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Advances in Social Sciences Research Journal – Vol. 10, No. 12
Publication Date: December 25, 2023
DOI:10.14738/assrj.1012.15936.
Silva, M. A., Corrêa, M. C. P., & Bacha, E. (2023). Cervical Cancer Screening: Integrative Review of National and International
Guidelines. Advances in Social Sciences Research Journal, 10(12). 51-63.
Services for Science and Education – United Kingdom
Cervical Cancer Screening: Integrative Review of National and
International Guidelines
Mayra Alencar da Silva
ORCID:0000-0002-3705-6505
School of Medicine, Centro Universitário de Maceió, Alagoas, Brazil
Maria Claudia Pereira Corrêa
ORCID:0000-0002-6950-8254
School of Medicine, Centro Universitário de Maceió, Alagoas, Brazil
Elizabeth Bacha
ORCID:0000-0002-8971-8582
School of Medicine, Centro Universitário de Maceió, Alagoas, Brazil
ABSTRACT
Cervical cancer is one of the most preventable and treatable malignancies, yet it still
has high incidence and mortality rates, especially in less developed countries.
Despite this, vaccines against HPV (the main cause of cervical cancer) are effective
and promote a significant reduction in infections and neoplastic lesions of the
cervix, as well as the early detection of HPV with or without its initial lesions. This
paper is an integrative review, with the aim of demonstrating the main national and
international guidelines for the diagnosis of HPV. Using the databases PubMed,
MEDLINE, and SciELO, a search was carried out using the descriptors "Cervical
Neoplasms", "Screening" and "Guidelines", selecting at the end 12 articles. The
results showed that the recommendations for the early diagnosis of HPV have
undergone several strategic changes over time, especially on the following points:
use of co-testing (combined test with cytology and HPV test) and self-test.
Previously in other countries, only cervical cytology (Pap smear) was offered.
However, cervical cytology has to be repeated frequently due to its limited
sensitivity and reproducibility and, even though it is freely available, studies point
to the difficulty of achieving and maintaining diagnostic coverage for cervical
cancer. Among the factors hindering success is health illiteracy, which is mainly due
to social inequality and the lack of educational actions by the government,
demonstrating the need to plan effective strategies in this regard.
Keywords: cervical cancer, guidelines, screening, HPV.
INTRODUCTION
The Human Papillomavirus (HPV) is mainly sexually transmitted and promotes abnormal
proliferation of the mucosal epithelium, being responsible for the most frequent infections of
the genital tract. It can also affect the oral cavity, trachea, bronchi, esophagus, rectum and anus.
HPV subtypes 16, 18, 31, 33, 45, 52, and 58 are oncogenic and together account for more than
95% of cervical cancer cases [1].
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Cervical cancer is the fourth most common type of cancer in women, with around 90% of
estimated deaths worldwide occurring mainly in low- and middle-income countries that have
failed to establish or maintain effective screening programs for the disease [2]. Thus, they
continue to have high incidence and mortality rates [3] (Figure 1).
Figure 1: Cervical cancer incidence and mortality rates in the world
Source: International Agency for Research on Cancer - OMS (2020)
In Brazil, between 2008 and 2018, the mortality rate from this type of cancer increased by 33%
according to data from the Ministry of Health [4]. Scientifically, this increase is unacceptable
because, according to Shami and Coombs (2021), cervical cancer is one of the most easily
preventable and treatable malignancies, with primary prevention measures (vaccination and
condom use), secondary prevention (screening tests to detect infection and pre-malignancies)
and tertiary prevention (early treatment of initial lesions).
It is also worth noting that cervical cancer is a disease that develops slowly and silently and can
be asymptomatic in the early stages, or with precursor lesions, and evolve after 15 to 20 years
[5].
In August 2020, intending to reduce morbidity and mortality from the disease, the World Health
Organization (WHO) developed a campaign that aims to eliminate cervical cancer worldwide
by 2030, advocating the intensification of primary prevention with vaccination against the
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Silva, M. A., Corrêa, M. C. P., & Bacha, E. (2023). Cervical Cancer Screening: Integrative Review of National and International Guidelines. Advances
in Social Sciences Research Journal, 10(12). 51-63.
URL: http://dx.doi.org/10.14738/assrj.1012.15936
human papillomavirus (HPV) and secondary prevention with screening for this type of cancer
at a population level for women most at risk [3].
The new guidance recommended by the WHO includes some important changes in approaches
to cervical cancer screening. In particular, a DNA-based HPV test (HPV-DNA test) is
recommended as the preferred method, rather than visual inspection with acetic acid (VIA) or
cytology (Pap smear), currently, the most commonly used methods worldwide to detect
precancerous lesions [6].
The main objective of the fight against cervical cancer is to detect and treat precursor lesions,
not to diagnose the cancer. The old guidelines only assumed cervical cytology collection
programs, which had to be repeated frequently due to their limited sensitivity and
reproducibility. Currently, the HPV Test, either as a co-test or self-test, is widely accepted as the
preferred strategy for cervical screening because it has several benefits [7].
Thus, knowing the national and international guidelines against cervical cancer and comparing
them can lead us to better ways of substantially reducing the incidence and mortality of cervical
cancer.
METHODS
This study is characterized as an integrative review, with the aim of comparing the guidelines
established for cervical cancer screening, both nationally and internationally. Using the
PubMed, MEDLINE, and SciELO databases, a search was carried out for scientific articles using
the descriptors "Uterine Cervical Neoplasms", "Screening" and "Guidelines", as well as the
Boolean operator "AND" between the three descriptors.
The search resulted in a total of 2,063 articles, followed by the use of filters: publications in
English or Portuguese, resulting in 1,931 articles; articles published in the last two years,
resulting in 249 articles; only work carried out on the human species was considered, resulting
in 247 articles; finally, free access to the text was also considered, resulting in 238 publications.
After they had been selected, titles and abstracts were read, of which only 25 publications were
suitable for the purpose of this study, and 2 articles were excluded because they did not contain
the full text. Finally, after thoroughly reading the articles and analyzing the methodology, 12
publications fell within the objective of the current systematic review (Figure 2).
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Figure 2: Flowchart of the research methodology
Source: own authors (2023)
RESULTS
Cervical Cancer Screening-Past, Present, and Future. Authors and year of publication:
Wentzensen e A Clarke (2021).
• Country referenced: United States.
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Silva, M. A., Corrêa, M. C. P., & Bacha, E. (2023). Cervical Cancer Screening: Integrative Review of National and International Guidelines. Advances
in Social Sciences Research Journal, 10(12). 51-63.
URL: http://dx.doi.org/10.14738/assrj.1012.15936
• The US Preventive Services Task Force (USPSTF) Guidelines include three screening
modalities: cytology (Pap smear), primary HPV testing, and co-testing. However,
considering the benefits and harms, it suggests primary HPV testing with cytology
screening at 5-year intervals from the age of 30. With regard to co-testing, performing it
at 5-year intervals from the age of 30 was associated with 60% more total lifetime tests
and 12% more colposcopies with a similar number of detected cases compared to the
analogous strategy with primary HPV testing and cytology screening.
Dominican Provider Practices for Cervical Cancer Screening in Santo Domingo and
Monte Plata Provinces. Authors and year of publication: Liebermann et al. (2022).
● Country referenced: Dominican Republic.
● The Dominican National Guidelines were based on a survey of health professionals in
the Dominican Republic who commonly screen for cervical cancer. These providers
report that they follow national and/or international screening guidelines and that they
do not follow age-based guidelines or adopt an extended interval for screening and
continue to recommend it at least annually.
● In the Dominican Republic, the screening tests used are liquid-based cytology, and HPV
tests less frequently, and conventional cytology or Pap smears. The latter is the most
widely used and has not shown an adequate reduction in mortality from cervical cancer.
Colposcopy was most often recommended for all abnormal Pap smear results.
Health Care Provider's Experience and Perspective of Cervical Cancer Screening in
Singapore: A Qualitative Study. Authors and Year of Publication: Chua et al. (2022).
• Country referenced: Singapore.
• In Singapore, public services follow national standards and offer HPV testing, while
private services offer co-testing, HPV testing, and Pap smears. Cervical Cancer Screening
(CCS) encompasses women aged 25-69 for screening and, since 2019, the national
screening guideline (recommended by the Singapore Society of Colposcopy and Cervical
Pathology) recommends HPV testing every 5 years as a cervical cancer screening
strategy.
• The barriers to screening are compounded by a poor understanding of the natural
history of HPV infection and consequent anxiety about possible relational fidelity. Often,
the national cervical cancer screening (CCS) program was considered unnecessary by
patients due to their good health, advanced age, and lack of sexual activity.
Towards The Elimination of Cervical Cancer in Low-Income and Lower-Middle-Income
Countries: Modeled Evaluation of The Effectiveness and Cost-Effectiveness of Point-Of- Care HPV Self-Collected Screening and Treatment in Papua New Guinea. Authors and
Year of Publication: Nguyen et al. (2022).
• Country referenced: Papua New Guinea.
• Although the disease burden is high in the country, cervical screening or vaccination
programs against the human papillomavirus (HPV) are not currently available.
• The effectiveness, cost-effectiveness, and resource implications of a national cervical
screening program using the HPV self-collection test compared to the visual inspection
with acetic acid (VIA) test in Papua New Guinea (PNG) were evaluated.
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• HPV self-collection has been effective and cost-effective in PNG's high-burden, low- resource setting and, if scaled up quickly, could prevent more than 20,000 deaths over
the next 50 years. VIA screening was not effective or cost-effective. These findings
support, at a national level, the updated WHO cervical screening guidelines and indicate
that similar approaches may be appropriate for other low-resource settings.
• In both screening tests (HPV self-collection test or VIA), women who show a cervical
lesion on visual assessment, but are not suspected of cancer, are immediately treated
with ablation, and women whose lesions are large or suspected of cancer are referred
to a specialist for further evaluation. For both pathways, women who were referred for
diagnosis with a suspected neoplasm and who presented CIN3 would be treated with
hysterectomy or conization, depending on the patient's clinical circumstances (based on
local expert opinion). Otherwise, women who are negative can return for screening, and
women who have received treatment for precancerous lesions can have a "cure test"
using the same test as the primary test.
Cervical Cancer Screening with HPV Testing: Updates on the Recommendation. Authors
and Year of Publication: Carvalho et al. (2022).
• Country referenced: Brazil.
• For women over 30, the HPV test alone should replace cytology, which should only be
used in the event of a positive HPV test, for screening purposes. The co-test is not
recommended for primary screening, as there is no evidence that it has any difference
in detecting precursor lesions when compared to the HPV test. Women between the ages
of 25 and 29 should be screened for HPV, preferably through genotyping tests, to reduce
overdiagnosis.
Cervical Cancer Screening Outcomes in Zambia, 2010-19: A Cohort Study. Authors and
Year of Publication: Pry et al. (2021).
• Country referenced: Zambia.
• According to the Cervical Cancer Prevention Program in Zambia (CCPPZ), screening is
by visual inspection with acetic acid and digital cervicography (VIAC) in women aged
30-59 every 5 years, while the screening interval for women living with HIV is between
25-59 years, with an interval of 3 years (in the case of a previous negative result).
Secondary Prevention of Cervical Cancer: ASCO Resource-Stratified Guideline Update.
Authors and Year of Publication: Shastri et al. (2022).
• Country referenced: United States.
• The HPV DNA test is recommended and can be either self-collected or collected by a
doctor.
• Screening should be carried out between the ages of 25 and 65 and repeated every 5
years.
• VIA can be used in basic settings and should move on to population screening with HPV
tests at the earliest opportunity.
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Silva, M. A., Corrêa, M. C. P., & Bacha, E. (2023). Cervical Cancer Screening: Integrative Review of National and International Guidelines. Advances
in Social Sciences Research Journal, 10(12). 51-63.
URL: http://dx.doi.org/10.14738/assrj.1012.15936
"So, if she wasn't aware of it, then how would everybody else out there be aware of it?"-Key
Stakeholder Perspectives on the Initial Implementation of Self-Collection in Australia's Cervical
Screening Program: A Qualitative Study. Authors and year of publication: Zammit et al. (2022).
• Country referenced: Australia.
• The National Cervical Screening Program (NCSP) advocates testing through primary
HPV testing (partial HPV genotyping and liquid-based reflex cytology screening) with
invitations and reminders to be sent every 5 years to women aged 25-69, with an exit
test for women up to the age of 74; self-collection of an HPV sample, for a poorly
screened or never screened patient (facilitated by a doctor or nurse who also offers
conventional cervical screening tests).
Shifting from Cytology to HPV Testing for Cervical Cancer Screening in Canada. Authors
and Year of Publication: Delpero e Selk (2022).
• Country referenced: Canada.
• The HPV test will soon replace the pap smear for primary cervical cancer screening
because it is more sensitive, cost-effective, and safer.
• There is a discrepancy between Canadian guidelines: the Canadian Cervical Cancer
Screening Network starts screening at 21, while the Canadian Task Force on Preventive
Health Care recommends starting at 25.
• The Health Technology Expert Review Panel (HTERP) recommends that if you decide to
replace cytology with HPV-based testing as the primary test for programmatic cervical
cancer screening, five-year testing intervals between the ages of 25 and 69 are
appropriate. HPV-based screening should be carried out using a test with genotyping
capabilities.
Validation of the Indication for Colposcopy Proposed by the 2019 ASCCP Risk-Based
Management Consensus Guidelines: A Single-Center Study in China. Authors and Year of
Publication: Gui T, Chen Z e Chen F (2021).
• Country referenced: China.
• The Chinese population uses the American ASCCP guideline and indicates colposcopy
for abnormal screening tests.
Cervical Cancer Screening Guidelines: An update. Authors and Year of Publication: Shami
e Coombs (2021).
• Country referenced: United States.
• The American Cancer Society (ACS) recommends screening between the ages of 25 and
65, with a primary HPV test every 5 years OR a Pap smear every 3 years OR a Pap smear
with HPV (co-test) every 5 years. The US Preventive Services Task Force (USPSTF) and
the American Academy of Family Practice (AAFP) recommend screening between the
ages of 21 and 65 by Pap smear every 3 years, but between the ages of 30 and 65,
primary HPV testing is added every 5 years OR Pap smear plus HPV (co-testing) every 5
years. The American College of Obstetricians and Gynecologists (ACOG) and the
American Society for Colposcopy and Clinical Pathology (ASCCP) recommend Pap
smears every 3 years between the ages of 21 and 65, and Pap smears plus HPV (co- testing) every 5 years between the ages of 30 and 65.
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WHO guideline for Screening and Treatment of Cervical Pre-Cancer Lesions for Cervical
Cancer Prevention, Second Edition. Authors and Year of Publication: World Health
Organization- WHO (2021).
• The 2021 WHO guidelines recommend primary HPV screening and treatment for
women aged 30 to 49 using primary HPV DNA testing. For women living with HIV, it is
recommended from the age of 25.
• The testing interval for HPV DNA as a primary test should be every 5 to 10 years in the
general population of women. In the case of women living with HIV, 3 to 5 years apart.
• After the age of 50, the guidelines suggest stopping screening after 2 consecutive
negative results.
• Where HPV DNA testing is not yet available, the WHO suggests regular screening every
3 years when using VIA or cytology as primary tests, both in women living with and
without HIV.
• The WHO has 2 approaches, (1) screening and treatment and (2) screening, selection,
and treatment.
Below is a table summarizing all the guidelines studied (Table 1).
Table 1: Table comparing the recommendations of the guidelines
Country/
Institution
Recommended
Age
Screening Test Observation
WHO 30 to 49 years old ● HPV testing every 5 to 10
years.
OR
● VIA or cytology every 3
years.
● In women living with HIV,
screening begins at 25
years of age.
● The interval between
tests should be 3 to 5
years.
Dominican
National
Guidelines
(Dominican
Republic)
35 to 64 years old ● Liquid-based cytology, HPV
testing, conventional
cytology, VIA.
● HPV testing for “at risk”
women at health centers
that have availability and,
when available, for
ASCUS/abnormal Pap smear
screening.
● Annually every 2 years, if
normal, repeat every 1-3
years.
● Prioritizes women who
began sexual activity at an
early age, had multiple
sexual partners, have
never been examined
and/or those who have a
history of abnormal Pap
smears.
Singapore
National
Screening
Guideline
25 to 69 years old ● HPV testing every 5 years. -
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Silva, M. A., Corrêa, M. C. P., & Bacha, E. (2023). Cervical Cancer Screening: Integrative Review of National and International Guidelines. Advances
in Social Sciences Research Journal, 10(12). 51-63.
URL: http://dx.doi.org/10.14738/assrj.1012.15936
United States
of America –
ACS
25 to 65 years old ● Primary HPV test every 5
years
OR
● Pap test only every 3 years
OR
● Pap smear plus HPV (co- test) every 5 years.
-
United States
of America –
USPSTF
21 to 65 years old ● Primary HPV testing with
cytology screening at 5-year
intervals starting at age 30.
● Between 30 and 65 years
old: add primary HPV
testing every 5 years
OR
● Pap smear + HPV (co-test)
every 5 years.
United States
of America –
ACOG
21 to 65 years old ● Pap test only every 3 years. ● Between 30 and 65 years
old: Pap smear + HPV (co- test) every 5 years.
United States
of America –
AAFP
21 to 65 years old ● Pap test only every 3 years. ● Between 30 and 65 years
old: primary HPV test only
every 5 years
OR
● Pap smear + HPV (co-test)
every 5 years.
United States
of America –
ASCCP
21 to 65 years old ● Pap test only every 3 years. ● Between 30 and 65 years
old: Pap smear + HPV (co- test) every 5 years.
Papua New
Guinea
30 to 50 years old ● HPV self-collection test and
visual inspection test (VIA).
● Study analyzes the
effectiveness and cost- effectiveness of screening
up to three times in life
from the age of 30,
concluding the HPV self- collection test as the best
option.
● The country does not yet
have a well-established
national guideline.
Brazil 25 to 64 years old ● Pap test annually and, after
two consecutive negative
annual exams, is repeated
every three years.
● For women over 30, HPV
testing should replace
cytology.
● Co-testing is not
recommended for primary
screening.
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Zambia 30 to 59 years old ● Visual inspection test with
acetic acid every 5 years.
-
Canada Canadian Cervical
Cancer Screening
Network: 21 to 69
years old.
Canadian Task
Force on
Preventive Health
Care: 25 to 69
years old.
● HPV test every 5 years. -
Australia 25 to 69 years old ● Primary HPV testing (partial
HPV genotyping and
cytology screening) with
invitations and reminders
to be sent every 5 years,
with an exit test for women
up to age 74.
● Self-collection of an HPV
sample for an
infrequently or never- examined patient
(facilitated by a doctor or
nurse who also offers
conventional cervical
screening tests).
China 21 to 65 years old ● Pap tests every 3 years.
● Between 30 and 65 years
old: Pap smear + HPV (co- test) every 5 years.
● The American ASCCP
guidelines are applied to
the Chinese population.
Source: own authors (2023)
DISCUSSION
This study found that developed countries concerned with protecting their population from
cervical cancer (USA, Australia, and Canada), following WHO guidelines, have adopted HPV
testing earlier (co-testing or self-testing), and were also the first to implement the HPV vaccine,
which will ultimately lead to a reduction in the number of cervical cancer cases in these
countries [8].
Ogilvie et al. in Canada, carried out a study called HPV FOCAL, with more than 25.000 healthy
women divided into two groups: one examined with the HPV test and the other with a Pap test,
found that cervical pre-cancer was discovered earlier in women who had HPV tests, allowing
them to be treated before invasive cervical cancer could develop. In other words, using the HPV
test for cervical cancer screening resulted in a lower probability of having high-grade cervical
pre-cancer 4 years later [9].
These results reinforced previous research and the argument for replacing the Pap smear, but
did not stimulate sudden changes in Canada: in May 2023, Prince Edward Island became the
first province to publicly fund HPV testing as the primary means of cervical cancer screening,
but without self-collection at home as an option; Quebec and New Brunswick have publicly
announced plans to change, but have not yet done so. Other provinces are laying the
groundwork for change and running pilot projects, including British Columbia, which hosted
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Silva, M. A., Corrêa, M. C. P., & Bacha, E. (2023). Cervical Cancer Screening: Integrative Review of National and International Guidelines. Advances
in Social Sciences Research Journal, 10(12). 51-63.
URL: http://dx.doi.org/10.14738/assrj.1012.15936
the clinical trial of Gottschlich et al., taking too long to make a change that several of its peers,
including Australia and Great Britain, have already adopted [10][11].
Vaginal self-testing for human papillomavirus (HPV) DNA could increase screening
participation rates. In the clinical setting, the vaginal HPV test is at least as sensitive as cytology
in detecting cervical intraepithelial neoplasia (CIN) level 2 or more severe; however, its
effectiveness in the home setting is unknown.
Researchers in Mexico aimed to establish the relative sensitivity and a positive predictive value
for HPV testing from self-collected vaginal samples at home when compared to cervical
cytology performed in a clinic. They carried out a community-based randomized equivalence
trial in Mexican women from low socio-economic conditions aged between 25 and 65; 9202
women from the HPV testing group adhered to the protocol, as did 11,054 from the cervical
cytology group. The positive predictive value of the HPV self-test for CIN 2 or more severe was
12.2% compared to 90.5% for cytology. The researchers concluded: "Despite the much lower
positive predictive value for HPV testing or self-collected vaginal samples compared to
cytology, such tests may be preferable for detecting CIN 2 or more severe in low-resource
settings where restricted infrastructure reduces the effectiveness of cytology screening
programs. Because women in these locations will only be tested a few times in their lives, the
high sensitivity of an HPV test is of paramount importance [12].
Currently, the disease is only diagnosed by the cytopathological test (Pap smear) in Brazil's
Unified Health System (SUS). Recently, in July 2023, the Brazilian Ministry of Health launched
a new strategy for detecting the HPV virus, with the inclusion of HPV testing by PCR, a molecular
test, in the SUS. The city of Recife is a pioneer in the project, and around 400,000 women will
be tested, in the 25 to 64 age group served by the SUS. The Ministry's guidance is that if the test
is positive, the diagnosis should be confirmed by cytological examination and the patient
referred for treatment. In the event of a negative result, the HPV PCR test should be repeated in
five years. Based on the results, the Ministry of Health aims to expand the new strategy to the
whole country [13].
Gomes et al. conducted a systematic review to identify the recommendations for 2022 made by
the ministries of health in the 13 countries and areas of South America for human
papillomavirus (HPV) vaccination and cervical cancer screening. Recommendations for cervical
cancer screening were found in official documents from 11 countries, except for Venezuela and
Suriname. A total of 12 countries uses cytology to screen for cervical cancer. Four countries
(Bolivia, Colombia, Guyana, and Peru) use visual inspection with acetic acid and the screening
and treatment strategy. Six countries (Argentina, Chile, Colombia, Ecuador, Paraguay, and Peru)
are transitioning from cytology to HPV testing. They concluded that South American countries
should update their guidelines for HPV vaccination and cervical cancer screening [14].
In developed countries such as England, the NHS (National Health Service), has the Cervical
Screening Program (CSP), which includes training professionals to guarantee the quality of the
tests, and educating the population (health literacy) it also has Cervical Screening
Administration Service (CSAS) that invites women between the ages of 25 and 64 to attend the
screening. The first screening test used is HPV detection, and if the result is positive for high
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risk, a cervical cytology test is carried out. If the cytology is negative, repeat the test in 12
months, if the cytology is abnormal: refer to colposcopy [15].
CONCLUSION
The positive impact against cervical cancer, in terms of public health, will occur if there is an
effective operationalization of this objective, which can happen through the combination of
multiple factors, such as the creation and implementation of effective public health measures -
with the evaluation of immunization and early diagnosis strategies, for example - as well as the
recognition of the difficulties and limitations of the factors associated with possible inequities
in vaccination coverage and diagnostic tests, inexorably going through health literacy.
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