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Collegian (2012) 19, 4550

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/coll

Issues and challenges in implementing cervical


cancer screenings in the emergence of HPV
vaccination in Thailand
Phanida Juntasopeepun a,, Patricia M. Davidson b, Jatupol Srisomboon c
a

Faculty of Nursing, Chiang Mai University, Chiang Mai, Thailand


Centre of Cardiovascular and Chronic Care, University of Technology Sydney, Curtin University, Australia
c
Department of Obstetrics and Gynecology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
b

Received 27 April 2011; received in revised form 4 August 2011; accepted 5 August 2011

KEYWORDS
Thailand;
HPV vaccination;
Cervical cancer
screening

Summary The discovery of the HPV vaccine has been a major breakthrough in preventing
cervical cancer and other HPV-related diseases around the globe. Cervical cancer is a significant public health problem in Thailand. Despite the long-time availability of cervical cancer
screening programs in Thailand, the uptake among the target female population remains low.
HPV vaccines were approved by the Food and Drug Administration of Thailand in 2007. As
of March 2011, due to nancial limitations, HPV vaccines have still not been included in the
national immunization program under the public health benet plans although individuals has
the option to pay privately for the vaccine. This paper discusses the issues and challenges in
implementing cervical cancer screening programs in the era of HPV vaccination in Thailand.
Recommendations to increase the uptake of cervical cancer screening and further research to
inform a policy regarding the cervical cancer screening measures are proposed.
2011 Royal College of Nursing, Australia. Published by Elsevier Australia (a division of Reed
International Books Australia Pty Ltd). All rights reserved.

Introduction
Cervical cancer is the third most common cancer among
women worldwide. In 2010, it was estimated that there
were 553,000 new cases of cervical cancer diagnosed among
women. The incidence of cervical cancer is generally higher
in developing countries, accounting for more than 85% of all
cases around the globe. In terms of mortality rates, cervi-

Corresponding author. Tel.: +66 53 949 019; fax: +66 53 217 145.
E-mail address: phanida@chiangmai.ac.th (P. Juntasopeepun).

cal cancer leads to more than 288,000 deaths among women


worldwide. Almost 90% of women who die from cervical cancer reside in developing countries (56,000 in Africa, 34,000
in Latin America and the Caribbean, and 168,000 in Asia)
(Ferlay et al., 2008). The 5-year survival rate of cervical
cancer patients in developing countries is less than 50% compared with 66% in the developed world (Parkin & Bray, 2006).
Currently, Thailand has a population of approximately
63.87 million, with about 25.83 million women aged 15
years and older who are at risk of developing cervical cancer (Department of Provincial Administration/Ministry of
Interior, 2011). In Thailand, cervical cancer is the second
most frequent cancer among women between 15 and 44

1322-7696/$ see front matter 2011 Royal College of Nursing, Australia. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.

doi:10.1016/j.colegn.2011.08.002

46
years of age, occurring at an aged adjusted incidence of
29.2 per 100,000 which is relatively high among developing
countries in southern and southeastern Asia and the world
(Ferlay et al., 2008).

Cervical cancer screenings


Cervical cancer is preventable through both primary and secondary preventive measures. Primary prevention of cervical
cancer through HPV vaccination has recently become available and secondary prevention of cervical cancer can be
achieved through various screening methods. Cervical cytology either conventional Pap smear or liquid-based cytology,
high-risk human papillomavirus (HPV) testing, and visual
inspection with acetic acid (VIA) are methods of screening
(Franco, Duarte-Franco, & Ferenczy, 2001). In many developed countries where the resources exist, well-organized
cervical cancer screening programs to detect and treat precancerous abnormalities and the early stages of cervical
cancer have been very successful and proven to signicantly
reduce cervical cancer incidence and mortality rates (Denny,
Quinn, & Sankaranarayanan, 2006). However, effective cervical cancer screening services and referral of patients
with abnormal tests for further histological diagnosis and
treatment usually are not well performed in low-resource
countries. As a result, the majority of women with cervical cancer in these countries are diagnosed at an advanced
stage and incurable by the time they go to hospital, leading to higher death rates and shorter survival rates (Denny
et al., 2006).
In Thailand, cervical cancer prevention and control has
been the responsibility of the Ministry of Public Health
(MOPH). The Pap smear test has been used in health
care facilities for almost 60 years since 1952 under the
supervision of the Department of Medical Services, MOPH
(Kietpeerakool, 2006). The test was used mainly for diagnostic purposes rather than for cervical cancer screening
and available for screening on a demand basis. In 2000,
the VIA test was launched for women aged 3045 years
in some areas of Thailand. The Department of Health,
MOPH is responsible for this screen-and-treat service.
This preventive method combines VIA with cryotherapy as
a single-visit approach which would minimize loss to followup. Studies on VIA in Thailand have demonstrated that this
method is programmatically feasible and sustainable and
should therefore be considered in a national investments to
control cervical cancer (Gafkin, Blumenthal, Emerson, &
Limpaphayom, 2003). When Thailand launched a new public
health insurance policy under the Universal Coverage (UC)
Scheme in 2004, these two screening measures were added
into the public health benet package for disease prevention
which is available free of charge in all government health
care settings in Thailand (Tangcharoensathien et al., 2008).
Due to a lack of laboratories, trained pathologists and technicians, as well as nancial resources, Thailand is similar
to other developing countries in that it is unable to screen
women with Pap smear or VIA as frequently as recommended
by some Western-developed country guidelines (American
Cancer Society, 2010). Throughout 20052009, the MOPH
introduced the organized cytology-based screening program
for the entire Thai female population aged 3560 years to

P. Juntasopeepun et al.
undergo Pap smear every 5 years. Due to the limited budget,
only 4 million out of a total 10 million women were targeted (Yothasamut, Putchong, Sirisamutr, Teerawattananon,
& Tantivess, 2010). At the end of the program, only 2 million women were screened resulting in only 20% coverage of
the total women at risk. In 2010, a major effort was subsequently made to scale up cervical cancer screenings in
Thailand when the MOPH launched the nationwide screening initiative to increase public awareness and the coverage
of cervical cancer screening programs. The target age of
women was 3060 years, translating to 13 million screened
every 5 years or 2.6 millions per year (Yothasamut et al.,
2010).
Despite the long-time availability of cervical cancer
screening programs in Thailand, these programs are considered inefcient because the coverage of the target
female population remains low (Sriamporn, Khuhaprema, &
Parkin, 2006) and incidence and mortality rates from the
disease among Thai women are still high. Recent statistical reports from World Health Organization (WHO)/Institut
Catal dOncologia (ICO) Information Centre on HPV and
Cervical Cancer estimate that annually 9999 Thai women
are diagnosed with cervical cancer, 5216 of which will
die from the disease (WHO/ICO Information Centre on
HPV and Cervical Cancer, 2010). Like other countries
in the developing world, it is obvious that the coverage of cervical cancer screening programs are inadequate
in Thailand, and access to precancerous treatment is
limited as it is only available in certain health care
facilities (Tangcharoensathien et al., 2008). A number
of studies throughout Thailand have reported that signicant numbers of Thai women have never received
any cervical screenings despite the fact that the services are available free of charge under the UC Scheme
(Boonpongmanee & Jittanoon, 2007; Sriamporn et al., 2006)
and delay in seeking treatment for abnormal cervical cancer symptoms, leading to advanced stage of disease at
diagnosis (Ratanasiri, Boonmongkon, Upayokin, Pengsaa, &
Vatanasapt, 2000).
Attempts have been made to identify obstacles for implementing cervical cancer screening programs in Thailand. In
relation to health care service and policy, one study found
that the lack of effective program coordination for the two
screening measures, which are managed separately by two
departments of the Ministry of Public Health, leads to inadequate performance of cervical cancer screening services
in Thailand (Tangcharoensathien et al., 2008). The political
crisis in Thailand over the past few years has interfered with
several government plans, including the MOPHs national
cervical screening campaign programs. The campaign was
considered not successful and did not achieve desirable target numbers (Yothasamut et al., 2010). One reason for low
rates of cervical cancer screening utilization in Thailand may
stem from womens preventive health behaviors. A complex network of womens knowledge, attitudes, beliefs, and
sociocultural factors also play a crucial role in limiting Thai
womens uptake of cervical cancer screening. Past attempts
have been made to identify factors inuencing cervical cancer screening behaviors in Thailand. For example, perceived
low susceptibility and seriousness of cervical cancer, lack of
knowledge about screening measures, and lack of awareness of the importance of early detection were signicantly

Issues and challenges of cervical cancer screenings in Thailand


associated with cervical cancer screening among Thai
women (Duangsong, 2004; Keelapang, 2005).
The Thai cultural value of respect to modesty is
considered a barrier to cervical screening practice. Embarrassment about exposing the genital area for examination
by male health care providers has repeatedly been reported
in the literature (Boonpongmanee & Jittanoon, 2007;
Rungsrisuwan, 1999; Tsui & Tanjasiri, 2008). The inuence
of signicant others (e.g. female relative, partner) is also
a signicant predictor of cervical cancer screening behaviors. Some Thai women seek screening tests only after
being prompted by others (Supanaum, 2008). This could
be explained based on the fact that Thailand is viewed
as a collectivist society. People in collectivist societies
see themselves as interdependent with their groups, pay
more attention to the relationships within their groups, and
behave primarily based on group norms (Triandis, 2001).
Additionally, cervical cancer is primarily a cancer of women.
Some women hold multiple roles, such as mother, wife, and
employee. They may have several responsibilities in their
daily lives. These responsibilities interfere with their ability to seek screening tests (Mongkondee, 2005). Thai society
still assumes that women should take a traditionally subordinate role. Thai women are expected to support their
husbands efforts and decisions, are in charge of childcare
and the household, and take care of parents. As a result,
in Thai culture, it is expected that women will sacrice
themselves for their families, prohibiting them from seeking
screening services. These issues must be taken into consideration when designing interventions to scaling up cervical
cancer screenings in Thailand.

HPV vaccination
HPV infection is the most common sexually transmitted disease. Contracting HPV is considered the greatest risk factor
for developing cervical cancer (Hutchinson & Klein, 2008).
Factors associated with HPV persistence and development
of cervical cancer include long-term use of hormonal contraceptives, early sexual debut, multiple sexual partners,
having sex with a partner who has had multiple sex partners,
and vulnerable immune systems (Bedford, 2009; Franco
et al., 2001; Louie et al., 2009; World Health Organization,
2007). There are more than 100 types of HPV and at least 13
of these types are cancer-causing. The most common HPV
types that infect the anogenital tract are HPV types 6, 11,
16, and 18. Among these, HPV types 16 and 18 are the major
causative agents for cervical cancer which cause approximately 70% of all cervical cancer worldwide, whereas HPV
types 6 and 11 are most commonly associated with benign
lesions such as genital warts and low-grade lesions of the
cervix (World Health Organization, 2007).
The recent discovery of the HPV vaccine is a major breakthrough in preventing cervical cancer and other HPV-related
diseases around the globe. Currently, two HPV vaccines,
the quadrivalent HPVs 6/11/16/18 vaccine (Gardasil ) and
the bivalent HPVs 16/18 vaccine (Cervarix ) are available
for primary prevention of cervical cancer. The Food and
Drug Administration (FDA) in the United States approved
the quadrivalent vaccine in 2006 and the bivalent vaccine
in 2010. The quadrivalent vaccine is targeted to prevent

47
cancer precursors of the cervix, vulva, and vagina caused
by HPV 16 and 18 and external genital lesions caused by
HPV 6 and 11, while the bivalent vaccine aims to prevent
cervical cancer caused by HPV 16 and 18 only (World Health
Organization, 2007). Clinical trials have shown that HPV vaccination is most effective in preadolescent or adolescent and
young women prior to the onset of sexual activity because
they have not yet acquired any of the HPV types covered
by the vaccine. The two vaccines have been proven more
than 90 percent effective in preventing precancerous cervical lesions when administered prior to the onset of sexual
activity (World Health Organization, 2007). Due to the difference of epidemiology and age of sexual debut, the age
range recommended for HPV vaccination are likely to vary
from country to country (Wright, Van Damme, Schmitt, &
Meheus, 2006). Both vaccines were approved by the FDA of
Thailand in 2007, the bivalent for women aged 1025 years
and the quadrivalent for women aged 926 years. The Royal
Thai College of Obstetricians and Gynaecologists (RTCOG)
and Thai Gynecologic Cancer Society (TGCS) recommend
young women aged 1126 years receive HPV vaccine especially before commencing sexual intercourse. The use of the
HPV vaccination in women older than 26 years and in sexually exposed women should be individualized (The Royal
Thai College of Obstetricians & Gynaecologists, 2010).
Approximately 8.6% of Thai women in the general population are estimated to harbor HPV infection at a given
time, and 73.8% of invasive cervical cancers are attributed
to HPVs type 16 or 18 (WHO/ICO Information Centre on HPV
and Cervical Cancer, 2010). In many industrialized countries,
the HPV vaccines have been introduced into the national
immunization program where young girls can be vaccinated
free of charge. However, the situation is different in lowresource countries where the cost of vaccines is the greatest
concern of the government, Thailand included. Soon after
the launch of the HPV vaccines in Thailand, the Director
General of the Department of Disease Control, the Ministry
of Public Health revealed that Thailand is unable to afford
the high price of the HPV vaccine due to government budget limitations and suggested that the conventional cervical
screening measures, Pap smear and VIA, are still effective.
However, HPV vaccines are available and widely used within
the private sector, if an individual can afford the vaccine
themselves (Sarnsamak, 2007).
Additional efforts have been made to study the costeffectiveness of HPV vaccination and to conduct an
economic comparison of the HPV vaccination and other cervical screening measures in Thailand. In 2008, one study
entitled Research for the development of an optimal policy strategy for prevention and control of cervical cancer
in Thailand was conducted by health policy researchers
from two institutes under the Ministry of Public Health the International Health Policy Program Thailand (IHPP) and
the Health Intervention and Technology Assessment Program
(HITAP) (Tangcharoensathien et al., 2008). Both institutes
have a signicant role in generating evidence-based information on health for policy makers in Thailand. Findings
from this study suggested that the Pap smear and VIA are
proven to be effective and cost-saving and have the potential to signicantly reduce the morbidity and mortality of
cervical cancer in Thailand, both services of which are
covered by the UC Scheme in Thailand. The study also

48
illustrated difculties and barriers of the current cervical
cancer screening services and proposed a number of strategies to prevent and control the disease. However, given the
current market price of the HPV vaccines in Thailand, HPV
vaccination was not a cost-effective policy choice suggesting that Thailand should not adopt this new HPV vaccine as
public policy (Tangcharoensathien et al., 2008).
When it was evident that the affordability of the HPV vaccine was a key consideration of the Thai government, the
two vaccine producers offered Thailand a price reduction
in 2009 (Yothasamut et al., 2010). Given the fact that the
vaccine producers decreased the vaccine cost by almost 50
percent, another major study was conducted to assess the
cost-effectiveness of the HPV vaccines again. In contrary to
the previous studys ndings when the vaccine price was still
high, results from this more recent study revealed that the
HPV vaccine is cost-effective in the long term, encouraging a
government decision to include it in the national immunization plan to reduce the burden of cervical cancer in Thailand
in the future. Researchers held a national press conference in November 2010 to disseminate the study results and
to call for the Thai governments decision and action for
instance, negotiating the vaccine price with the pharmaceutical companies for the large-volume vaccine purchases
(Bangkokbiznews, 2010). As of March 2011, the HPV vaccines
have not still been incorporated into the national immunization program under the public health benet plans.

Future directions
Cervical cancer is a signicant public health problem. In
Thailand, cancer screening programs exist, but have not
been well-performed/organized because the target population coverage of Pap smear and VIA remains low. Barriers
to the screening programs have been highlighted in the
literature. Lack of nancial resources and inadequate quality of cervical cancer screening programs play a critical
role in hampering the success of cervical cancer prevention
and control in Thailand. These issues pose a challenge to
Thailand while it is still faced with nancial resource limitations, political instabilities, and other competing health
priorities other than cervical cancer such as the human
immunodeciency virus (HIV) infection.
Increasing coverage of cervical screening services either
with Pap smear or VIA in Thailand should be continued. However, there is a great need to improve cervical
screening systems that identify target populations, and
invite screening and follow-up, including systems to manage abnormalities, refer, and follow-up those treated in
Thailand. Increasing the uptake of cervical cancer screening in the context of Thai society, community-based health
care providers play a major role in educating women about
screening of cervical cancer. It is crucial to understand the
variables associated with underutilization of cervical cancer
screening services in order to enable Thai women to respond
positively to cervical cancer screening. The designing of
programs to increase the uptake of cervical cancer screening in Thailand should be locally and culturally appropriate
and be aware of multiple barriers that women may experience in accessing services. It would be unwise to mimic
the screening programs of Western countries which have

P. Juntasopeepun et al.
different socio-cultural backgrounds and different health
care systems from those in Thailand.
In terms of HPV vaccination, it is evident that the vaccine
price is the greatest barrier that inuences vaccine program
decisions. HPV vaccines will have an enormous impact on
the reduction of cervical cancer morbidity and mortality
in the future (next 1030 years) if they are delivered to
all target populations. Achieving broad coverage of adolescents will be a challenging issue for the Thai government
to reduce the burden of cervical cancer. The Thai government must make careful decisions to create systems to
vaccinate adolescents at the population level. To inform
government decision making, clear and accurate information must be made available to the government decision
makers on the knowledge, attitudes and practices of adolescents. More research is needed to provide policy makers with
evidence-based information within in the social, cultural,
and economic context of Thailand. Presently, it is obvious
that further actions from the Thai government are needed
to negotiate the vaccine price with the vaccine companies
to lower the cost for mass vaccine purchases. HPV vaccines
should possibly be injected to girls aged 1214 years nationwide. This measure would take a long time, certainly 1030
years to show the reduction in the incidence of cervical cancer. However, it is expected that Thai girls/women in next
1030 years will not develop cervical cancer caused by HPV
16/18. At least 7075% of cervical cancer will be eliminated
from Thai women in the future. The remaining cervical cancer caused by non-HPV 16/18 are not aggressive and take a
long time to develop.
It is clear that adolescents worldwide have limited knowledge and awareness about HPV and related issues, which is
likely to affect their vaccine acceptance (Klug, Hukelmann,
& Blettner, 2008). HPV vaccines have been available in the
private sector in Thailand for a few years. To date, little is
known about Thai adolescents knowledge, attitudes, and
adoption of this vaccine. Since HPV vaccines are targeted
towards young children, parents will obviously play a critical role, such as whether or not they can afford or are
willing to have their children vaccinated. Previous research
has demonstrated that young adolescents and parents of
adolescents in developed countries had positive attitudes
towards HPV vaccination (Dempsey, Zimet, Davis, & Koutsky,
2006; Lazcano-Ponce et al., 2001), although some parents
were concerned that the HPV vaccine would encourage risky
sexual behavior (Davis, Dickman, Ferris, & Dias, 2004). Additionally, studies have illustrated that health care provider
recommendations also play a crucial role in HPV vaccine
acceptability in developed countries and have been identied as an important source of HPV information (Daley
et al., 2006; Kahn et al., 2005; Riedesel et al., 2005). Successful HPV vaccination programs will depend on health
care providers recommendation of the HPV vaccination to
parents. To date, there is a great need in Thailand for
more research on knowledge, attitudes, and acceptability
of HPV vaccines for adolescents and parents of adolescents,
including health care providers attitudes about HPV vaccine recommendation. If Thai adolescents and parents have
a clear understanding of HPV infection and its association
with cervical cancer, it is likely that they will be more willing to accept HPV vaccines. While the HPV vaccines have
not yet been included in the national immunization program

Issues and challenges of cervical cancer screenings in Thailand


for Thai adolescents who are not able to afford the vaccine out of their own pocket, efforts should be made to
provide information about the prevention of HPV infection.
HPV education campaigns, particularly school or collegebased cervical cancer education will be needed to increase
awareness and educate young adolescents in preventing HPV
infection.

Conclusions
Cervical cancer is a common cancer among women in
Thailand and is largely preventable through screening and
vaccination programs. Developing affordable and accessible programs that are culturally appropriate is critical in
decreasing the disease burden among Thai women.

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