Factors Underlying Disparities in

Cervical Cancer Incidence,

Screening, and Treatment in the
United States
W
orldwide, an estimated 493,243, cases of invasive cervical
cancer (ICC) occur each year and 273,505 women die of the
disease.
1
There is a global disparity in the incidence of cervical
cancer, with the burden of cases occurring in less developed countries
(83%), where effective cervical cancer screening and treatment
services have often been difcult to implement
1
(Fig 1). In more
developed countries, such as the United States, the incidence of
cervical cancer has decreased dramatically (75%) since the 1940s,
2,3
largely as a result of the introduction of cervical cancer screening
programs. An estimated 20,000 new cases of cervical cancer are
diagnosed in the United States each year, and approximately 5000
women die from this preventable disease.
4
However, the incidence of
cervical cancer and treatment of the disease show marked disparities
based on socio-demographic and health care access characteristics.
Papanicolaou (Pap) smears were designed to detect cervical changes
which may represent premalignant forms of squamous cell cervical
cancer, the most common type of cervical cancer. Squamous cell
cervical cancer, hereafter called cervical cancer, results from infection
with oncogenic human papillomavirus (HPV) types which are ac-
quired through sexual intercourse.
5,6
Major risk factors for acquiring
HPV include an early age at the onset of sexual activity, having
multiple sexual partners, and having promiscuous male partners.
Several cofactors may act in conjunction with HPV to increase the risk
of cervical cancer, including cc-interferon with other sexually trans-
mitted infections,
7,8
smoking,
9,10
multiparity,
11,12
oral contraceptive
use,
10,13-15
immunodeciency,
16,17
and dietary factors, such as low
carotene, low vitamin C intake, or folate deciency.
18-20
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Curr Probl Cancer, May/June 2007 157
In the United States, cervical cancer screening with Pap smears is
recommended for all women within 3 years of the onset of sexual activity
or at age 21, whichever comes rst.
21
Although clinical guidelines
vary,
21-23
annual Pap smears are generally recommended for women
under the age of 30, whereas the interval may be extended to every 2 to
3 years for older women who have had three negative smears, no history
of CIN II/III, and are not immuno-compromised or DES-exposed in utero.
Screening conducted every 3 years among women aged 20 to 64 reduces
the cumulative incidence of ICC by 91% according to data from the U.S.
Preventive Services Task Force.
24
Survival rates for women with early
stage disease are excellent, with a 5-year survival rate of almost 100% for
those with in situ disease, but only 10% for women with stage IV
disease.
25
In the United States, lack of Pap test screening is the single most
powerful factor in the development of ICC, and disparities in ICC
incidence are largely due to differences in Pap test coverage.
26,27
More
than half of newly diagnosed cases of ICC occur in women who have
either never been screened or who have not been recently screened.
28
Rates of ICC have consistently been shown to decrease when Pap test
screening rates rise.
29,30
Data from the National Breast and Cervical
Cancer Early Detection Program (NBCCEDP) demonstrate that the
cumulative incidence of ICC is reduced by 94% when the interval
FIG 1. Global estimated incidence of ICC in developed and less developed countries (Globocan
2002). (Color version of gure is available online.)
158 Curr Probl Cancer, May/June 2007
between Pap smears was 1 year, 84% at 5-year testing intervals, but only
64% when the interval was 10 years.
31
Despite overall decreases in the incidence of ICC over the last 2 decades
in the U.S., the burden of ICC is not evenly distributed across all
segments of the U.S. population. Cervical cancer screening, incidence,
mortality, and treatment varies widely according to socio-demographic
factors and measures of health care access and quality. Women who are
most likely to have high ICC incidence rates are those with low incomes,
low educational attainment, no insurance or public insurance, and those
from minority or immigrant groups. Although the gaps in cervical cancer
incidence between some groups (ie, Blacks and whites) have narrowed in
the last few decades, the gaps for others (eg, immigrants versus U.S.-born
individuals) have continued to increase.
In this paper, we will explore some of the factors underlying persistent
disparities in cervical cancer incidence, screening, and treatment in the
United States.
Methods
Analyses of the incidence and mortality of cervical cancer, stratied
by race/ethnic group (black, Hispanic, white, American Indian/Alaska
Native, Asian, or Pacic Islander), were obtained from the 2002
SEERS database.
32
We used the same search terms as Newmann and
coworkers,
33
including cervical cancer and cervix cancer and the
following domains of social inequality: race/ethnicity, racism, socio-
economic position, social position, gender, age, language, literacy,
immigrant status, insurance, and geography. Additional publications
were identied by reviewing the reference section of articles found
during the initial search. A total of 95 articles were identied. The
causes of disparities in cervical cancer incidence, screening, and
treatment were divided into 2 groups: socio-demographic and health
care factors (Table 1).
TABLE 1. Etiology of disparities in cervical cancer screening, diagnosis, treatment, and mortality
Socio-demographic disparities Health care disparities
Race/ethnicity Access
Age Geography
Immigration/acculturation Provider characteristics
Health literacy Health system deciencies
Socio-economic position
Curr Probl Cancer, May/June 2007 159
Socio-Demographic Factors
Race/Ethnicity
Race/ethnicity has often been implicated as a major factor underlying
disparities in cervical cancer rates. ICC incidence in the U.S. between
1992 and 1998 was notably higher among black, Hispanic, and Asian and
Pacic Islander women as compared with white, Alaska Native, and
American Indian women (Figs 2 and 3A).
32
Racial/ethnic differences in
ICC incidence may be related to differences in cervical cancer screening
rates, follow-up rates of abnormal Pap smears, and treatment rates of
cervical dysplasia. The observed differences in ICC incidence by race/
ethnicity are problematic as they suggest a biologically valid basis for the
observed differences may exist. However, recent studies have noted that
social and health system characteristics may play a larger role in
mediating the observed differences in cervical cancer screening rates
between racial and ethnic groups.
34,35
Assessing racial/ethnic differences in cervical cancer rates is challeng-
ing because population-based studies and nationally representative data-
bases vary in the degree to which they stratify the population by
race/ethnicity. Most studies have examined differences between Blacks,
whites, and, increasingly, Hispanics. In contrast, data on Asian Americans
FIG 2. Incidence of ICC (SEER 1992 to 1998), stratied by race/ethnicity.). (Color version of
gure is available online.)
160 Curr Probl Cancer, May/June 2007
(AA), Pacic Islanders (PI), Alaska Natives (AN), and American Indians
(AI) are included less often. Recent studies indicate that the incidence of
cervical cancer may be higher in AA and PI (Figs 2 and 3A), and that ICC
mortality rates may be higher in AI/AN (Fig 3B)
32
than in traditionally
studied racial/ethnic groups.
36-38
In addition, many studies fail to distin-
guish between foreign-born and U.S.-born racial/ethnic minority groups.
This distinction is important since foreign-born women, particularly those
from Latin America and South East Asia, generally have lower rates of
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1
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A
B
FIG 3. Estimated ICC incidence (A) and mortality (B), stratied by age and race/ethnicity (SEERS
2002).
Curr Probl Cancer, May/June 2007 161
Pap test screening and higher cervical cancer-attributed mortality rates
than their U.S.-born racial/ethnic counterparts.
37
The degree to which cervical cancer screening rates vary according to
race/ethnicity is unclear. Overall, Blacks and non-Hispanic whites have
been noted to have the highest cervical cancer screening rates among all
ethnic groups,
3
whereas Hispanics
29,39
and AA/AN/PI women
36,37
are
less likely to have ever had a Pap or to have been screened within the past
3 years. Other studies have suggested that race/ethnicity is likely not the
primary mediator of disparities in cervical cancer screening rates. Instead,
these studies indicate that race/ethnicity is a proxy for other factors, such
as lifestyle differences that may increase a womans risk of HPV infection
(eg, number of sexual partners, age at sexual initiation), differences in
health behaviors (eg, screening rates, follow-up for abnormal Pap smears,
smoking), and health care access (eg, insurance status, usual source of
care, contact with a health provider in the last year). This is evidenced by
the fact that the effect of race is signicantly reduced or eliminated after
controlling for these factors.
34,35,40
Studies examining disparities in cervical cancer treatment have shown
mixed results. Several studies have demonstrated differences in treatment
for cervical cancer based on race.
35,41-45
Two studies noted that Black
women were more likely to receive no treatment or radiation alone as
opposed to surgery or combination chemotherapy/radiotherapy compared
with whites and Hispanics, even after controlling for stage of disease at
diagnosis.
41,42
Another study noted that racial differences in treatment
persisted even after controlling for age and stage of disease at diagnosis.
43
In this study, Black women under age 35 were more likely to receive
fertility-sparing treatment compared with whites or Hispanics, whereas
both Black and Hispanic women over age 35 were less likely to receive
a hysterectomy compared with whites. On the other hand, several studies
have shown that treatment differences may be reduced or eliminated after
adjusting for socio-demographic characteristics and disease severity (eg,
tumor stage, histology, and grade).
40,46
A study conducted in the U.S.
military health system where access biases are limited, found no racial
differences in age at diagnosis, stage at diagnosis, therapy received, or
survival.
40
This study suggests that race-related barriers to care may
underlie disparities in cervical cancer mortality. Patient factors may also
affect the observed racial differences in treatment modalities. For exam-
ple, African American women may be more likely to refuse treatment
45,47
or select fertility-sparing treatments
43
compared with women from other
ethnic groups.
162 Curr Probl Cancer, May/June 2007
Age
Cervical cancer screening rates vary by age with higher screening rates
observed among reproductive age women compared to older women,
regardless of race/ethnicity.
27,33,48-51
Among younger women, not only
are cervical cancer screening rates high, but they tend to be similar across
all race/ethnic groups.
3
As a consequence, young women are generally
diagnosed at earlier stages than older women.
33
Younger women who
have not been screened recently (i.e., within the last 3 years) are more
likely to be from an ethnic minority group, uninsured, have low income,
low health literacy, or are recent immigrants.
52-56
ICC incidence generally increases with age among all racial/ethnic
groups (Fig 3A). However, older women are disproportionately repre-
sented among new cervical cancer cases (Fig 3A) and deaths (Fig 3B),
particularly women over age 65.
57
Women over 65 in the U.S. with
late-stage ICC represent approximately 25% of ICC cases and account for
40% of ICC deaths.
57
Many of these women have either never had a
cervical smear or have not been screened within the three year prior to
diagnosis,
58-61
despite having visited a physician.
62
The lower ICC
incidence rates among older American Indian/Alaska Native women may
not reect a true decrease in ICC incidence after the fourth decade, but
may reect erratic screening practices of women over age 40, due to less
frequent entry into the health care system after their reproductive years.
The higher incidence of ICC among Black and Asian and Pacic Islander
women after the fourth decade is likely attributed to decreased screening
and treatment of cervical dysplasia among these women with increasing
age.
As age increases, disparities in cervical screening rates become more
evident. Cervical screening rates among young Black women are the
same if not higher than those for their age-matched white peers. However,
at older ages Black women are less likely to be screened than their white
counterparts and, consequently, more likely to be diagnosed with a higher
disease stage and suffer higher mortality rates.
30,43
This difference in
age-related ICC mortality among Black women likely reects multiple
factors. The progressively lower cervical screening rates among Black
women as they grow older results in a higher disease stage at diagnosis
which limits Black womens treatment options. Older Black women have
also been found to have more co-morbid conditions compared to
whites.
34,44,47
Co-morbid medical conditions affect treatment recommen-
dations and tolerance and may therefore help explain some of the
observed differences in ICC treatment based on race/ethnicity. In addition
Curr Probl Cancer, May/June 2007 163
to race, insurance status also affects cervical cancer screening among
older women. In a recent study, older women with Medicare/HMO were
1.35 times more likely to be diagnosed with in situ or local stage disease
compared with Medicare/fee-for-service patients even after controlling
for socio-demographic and socio-economic factors.
63
This suggests that
insurance status among older women acts as a barrier to screening
services.
The clinical utility of Pap screening among women over age 65 is
controversial.
64
Although the benets of Pap screeningearly disease
detection, treatment, and improved survivalare well known, the poten-
tial harms of screening for older women may actually outweigh these
benets. Menopause causes physiologic changes to the cervix which
increases the likelihood that cytological abnormalities may be found on
cervical smears. Such cytologic abnormalities could result in additional
diagnostic procedures such as cervical biopsies, cervical excision proce-
dures, or hysterectomies, which carry higher risks of morbidity among
older women compared to younger women.
64
Since pre-malignant cervi-
cal lesions detected with screening are not likely to progress to ICC prior
to an older woman dying from an unrelated cause, treatment of pre-
malignant lesions may present more risks than benets. Thus, most
clinical guidelines currently recommend discontinuation of cervical
screening at age 65 or 70 in women with repeatedly normal cervical
smears or those who have a short life expectancy. Thus, when considering
cervical screening among older women, their cervical screening history
must be considered as some older women may lack recent screening for
valid clinical reasons.
With regards to treatment disparities, older women tend to be offered
more conservative treatment options compared to younger women and
have lower survival rates.
44,45,65-67
However, older women often have
competing health issues that affect both their treatment options and
survival. Older women are more likely to have co-morbid chronic
illnesses and to present at more advanced disease stages which affects
their candidacy for surgery versus radiation treatment.
66
These co-
morbidities may also limit the radiation dose and treatment duration an
older woman can tolerate.
34,44,45,47,64,66
Women presenting with ad-
vanced disease including pelvic and para-aortic lymph node metastases
have signicantly reduced survival prognosis and are generally offered
palliative rather than curative treatment. Younger women, on the other
hand, are more likely to be diagnosed at earlier disease stages and
therefore more likely to receive treatments with a curative intent than are
older women.
43
Women presenting with early stage cervical cancer are
164 Curr Probl Cancer, May/June 2007
generally more likely to undergo surgical therapy whereas those with a
large tumor burden or invasive disease generally receive radiation or
combination therapy. Thus, despite evidence suggesting that ICC treat-
ment disparities exist based on age, we must remember that cancer
treatment regimens do need to be tailored to the individual.
Immigration Status and Acculturation
In the last three decades, the immigrant population in the United States
has increased from 9.6 million in 1970 to 32.5 million in 2002.
68
This
demographic change has not been accompanied by a parallel increase in
the monitoring of the health status of immigrants. Most national surveil-
lance systems do not routinely include health statistics stratied by
immigrant status or country of origin. Available studies have consistently
shown that cancer screening rates are lower among immigrant groups
compared with the general U.S. population.
69,70
For cervical cancer
specically, women from immigrant groups appear to be less likely to
undergo cervical cancer screening and more likely to be diagnosed at later
disease stages and therefore have lower survival rates compared with
U.S.-born women.
69-72
This is particularly true for women from Latin
America and South East Asia, which comprise the largest groups of
immigrants.
69,71
Several factors are thought to account for the low cervical cancer
screening rates among immigrant women. Lack of access to health
care as measured by either a lack of health insurance or lack of a usual
source of care is thought to account, at least in part, for reduced
cervical cancer screening among immigrant populations.
69,70
In addi-
tion, cultural beliefs, such as having a nonwestern orientation toward
disease prevention, have also been strongly associated with a lower
probability of cervical cancer screening.
38,73-79
For example, a study
of Mexican immigrants in California found that womens compliance
with cervical screening guidelines was related to their knowledge of
the causes of cervical cancer and their belief that screening was
necessary only in the presence of symptoms of a vaginal infection.
75
A study in San Francisco found that Muslim women were hesitant to
obtain Pap smears due to cultural concerns about modesty and the
perception that they would lose their virginity as a result of the
gynecologic examination.
73
Other common barriers to cervical cancer
screening among immigrant women, regardless of their racial or ethnic
background, include holding fatalistic health beliefs
76-78,80,81
and
having a low degree of acculturation,
29,60,72,79,80,82-84
which is dened
as either shorter residency in the U.S. or lack of English uency.
Curr Probl Cancer, May/June 2007 165
Few studies have examined cervical cancer treatment patterns among
women from immigrant communities. One study conducted among Latina
immigrants in a Los Angeles county hospital found signicantly lower
rates of adherence to radiation treatment compared with women in the
general population (16% versus 63%) and noted that a signicant
proportion of patients elected to discontinue treatment without a medical
reason for doing so.
85
Selected patient interviews revealed that cultural
and logistical barriers to care interfered with treatment. This suggests that
women from some immigrant groups may need targeted interventions to
overcome these cultural and logistic barriers to care if treatment adher-
ence and improved outcomes are to be achieved.
Health Literacy
Health literacy has been dened as the degree to which individuals
have the capacity to obtain, process, and understand basic health
information and services needed to make appropriate health decisions.
86
Low health literacy rates are more common in certain populations, such
as the very young or elderly, ethnic minorities, immigrants and nonnative
English speakers, and those with limited education and low in-
come.
61,87,88
Low health literacy has consistently been associated with
inadequate knowledge about disease, reduced health screening behaviors,
delays in disease diagnosis, and poor health outcomes for a variety of
health conditions.
62,89-92
Few studies have examined the effect of health
literacy on Pap screening or ICC incidence. One study found that health
literacy (in English) was the only factor independently associated with
cervical cancer screening knowledge even after controlling for socio-
demographics and insurance status.
62
A second study found that low
health literacy among Spanish speakers also correlated with low cervical
cancer screening rates.
93
Lack of knowledge about the importance of cervical cancer screening,
early detection, and treatment is one aspect of health literacy that has been
studied, particularly among ethnic minorities and women from low
socio-economic groups.
58,62,94-97
Studies have found that women who are
younger, non-white, and those with low educational attainment or low
income are more likely to be unaware of the purpose of Pap testing and
to not be screened.
58,73,74,98
One study looking at the effect of health
literacy on cervical cancer-related health behaviors and found that women
with low health literacy were more likely to not seek medical attention for
an abnormal Pap smear compared with those with adequate health
literacy.
62
166 Curr Probl Cancer, May/June 2007
Conventional cancer health education campaigns and literature tend to
be written for women with adequate health literacy. This may result in
alienation, confusion, or inadequate health knowledge among women
with low literacy thereby compounding the problem of low cervical
cancer screening rates and low rates of follow-through with treatment
guidelines.
61
Socio-Economic Position
The most common markers of socio-economic position that have been
examined for their association with cervical cancer screening rates
include income,
38,48,59,63,67,74,80,99-104
poverty level,
105
educational sta-
tus,
59,84
and residence in socio-economically disadvantaged areas.
105-111
In general, these studies have found that higher socio-economic status
correlates with higher cervical cancer screening rates, a lower stage at
cervical cancer diagnosis, and decreased ICC incidence and mor-
tality.
3,84,106,112
In a number of these studies, socio-economic position
has been noted to explain differences in cervical cancer screening rates
better than race/ethnicity.
48,108,112,113
This has led to the conclusion that
women from low socio-economic backgrounds face signicant barriers to
screening services. This conclusion is supported by the ndings of a study
conducted in the military health system which provides equal access to
care regardless of socio-economic status.
40
No differences were found in
cervical cancer screening, incidence, mortality, or stage disease at
diagnosis, despite variations in womens race and socio-economic status.
Several hypotheses have been proposed to explain the inverse relation-
ship between socio-economic position and cervical cancer incidence.
Women from low socio-economic groups often have limited access to
quality medical care and cervical cancer screening services, poor fol-
low-up for abnormal cytology and low health literacy, which represent
important confounders of the relationship between socio-economic posi-
tion and cervical cancer screening. In addition, women from lower
socio-economic positions are at a higher risk of exposure to high-risk
HPV types due to their relatively younger age at rst intercourse,
112
increased likelihood of being smokers,
114
and poor nutritional status. The
last two factors increase their risk of cervical neoplasia progression and
cervical cancer. Furthermore, women from lower socio-economic groups
may face signicant personal challenges that limit their ability to either
seek or follow-through with care, such as transportation limitations, child
care, or employment restrictions.
Although socio-economic position may account for a signicant portion
of the variability in cervical cancer screening, it does not account for all
Curr Probl Cancer, May/June 2007 167
of the observed differences. Studies in socio-demographically diverse
populations have found that disparities in cervical cancer screening
persist even after controlling for income and education.
36,48,59,80,83,113,115
Comparison of these studies is difcult since their source populations,
methodology, and the variables included in their regression models vary.
The relationship between socio-economic position and cervical cancer
screening remains to be fully explained but appears to vary depending on
the socio-demographic characteristics of the population being studied.
Understanding the relationship between socio-economic position and ICC
treatment is difcult because many studies examining disparities in cervical
cancer treatment have not accounted for socio-economic factors. Those
which have suggest that women from lower socio-economic groups may be
less likely to receive denitive treatment or full-course therapy.
47,67
For
example, one study examining the effects of insurance status on the use of
guideline-based therapy in a nationally representative sample of cervical
cancer patients found that privately insured patients were more likely to
receive guideline-based therapy than Medicaid patients.
67
It must be noted
that women from lower socio-economic groups may also have more
comorbidities or present at more advanced disease stages, both of which
affect treatment recommendations and tolerance.
44
Two studies conducted in
health systems with equal access to treatment based on age and stage at
diagnosis found no differences in survival rates between black and white
women when treatment was standardized across age, race, and socio-
economic groupings.
40,46,59,63,99,101,103,105,111,116
Health Care-Related Factors
Access
Lack of access to health care has been correlated with reduced cervical
cancer screening and treatment.
67,101,105,111
In most studies, health care
access is measured by insurance status or having a usual source of care.
Having insurance, particularly private insurance, has been positively
associated with cervical cancer screening, earlier stage at diagnosis,
receipt of guideline-based therapy, and improved survival.
67,99
In con-
trast, women who lack insurance coverage
100
or who are covered by
public insurance
101
appear less likely to receive cervical cancer screening
and more likely to be diagnosed at later stages and have decreased
survival. In a study to evaluate a culturally-appropriate cervical cancer
intervention, women with private health insurance were found to be more
likely to obtain cervical cancer screening compared with those who were
168 Curr Probl Cancer, May/June 2007
uninsured or who had Medicaid or Medicare.
104
Similarly, having a
regular physician or a usual source of care is also associated with
increased cervical cancer screening rates.
109,118
An evaluation of three
interventions to increase cervical cancer screening rates in a multi-ethnic
sample found that having private insurance and/or a usual source of care
were the strongest predictors of cervical cancer screening behav-
ior.
59,74,104,117
Geography
There are regional differences in cervical cancer incidence rates exist in
the United States. Table 2 depicts the 10 U.S. states at the highest and
lower risk of cervical cancer. Cervical cancer screening rates also differ
by geographical location, with women in rural areas and those in
economically deprived non-rural communities having the lowest screen-
ing rates in the United States.
39,109,118-120
These differences are thought
to stem from geographic differences in health system infrastructure,
provider availability, provider behaviors, and patient characteristics.
39
In
terms of health system infrastructure, the number of hospital beds in rural
areas has declined, and the majority of counties lack that a hospital are in
rural communities.
39
This limits access to cervical screening services.
Regional differences in the availability of primary care and subspecialty
TABLE 2. U.S. States with the highest and lowest incidence rates of cervical cancer, annual SEER
incidence, and mortality rates of cervical cancer
US States with highest cervical cancer
incidence
US States with lowest cervical cancer
incidence
State
Annual
incidence
rate per
100,000*
Annual
mortality
rate per
100,000
State
Annual
incidence
rate per
100,000*
Annual
mortality
rate per
100,000
West Virginia 12.2 3.1 Connecticut 5.9 1.7
Oklahoma 12.1 3.0 Massachusetts 6.3 1.5
Arkansas 11.2 4.1 Vermont 6.3
District of Columbia 10.9 Idaho 6.7 2.7
Florida 10.5 2.9 New Hampshire 6.7 2.3
Kentucky 10.3 2.4 Minnesota 7.0 1.3
Louisiana 10.1 3.0 Wyoming 7.0
Texas 10.1 3.2 Hawaii 7.0
Illinois 9.7 3.1 Utah 7.1
South Carolina 9.5 2.9 Washington 7.1 1.4
*Rate period of 2001 or 2002.
Data not available for Delaware, Georgia, Maryland, Mississippi, North Dakota, South
Dakota, Tennessee, and Virginia.
Rate period of 2002.
Curr Probl Cancer, May/June 2007 169
providers also affect womens access to cervical cancer screening and
treatment services with availability in rural areas generally more limited
than in urban areas.
39,119
In terms of provider behaviors, rural physicians
may be less likely to offer cervical cancer screening compared with
providers in nonrural areas.
39
Regional differences have been observed in
the availability of quality laboratory services for reading Pap smears.
39,114
Transportation problems, such as large distances between womens
residence and health facilities and the absence of mass transit systems,
may also present barriers to regular screening. Lastly, certain patient
characteristics that are associated with decreased cervical cancer screen-
ing rates are common among rural women, such as greater poverty, older
age, and low educational achievement.
39,51,121
Provider Characteristics
One of the strongest predictors of cervical cancer screening is provider
recommendation.
82,122
However, provider characteristics, such as pro-
vider type, gender, and ethnicity may affect whether providers actually
offer cervical cancer screening.
123
A study of 200 employee-based health
insurance plans found that obstetrician/gynecologists are most likely to
provide cervical screening, followed by family physicians, internists, and
lastly subspecialists.
28
In another study, a review of the medical records
of women recently diagnosed with cervical cancer found that almost half
had been recently seen by a family practitioner or internist, yet did not
receive a Pap test.
82,122,124
Physician gender is correlated with the
provision of cervical cancer screening with female physicians consis-
tently noted to screen women more than their male counterparts.
125-127
It
has been hypothesized that ethnic minorities often prefer to have a
physician of the same ethnicity to minimize cultural and linguistic
barriers to care. Several studies have noted that having a physician of the
same ethnicity may be associated with lower rates of cervical cancer
screening.
27,128
However, none of these studies examined physician
characteristics, such as physician gender, physician type, or being trained
outside the U.S., so it is unclear whether these ndings are mediated by
other potential confounders.
Health System Deciencies
Disparities in cervical cancer rates may result from health care system
deciencies, such as a failure to screen patients (ie, screening failures),
failure to detect cervical cytological abnormalities by Pap test (ie,
detection failure), or failure of follow-up with patients for abnormal Pap
170 Curr Probl Cancer, May/June 2007
smears (ie, incidence with follow-up). Two studies assessed the preva-
lence of these system failures among women diagnosed with ICC in
prepaid health plans in the United States.
49,123,128,129
Both studies found
that more than half of women with ICC had not been appropriately
screened within the 3 years before ICC diagnosis, a third were detection
failures, and approximately 10% had inadequate follow up. Women
characterized as screening failures were more likely to be older, live in
high poverty areas, and have low educational attainment.
Cervical cancer screening failures appear to be the most common type
of system deciency contributing to the development of cervical cancer.
Screening failures have been reported to occur in 30% to 69% of insured
women over a 3-year screening period.
123,129
Screening rates do appear to
vary based on the type of health system.
63
Among women with Medicare,
those in an HMO appear more likely to be screened than those in
fee-for-service plans.
123,128
Several studies have demonstrated that cer-
vical cancer screening may not occur among insured women even when
they have made multiple health care visits.
27
This indicates that insurance
coverage alone does not ensure receipt of adequate cervical cancer
screening.
Detection failures result from misclassication of abnormal Pap smears
as normal. In a study of seven U.S. health plans, the Pap test reports for
women diagnosed with ICC were reviewed for the 36-month period
preceding their diagnosis.
130
Eighty percent of the reports had been read
as normal, thus, almost half the women did not have a repeat Pap within
the subsequent 3 years. ICC detection failures may result in missed
diagnoses and an increased risk of developing ICC. Inadequate follow-up
failures may result either from patient non-compliance with follow-up
recommendations or inadequate follow-up on the part of providers or the
health system. Many studies fail to distinguish these categories of
non-adherence, making it difcult to determine where the main barriers
lie. In terms of patient characteristics are also associated with non-
adherence. Women who are older, from low socioeconomic groups, or
racial/ethnic minority groups appear more likely to have inadequate
follow-up. Results from the National Breast and Cervical Cancer Early
Detection Program (NBCCEDP) found that 56% of low-income women
with abnormal Pap smears did not have appropriate follow-up according
to national recommendations.
27
Black women were most likely to have
had no follow up. Older women and AN/AI women were the least likely
to be followed according to recommended clinical guidelines. Another
study specically examined reasons for patient nonadherence to clinical
follow-up guidelines and found that almost half had seen a gynecologist
Curr Probl Cancer, May/June 2007 171
but diagnostic testing was not ordered. Almost half of patients received
inconsistent follow up, although it is not clear whether this deviation from
guidelines was due to patient, provider, or system factors.
HPV Vaccine
In June 2006, the rst vaccine targeted against the HPV virus was
released (GARDASIL, manufactured by Merck and Co., Inc.,
Whitehouse Station, New Jersey). This is a quadrivalent HPV vaccine
which protects against four HPV types, that together cause 70% of
cervical cancers and 90% of genital warts.
1
The vaccine is currently
licensed for use among females aged 9 to 26 years for prevention of
HPV-related cervical cancer precursors, cervical cancer, vaginal and
vulvar cancer precursors, and anogenital warts. The vaccine will not
eliminate the need for cervical cancer screening in the U.S. because
not all HPV types that can cause cervical cancer are included in the
vaccine. However, it is expected that the vaccine will signicantly
reduce the number of abnormal cervical cytology screens obtained in
the U.S. annually thereby signicantly reducing the costs to the health
system related to cervical cancer screening and follow-up of cervical
cytological abnormalities. Each year, approximately 50 million
women in the U.S. undergo cervical screening and 4-10% (4 to 5.0
million) of these tests require some follow-up.
2-4
In clinical trials, the
vaccine was almost 100% effective at protecting against HPV types
16- or 18-related cervical dysplasia in HPV-nave women
5
and was
also highly effective at preventing cervical dysplasia among women
previously exposed to one of the vaccine subtypes.
6
The estimated cost of preventing and treating cervical HPV-related
disease is $3.4 billion.
7-9
Different models have been developed to
evaluate the impact of HPV vaccine on the incidence of abnormal
cytology, preinvasive and invasive cervical cancers.
10
These models
demonstrate that HPV vaccines could signicantly reduce the incidence
of cervical cytologic abnormalities and pre-invasive cancer as well as
reduce a womans lifetime risk of cervical cancer by 20-75%.
11-14
Although these vaccines appear promising, they still require that adoles-
cent girls and young women see a health provider to be immunized. Thus,
while vaccine provides an important new public health tool for reducing
cervical disease, it cannot circumvent the challenges presented by
populations with access barriers to health care services or limited health
seeking behaviors.
172 Curr Probl Cancer, May/June 2007
Reducing Disparities in Cervical Cancer Incidence,
Screening, and Treatment
This review provides some insights about the factors underlying
disparities in cervical cancer incidence, screening, and treatment. It is
important to recognize that no one factor completely accounts for these
disparities. Rather, there are complex relationships between patient,
provider, and health system factors that underlie the observed differences.
Thus, efforts to reduce these disparities should target these different areas
if we are to further increase cervical cancer screening rates.
Patient-targeted interventions need to focus on women with low
cervical cancer screening rates, such as those residing in rural areas,
US-born ethnic minority women, immigrant women, older women, and
the uninsured. These intervention efforts should educate women about
cervical cancer screening guidelines, where to obtain screening, and the
importance of following up after an abnormal test. We also need to focus
on developing culturally-appropriate programs to increase cervical cancer
screening rates among both US-born ethnic minority women as well as
immigrant women who may not come from cultures that lack orientation
toward preventive health behaviors. Public health interventions need to be
developed that reduce barriers to cervical cancer screening faced by other
subgroups of women, such as the uninsured and those in rural areas.
Providing screening and treatment opportunities in non-traditional sites
could also be particularly helpful for immigrant women as well as those
from low socio-economic groups who may have difculty accessing
healthcare and treatment services. At the health system level, efforts to
reduce disparities should focus on increasing screening behaviors among
providers and ensuring that appropriate follow up for abnormal tests is
offered. One solution would be for health insurance plans to develop
guidelines to improve compliance with Pap screening or follow-up
protocols among their providers.
Increases in cervical cancer screening rates in the United States have led
to remarkable reductions in the incidence and mortality from cervical
cancer. Although this success has not been seen in all segments of the
populace equally, our ability to identify those who can benet most from
focused cervical cancer screening efforts represents a call to action.
Acknowledgments
We thank Rachel Palmeri and Brooke Hoots for their assistance in
preparing the gures for this paper.
Curr Probl Cancer, May/June 2007 173
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