma (HNSCC)?
diation therapy (PORT) within 6 weeks of surgery is the stan-
Findings In this prospective cohort study of 171 participants who
dard to achieve optimal oncologic outcomes, most patients do
received primary surgery and PORT for HNSCC, lower levels of
not begin adjuvant therapy within this window.3-5 In early written health literacy were significantly associated with PORT
2022, the Commission on Cancer made initiation of radiation delays when controlling for demographic and clinical factors. The
within 6 weeks of surgery its first and only head and neck can- addition of health literacy and the community-level area deprivation
cer quality measure.6 Factors associated with an increased risk index improved the model’s prediction of PORT delay risk.
of PORT delay in prior studies include oral cavity and advanced- Meaning Precise measures of baseline risk for PORT delay at
stage tumors, PORT outside the surgical facility, Medicaid in- multiple social-ecologic levels are necessary to develop and
surance or uninsured status, minority race and ethnicity, implement precise resource-conscious interventions for at-risk
rural geographic location, lower education level, lack of inter- patients.
disciplinary care coordination, and lower social support.7-11
Prior studies12-14 have demonstrated that delays in initi- measures at the individual and community levels will outper-
ating PORT are associated with worse overall survival and in- form a model with individual-level factors alone when pre-
creased recurrence. The interval between primary surgery and dicting delays in PORT initiation.
initiation of PORT is the primary driver of total treatment pack-
age time, affecting survival independent of diagnosis-to-
treatment interval or duration of radiation therapy.12,15,16 De-
lays in PORT initiation disproportionately affect racial and
Methods
ethnic minorities, those with Medicaid insurance, and those This study received approval by the institutional review
in medically underserved areas.13,17-19 board at the University of Kansas Medical Center (KUMC)
To guide targeted interventions to improve the delivery of (#00001732), and all participants provided written informed
timely, equitable, guideline-adherent PORT, better predic- consent. Adult patients eligible for enrollment into the KUMC
tive tools are needed to identify patients at risk for delay. The Head and Neck Registry were those receiving primary evalu-
social-ecological model, originally developed to guide vio- ation and treatment for HNSCC at KUMC, a tertiary care refer-
lence prevention, recognizes the influence of individual char- ral center. This registry has been described in detail in prior
acteristics, interpersonal or relationship influences, commu- work.26 Patients who completed radiation therapy between
nity factors, and society-level influences on health behavior September 2018 and June 2022 were included in the analy-
and outcomes.20,21 The influence of individual contexts and sis. These dates corresponded to the earliest registry enroll-
community environments on health behaviors has been ment with available radiation records. Patients included in the
studied extensively over the past several decades.22 Like- current study were those requiring primary surgical ablation
wise, the social-ecological model has been applied across stud- followed by PORT with or without chemotherapy. Patients
ies in public health and otolaryngology, including understand- were enrolled at their initial consultation with a head and neck
ing disparities in human papilloma virus (HPV) vaccination oncologic surgeon. The decision to pursue PORT was deter-
uptake.23,24 Prior qualitative work has even referenced the so- mined by consensus recommendations of a multidisci-
cial-ecological model to evaluate and conceptualize barriers plinary tumor board, which reflected the National Compre-
to timely PORT in head and neck cancer.25 By identifying dis- hensive Cancer Center (NCCN) guidelines for treatment of head
parities in PORT delay at the individual, interpersonal, com- and neck mucosal squamous cell carcinomas. Surgery was per-
munity, and society level, the social-ecological model may formed at the primary facility, and patients received adju-
guide how to address key drivers of prevention, timely diag- vant radiation in or outside KUMC, depending on patient
nosis, timely completion of treatment, and support for survi- preference. Data regarding PORT initiation were captured pro-
vorship at each level of influence. Although a number of stud- spectively from the electronic medical record or end of treat-
ies have identified individual-level factors associated with ment summaries. Eight patients were excluded because
PORT delay using data from national databases,5 they have radiation records were unavailable.
been limited in their consideration of community-level fac-
tors affecting delays. Moreover, to our knowledge, no studies Individual-Level Measures
have applied these measures in a prospective cohort to quan- In the social-ecological framework, variables measured at the
titatively assess factors associated with PORT delay in pa- individual level included clinical data such as tumor site and
tients with head and neck cancer. The aim of this study was stage, health literacy and education levels, race and ethnic-
to evaluate factors from multiple levels of influence among pa- ity, age, sex, insurance, Charlson Comorbidity Index (CCI) score,
tients with HNSCC treated at a single Midwestern institution and whether the patient required free flap reconstruction. The
to develop a more comprehensive baseline risk assessment for CCI was coded as a categorical variable, excluding the index
PORT delay. We hypothesize that based on the social- tumor. A CCI score of 0 to 1 was considered low, a CCI score of
ecological framework, a model that incorporates baseline 2 to 4 as intermediate, and a CCI score of 5 or greater as high.

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Association of Social-Ecological Factors With Delay in Time to Initiation of Postoperative Radiation Therapy Original Investigation Research

The Brief Health Literacy Screening Tool (BRIEF) pro- Hypothesis Testing
vides a short assessment of confidence in understanding To test the central hypothesis, we generated several multi-
written and verbal health information.27 In this 4-item self- variable models that built toward including measures from
reported survey, scores range from 4 to 20, with 4 to 12 being multiple social-ecological levels of influence. In the first mul-
considered limited health literacy, 13 to 16 being marginal tivariable model, individual-level measures from the social-
health literacy, and 17 to 20 being adequate health literacy. ecological model were assessed, which included age, insur-
Mean BRIEF scores in the delayed and nondelayed groups were ance, overall stage, tumor site, and CCI score category (high,
calculated and compared as continuous measures. intermediate, or low CCI scores). A second individual-level
model was generated, incorporating the “learning” score from
Community-Level Measures the BRIEF to evaluate its effect on the model’s strength, as the
In the social-ecological model, the Rural-Urban Continuum effect of health literacy on PORT delay risk has not been di-
Code (RUCC) and Area Deprivation Index (ADI) were consid- rectly evaluated in prior studies. A third model was gener-
ered community-level variables. The RUCC uses measures of ated incorporating the community-level measure ADI.
population density and urbanization to classify US counties.28 Finally, a fourth model incorporated both community-level
The latest classifications from 2013 were used to calculate the ADI and RUCC.
RUCC. The ADI is a measure of socioeconomic disadvantage Multiple imputation was used to account for missing data
of a neighborhood in relation to either the corresponding state (0.96% of the total data set); most were missing BRIEF scores
or US as a whole, and incorporates 17 measures of housing qual- (n = 11). A description of values imputed is provided in eTable 1
ity, education, income/employment, and poverty. The ADI uses in Supplement 1. Multivariable imputation by chained equa-
the census block group as the geographic unit of construc- tions was performed using the mice package in R. Twenty-
tion, which is a subdivision in a census tract and more closely five data sets were generated, and sequential regression im-
approximates the “neighborhood” of a given address than the putation calculated each missing value based on all other
county or zip code reported in national databases.29 Patient variables in the regression equation. Residual variance was
addresses were obtained at baseline and used to calculate the added to the parameter estimates in the regression model using
ADI and RUCC. The ADI was calculated using the American the Bayesian method. A 2-sided α threshold of α = .05 was ap-
Community Survey from 2018. Current addresses were ex- plied for all tests of statistical significance. All statistical analy-
tracted from the electronic medical record and geocoded to lati- sis was performed using R Studio (version 4.2.1; R Founda-
tude and longitude coordinates using Geoapify,30 an online tion).
geocoding tool, and then merged with the corresponding poly-
gon associated with their census block using ArcGIS Pro (Esri,
version 2.9). Only participants residing in Kansas or Missouri
were included. Eight (4.5%) participants provided only PO box
Results
addresses, and for these ADI was manually mapped to the PO A total of 171 patients who received primary surgery and ad-
box location. The ADI national percentile was scored on a con- juvant radiation therapy were included in the overall cohort.
tinuous scale (1-99, with 1 the least disadvantaged, and 99 the Of these, 104 patients (60.8%) experienced a delay in initiat-
most disadvantaged). ing PORT. The mean (SD) age for the overall cohort was 61.0
(11.2) years. Overall, 161 patients were White (94.2%), and 105
Data Collection and Quantitative Analysis were men (61.4%) (Table 1), which is representative of the popu-
Demographic information, insurance status, and BRIEF lation of patients with head and neck cancer seen at KUMC.
survey were collected at baseline. Clinical data including This study categorized 14.97% of the US population as rural,
pathologic tumor stage, site, and radiation start date were in agreement with published federal data.34 In 154 patients who
obtained from the electronic medical record. All data were completed the BRIEF, overall health literacy score did not pre-
stored in a secure online database.31,32 Patients were divided dict PORT delay on univariable analysis (Table 2). When ex-
into 2 groups based on whether PORT was initiated within or amining individual subscores of the BRIEF, a lower self-
after 42 days. reported ability to learn written health information predicted
Univariable logistic regression was performed to gener- PORT delay (OR, 1.07; 95% CI, 1.00-1.16). In addition, a high
ate crude (unadjusted) odds ratios (ORs) based on patient CCI score category predicted delay (OR, 1.29; 95% CI, 1.06-
demographic information, clinical information, and survey 1.58).
scores. To better outline specific aspects of the BRIEF screen A series of multivariable logistic regression equations were
in relation to delays, individual question scores were com- generated, sequentially adding measures from different lev-
pared between cohorts. Multivariable logistic regression gen- els of influence in the social-ecological model. The first pre-
erated adjusted odds ratios (aORs) after controlling for other dictive model incorporating individual-level measures with-
variables in each model. With planned analysis of 8 variables out the BRIEF yielded a model with an area under the curve
spanning the levels of the social-ecological model, an enroll- (AUC) of 0.74 and R2 of 0.15 (eTable 2 in Supplement 1). A sec-
ment target of 135 patients was set, provided an expected in- ond predictive model incorporating the BRIEF with other in-
cidence of delays of 60% based on historical experience at our dividual-level measures yielded an improved model (AUC, 0.77;
institution. This would provide the “rule of thumb” of at least R2 = 0.17), and in which a low BRIEF learning score signifi-
10 events per variable prior to analysis.33 cantly predicted delay (aOR, 1.45; 95% CI, 1.02-2.13) (eTable 3

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Research Original Investigation Association of Social-Ecological Factors With Delay in Time to Initiation of Postoperative Radiation Therapy

Table 1. Demographics and Associations With Postoperative Radiation Therapy Delays

No. (%)
PORT delay
All Yes No
Characteristic (N = 171) (N = 104) (N = 67) Crude OR (95% CI)
Sex
Female 66 (38.6) 43 (41.3) 23 (34.3) 1.07 (0.92-1.25)
Male 105 (61.4) 61 (58.7) 44 (65.7) 1 [Reference]
White 161 (94.2) 63 (94.0) 98 (94.2) 1.01 (0.74-1.38)
RUCC, rurala 71 (41.8) 24 (36.4) 47 (45.2) 1.09 (0.94-1.27)
Age, mean (SD), y 61.0 (11.2) 62.3 (11.1) 59.0 (11.1) 1.01 (1.00-1.01)
Insurance
Employer-based 65 (38.5) 33 (32.4) 32 (47.8) 1 [Reference]
Public 75 (44.4) 50 (49.0) 25 (37.3) 1.17 (1.00-1.38)
Other 29 (17.2) 19 (18.6) 10 (14.9) 1.16 (0.94-1.43)
Employment
Full time 59 (35.3) 31 (30.7) 28 (42.4) 1 [Reference]
Part time 19 (11.4) 11 (10.9) 8 (12.1) 1.05 (0.82-1.36)
Unemployed 20 (12.0) 17 (16.8) 3 (4.5) 1.38 (1.08-1.77)
Retired 69 (41.3) 42 (41.6) 27 (40.9) 1.09 (0.92-1.29)
Education
High school 53 (31.9) 31 (31.3) 22 (32.8) 1 [Reference]
Some college 55 (33.1) 35 (35.4) 20 (29.9) 1.05 (0.87-1.27)
Completed college 35 (21.1) 21 (21.2) 14 (20.9) 1.02 (0.82-1.25)
Graduate education 23 (13.9) 12 (12.1) 11 (16.4) 0.94 (0.74-1.20)
Tumor site
Oral cavity 123 (71.9) 82 (78.8) 41 (61.2) 1 [Reference]
Oropharynx, HPV+ 23 (13.5) 9 (8.7) 14 (20.9) 0.76 (0.61-0.94)
Oropharynx, HPV− 4 (2.3) 1 (1.0) 3 (4.5) 0.66 (0.41-1.07)
Larynx 13 (7.6) 8 (7.7) 5 (7.5) 0.95 (0.72-1.25)
Other 8 (4.7) 4 (3.8) 4 (6.0) 0.85 (0.60-1.20)
AJCC clinical stage
1 19 (11.2) 7 (6.7) 12 (18.2) 1 [Reference]
Abbreviations: AJCC, American Joint
2 14 (8.2) 9 (8.7) 5 (7.6) 1.32 (0.94-1.84) Commission on Cancer; CCI, Charlson
3 29 (17.1) 18 (17.3) 11 (16.7) 1.29 (0.97-1.70) Comorbidity Index; HPV, human
4 108 (63.5) 70 (67.3) 38 (57.6) 1.32 (1.04-1.68) papilloma virus; PORT, postoperative
radiation therapy; RUCC, Rural Urban
Charlson Comorbidity Index (CCI) scoreb Continuum Codes.
Low (0-1) 34 (19.9) 17 (16.3) 17 (25.4) 1 [Reference] a
Urban corresponds to RUCC 1 to 2,
Intermediate (2-4) 75 (43.9) 40 (38.5) 35 (52.2) 1.03 (0.85-1.26) and rural corresponds to RUCC 3
to 9.
High (≥5) 62 (36.3) 47 (45.2) 15 (22.4) 1.29 (1.06-1.58)
b
Charlson Comorbidity Index was
Free flap reconstruction, yes 115 (67.3) 75 (72.1) 40 (59.7) 1.14 (0.98-1.34)
coded excluding the index cancer.

in Supplement 1). Including the community-level ADI yielded often insured through a public payer (4 [17%] vs 71 [49%]; dif-
a better-fitting model (AUC, 0.78; R2 = 0.18; eTable 4 in Supple- ference 32%; 95% CI, 11%-51%), less likely to present with stage
ment 1). The strength of the model was largely unchanged with 3 to 4 disease (3 [9%] vs 135 [92%]; difference 83%; 95% CI,
the addition of RUCC (Table 3). Although mean ADI was higher 68%-98%), and had significantly lower ADI (50th vs 62nd per-
among delayed patients, this result was not significant on mul- centile; difference 12 percentiles, 95% CI, 2nd percentile to 22nd
tivariable analysis (Table 2, Table 3). Controlling for all other percentile). Age, race and ethnicity, education level, rural sta-
factors, a high CCI score category significantly predicted de- tus, and BRIEF scores were not significantly different in par-
lay (aOR, 4.21; 95% CI, 1.11–17.60) (Table 3). ticipants with HPV-positive oropharyngeal tumors.
In addition, HPV-positive oropharyngeal tumors were pro- Further analysis was performed to assess the absolute dif-
tective of delays on multivariable analysis (aOR, 0.10; 95% CI, ferences in median days to PORT initiation between groups for
0.02-0.56) (Table 3). Compared with all other tumor sites in- each variable measured. Overall, median (IQR) days to PORT
cluding HPV-negative oropharyngeal cancers, participants with initiation in the delayed group was 53.5 (16.5) days. Patients
HPV-positive oropharyngeal tumors were less often women with public insurance were significantly more delayed in me-
(2 [9%] vs 64 [43%]; difference 34%; 95% CI, 18%-51%), less dian (IQR) days to PORT at 48.0 (18.5) days compared with 43.0

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Association of Social-Ecological Factors With Delay in Time to Initiation of Postoperative Radiation Therapy Original Investigation Research

Table 2. Association of Area Deprivation Index and Health Literacy With Postoperative Radiation Therapy Delay Abbreviations: ADI, area deprivation
index; BRIEF, BRIEF Health Literacy
Mean (SD)
Screening Tool; NA, not applicable;
PORT delay OR, odds ratio; PORT, postoperative
Variable All Yes No Crude OR (95%CI) radiation therapy.
a
No. 171 104 67 NA National percentile ranges from 1
ADI, national percentile, mean (SD)a
60.7 (24.2) 63.2 (22.6) 56.8 (26.2) 1.00 (1.00-1.01) (least disadvantaged) to 99 (most
disadvantaged).
Health literacy Alle NA NA NA b
Scores range from 4 to 12 (limited
No. 154 96 58 NA health literacy), 13 to 16 (marginal
BRIEF score, mean (SD)b 15.8 (3.8) 15.6 (3.7) 16.0 (4.0) 1.01 (0.99-1.03) health literacy), 17 to 20 (adequate
How often do you have… health literacy).
c
Scores range from 1 (always [lower
Someone to help you read hospital 3.7 (1.4) 3.8 (1.4) 3.6 (1.5) 0.98 (0.93-1.03)
materials?c level of health literacy]) to 5 (never
[higher level of health literacy]).
Problems learning about your medical 4.1 (1.1) 4.0 (1.1) 4.3 (1.0) 1.07 (1.00-1.16)
d
condition because of difficulty Scores range from 1 (not at all [lower
understanding written information?c level of health literacy]) to 5
A problem understanding what is told to 4.1 (1.0) 4.1 (0.9) 4.2 (1.1) 1.01 (0.93-1.09) (extremely [higher level of health
you about your medical condition?c literacy]).
How confident are you filling out medical 3.8 (1.2) 3.7 (1.2) 3.9 (1.2) 1.03 (0.96-1.10) e
Imputation was not performed for
forms by yourself?d
univariable analysis.

(16.0) days among patients with private insurance (P = .04).


Table 3. Multivariable Logistic Regression Model
of Postoperative Radiation Therapy Delay Risk Subsequent analysis of patients at extremes of delay revealed
Based on Individual and Community Factorsa that 40 (30.5%) patients were delayed past 56 days. Notably,
a significant association was found between low levels on the
Patient characteristic aOR (95%CI)
BRIEF learning score and extreme PORT delay (OR, 1.09; 95%
Age, y 1.03 (0.98-1.08)
CI, 1.03-1.16) (eTable 5 in Supplement 1).
Insurance
Employer-based 1 [Reference]
Public 1.23 (0.47-3.22)
Other 2.33 (0.84-6.79)
Discussion
CCI The prevalence of PORT delay in the present study (104
Low 1 [Reference] [60.8%]) supports the finding from national database stud-
ies that most patients with HNSCC do not receive timely ini-
Intermediate 0.63 (0.19-2.03)
tiation of adjuvant radiation therapy.10 The University of
High 4.21 (1.11-17.6)
Wisconsin Population Health Institute has estimated social
AJCC clinical stage
determinants of health and physical environment traced
1 1 [Reference] to an individual’s zip code account for 50% of health
2 4.40 (0.77-21.80) outcomes. 35 When considering health behaviors such as
3 1.67 (0.29-9.70) tobacco and alcohol use, interactions with the health care
4 1.35 (0.25-7.12) environment are only estimated to be driving 20% of out-
Tumor site
comes. Likewise, PORT delays are multifactorial, contribut-
ing to the complexity of predicting and mitigating their risk.
Oral cavity 1 [Reference]
Although not explicitly applying the social-ecological frame-
Oropharynx, HPV+ 0.10 (0.02-0.56)
work, prior studies have considered individual-level factors
Oropharynx, HPV− 0.21 (0.01-2.37) and added a level to the framework, with organization-level
Larynx 0.66 (0.17-2.65) factors increasing risk of PORT delay. Specifically, authors
Other 0.26 (0.04-1.60) include payers, separate surgical and PORT facilities, postop-
BRIEF, learning 1.43 (1.00-2.08) erative length of stay, advanced stage at presentation, and
ADI, national percentile 1.01 (0.99-1.03) tumor site.11,17,36 Contrary to these prior investigations, the
current study assessed the individual- and community-level
RUCC, rural 1.21 (0.53-2.75)
influences on delays and found that a predictive model
Abbreviations: ADI, area deprivation index; AJCC, American Joint Commission
incorporating multiple levels of influence from the social-
on Cancer; aOR, adjusted odds ratios; AUC, area under the curve; BRIEF, BRIEF
Health Literacy Screening Tool; CCI, Charlson Comorbidity Index; HPV, human ecological framework outperformed a model based on
papilloma virus; PORT, postoperative radiation therapy; RUCC, Rural Urban individual-level factors alone.
Continuum Codes. In addition, incorporating health literacy strengthened the
a
Multiple imputation was used to fill missing data (0.96% of data set). Using predictive model in this study. Disparities in cancer care have
multivariable logistic regression with individual-level factors and
been associated with lower levels of health literacy.37 Though
community-level factors, a significant model was found with an area under the
curve (AUC), 0.78; R2 of 0.18. objective measures of health literacy have not been used to pre-
dict PORT delay, the BRIEF screen has previously been used

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Research Original Investigation Association of Social-Ecological Factors With Delay in Time to Initiation of Postoperative Radiation Therapy

to predict self-directed behaviors in head and neck cancer, such to be independent factors affecting delays, but are also af-
as active engagement, positive attitude and self-monitoring, fected by social determinants of health emphasized in this
and skill acquisition.38 Lower scores have been associated with work. For example, the decision to pursue PORT at an out-
decreased functional well-being, socio-emotional quality of side facility is likely influenced by distance from facility, so-
life, and disease-specific health-related quality of life.38,39 cial support, and access to transportation.17 Lower baseline so-
Among individual-level factors in the current study, a lower cial support, health literacy, and access to a main tertiary
score specifically on the learning component of the BRIEF as- hospital are later compounded by fragmented coordination be-
sessment was significantly associated with PORT delay and tween surgical and radiation facilities.45 Similarly, clinical fac-
even extreme delays (past 56 days). Given the overwhelming tors previously associated with PORT delay in head and neck
information presented to patients with a new cancer diagno- cancer have included stage 4 disease and oral cavity site.11
sis, the tools in place to assist with information retention may Timely adjuvant therapy in patients with higher oncologic risk
not benefit individuals with lower written health literacy. For is critical, and appropriate risk stratification may guide ear-
example, these individuals may be less likely to reference or lier dental and radiation oncology referrals. In addition, pa-
understand information in after-visit summaries and online tients with higher baseline comorbidity status were at signifi-
medical record portals. Interventions targeting treatment de- cantly higher risk of delay in this study, which may reflect an
lays could benefit from improved communication methods via effect on downstream postsurgical factors such as length of
illustrations, videos, and teach-back methodologies em- stay or readmission not assessed in this study. By contrast, the
ployed by care coordinators reiterating priorities and track- favorable individual social circumstances plus insurance and
ing progress through treatment. This is the first study to in- income status in patients with HPV-mediated oropharyngeal
corporate the BRIEF in a discussion of PORT delay risk, and cancers in this study were likely the primary influencers con-
the strength of the predictive model emphasizes its applica- tributing to fewer delays, consistent with prior literature.46 Al-
tion in prospective risk stratification. though NCDB-based studies have been effective in outlining
Rural residence, as measured by the RUCC classification, the broad effect these factors have on delay risk, the present
was not associated with increased odds of PORT delay in the study offers a more precise understanding of the interplay be-
current study. These findings are contrary to what Shew and tween clinical and social factors to guide precise interven-
Levy et al found using data from the National Cancer Data- tions in clinical practice.
base (NCDB).8,11 There are a number of potential explana-
tions for these discrepant findings. First, county-level classi- Equity-Driven Interventions
fication may not have been sensitive enough to detect the true Preliminary trials aimed at targeting risk factors for PORT
influence of rurality in this cohort, where significant differ- delay have focused on improving care coordination through
ences in population density and urbanization exist in 1 county multidisciplinary referrals and tracking, clarifying patient
and where rurality may simply be a proxy for critical access navigator roles, community-based travel support, and
communities with limited health resources. Second, 71 (42%) patient education to emphasize goals.47,48 These interven-
participants in the cohort resided in rural communities, which tions have also targeted patients known to experience dis-
is much higher than in prior studies.8,11 Unfortunately, no op- parities in access to care through intentional recruitment.
timal measure has been developed to predict rural-urban health Pilot data from these interventions shows promising
disparities in all contexts.40 improvements in timely PORT initiation, and larger studies
Although ADI alone did not significantly predict delay in are under way to validate these findings.48 Though not spe-
initiating PORT, its interaction with individual-level factors cifically addressed in this study, the Medical Outcomes
strengthened the multivariable model. Factors potentially af- Study—Social Support Inventory (MOS-SSS) is a measure of
fecting its significance include the homogenous cohort, influ- social support evaluated in our prior work.45 Considered an
ence from historical exposures to disadvantage, or societal- interpersonal-level factor in the social-ecological model,
level influences such as Medicaid expansion, which was not social support has been shown to contribute to resilience
assessable in the nonexpansion state examined in this study. through cancer treatment, and has been associated with
The ADI was used to estimate social vulnerability, as it is a more increased follow-up, decreased travel burden, and improved
precise measure than income quartiles from zip code infor- depressive symptoms and psychological distress associated
mation available in the NCDB. Agreement exists in identify- with physical symptoms.7,17,49-51 In our prior study consist-
ing more significant delays and worse survival among indi- ing of a smaller cohort from the same patient population, a
viduals residing in lower-income areas.17,36,41 Furthermore, higher score on the MOS-SSS was indeed found to be a sig-
prior work across other disciplines suggests an individual’s nificant predictor of PORT delay, even when controlling for
address alone may predict risk without the need for individu- other baseline individual factors. In strengthening existing
ally reported household income information.42-44 Future mul- nomograms of risk factors for PORT delay, studies may con-
ticenter prospective studies may provide more robust assess- sider including individual, interpersonal, and community
ments of community-level influence, but the current study measures employed in this study and our prior work. Future
findings highlight the importance of environment on health trials could adopt these measures to better stratify patient
behavior. risk factors for delays, and offer more precise interventions
Structure and process factors relating to care coordina- that address both system care processes and negative social
tion and availability of consultation services have been shown determinant factors critical to timely therapy.

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Association of Social-Ecological Factors With Delay in Time to Initiation of Postoperative Radiation Therapy Original Investigation Research

Limitations evaluated this variable and found it to be significant on mul-


This is a single-institution study at a tertiary academic center tivariable analysis. However, because PORT facility is often not
with a relatively homogenous patient cohort of White men, known at baseline, we chose to include the RUCC and ADI
thus limiting generalizability across patient populations. Al- scores as community-level measures, which likely influence
though the BRIEF has been validated for use in more repre- the choice of PORT facility. Moreover, this study was not pow-
sentative samples, the present results are subject to selection ered to assess additional variables that may affect baseline
bias and should be replicated in other patient populations. PORT delay risk, such as BMI and smoking history. Future stud-
Inherent social acceptability and voluntary enrollment bias also ies may evaluate the influence of these individual-level vari-
exists in self-reported information obtained via in-person sur- ables on a predictive model of risk.
veys. We considered the potential for selection bias relating
to participant consent for enrollment and patient factors in-
fluencing the likelihood for consent. However, we offer en-
rollment to every new patient in our clinic, with a participa-
Conclusions
tion rate of no less than 90%, limiting this source of bias. Ample evidence exists to demonstrate the systemic inequi-
Estimates of rurality were made based on data from the 2013 ties that predispose certain individuals to PORT delay. As shown
edition of RUCC, which may not account for recent changes in in iterative predictive models presented in this prospective co-
populations. Among the 8 participants with only PO box lo- hort study, precise community-level measures of vulnerabil-
cations provided, we acknowledge the potential discrepancy ity provide additional predictive value, and may be consid-
between ADI closer to their physical residence. However, be- ered in multicenter studies examining the social determinants
cause this was such a small proportion of participants, it did of delays and outcomes. The current study presents patient-
not significantly influence our findings. In addition, resi- centered precise measures of risk that aid in identifying those
dence, insurance, and employment status were captured at a at highest risk for delays. Future studies may also apply these
single time point and do not account for changes between the measures to develop resource-conscious interventions, with
initial consultation and initiation of PORT. As PORT facility rela- the goal of reducing the effect of nonmodifiable risk factors
tive to surgical facility has been shown to affect delays, we on PORT delay.

ARTICLE INFORMATION JAMA-Otolaryngology Head & Neck Surgery. 4. Harris JP, Chen MM, Orosco RK, Sirjani D, Divi V,
No other disclosures were reported. Hara W. Association of survival with shorter time to
Accepted for Publication: February 14, 2023.
radiation therapy after surgery for US patients with
Published Online: April 20, 2023. Disclaimer: Dr Graboyes is on the JAMA
head and neck cancer. JAMA Otolaryngol Head Neck
doi:10.1001/jamaoto.2023.0308 Otolaryngol Head–Neck Surgery Editorial Board; but
Surg. 2018;144(4):349-359. doi:10.1001/jamaoto.
he was not involved in any of the decisions
Author Contributions: Dr Sykes had full access to 2017.3406
regarding review of the manuscript or its
all of the data in the study and takes responsibility acceptance. 5. Graboyes EM, Kompelli AR, Neskey DM, et al.
for the integrity of the data and the accuracy of the Association of treatment delays with survival for
data analysis. Data Sharing Statement: See Supplement 2. Due patients with head and neck cancer: a systematic
Concept and design: Sawaf, Virgen, Renslo, to the sensitive nature of this data, we are unable to review. JAMA Otolaryngol Head Neck Surg. 2019;
Farrokhian, Somani, Kakarala, Shnayder, Graboyes, make it publicly available. However, the senior 145(2):166-177. doi:10.1001/jamaoto.2018.2716
Sykes. author is willing to provide deidentified data upon
6. Commission on Cancer. ACS. Accessed August 3,
Acquisition, analysis, or interpretation of data: request. 2022. https://www.facs.org/for-medical-
Sawaf, Virgen, Renslo, Farrokhian, Yu, Bur, Gan, Additional Contributions: We thank Zack professionals/news-publications/news-and-
Graboyes, Sykes. Arambula, BA, and Joseph Penn, BS, at University articles/cancer-programs-news/030322/coc/
Drafting of the manuscript: Sawaf, Virgen, Renslo, of Kansas Department of Otolaryngology–Head & 7. Sykes KJ, Morrow E, Smith JB, et al. What is the
Farrokhian, Somani. Neck Surgery, for their extensive contributions to hold up?-Mixed-methods analysis of postoperative
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