Download Knowledge about Head and Neck Cancer

1
A Survey of Primary Care Providers’ Knowledge of HPV-associated Head and Neck
Cancers: A focus on clinical characteristics, presentation and outcomes
By
James Taylor
A Master’s Paper submitted to the faculty of
the University of North Carolina at Chapel Hill
in partial fulfillment of the requirements for
the degree of Master of Public Health in
the Public Health Leadership Program
Chapel Hill
2016
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Table of Contents
Abstract ...........................................................................................................................................3
Introduction ....................................................................................................................................5
Methods ...........................................................................................................................................6
Results .............................................................................................................................................7
Demographics and Response Rates .....................................................................................8
Knowledge of Head and Neck Cancer .................................................................................9
Knowledge of HPV-associated Head and Neck Cancer ......................................................9
Knowledge of HPV Infection ..............................................................................................9
Discussion........................................................................................................................................9
Tables ............................................................................................................................................14
References .....................................................................................................................................20
Appendix .......................................................................................................................................26
Title (2) ..........................................................................................................................................35
Introduction (2) ............................................................................................................................36
Methods (2) ...................................................................................................................................37
Results (2) .....................................................................................................................................39
Discussion (2) ................................................................................................................................42
References (2) ...............................................................................................................................46
Appendix (2) .................................................................................................................................52
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A Survey of Primary Care Providers’ Knowledge of HPV-associated Head and Neck
Cancers: A focus on clinical characteristics, presentation and outcomes
Importance: The epidemiology of head and neck cancer has changed in recent years,
particularly as related to those associated with human papillomavirus (HPV). Understanding
primary care physicians’ (PCPs) current knowledge about HPV-associated head and neck
cancers (HNC) will help inform educational efforts on this important topic.
Objective: To assess the knowledge and understanding of PCPs towards the rapidly changing
clinical characteristics, presentation and outcomes associated with HPV-positive HNCs
Design, Setting and Participants: Online survey of primary care physicians (pediatricians,
general internists and family medicine physicians) at two tertiary academic medical centers in
North Carolina between May and July of 2016.
Results: 275 PCPs at two tertiary academic medical centers were invited to participate via email,
95 PCPs completed the survey for a response rate of 34.5%. The majority of respondents were
female (67.0%), attending physicians (61.5%), had less than 10 years of practice experience
(46.0%), and practiced in an academic setting (85.3%). PCPs correctly answered 56% of
knowledge based questions about HPVs causative role in HNC. 79% of PCPs failed to correctly
identify the most common clinical presentation of the HPV-positive patient. Further, only 23%
of PCPs correctly identified that HPV is associated with a much improved prognosis in HNC.
Survey data indicate that PCPs most commonly consider the HPV-positive patient to be an
African American male presenting with a persistent sore throat or non-healing ulcer and to have
prior tobacco and alcohol consumption. However, PCPs demonstrated a high degree of
knowledge on HPV infection correctly answering 91% of questions regarding HPV infection.
4
Conclusions and Relevance: Although knowledgeable about HPV infection, PCPs are less
knowledgeable about HPV’s role in head and neck cancer. We demonstrate the need for
additional education among PCP physician groups with a focus on the clinical characteristics,
presentations, and outcomes of the HPV-positive HNC patient.
5
Introduction
Cancer of the head and neck is the sixth most common cancer worldwide with an
estimated incidence of 633,000 cases annually.1 Recently in the United States the overall
incidence of head and neck cancer (HNC) has declined, paralleling decreases in tobacco use.2
However, despite the overall decline in head and neck cancers, there has been an increase in the
incidence of oropharyngeal squamous cell carcinoma (OPSCC) driven by human papillomavirus
(HPV) infection.3 It is estimated that the incidence of HPV-associated OPSCC has increased by
225% from 1988-2004.4 Compared to patients with HPV-negative HNCs, patients with HPVpositive HNCs tend to be younger, from higher socioeconomic status, have less tobacco and
alcohol exposure, and are more likely to be caucasian.5-6 In addition, HPV-positive disease tends
to have superior oncologic outcomes and improved response to therapy.7,8 Due to the substantial
differences between patients who present with HPV-positive and HPV-negative HNC, it is
imperative that primary care physicians are knowledgeable about the rapidly changing
epidemiology, clinical characteristics and outcomes associated with HPV-driven HNC in order to
appropriately refer high-risk patients.
Currently, a paucity of data exist regarding the knowledge and awareness of HPVassociated HNCs among primary care physicians (PCPs).9 Previous studies have estimated that
nearly 20% of chief complaints in primary care involve the head and neck; thus, PCPs have the
difficult task of identifying, screening, and referring patients who are at highest risk for HNC
and serve a crucial role in primary prevention of these malignancies.10,11 Although questions
about tobacco and alcohol use could previously be used to effectively risk-stratify patients with
head and neck complaints, these questions may be less sensitive in light of the recent emergence
6
of HPV-related HNC. Overall, the rapid changes associated with HPV-positive HNC pose
significant clinical challenges for both PCPs and specialists.
The goal of this research is to build upon efforts by the American Head & Neck Society
(AHNS) to help educate providers from multiple specialties on the rapidly changing presentation
and outcomes associated with HPV-positive head and neck cancers by identifying areas where
additional educational resources would benefit PCPs. In order to gain insight into the knowledge
of PCPs with respect to HPV-positive HNC, a survey was developed and distributed at two
tertiary academic medical centers in North Carolina.
Methods
We developed a 29-question electronic survey to assess the current knowledge of PCPs in
regards to HPV-positive HNC. The survey included a broad assessment of three topics: general
knowledge of head and neck cancer, general knowledge about HPV, and specific knowledge
about the association of HPV with head and neck cancers. This survey instrument was
developed in a collaborative manner with input from head and neck oncology specialists,
radiation oncologists, family physicians, and epidemiologists at the University of North Carolina
at Chapel Hill (the full survey is located in the appendix). In addition, relevant literature and
practice guidelines were searched and incorporated into the development process. Finally,
several questions previously used in a survey of AHNS members on awareness of HPVassociated head and neck cancers were included with permission.12 Content and discriminant
validity were assessed by a group of 5 physicians and 5 medical students respectively.
The final survey was distributed to PCPs, including residents and attending physicians, at
the University of North Carolina at Chapel Hill and Wake Forest University in North Carolina.
7
For the purpose of this study, the term “PCPs” included general pediatricians, general internists
and family medicine physicians. The survey was made available to these physicians via an online
form (Google Forms, Alphabet Inc., Mountain View, CA) between March and July of 2016. No
compensation or incentive was provided for participation. The study was approved by the
institutional review board at the University of North Carolina at Chapel Hill.
Individual scores were calculated as percent for correct overall and for each category of
questions and stratified by specialty. Additionally, overall scores were calculated for each
knowledge based question. We compared means with either student’s t-test or ANOVA as
appropriate with SAS 9.4 (SAS Institute, Cary, NC).
Results
Demographics and Response Rates
The survey had an overall response rate of 34.5% with 95 of 275 PCPs responding and
completing the survey. One respondent answered less than 50% of the survey and was excluded
from data analysis. Provider characteristics for respondents can be found in Table 1. Over twothirds of respondents were female (67%). Pediatricians had the highest proportion of respondents
with a 41.7% response rate, followed by family medicine at 36.4%. The majority of respondents
were attending physicians (61%) and were practicing in an academic setting (85%). Of
responding attending physicians 46% had less than 10 years of practice experience.
Knowledge about Head and Neck Cancer
The overall percentage of correctly answered questions about general head and neck
cancer knowledge was 68% (Standard Deviation (SD): 18%). Survey questions and answers with
8
percentage of correct responses for general HNC can be found in Table 2. The most commonly
missed question was “the incidence of head and neck cancer is decreasing in the United States”
with only 19% responding correctly. When stratified by specialty, pediatricians had the average
highest percentage of correctly answered questions (72%) followed by family and internal
medicine (67% and 64% respectively). Results stratified by question category and specialty can
be found in Table 3.
Knowledge about HPV’s Causative Role in HNC
The percentage of correct responses was relatively low for knowledge regarding HPVdriven HNCs at 56% (SD 15%). The corresponding questions and percent correct can be found
in Table 4. Only 61% of respondents correctly identified the oropharynx as the most common
site for HPV-positive head and neck cancer to occur. Additionally, only 21% correctly identified
that a painless neck mass is the most common presentation for HPV-positive OPSCC.
Pediatricians had a 58% correct response rate followed by family medicine and internal medicine
at 56% respectively (p-value: 0.77).
Knowledge about HPV Infection
Overall, accuracy for knowledge about HPV infection was greater than for either general
HNC knowledge or knowledge of HPVs causative role in HNC as evidenced by Table 5. Most
respondents correctly indicated “most patients with HPV do not experience symptoms of
infection” (98%). The average percentage of correctly answered questions on general knowledge
of HPV infection was 91% (SD 14%). Although not statistically significant, we found that
family physicians were most knowledgeable about HPV infection with a 93% overall correct
response rate, followed by internal medicine and pediatrics at 90% and 87%, respectively.
9
Discussion
A growing body of literature has demonstrated that patients with HPV-positive OPSCC
have distinct risk factors, oncologic outcomes and improved survival compared with non-HPV
HNC cancer patients.13 These significant differences between HPV-positive and HPV-negative
HNCs indicate that cancers driven by HPV may be biologically and clinically distinct entities
from cancers caused by tobacco and alcohol. This rapid change in the incidence of HPV-positive
HNCs poses significant clinical challenges. Specifically, for PCPs who are often the first
providers to see a patient with various complaints, the presentation of the “classic” head and
neck cancer patient is changing. Correctly identifying high-risk patients among the
approximately 20% of primary care patients with complaints involving the head and neck will
require primary care physicians to be aware of clinical presentations and risk factors for HPVrelated HNC.10,14
To our best knowledge, no previous studies in the United States have been conducted to
assess the level of knowledge of PCPs about HPV-associated head and neck cancers. In our
study, PCPs correctly answered only 68% of questions assessing general head and neck cancer
knowledge. Respondents were most knowledgeable with respect to common risk factors for
developing HNC correctly identifying that tobacco and alcohol remain the most important risk
factors for HNC. However, as hypothesized, knowledge regarding the HPV-positive HNC
patient was lower compared with knowledge about general HNC patients. Overall, PCPs poorly
understood the most common demographics and presentation of the HPV-positive patient.
Survey data indicate that PCPs most commonly consider the HPV-positive patient to be an
African American male presenting with a persistent sore throat or non-healing ulcer and to have
prior tobacco and alcohol consumption. In reality the most common clinical picture is a younger
10
Caucasian male presenting with a painless neck mass without a significant alcohol and tobacco
history.15,16 This information indicates that PCPs are not fully aware of the demographic
differences between the HPV-positive and HPV-negative HNC populations. These
misunderstandings hold the potential to lead to delayed initial diagnosis, as well as a decreased
likelihood of the providers obtaining a relevant sexual history to evaluate for risk factors for
HPV transmission.
Additionally, most PCPs believe that HPV-positive patients respond worse to
chemoradiotherapy and have worse outcomes overall in regards to morbidity and survival. This
is the opposite of the clinical picture associated with HPV-positive patients who have improved
response to therapy and clinical outcomes.17 Although a detailed understanding of HPV HNC
prognosis and treatment is unnecessary in the context of appropriate primary care, basic
awareness of treatment modalities and outcomes can dramatically alter physician approaches to
initial patient counseling and referral. For example, the presence of regional lymph node
metastasis in HPV-negative HNC patients is considered to be a major indicator of poor
prognosis.15 In contrast, HPV-positive OPSCC patients tend to have more extensive lymph node
metastasis at time of diagnosis, but this is not associated with major changes in outcome.18
Considering that HNCs can often present with relatively general, insidious symptoms,
PCPs are likely to be the first providers to assess many of these patients and play a vital role in
preventing diagnostic delay.14 In the absence of national HNC screening guidelines from the
United States Preventive Services Task Force (USPSTF), early detection of HNC is even more
reliant on the judgment and knowledge of PCPs. Furthermore, errors or delays in diagnosis can
have grave consequences as patients diagnosed with late stage disease often require more
aggressive treatment and have a poorer prognosis.19 Therefore, education specifically directed
11
towards PCPs to increase awareness of the common clinical characteristics and presentations of
HPV-positive HNC patients has the potential to improve outcomes through increased
surveillance and early detection.
Despite this clear importance of HNC awareness among PCPs, there is evidence that
current levels of HNC and otolaryngology knowledge among this group may be sub-optimal. A
2012 survey found that significant portions of PCPs incorrectly identified common presentations
of otolaryngology diseases.20 Furthermore, a study conducted by Jackowska et al in Poland
found that general practitioners (GPs) were less knowledgeable regarding the association
between HPV and head and neck cancer compared with otolaryngologists.9 A similar study of
GPs in Italy found that GPs were considerably less knowledgeable about the association of HPV
and HNC, compared to HPV’s role in the development of cervical, vulvar and vaginal cancers.21
Overall, when queried, the vast majority of PCPs subjectively desired further education and
training about otolaryngology.22
Overall, despite previous studies showing that otolaryngologists are quite knowledgeable
about these HPV-related shifts in head and neck oncology, our results clearly indicate that novel
and clinically important HPV research is inconsistently being presented to clinicians in primary
care fields.12 Furthermore, our study provides evidence about where knowledge gaps exist
among PCPs’ understanding of HPV-positive HNC, specifically, the common presentations, risk
factors, demographics, and outcomes of this disease. Assessing these awareness gaps objectively
allows for specialty societies, such as the American Head and Neck Society, to collaboratively
work with family medicine, pediatric, and internal medicine groups to develop educational tools.
In fact, a 2013 survey-based study found that 96% of AHNS members support efforts by the
AHNS to educate other clinicians about the link between HPV infection and head and neck
12
cancer.12 Overall, we demonstrate the need for increased education among primary care
providers with a focus on the HPV-positive patient.
The solutions to this challenge will likely be multifold. One potential avenue is
addressing the knowledge gaps early by incorporating additional otolaryngology education into
medical school curriculums in the United States. Currently, less than 2/3 of American medical
schools require any clinical otolaryngology experience.23 This gap likely contributes to the fact
that several previous studies have shown insufficient HNC knowledge and physical exam skills
among medical students, as well as to ongoing HNC knowledge deficits later in these students’
careers.24-22 Additionally, otolaryngology professional societies should continue to encourage
primary care providers to attend otolaryngology conferences or work in unison to organize multispecialty conferences where relevant HNC and HPV research can be presented to both PCP and
otolaryngology researchers.
Overall, we believe that our study is the first to objectively measure the awareness of
HPV-related trends in HNC among PCPs in the United States and builds upon the AHNS’ recent
emphasis on education.12 Strengths of our study include a multidisciplinary team of clinicians
and researchers who assisted in the survey development process, a high response rate by
attending physicians, and survey distribution at two large academic medical centers. Limitations
include an overall response rate of 34.5% that could possibly lead to nonresponder bias and
limited geographical distribution that could potentially fail to capture a more diverse practice
setting. Although relatively low, this response rate is comparable to previous electronic surveys
of physicians.25
13
Our study provides evidence that PCPs, although knowledgeable with respect to the
“classic” head and neck cancer patient, are less knowledgeable about the HPV-positive head and
neck cancer patient. We demonstrate a need for additional education among PCPs with respect to
HPV-positive HNCs. Innovative and collaborative efforts, directed at increasing both
otolaryngology training in medical education and among active PCPs will be needed in a timely
manner to improve current knowledge gaps. Such collaborative efforts should be conducted in a
manner that maximizes the role of the primary care physician within the multidisciplinary
oncologic treatment team.
14
Table 1. Provider Characteristics
Respondents ,%
Provider Characteristics
(n=95)
Sex
Male
33.0
Female
67.0
Practice Time (years)
Resident/Fellow
41.0
1-10
26.3
11-20
14.8
>20
17.9
Practice Setting
Academic
85.3
Clinic or Public Hospital
10.5
Other
4.2
Primary Discipline
Internal Medicine
23.4
Pediatrics
26.6
Family Medicine
48.9
Other
1.1
15
Table 2. General Knowledge of HNC
Question
Answer (True/False)
Mean Percent
Correct
Head and neck cancer patients commonly present with
False
92.5%
True
88.3%
True
86.2%
False
52.1%
False
19.1%
early stage disease
Head and neck cancer occurs more commonly in males
than females
Alcohol and tobacco remain the most important risk factors
for head and neck cancer
Cancer of the larynx is the most common site for head and
neck cancer to occur
The incidence of head and neck cancer is decreasing in the
United States
16
Table 3. Percent correct by question category and specialty
Question Category
Mean Percent Correct
P-value
(SD)
General Head and Neck Cancer
Pediatrics
72% (17%)
Family Medicine
67% (16%)
Internal Medicine
64% (19%)
0.26
General HPV
Pediatrics
87% (15%)
Family Medicine
93% (15%)
Internal Medicine
90% (13%)
0.21
HPV-related head and neck
cancer
58% (13%)
Pediatrics
56% (14%)
Family Medicine
56% (19%)
Internal Medicine
0.77
17
Table 4. HPV-associated HNC Knowledge
Question
All types of HPV can lead to head and neck cancer
Answer
Mean Percent Correct
False
86.2%
Have a younger
83.0%
True
False
HPV positive vs HPV negative head and neck cancer
patients are more likely to?
Have a younger mean age at diagnosis
mean age at
diagnosis
Have an older mean age at diagnosis
Have a similar mean age at diagnosis
Where is the most common site for HPV positive head and
Oropharynx
60.6%
HPV positive vs HPV negative patients are more likely to
Less tobacco and
53.2%
have
alcohol exposure
neck cancer
Oral cavity
Oropharynx
Hypopharynx
Oral tounge
Greater tobacco and alcohol exposure
Less tobacco and alcohol exposure
Similar tobacco and alcohol exposure
HPV positive vs HPV negative head and neck cancer is
False
45.7%
18
more likely to occur in African Americans
True
False
HPV positive head and neck cancers respond worse to
False
45.7%
True
22.6%
Painless neck mass
21.3%
chemoradiotherapy
True
False
HPV is associated with a much improved prognosis for
patients with head and neck cancer
True
False
What is the most common presenting sign for patient with
HPV-positive oropharynx cancer
Non healing ulcer
Painless neck mass
Dysphagia
Persistant sore throat
19
Table 5. General knowledge of HPV Infection
Question
Answer
Mean Percent Correct
(True/False)
Most patients with HPV experience symptoms of the
False
97.8%
False
95.7%
False
94.7%
False
74.2%
infection
Patients with a history of HPV infection should not be
offered the HPV vaccination
HPV is a relatively uncommon sexually transmitted
infection
Current HPV vaccinations do not cover serotypes
associated with head and neck cancers
20
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Appendix
Head and Neck Cancer: A Changing Presentation
Please tell us about your medical practice.
Provider Characteristics
Please choose the most appropriate answer by marking in the oval:
In what discipline did you receive your primary training?
Mark only one oval.
o
Family Medicine
o
Internal Medicine
o
Pediatrics
o
Other
If you answered "other" for the previous question, please provide what you consider your
primary discipline:
How many years have you been in practice?
Mark only one oval.
o
Resident
o
Clinical Fellow
o
1-5
o
6-10
o
11-15
27
o
16-20
o
>20
In which practice setting do you most commonly practice?
Mark only one oval.
o
Private Practice
o
Academic Setting
o
Clinic or Public Hospital
o
Managed Care Organization
o
Other
What gender do you identify with?
Mark only one oval.
o
Male
o
Female
General Knowledge Regarding Head and Neck Cancers
Please indicate either True or False:
The incidence of head and neck cancer is decreasing in the United States.
Mark only one oval.
o
True
o
False
28
Cancer of the larynx is the most common site for head and neck cancer to occur.
Mark only one oval.
o
True
o
False
Head and neck cancer patients commonly present with early stage disease.
Mark only one oval.
o
True
o
False
Alcohol and tobacco remain the most important risk factors for head and neck cancer.
Mark only one oval.
o
True
o
False
GENERAL KNOWLEDGE OF HUMAN PAPILLOMAVIRUS AND
PREVENTION
Please indicate either True or False:
All types of Human Papillomavirus (HPV) can lead to head and neck cancer.
Mark only one oval.
o
True
o
False
29
HPV-positive head and neck cancers respond worse to chemoradiation therapy.
Mark only one oval.
o
True
o
False
HPV is a relatively uncommon sexually transmitted infection.
Mark only one oval.
o
True
o
False
HPV is associated with a much improved prognosis for patients with head and neck
cancer.
Mark only one oval.
o
True
o
False
Head and neck cancer occurs more commonly in males than females.
Mark only one oval.
o
True
o
False
Patients with a history of HPV infection should not be offered the HPV vaccination.
Mark only one oval.
30
o
True
o
False
Most patients with HPV experience symptoms of the infection.
Mark only one oval.
o
True
o
False
Current HPV vaccinations do not cover serotypes associated with head and neck cancers.
Mark only one oval.
o
True
o
False
Knowledge of HPV Head and Neck Cancer Patients
Please choose the most appropriate answer:
Where is the most common site for HPV positive head and neck cancer?
Mark only one oval.
o
Oral Cavity
o
Oropharynx
o
Hypopharynx
o
Oral Tongue
HPV positive vs HPV negative head and neck cancer patients are more likely to:
31
Mark only one oval.
o
Have a younger mean age at diagnosis.
o
Have an older mean age at diagnosis.
o
Have a similar mean age at diagnosis.
What is the most common presenting sign for a patient with HPV positive oropharynx
cancer?
Mark only one oval.
o
Nonhealing ulcer
o
Dysphagia
o
Painless neck mass
o
Persistent sore throat
HPV positive vs HPV negative head and neck cancer is more likely to occur in African
Americans.
Mark only one oval.
o
True
o
False
HPV negative vs HPV positive head and neck cancer patients are more likely to have:
Mark only one oval.
o
Greater tobacco and alcohol exposure.
o
Less tobacco and alcohol exposure.
32
o
Similar tobacco and alcohol exposure.
Current Practice Trends
Please select the most appropriate answer:
When you discuss alcohol related diseases with patients, how often do you discuss
alcohol as a risk factor for head and neck cancer?
Mark only one oval.
o
Always
o
Often
o
Sometimes
o
Seldom
o
Never
When you discuss smoking related diseases with patients, how often do you discuss
smoking as a risk factor for head and neck cancer?
Mark only one oval.
o
Always
o
Often
o
Sometimes
o
Seldom
o
Never
33
When you discuss smokeless tobacco related diseases with patients, how often do you
discuss smokeless tobacco as a risk factor for head and neck cancer?
Mark only one oval.
o
Always
o
Often
o
Sometimes
o
Seldom
o
Never
How often do you recommend the HPV vaccination to eligible female patients?
Mark only one oval.
o
Always
o
Often
o
Sometimes
o
Seldom
o
Never
o
N/A
How often do you recommend the HPV vaccination to eligible male patients?
Mark only one oval.
o
Always
o
Often
o
Sometimes
34
o
Seldom
o
Never
o
N/A
When you discuss the benefits of the HPV vaccination with female patients, how often do
you discuss protection from head and neck cancer as a potential benefit?
Mark only one oval.
o
Always
o
Often
o
Sometimes
o
Seldom
o
Never
o
N/A
When you discuss the benefits of the HPV vaccination with male patients, how often do
you discuss protection from head and neck cancer as a potential benefit?
Mark only one oval.
o
Always
o
Often
o
Sometimes
o
Seldom
o
Never
o
N/A
35
A Systematic Review of the Knowledge, Attitudes and Beliefs of Primary Care Physicians
towards Human Papillomavirus-Positive Head and Neck Cancer
36
Introduction
Cancers of the head and neck are a heterogenous group of malignancies that share
common anatomical origins.6 Historically, head and neck cancers (HNCs) have been classified
based upon their anatomic locations.26 Recently, due to many clinical and biological differences,
a subset of HNCs oropharyngeal squamous cell carcinomas (OPSCC) have been further divided
based upon their association with Human Papillomavirus (HPV). 1 In the United States, it is
estimated that the incidence of HPV-positive OPSCC has increased by 225% from 1988 to
2004.2,27,4 Several theories have been proposed to explain this trend, yet the causative
mechanisms underlying this increase have not been fully elucidated.5 Compared with HPVnegative OPSCC, patients with HPV-positive OPSCC have distinct risk factor profiles, treatment
strategies, and clinical outcomes.7,28 Additionally, these patients tend to be younger, from higher
socioeconomic status, have less tobacco and alcohol exposure, and are more likely to be
Caucasian.4 HPV-positive disease may require less aggressive treatments compared with HPVnegative disease and has demonstrated superior oncologic outcomes and improved response to
therapy over various treatment modalities.7,29 Due to these substantial differences, it is
imperative that primary care physicians (PCPs) are knowledgeable about the rapidly changing
clinical picture of the HPV-positive OPSCC patient.
Currently, limited data exist that detail the present knowledge, attitudes, and beliefs
towards HPV-positive OPSCC among primary care physicians (PCPs).9 PCPs form the backbone
of the healthcare system and provide the referral base to head and neck surgeons. Therefore, their
knowledge of HPV-positive OPSCC plays a critical role in ensuring the timely referral of
patients to head and neck specialists.30,31Additionally, many primary care physicians serve as a
patient’s primary medical resource. In this role, primary care physicians seek to educate their
37
patients on preventive health measures, inform their patients of screening recommendations, and
aid their patients in shared medical decision making. Additionally, with the advent of the HPV
vaccine, there is an added interest in its role in prevention of HPV-positive OPSCC. Therefore,
without formal screening guidelines for head and neck cancers, the rapid changing factors
associated with HPV-positive OPSCC and the potential for prevention through increased
vaccination, it is imperative that PCPs are knowledgeable with respect to this evolving disease.
The purpose of this systematic review is to examine the current literature regarding
studies which provide insight into the overall knowledge, attitudes, and beliefs of PCPs (and
head and neck surgeons) towards HPV-positive OPSCC. The objectives (key principles) of the
review are to (1) examine the current level of knowledge among PCPs on HPV-positive OPSCC
(2) examine the practice patterns of PCPs towards HPV-positive OPSCC with a focus on risk
factor counseling and (3) examine the beliefs of PCPs towards the HPV-vaccination as a method
of prevention for OPSCC.
Methods
Search Criteria
A computerized search of PubMed, CINHAL and SCOPUS was performed to identify
pertinent articles published between January 1, 2000 and July 2, 2016. The date January 1, 2000
was selected to reflect the Gillison et al. paper which first reported on HPV status in HNSCC
patients.32 Prior to 2000, HPV status was not widely reported in head and neck cancer, and it was
determined that expanding the search beyond January 1, 2000 would not be relevant for the
current study. Additionally, due to limited data on PCPs knowledge of HPV-positive OPSCC,
terms for head and neck surgeons were added to the search criteria as several studies contain
38
information comparing head and neck surgeons’ knowledge to that of PCPs. The full search
strategy for each database can be found in Table 1. Briefly, we used combinations of key terms
to search each database based on database specific criteria.
Additionally, to ensure the thoroughness of the search, hand searches were performed on
relevant articles returned from the initial search strategy. Articles identified by hand searches
were reviewed, critically appraised and, when deemed appropriate, incorporated into the review.
Finally, ClinicalTrials.gov was searched to identify any unpublished studies and results. Studies
were screened at the abstract level and during full text review. Ultimately, articles were included
only if they had relevant information pertaining to (1) oropharyngeal squamous cell carcinoma,
(2) head and neck cancer, (3) primary care physicians (pediatricians, internal medicine
physicians and family medicine physicians) or head and neck surgeons, (4) contained data
commenting on one of the three principles established for the current review and (5) included
information from surveys, questionnaires, or focus groups. For details on inclusion and exclusion
criteria see Table 2. Studies were excluded if PCPs knowledge, attitudes, and beliefs were
modeled (Table 2). Only English language studies were included in the analysis and any studies
published from countries outside of the Organisation for Economic Co-Operation and
Development (OECD) were excluded.
Data Extraction
We reviewed all titles and abstracts of studies identified using the defined search
strategies. Articles that did not meet inclusion criteria based upon their titles and abstracts were
excluded from full text review. We designed and used prespecified structured forms to extract
pertinent information from each article, including but not limited to, number of participants
39
(respondents), type of participants, study design, survey (or questionaire) response rates, survey
(or questionaire) questions, location where research was conducted, and study outcomes.
Assesment of Risk of Bias
The quality of each study was assessed by a single reviewer (JT) using a pre-specified
critical appraisal and risk of bias template consisting of 15 quality assessment metrics. All
studies, regardless of the number of subjects, were considered equally. Due to the types of
studies included in the current review (survey based studies), non-responder bias was critically
appraised and commented on below.
Results
As of July 2nd, 2016, the aforementioned search strategy returned 131 citations. After
removing 31 studies identified as duplicates, 100 original studies remained (Figure 1. Prisma
Flow Diagram). Of these studies, 93 were excluded during abstract and title review because they
did not fulfill the defined selection criteria. Following title and abstract review, seven studies
remained and were included in the full text review process. Of the remaining studies, five were
excluded because they did not fulfill study criteria and were deemed inappropriate for the current
review (Table 3.). In total, two articles were included for review.
Table 4 lists pertinent information on each included study. The first study entitled “A
Survey of Current Practices, Attitudes, and Knowledge Regarding Human Papillomavirus–
Related Cancers and Vaccines Among Head and Neck Surgeons” by Malloy et al. was published
in JAMA otolaryngology- head and neck surgery and contained information on head and neck
surgeons understanding of HPV-positive OPSCC.33 The second study identified by Jackowska et
40
al. was published in PLoS ONE, a free online open access journal, and contained information on
general practitioners (GPs) as well as otolaryngologists in Poland.9
The paper published by Malloy et al. had a response rate of 27.5% while the paper by
Jackowska et al. had a response rate of only 19.2%. For details on study characteristics and
response rates, see Table 5. Key questions, answers, and responses from the study by Malloy et
al. can be found in Tables 6 and 7. Lastly, Table 8 includes key information from the paper by
Jackowska et al. The tables do not include an exhaustive list of the questions or answers asked
from each survey based study, but instead represent key questions that address one or more of
the three principles established for the current review. A rating of moderate has been assigned to
each study when assessing for risk of bias. This grade was assigned due to low response rates
leading to risk of non-responder bias.
The study by Malloy and colleagues demonstrates that head and neck surgeons are
knowledgeable with respect to HPV and its role in head and neck cancers. Table 6 and Table 7
present the results from knowledge and practice pattern based questions respectively.
Furthermore, this study demonstrates that head and neck surgeons are knowledgeable about
general aspects of HPV. Importantly, the authors demonstrate that head and neck surgeons in the
United States desire to play a larger role in prevention and educational efforts regarding the link
between HPV and head and nek cancers. The authors conclude that additional educational efforts
led by the American Head & Neck Society would benefit primary care physicians and other
specialty groups. In agreement with this statement, the authors suggest that similar surveys of
PCPs in the United States be conducted in order to assess their current understanding of the
association between HPV and HNC.
41
The paper by Jackowska and colleagues also provides important information into this
topic. This survey based study was more in alignment with the goals of the current systematic
review. The authors conducted a nationwide survey of GPs, otolaryngologists, and trainees to
assess their current knowledge of HPV and head and neck cancer. This study demonstrates that
in Poland, otolaryngologists are more knowledgeable with respect to HPV and its association
with HNC than are GPs (Table. 8). In addition, the authors also demonstrate that few GPs are
knowledgeable about the potential use of the HPV vaccination for the prevention of upper
aerodigestive tract tumors (HNCs). When compared with otolaryngologists, PCPs were less
aware of a potential benefit of the HPV vaccination for prevention of head and neck cancers.
Discussion
Currently, few studies exist that detail the knowledge, attitudes, and beliefs of PCPs
towards HPV-positive OPSCC, and our study supports this claim. We developed three search
strateges each tailored to a specific database to identify studies that would provide insight into
this topic. After each database was searched, titles and abstracts were screened, and a full text
review was completed, only two articles remained. Despite a low yield, we believe important
information can be gained from studying these two physician groups.
The study by Malloy and colleagues, although not of PCPs, provides evidence that
specialists are knowledgeable with respect to this rapidly changing disease. More importantly,
specialists in the United States desire a greater role in educating other groups of physicians on
the changes associated with HPV-positive OPSCC. We believe this will be an important step in
increasing awareness on the changing aspects of head and neck cancer. Currently, over 90% of
all OPSCC is associated with HPV, and it is predicted that the incidence of HPV-positive
42
OPSCC will surpass the incidence of HPV-positive cervical cancer by 2020.34,35 These rapid
changes demand that innovative solutions are developed to increase awareness among PCPs and
the general population. Increasing educational efforts to PCPs has the potential to improve
patient outcomes through increased vaccination efforts, early detection, and timely referral of
patients presenting with early signs of malignancy
The paper by Jackowska et al. found that in Poland, GPs are less knowledgeable about
HPV and its role in head and neck cancers. Although this study was not conducted in the United
States, we believe it demonstrates an important issue; GPs who have the ability to act in a
preventive manner through vaccination efforts were less knowledgeable about the potential use
of the HPV vaccination for the prevention of HNCs. Although we expect specialists to be more
knowledgeable, they are less able to play a preventive role due to most commonly only seeing
patients after diseases have developed. Increasing vaccination efforts is predicated upon a strong
knowledge base among GPs who have the ability to offer vaccinations to patients at appropriate
ages and before diseases have developed. As in the United States, increasing the knowledge base
of PCPs may have the largest effect on HPV-positive OPSCC through increased prevention,
surveillance, and early detection.
Both studies conclude that additional targeted education strategies are needed to increase
awareness of HPV and its role in head and neck cancer. The results of our systematic review are
in agreement with these points. We were unable to identify a single English language article that
addresses the current knowledge of HPV-positive OPSCC among primary care physicians in the
United States or other OECD countries. A first step in developing targeted educational resources
for PCPs is to develop a greater understanding of the current level of knowledge among these
physicians groups. This process allows knowledge gaps to be identified, which informs the
43
development of educational resources tailored to address these gaps. By identifying areas where
knowledge gaps exist and directing resources to address these gaps, educational programs can be
maximized.
Our study is limited by the low yield from the search strategy and the potential of nonresponder bias to have driven the results of each study. Although we acknowledge these studies
may suffer from non-responder bias, similar low response rates for surveys have recently been
reported among physicians.25,14. Additionally, title, abstract, and full text review was done by a
single author. This could potentially bias the results by failing to include studies that may have
been included if dual review was used. Finally, limiting the search to English language articles
only could have missed studies published from OECD countries that did not have English
translations. Furthermore, our study has several strengths, including a comprehensive search
strategy collaboratively developed with the assistance of a professional librarian. Additionally,
we searched three databases through two separate electronic libraries to ensure the thoroughness
of the search. Although the yield was small and only single review was used, we believe the
thoroughness of the search ensures that the majority of relevant articles were assessed.
In conclusion, we have identified a need for additional studies of key physician groups,
including pediatricians, internal medicine physicians, and family medicine physicians in the
United States to provide insight into this important topic. The goal of such future reseach should
be to identify where knowledge gaps exist in the presentation, outcomes, and prevention of HPVpositive OPSCC in order to inform the development of educational resources to address these
gaps. Due to the rapid changes in presentation and outcomes associated with HPV-positive
OPSCC patients, these studies should be performed in a timely manner. By increasing the
44
knowledge base of the primary care network, the role of the PCP can be maximized and patient
outcomes improved through preventive measures, early detection, and timely referral.
45
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Chera BS, Amdur RJ, Tepper J, et al. Phase 2 trial of de-intensified chemoradiation
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Scott JR, Wong E, Sowerby LJ. Evaluating the referral preferences and consultation
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33.
Malloy KM, Ellender SM, Goldenberg D, Dolan RW. A survey of current practices,
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among head and neck surgeons. JAMA Otolaryngol Head Neck Surg. 2013;139(10):10371042. doi:10.1001/jamaoto.2013.4452.
50
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Appendix
51
Figure 1. Prisma Diagram detailing article selection process from the three searched databases
Table 1. Database Specific Search Strategies
52
Database
PubMed
Key Terms (connected with
Expansion Terms (connected
“AND”)
with “OR”)

Carcinoma, Squamous

Otolaryngeal
cell

Head and Neck
Neoplasm

Alphapapillomavirus

Neoplasms

Head and Neck Cancers

Human papillomavirus

Papillomavirus
infections

Human
Papillomaviruses

Primary Care Physicians

HPV

HPV-6

Education

Early Detection of
Cancer

Practice Patterns,
Physicians

Health Knowledge,
Attitudes, Practice
53

Attitudes of Health
Personnel
CINHAL




SCOPUS


Healthcare Surveys

Specialists Surgical
Carcinoma, Squamous

Neoplasms
Cell

Malignancy
Human Papillomavirus

HPV

Papillomavirus

Alphapapillomavirus

Pediatricians

Family medicine

Internal medicine

surgery

Medical Surveys

Knowledge

Attitudes

Beliefs

Practice Patterns

Malignancy

Cancer

Head and neck

oropharyngeal
Primary Care Physicians
Surveys
Neoplasms
54



Human Papillomavirus
Primary Care Providers
Medical Surveys

HPV

Alphapapillomavirus

Family medicine

Internal medicine

pediatrics

Surveys
Table 2. Key Inclusion and Exclusion Criteria
Key Inclusion and Exclusion Criteria
Key Inclusion
Information pertaining to HPV-Positive:
Key Exclusion
Information pertaining to HPV-negative
OPSCC
OPSCC
HNC
HNC
Information obtained from
PCPs
Studies Using Modeling to Predict PCPs:
Knowledge
Pediatricians
Practice Patterns
Inernal Medicine Physicians
Attitudes
Family Medicine Physicians
Beliefs
Head and Neck Surgeons
Included 1 of the following 3 key principles:
Knowledge of PCPs
Practice Patterns of PCPs
55
Beliefs of PCPs
Information Obtained From:
Information not obtained from:
Surveys
Surveys
Focus Groups
Focus Groups
Questionnaires
Questionnaires
English Language Only
Non-English Language Articles
Published in an OECD Country
Published outside of an OECD Country
Table 3. Studies excluded during full text review with reasons for exclusion
Study Title
Reason for Exclusion
North American Survey on HPV-DNA and p-
Survey results did not fulfill one of the 3 key
16 testing for head and neck carcinoma
principles of the current review
Human Papillomavirus infection and
Non-English Language Article
vaccination: knowledge and attitudes of Italian
general practitioners
Cancers That U.S. Physicians Believe that the
Did not include oropharynx or head and neck
HPV Vaccine Prevents: Findings from a
cancer
Physician Survey , 2009
Educational value of a medical student-led
Did not include PCPs or head and neck
head and neck cancer screening event
surgeons
Awareness and knowledge of human
Did not include PCPs or head and neck
papillomavirus-related diseases are still
surgeons
56
dramatically insufficient in the era of highcoverage vaccination programs
Table 4. Article Specifics
Study Authors
Journal
Study Design
Date Published
Malloy et al.
JAMA
Online Electronic
August 29,2013
otolaryngology- head
Survey
and neck surgery
Jackowska et al.
Plos ONE
Online Electronic
October 26, 2015
Survey
Table 5. Study Survey Response Rates
Study Authors
Study Population
Physicians surveyed
Responses (Response
Rate)
Malloy et al.
American Head &
Head and Neck
Neck Society
Surgeons
297 (27.5%)
Members
Jackowska et al.
Poland Physicians
Head and Neck
404 (19.2%)
57
Surgeons, General
Practitioners and
Trainees
Table 6. Key knowledge questions from Malloy et al.
Question
Answer
Percent Correct
HPV is associated with a
True
94.9%
False
42.4%
False
99.0%
False
96.3%
False
95.6%
much improved response for
patients with head and neck
cancer
Patients with a history of HPV
infection should not be offered
the HPV vaccine
Most patients with HPV
experience symptoms of
infection
The oral tongue is the
principal head and neck cancer
site associated with HPV
HPV is a relatively uncommon
sexually transmitted infection
58
All types of HPV can lead to
False
96.3%
head and neck cancer
Table 7. Key practice questions from Malloy et al.
Question
Options with response percentages
I Strongly
Agree
Pediatricians should remain the sole
I
I
somewhat somewhat
I strongly
Disagree
Agree
Disagree
8.8%
22.9%
24.6%
44.3%
23.2%
33.0%
23.2%
20.5%
16.5%
43.1%
28.3%
12.1%
9.1%
22.2%
36.7%
32.0%
appropriate source of information regarding the
HPV vaccine
It is necessary to discuss issues of sexuality
before recommending HPV vaccines to
patients
The efficacy and safety of new vaccines can
only be sufficiently established after the
vaccine has been on the market for 5 to 10
years.
My patients are sufficiently informed of the
risks of becoming infected with HPV and the
59
potential consequences of such an infection.
Table 8. Key questions and answers from Jackowska et al.
Question
Answer with Response Percentage
General Practitioners
Have you heard about the
Otolaryngologists
Yes 100.0%
No 0.0%
Yes 100.0%
No 0.0%
Yes 23.4%
No 76.6%
Yes 44.4%
NO 55.6%
Yes 93.0%
No 7.0%
Yes 80.0%
No 20.0%
impact of vaccination on the
reduction of cervical cancer
incidence?
Have you heard about the
potential value of HPV
vaccination in preventing
oropharyngeal cancer?
Have you heard about the
association between HPV and
upper aerodigestive tract
tumors?
60