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Organization and evolution of organized cervical cytology screening in Thailand
International Journal of Gynecology and Obstetrics 118 (2012) 107–111
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International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Organization and evolution of organized cervical cytology screening in Thailand Thiravud Khuhaprema a, Pattarawin Attasara b, Petcharin Srivatanakul c, Suleeporn Sangrajrang c, Richard Muwonge d, Catherine Sauvaget d, Rengaswamy Sankaranarayanan d,⁎ a
Surgical Oncology Division, National Cancer Institute, Bangkok, Thailand Cancer Registration Unit, National Cancer Institute, Bangkok, Thailand Research Division, National Cancer Institute, Bangkok, Thailand d Early Detection and Prevention Section and Screening Group, International Agency for Research on Cancer (WHO-IARC), Lyon, France b c
a r t i c l e
i n f o
Article history: Received 13 October 2011 Received in revised form 6 March 2012 Accepted 23 April 2012 Keywords: Cervical cancer Cytology National program Pilot project Screening Thailand
a b s t r a c t Objective: To describe phase 1 of an organized cytology screening project initiated in Thailand by the Ministry of Public Health and the National Health Security Office. Methods: Women aged 35–60 years were encouraged to undergo cervical screening in primary care units and hospitals through awareness programs. Papanicolaou smears were processed and reported at district or provincial cytology laboratories. Women with normal test results were advised to undergo repeat screening after 5 years, while those with precancerous and cancerous lesions were referred for colposcopy, biopsy, and treatment. Information on screening, referral, investigations, and therapy were logged in a computer database. Results: Between 2005 and 2009, 69.2% of the 4 030 833 targeted women were screened. In all, 20 991 women had inadequate smears; 27 253 had low-grade squamous intraepithelial lesions; 15 706 had high-grade squamous intraepithelial lesions; and 2920 had invasive cancers. Information on the management of precancerous lesions was available for only 17.4% of women referred for colposcopy. Conclusion: Although follow-up data on women with positive test results were inadequately documented, the present findings indicate that provision of cytology services through the existing healthcare system is feasible. © 2012 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Cervical cancer is the second most common cancer among all women in Thailand but the most frequent among those living in rural areas of the country. In 2008, the estimated annual numbers of new cases and deaths from cervical cancer were 9999 and 5216, respectively [1]. The age-standardized incidence rates during 2000–2003 ranged from 17.8 to 28.9 per 100 000 women in different provinces of Thailand [2,3]. Opportunistic cytology screening has been widely available in urban areas of Thailand for several years. Estimates from national surveys suggest that, before 2005, approximately 25% of women in the 30–65 year age group underwent a Papanicolaou (Pap) smear in the preceding 5 years [4]. Nonetheless, it remains unclear what proportion of women with abnormal cytology results received diagnosis and treatment and what impact screening had on cervical cancer incidence and mortality over the past 3 decades. A pilot demonstration project with Pap smear screening was initiated in Nakhon Phanom province in 1999 to inform and guide the development of an organized cytology screening program for Thailand [5,6].
⁎ Corresponding author at: Early Detection and Prevention Section and Screening Group, WHO-IARC, 150 cours Albert Thomas, 69372 Lyon Cedex 08, France. Tel.: + 33 472738599; fax: + 33 472738518. E-mail address: [email protected] (R. Sankaranarayanan).
This project covered 45% of the targeted women aged 35–59 years with a single screen and showed the feasibility of integrating cervical cancer screening and treatment services with the existing healthcare infrastructure. Another important development in cervical cancer prevention in Thailand was the initiative by the Royal Thai College of Obstetrics and Gynecology in collaboration with the Johns Hopkins Program for International Education in Gynecology and Obstetrics [7]. The aim of this collaboration was to introduce a screen-and-treat demonstration program that utilized visual inspection with acetic acid (VIA) and cryotherapy to 4 districts of Roi Et province and establish the safety, acceptability, and feasibility of this approach [7]. The findings from the above studies and other experiences in Thailand and elsewhere prompted a government policy that enabled the provinces to provide population-based screening with VIA screenand-treat, cervical cytology, or both approaches. This policy led to the initiation in 2005 of a 5-year organized cytology screening project in 75 provinces of Thailand (all provinces except Bangkok) by the National Health Security Office (NHSO) and the Ministry of Public Health (MOPH) and the expansion of VIA screen-and-treat program targeting women aged 30–45 years to 29 provinces in 2006. Thailand has made considerable progress in improving maternal and child health, as indicated by low maternal mortality (48 per 100 000 live births in 2008) and low infant mortality (12 per 1000 live births in 2009) [8,9]. Currently, there are more cervical cancer deaths than maternal deaths in Thailand. The pilot project on cervical cytology screening and the VIA
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screen-and-treat efforts have been organized to emulate this success at reducing maternal and infant deaths. The present study describes the organization and process measures of phase 1 of the cervical cytology screening program in Thailand. The overall objective of this phase was to use Pap smears to screen 800 000 women aged 35–60 years each year so that 4 million out of the total 10.1 million Thai women within this age group were screened in 5 years using the government health services in Thailand. In conjunction with this program, measures were introduced to increase the capacity for obtaining and interpreting Pap smears, colposcopy, diagnosis, and treatment services for women with cervical cancer precursor lesions within the public health services. 2. Materials and methods The Thai cervical cancer screening program targeted women aged 35–60 years during the years 2005–2009 (January 1, 2005, to December 31, 2009); the designated Pap smear screening interval was 5 years (i.e. the women were advised to undergo routine screening via Pap smear every 5 years). The MOPH Department of Medical Services was responsible for conducting the screening program, which was integrated within the routine health services of Thailand. The National Cancer Institute (NCI) in Bangkok was responsible for monitoring the screening process and the outcome measures. The study was exempt from Institutional Review Board approval as it used routinely collected data in a public health program. Informed consent was obtained from women undergoing colposcopy, biopsy, and treatment. The flow of healthcare services is shown in Fig. 1. The lowest basic level of health care in Thailand is the primary care unit (PCU). Each PCU is staffed by 7–10 personnel (registered nurses, health educators, and health workers) and provides services to approximately 5000 people resident in 10–20 villages at the sub-district level. Most villages in the PCU have a public health center that is visited by PCU staff at periodic intervals. A total of 9804 PCUs and 69 331 primary public health centers serve 40 million people in rural Thailand (and were included in the screening program) providing prenatal and postnatal care, immunization, cervical screening, and treatment of minor ailments, as well as health education and creating health awareness. There are 722 community hospitals at the district level, each with 30–120 beds, and 94 general (provincial) hospitals at the secondary care level in the 76 provinces of Thailand. Tertiary care is provided by 58 large hospitals. All of these district, secondary, and tertiary centers were involved in the screening program. Cytology and histology laboratories are organized in selected community, provincial, and tertiary hospitals at the secondary and tertiary care level. Cytology services are provided by approximately 145 cytology laboratories; of the 475 cytotechnologists in the Thai health services, 299 are committed to processing and reporting Pap smears in various regions of the country. All 145 cytology services and 299 of the 475 cytotechnologists were involved in the screening program. Finally, the level of human resources available within the Thai health services included 112 698 nurses and 18 982 doctors, yielding a nurse population ratio of 1:619 and a doctor population ratio of 1:2975. Ahead of enrollment in the screening program, staff attached to the PCUs delivered messages in the community about the importance of cervical cancer screening during their routine visits to the villages and health centers to sensitize women. These staff delivered cervical cancer prevention talks, describing the target age group, the screening test, diagnosis, treatment, and follow-up care facilities to inform and empower women to attend screening clinics. Printed pamphlets and posters were provided in the waiting rooms of all healthcare establishments. A handbook describing the cervical screening program was prepared by the MOPH and used to train school teachers, village health volunteers, community leaders, health workers, and nurses in the PCUs in order to facilitate dissemination of information about the screening program, to improve awareness of
cervical cancer, and to augment participation in screening, diagnosis, and treatment. Women in the target age range were encouraged to attend health centers, PCUs, and hospitals where Pap smears were collected using an Ayre spatula and fixed using spray fixatives or 70% ethyl alcohol. Nurses, health workers, and doctors were trained and reoriented in the collection of cervical cells and the referral of women with positive test results for further investigation and treatment. They were also taught how to enter data in the program information system, with the help of customized manuals developed for the program, and through contact refresher training courses conducted by the NCI. The Pap tests and computerized personal identifier data were sent to the government cytology laboratory in the district or provincial hospital by messenger. Smears were initially processed and reported by cytotechnologists. However, all tests with apparent high-grade squamous intraepithelial lesions (HSIL) or invasive cancerous lesions were routinely reviewed by cytopathologists before final reporting. The cytotechnologists and cytopathologists involved in the program underwent NCI refresher courses to improve processing and reporting. The cytology results were returned to the PCU or hospital within 1 week of collection. Participants were notified of their test results either by post or at an appointment with a health worker. Women with normal test results were advised to undergo a repeat smear after 5 years. Women with low-grade squamous intraepithelial lesions (LSIL) or worse on cytology were referred to the colposcopy clinic in the community or provincial hospital. Biopsies were performed in women with colposcopic abnormalities and the findings documented in the colposcopy record. Biopsies were predominantly processed and reported by the pathology laboratories in the secondary care level district or provincial hospitals. Women with histologically confirmed high-grade cervical intraepithelial neoplasia 2 or 3 were treated with cryotherapy or the loop electrosurgical excision procedure. Doctors were reoriented in colposcopic assessment and in performing the loop electrosurgical excision procedure in short training courses conducted by the NCI in collaboration with the Thai Society of Colposcopy. The International Agency for Research on Cancer manual on colposcopy and treatment of cervical neoplasia was used as the training resource [10]. Personnel involved in collection and reporting of Pap smears and doctors involved in colposcopy and treatment of precancerous lesions were provided with incentives ranging from 60 Thai Bahts (US $2) to 150 Thai Bahts (US $5) per case by the NHSO after the data had reached the central database kept at the NCI. National sample surveys involving approximately 13 375 women were conducted in 2005 and 2007 to estimate the proportion of women aged 35–59 years who had undergone a Pap smear in the preceding 5 years in order to assess the overall coverage of women with cytology screening [4,11]. These surveys were conducted by the Thai Government, independent of the screening program, to assess screening coverage. Demographic details and the cytology results were captured both at the primary and secondary care level in the Papreg computer database, commercially available software developed using Access (Microsoft, Redmond, WA, USA). Pap smear test results were given a serial number linked to the Thai citizen identity number of the participant. Papreg also captured screening, colposcopy, biopsy, treatment, and referral data. 3. Results Phase 1 of the Thai cervical cytology screening program for women aged 35–60 years was operational in 75 provinces during the period 2005–2009. The eligible population, the target population, and the population that actually underwent Pap testing each year are presented in Table 1. Of the 4 030 833 women targeted in this phase of the program, 3 124 855 (77.5%) were screened. Because no age information
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Community
Women aged 35-60 years Repeat screen every 5 years Screen-negatives
Primary care level
•
Health education
•
Awareness creation
•
Pap smear screening
•
Referral of screen-positive women
Primary care units + Health centers
Cytology laboratory Pap test
Screen-positives
Secondary care level
•
Processing and reporting of Pap smears
•
Colposcopy and biopsy
•
Diagnosis and treatment of precancerous lesions
•
Colposcopy clinic
Pathology laboratory
Suspected and frank cancer cases
Referral of invasive cancer cases Treatment of precancerous lesions
Tertiary care level
•
Treatment of large precancerous lesions
Gynecology oncology units
•
Staging and treatment of invasive cancer cases
Comprehensive cancer centers
Fig. 1. Organization and flow of healthcare services in phase 1 of the Thailand cervical cytology screening program, 2005–2009. Abbreviations: Pap; Papanicolaou; PCU, primary care unit.
Table 1 Eligible, target, and screened population by age and year screened for cervical cytology, 2005–2009.a Fiscal year of screening 2005 Eligible population Target population Population screened with Pap smear Age at screening, y b35 35–39 40–44 45–49 50–54 55–60 >60 Coverage rate c Compliance to screening d
b
2 000 000 834 394 405 756
2006
2007
2008
2009
2005–2009
2006–2009
2 000 000 800 000 586 981
2 000 000 796 439 855 090
2 000 000 800 000 642 155
2 000 000 800 000 634 873
10 000 000 4 030 833 3 124 855
8 000 000 3 196 439 2 719 099
68 427 98 403 111 750 105 476 92 471 94 546 15 908 25.1 62.8
(11.7) (16.8) (19.0) (18.0) (15.8) (16.1) (2.7)
128 511 138 703 153 755 147 607 125 642 131 924 28 948 34.9 87.6
(15.0) (16.2) (18.0) (17.3) (14.7) (15.4) (3.4)
109 428 102 124 113 541 105 031 87 892 102 157 21 982 25.5 63.8
(17.0) (15.9) (17.7) (16.4) (13.7) (15.9) (3.4)
111 656 96 954 104 950 104 527 88 634 106 539 21 613 25.1 62.7
(17.6) (15.3) (16.5) (16.5) (14.0) (16.8) (3.4)
418 022 436 184 483 996 462 641 394 639 435 166 88 451 27.7 69.2
(15.4) (16.0) (17.8) (17.0) (14.5) (16.0) (3.3)
Abbreviation: Pap, Papanicolaou. a Values are given as number or number (percentage). b Age information not available in 2005. c Coverage rate = screened population (35–60 years)/eligible population. d Compliance rate = screened population (35–60 years)/target population. Target population was 40% of the eligible population for whom government funding was available.
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Table 2 Cervical cytology results by year of screening, 2005–2009.a Fiscal year of screening Pap smear result
2005
Inadequate Normal LSIL HSIL Cancer Total
2924 399 663 1814 1141 214 405 756
2006 (0.7) (98.5) (0.4) (0.3) (0.1) (100.0)
4616 572 565 5645 3541 614 586 981
2007 (0.8) (97.5) (1.0) (0.6) (0.1) (100.0)
2008
6136 834 159 8834 5116 845 855 090
(0.7) (97.6) (1.0) (0.6) (0.1) (100.0)
4390 628 560 5524 2994 687 642 155
2009 (0.7) (97.9) (0.9) (0.5) (0.1) (100.0)
2925 623 038 5436 2914 560 634 873
2005–2009 (0.5) (98.1) (0.9) (0.5) (0.1) (100.0)
20 991 3 057 985 27 253 15 706 2920 3 124 855
(0.7) (97.9) (0.9) (0.5) (0.1) (100.0)
Abbreviations: HSIL, high-grade squamous intraepithelial lesions; LSIL, low-grade squamous intraepithelial lesions; Pap, Papanicolaou. a Values are given as number (percentage).
was recorded for the year 2005, Table 1 also includes the age-specific totals for the period 2006–2009. Except for the over 60-year-old age group, the numbers of women screened were evenly distributed across the different age strata. More than one-quarter of the eligible women were screened. However, because government funding for the screening program targeted 40% of the eligible population, the compliance to screening (which was based on the targeted women) was 69.2% during the period 2006–2009 (Table 1). Pap smear results by year of screening are given in Table 2. Tests results were normal in most cases (97.9%). Among the remaining women screened, 20 991 (0.7%) had inadequate smears; 27 253 (0.9%) had LSIL; 15 706 (0.5%) had HSIL; and 2920 (0.1%) had features of invasive cancer. “Inadequate” or “unsatisfactory” smears indicated a poor-quality smear with 1 or more of the following attributes: inadequate numbers of squamous or endocervical cells; poorly preserved and/or fixed smears; and presence of obscuring elements such as blood, inflammation cells, and other debris. Pap smear results by age at screening are given in Table 3. LSIL, HSIL, and cancerous lesions were similar across the age strata. In the 35–60-year-old targeted population, LSIL was detected in 0.8%–0.9%, while 0.4%–0.7% had HSIL on cytology. Although repeat smears were advised for those women with inadequate smears, this information was not captured in the database. Of the 2 719 099 Pap smears processed, results were reported within 1 week from receiving the smears for 572 738 women (21.1%); between 1 and 2 weeks for 547 723 (20.1%); between 3 and 4 weeks for 713 185 (26.2%); between 1 and 3 months for 693 208 (25.5%); and after 3 months for 192 245 (7.1%) (data not shown). Follow-up of women with positive test results was not well documented in the screening program. Of the 45 879 women detected with precancerous or cancerous lesions eligible for colposcopy, information was included in the database for only 3814 (8.3%). Treatment information was recorded for 240 women with precancerous lesions and referral information for 148 women with cancer. Approximately 500 000 smears were taken annually as part of the opportunistic cytology screening provided by private practitioners and private hospitals during 2005–2009 (i.e. outside the present
program). The results of national sample surveys of women aged 35–59 years that were conducted in 2005 and 2007 indicated that 37.7% and 71.9% of women had undergone a Pap smear in the preceding 5 years; in 2007, the frequency ranged from 66.7% in Bangkok to 78.8% in the northern region of Thailand. These surveys were conducted independently from the present study. 4. Discussion Phase 1 of the Thai cervical cancer screening program has shown that it is feasible to provide cytology services through the existing healthcare system. Two-thirds of women targeted had a cytology screen, although data on follow-up investigations for women with positive test results were inadequately documented. For more than 60% of the women screened, Pap smears results were reported within 1 month of collection. Approximately 4 million cervical smears were taken as part of the opportunistic screening during 2005–2009 and it is quite likely both these activities (i.e. smears taken in the screening program [current study] and smears taken by private doctors and private hospitals) have increased the overall coverage. This finding is substantiated by the fact that 71.9% of the women surveyed as part of the 2007 national sample survey reported having undergone a Pap smear in the preceding 5 years [11]. Encouraged by the outcomes of the present study, phase 2 was initiated in 2010 with the aim of screening 13 million women aged 30–60 years over 5 years. Nonetheless, there remains much to be improved in the program and in the way data are captured. Information about referral, adherence to referral, colposcopy, and management of precancerous lesions was not fully captured in the database owing to lack of regular feedback from the colposcopy services and hospitals involved to the program organizers. As a consequence, the proportion of women undergoing colposcopy, biopsy, and treatment after a positive test result cannot be reported, indicating a major lapse in assessing the entire range of process measures in the present phase of the screening program. Efforts are underway to ensure complete capture of colposcopy and treatment information in the next phase of the program, along with utilization of cancer registry data in evaluating the outcomes. Another
Table 3 Cervical cytology results by age at screening, 2006–2009.a Pap smear result Age at screen, y
Inadequate
b 35 35–39 40–44 45–49 50–54 55–60 > 60 Total
2145 2557 2873 2824 2714 4000 954 18 067
Normal (0.5) (0.6) (0.6) (0.6) (0.7) (0.9) (1.1) (0.7)
409 589 427 710 473 765 452 106 385 118 424 631 85 403 2 658 322
LSIL (98.0) (98.1) (97.9) (97.7) (97.6) (97.6) (96.6) (97.8)
4898 3833 4367 4341 3708 3423 869 25 439
HSIL (1.2) (0.9) (0.9) (0.9) (0.9) (0.8) (1.0) (0.9)
1311 1920 2631 2934 2616 2391 762 14 565
Cancer (0.3) (0.4) (0.5) (0.6) (0.7) (0.5) (0.9) (0.5)
Abbreviations: HSIL, high-grade squamous intraepithelial lesions; LSIL, low-grade squamous intraepithelial lesions; Pap, Papanicolaou. a Values are given as number (percentage).
79 164 360 436 483 721 463 2706
Total (b 0.1) (b 0.1) (0.1) (0.1) (0.1) (0.2) (0.5) (0.1)
418 022 436 184 483 996 462 641 394 639 435 166 88 451 2 719 099
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limitation is that a large number of women outside the target age range (35–60 years) underwent a Pap test because screening was not denied to any woman who requested it. Furthermore, monetary incentives for undergoing a Pap smear may have also contributed to obtaining smears from women under 35 years and those over 60 years. Information on screening coverage is an important input measure when monitoring and evaluating cervical cancer screening programs. Before the initiation of the present pilot project, screening coverage in Thailand was poor, with one-third of women reporting previously undergoing a Pap smear in cross-sectional surveys [4,12–14]. It is not clear what proportion of women with abnormal smears received diagnosis and treatment in the present study. A study by Thinkhamrop et al. found that 41% of women with abnormal tests were lost to follow-up. The primary reason given for non-attendance was poor communication: 36% of non-participants did not receive the appropriate letter informing them of the results; 10% did not understand the information provided in the letter; 5% received a letter stating that their test was normal; and 14% believed that their test result was not serious [15]. A secondary reason for non-attendance involved travel-related issues. Previous studies have shown that risk of invasive cancer decreased with increasing frequency of having a Pap smear; that a history of previous Pap smear was protective; and that the risk of cervical cancer increased with the interval since the previous Pap smear [14,16–18]. One-third of women in Khon Kaen province had never been screened for cervical neoplasia according a survey conducted in 2000 [12]. Half of the women in a cohort study involving 16 000 women in Khon Kaen province had undergone no prior screening and many screen-positive women did not have further investigation and treatment [13]. Population-based cancer registries provide a useful source of cancer incidence data for evaluating the outcome of cancer screening programs. Such registries were organized in Chiang Mai, Khon Kaen, Songkhla, Bangkok, and Lampang during the period 1986–1993 [3]. Population-based cancer registration has been organized in 20 Thai provinces since 2005; such registration has since been extended to cover 15 additional provinces where the Pap smear and VIA screenand-treat programs are functioning. An extensive cancer registration network will facilitate evaluation of these 2 screening programs in terms of trends in cervical cancer incidence and the negative predictive value of negative screens by linking the screening and cancer registration databases. New developments in cervical cancer screening are being taken into account for possible future applications in Thailand. Increasing evidence suggests that testing for the presence of human papillomavirus (HPV) is a more objective and effective approach than cytology. Furthermore, tests negative for HPV have a high negative predictive value for high-grade precancerous and cancerous cervical lesions [19,20]. Rapid, simple, affordable, yet accurate HPV tests designed for use in low-resource settings will soon be available [21]. As a consequence, Thailand may consider a national screening policy of primary HPV testing of women older than 30 years with cytology triage of HPV-positive women once affordable HPV tests become commercially available. The present study has provided invaluable experience in organizing and expanding cervical cancer prevention services. The necessary infrastructure, human resources, expertise, and information systems have been established so that a program based on objective testing,
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such as HPV testing with cytology or VIA triage, may be successfully implemented in Thailand. Conflict of interest The authors have no conflicts of interest. References [1] Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. GLOBOCAN 2008: Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10. Published 2010. http://globocan.iarc.fr. [2] Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, et al. Cancer Incidence in Five Continents, Vol. IX. IARC Scientific Publications No. 160. Lyon: International Agency for Research on Cancer; 2007. [3] Khuhaprema T, Attasara P, Srivatanakul P, Sriplung H, Wangnon S, Sumitsawan Y. Cancer in Thailand 2001–2003. Bangkok: National Cancer Institute; 2010. [4] Ministry of Public Health. The Survey Report of Behavioural Risk Factors of Noncommunicable Diseases and Injuries in Thailand, 2005. Nonthaburi: MOPH; 2008. [5] Deerasamee S, Srivatanakul P, Sriplung H, Hong-Ngam A, Tansuwan T, Nilvachararung S, et al. Prevention and early detection of cervical cancer in Nakornpanom Province: implementation of a model demonstration project for the control of cervical cancer in Thailand. Int J Cancer 2002;100(Suppl. 13):97. [6] Deerasamee S, Srivatanakul P, Sriplung H, Nilvachararung S, Tansuwan U, Pitakpraiwan P, et al. Monitoring and evaluation of a model demonstration project for the control of cervical cancer in Nakhon Phanom province, Thailand. Asian Pac J Cancer Prev 2007;8(4):547–56. [7] Gaffikin L, Blumenthal PD, Emerson M, Limpaphayom K. Safety, acceptability, and feasibility of a single-visit approach to cervical-cancer prevention in rural Thailand: a demonstration project. Lancet 2003;361(9360):814–20. [8] United Nations Statistics Division. UNdata – a data access system to UN databases. http://data.un.org/Data.aspx?q=maternal+mortality&d=MDG&f=seriesRowID% 3a553. Accessed April 18, 2012. [9] United Nations Statistics Division. UNdata – a data access system to UN databases. http://data.un.org/Data.aspx?q=infant+mortality+rate&d=MDG&f=seriesRowID% 3a562. Accessed April 18, 2012. [10] Sellors JW, Sankaranarayanan R. Colposcopy and Treatment of Cervical Intraepithelial Neoplasia: A Beginners' Manual. IARC Non serial publication. Lyon: International Agency for Research on Cancer; 2003. [11] Ministry of Public Health. The Survey Report of Behavioural Risk Factors of Noncommunicable Diseases and Injuries in Thailand, 2007. Nonthaburi: MOPH; 2008. [12] Kritpetcharat O, Suwanrungruang K, Sriamporn S, Kamsa-Ard S, Kritpetcharat P, Pengsaa P. The coverage of cervical cancer screening in Khon Kaen, northeast Thailand. Asian Pac J Cancer Prev 2003;4(2):103–5. [13] Sriamporn S, Parkin DM, Pisani P, Suwanrungruang K, Pengsaa P. Behavioural risk factors for cervical cancer from a prospective study in Khon Kaen, Northeast Thailand. Cancer Detect Prev 2004;28(5):334–9. [14] Sriamporn S, Khuhaprema T, Parkin M. Cervical cancer screening in Thailand: an overview. J Med Screen 2006;13(Suppl. 1):S39–43. [15] Thinkhamrop J, Lumbiganon P, Jitpakdeebodin S. Loss to follow-up of patients with abnormal Pap smear: magnitude and reasons. J Med Assoc Thai 1998;81(11): 862–5. [16] Chichareon S, Herrero R, Muñoz N, Bosch FX, Jacobs MV, Deacon J, et al. Risk factors for cervical cancer in Thailand: a case-control study. J Natl Cancer Inst 1998;90(1): 50–7. [17] Thomas DB, Ray RM, Koetsawang A, Kiviat N, Kuypers J, Qin Q, et al. Human papillomaviruses and cervical cancer in Bangkok. I. Risk factors for invasive cervical carcinomas with human papillomavirus types 16 and 18 DNA. Am J Epidemiol 2001;153(8):723–31. [18] Wangsuphachart V, Thomas DB, Koetsawang A, Riotton G. Risk factors for invasive cervical cancer and reduction of risk by 'Pap' smears in Thai women. Int J Epidemiol 1987;16(3):362–6. [19] Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial. Lancet Oncol 2010;11(3):249–57. [20] Sankaranarayanan R, Nene BM, Shastri SS, Jayant K, Muwonge R, Budukh AM, et al. HPV screening for cervical cancer in rural India. N Engl J Med 2009;360(14): 1385–94. [21] Qiao YL, Sellors JW, Eder PS, Bao YP, Lim JM, Zhao FH, et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol 2008;9(10):929–36.
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International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Organization and evolution of organized cervical cytology screening in Thailand Thiravud Khuhaprema a, Pattarawin Attasara b, Petcharin Srivatanakul c, Suleeporn Sangrajrang c, Richard Muwonge d, Catherine Sauvaget d, Rengaswamy Sankaranarayanan d,⁎ a
Surgical Oncology Division, National Cancer Institute, Bangkok, Thailand Cancer Registration Unit, National Cancer Institute, Bangkok, Thailand Research Division, National Cancer Institute, Bangkok, Thailand d Early Detection and Prevention Section and Screening Group, International Agency for Research on Cancer (WHO-IARC), Lyon, France b c
a r t i c l e
i n f o
Article history: Received 13 October 2011 Received in revised form 6 March 2012 Accepted 23 April 2012 Keywords: Cervical cancer Cytology National program Pilot project Screening Thailand
a b s t r a c t Objective: To describe phase 1 of an organized cytology screening project initiated in Thailand by the Ministry of Public Health and the National Health Security Office. Methods: Women aged 35–60 years were encouraged to undergo cervical screening in primary care units and hospitals through awareness programs. Papanicolaou smears were processed and reported at district or provincial cytology laboratories. Women with normal test results were advised to undergo repeat screening after 5 years, while those with precancerous and cancerous lesions were referred for colposcopy, biopsy, and treatment. Information on screening, referral, investigations, and therapy were logged in a computer database. Results: Between 2005 and 2009, 69.2% of the 4 030 833 targeted women were screened. In all, 20 991 women had inadequate smears; 27 253 had low-grade squamous intraepithelial lesions; 15 706 had high-grade squamous intraepithelial lesions; and 2920 had invasive cancers. Information on the management of precancerous lesions was available for only 17.4% of women referred for colposcopy. Conclusion: Although follow-up data on women with positive test results were inadequately documented, the present findings indicate that provision of cytology services through the existing healthcare system is feasible. © 2012 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Cervical cancer is the second most common cancer among all women in Thailand but the most frequent among those living in rural areas of the country. In 2008, the estimated annual numbers of new cases and deaths from cervical cancer were 9999 and 5216, respectively [1]. The age-standardized incidence rates during 2000–2003 ranged from 17.8 to 28.9 per 100 000 women in different provinces of Thailand [2,3]. Opportunistic cytology screening has been widely available in urban areas of Thailand for several years. Estimates from national surveys suggest that, before 2005, approximately 25% of women in the 30–65 year age group underwent a Papanicolaou (Pap) smear in the preceding 5 years [4]. Nonetheless, it remains unclear what proportion of women with abnormal cytology results received diagnosis and treatment and what impact screening had on cervical cancer incidence and mortality over the past 3 decades. A pilot demonstration project with Pap smear screening was initiated in Nakhon Phanom province in 1999 to inform and guide the development of an organized cytology screening program for Thailand [5,6].
⁎ Corresponding author at: Early Detection and Prevention Section and Screening Group, WHO-IARC, 150 cours Albert Thomas, 69372 Lyon Cedex 08, France. Tel.: + 33 472738599; fax: + 33 472738518. E-mail address: [email protected] (R. Sankaranarayanan).
This project covered 45% of the targeted women aged 35–59 years with a single screen and showed the feasibility of integrating cervical cancer screening and treatment services with the existing healthcare infrastructure. Another important development in cervical cancer prevention in Thailand was the initiative by the Royal Thai College of Obstetrics and Gynecology in collaboration with the Johns Hopkins Program for International Education in Gynecology and Obstetrics [7]. The aim of this collaboration was to introduce a screen-and-treat demonstration program that utilized visual inspection with acetic acid (VIA) and cryotherapy to 4 districts of Roi Et province and establish the safety, acceptability, and feasibility of this approach [7]. The findings from the above studies and other experiences in Thailand and elsewhere prompted a government policy that enabled the provinces to provide population-based screening with VIA screenand-treat, cervical cytology, or both approaches. This policy led to the initiation in 2005 of a 5-year organized cytology screening project in 75 provinces of Thailand (all provinces except Bangkok) by the National Health Security Office (NHSO) and the Ministry of Public Health (MOPH) and the expansion of VIA screen-and-treat program targeting women aged 30–45 years to 29 provinces in 2006. Thailand has made considerable progress in improving maternal and child health, as indicated by low maternal mortality (48 per 100 000 live births in 2008) and low infant mortality (12 per 1000 live births in 2009) [8,9]. Currently, there are more cervical cancer deaths than maternal deaths in Thailand. The pilot project on cervical cytology screening and the VIA
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screen-and-treat efforts have been organized to emulate this success at reducing maternal and infant deaths. The present study describes the organization and process measures of phase 1 of the cervical cytology screening program in Thailand. The overall objective of this phase was to use Pap smears to screen 800 000 women aged 35–60 years each year so that 4 million out of the total 10.1 million Thai women within this age group were screened in 5 years using the government health services in Thailand. In conjunction with this program, measures were introduced to increase the capacity for obtaining and interpreting Pap smears, colposcopy, diagnosis, and treatment services for women with cervical cancer precursor lesions within the public health services. 2. Materials and methods The Thai cervical cancer screening program targeted women aged 35–60 years during the years 2005–2009 (January 1, 2005, to December 31, 2009); the designated Pap smear screening interval was 5 years (i.e. the women were advised to undergo routine screening via Pap smear every 5 years). The MOPH Department of Medical Services was responsible for conducting the screening program, which was integrated within the routine health services of Thailand. The National Cancer Institute (NCI) in Bangkok was responsible for monitoring the screening process and the outcome measures. The study was exempt from Institutional Review Board approval as it used routinely collected data in a public health program. Informed consent was obtained from women undergoing colposcopy, biopsy, and treatment. The flow of healthcare services is shown in Fig. 1. The lowest basic level of health care in Thailand is the primary care unit (PCU). Each PCU is staffed by 7–10 personnel (registered nurses, health educators, and health workers) and provides services to approximately 5000 people resident in 10–20 villages at the sub-district level. Most villages in the PCU have a public health center that is visited by PCU staff at periodic intervals. A total of 9804 PCUs and 69 331 primary public health centers serve 40 million people in rural Thailand (and were included in the screening program) providing prenatal and postnatal care, immunization, cervical screening, and treatment of minor ailments, as well as health education and creating health awareness. There are 722 community hospitals at the district level, each with 30–120 beds, and 94 general (provincial) hospitals at the secondary care level in the 76 provinces of Thailand. Tertiary care is provided by 58 large hospitals. All of these district, secondary, and tertiary centers were involved in the screening program. Cytology and histology laboratories are organized in selected community, provincial, and tertiary hospitals at the secondary and tertiary care level. Cytology services are provided by approximately 145 cytology laboratories; of the 475 cytotechnologists in the Thai health services, 299 are committed to processing and reporting Pap smears in various regions of the country. All 145 cytology services and 299 of the 475 cytotechnologists were involved in the screening program. Finally, the level of human resources available within the Thai health services included 112 698 nurses and 18 982 doctors, yielding a nurse population ratio of 1:619 and a doctor population ratio of 1:2975. Ahead of enrollment in the screening program, staff attached to the PCUs delivered messages in the community about the importance of cervical cancer screening during their routine visits to the villages and health centers to sensitize women. These staff delivered cervical cancer prevention talks, describing the target age group, the screening test, diagnosis, treatment, and follow-up care facilities to inform and empower women to attend screening clinics. Printed pamphlets and posters were provided in the waiting rooms of all healthcare establishments. A handbook describing the cervical screening program was prepared by the MOPH and used to train school teachers, village health volunteers, community leaders, health workers, and nurses in the PCUs in order to facilitate dissemination of information about the screening program, to improve awareness of
cervical cancer, and to augment participation in screening, diagnosis, and treatment. Women in the target age range were encouraged to attend health centers, PCUs, and hospitals where Pap smears were collected using an Ayre spatula and fixed using spray fixatives or 70% ethyl alcohol. Nurses, health workers, and doctors were trained and reoriented in the collection of cervical cells and the referral of women with positive test results for further investigation and treatment. They were also taught how to enter data in the program information system, with the help of customized manuals developed for the program, and through contact refresher training courses conducted by the NCI. The Pap tests and computerized personal identifier data were sent to the government cytology laboratory in the district or provincial hospital by messenger. Smears were initially processed and reported by cytotechnologists. However, all tests with apparent high-grade squamous intraepithelial lesions (HSIL) or invasive cancerous lesions were routinely reviewed by cytopathologists before final reporting. The cytotechnologists and cytopathologists involved in the program underwent NCI refresher courses to improve processing and reporting. The cytology results were returned to the PCU or hospital within 1 week of collection. Participants were notified of their test results either by post or at an appointment with a health worker. Women with normal test results were advised to undergo a repeat smear after 5 years. Women with low-grade squamous intraepithelial lesions (LSIL) or worse on cytology were referred to the colposcopy clinic in the community or provincial hospital. Biopsies were performed in women with colposcopic abnormalities and the findings documented in the colposcopy record. Biopsies were predominantly processed and reported by the pathology laboratories in the secondary care level district or provincial hospitals. Women with histologically confirmed high-grade cervical intraepithelial neoplasia 2 or 3 were treated with cryotherapy or the loop electrosurgical excision procedure. Doctors were reoriented in colposcopic assessment and in performing the loop electrosurgical excision procedure in short training courses conducted by the NCI in collaboration with the Thai Society of Colposcopy. The International Agency for Research on Cancer manual on colposcopy and treatment of cervical neoplasia was used as the training resource [10]. Personnel involved in collection and reporting of Pap smears and doctors involved in colposcopy and treatment of precancerous lesions were provided with incentives ranging from 60 Thai Bahts (US $2) to 150 Thai Bahts (US $5) per case by the NHSO after the data had reached the central database kept at the NCI. National sample surveys involving approximately 13 375 women were conducted in 2005 and 2007 to estimate the proportion of women aged 35–59 years who had undergone a Pap smear in the preceding 5 years in order to assess the overall coverage of women with cytology screening [4,11]. These surveys were conducted by the Thai Government, independent of the screening program, to assess screening coverage. Demographic details and the cytology results were captured both at the primary and secondary care level in the Papreg computer database, commercially available software developed using Access (Microsoft, Redmond, WA, USA). Pap smear test results were given a serial number linked to the Thai citizen identity number of the participant. Papreg also captured screening, colposcopy, biopsy, treatment, and referral data. 3. Results Phase 1 of the Thai cervical cytology screening program for women aged 35–60 years was operational in 75 provinces during the period 2005–2009. The eligible population, the target population, and the population that actually underwent Pap testing each year are presented in Table 1. Of the 4 030 833 women targeted in this phase of the program, 3 124 855 (77.5%) were screened. Because no age information
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Community
Women aged 35-60 years Repeat screen every 5 years Screen-negatives
Primary care level
•
Health education
•
Awareness creation
•
Pap smear screening
•
Referral of screen-positive women
Primary care units + Health centers
Cytology laboratory Pap test
Screen-positives
Secondary care level
•
Processing and reporting of Pap smears
•
Colposcopy and biopsy
•
Diagnosis and treatment of precancerous lesions
•
Colposcopy clinic
Pathology laboratory
Suspected and frank cancer cases
Referral of invasive cancer cases Treatment of precancerous lesions
Tertiary care level
•
Treatment of large precancerous lesions
Gynecology oncology units
•
Staging and treatment of invasive cancer cases
Comprehensive cancer centers
Fig. 1. Organization and flow of healthcare services in phase 1 of the Thailand cervical cytology screening program, 2005–2009. Abbreviations: Pap; Papanicolaou; PCU, primary care unit.
Table 1 Eligible, target, and screened population by age and year screened for cervical cytology, 2005–2009.a Fiscal year of screening 2005 Eligible population Target population Population screened with Pap smear Age at screening, y b35 35–39 40–44 45–49 50–54 55–60 >60 Coverage rate c Compliance to screening d
b
2 000 000 834 394 405 756
2006
2007
2008
2009
2005–2009
2006–2009
2 000 000 800 000 586 981
2 000 000 796 439 855 090
2 000 000 800 000 642 155
2 000 000 800 000 634 873
10 000 000 4 030 833 3 124 855
8 000 000 3 196 439 2 719 099
68 427 98 403 111 750 105 476 92 471 94 546 15 908 25.1 62.8
(11.7) (16.8) (19.0) (18.0) (15.8) (16.1) (2.7)
128 511 138 703 153 755 147 607 125 642 131 924 28 948 34.9 87.6
(15.0) (16.2) (18.0) (17.3) (14.7) (15.4) (3.4)
109 428 102 124 113 541 105 031 87 892 102 157 21 982 25.5 63.8
(17.0) (15.9) (17.7) (16.4) (13.7) (15.9) (3.4)
111 656 96 954 104 950 104 527 88 634 106 539 21 613 25.1 62.7
(17.6) (15.3) (16.5) (16.5) (14.0) (16.8) (3.4)
418 022 436 184 483 996 462 641 394 639 435 166 88 451 27.7 69.2
(15.4) (16.0) (17.8) (17.0) (14.5) (16.0) (3.3)
Abbreviation: Pap, Papanicolaou. a Values are given as number or number (percentage). b Age information not available in 2005. c Coverage rate = screened population (35–60 years)/eligible population. d Compliance rate = screened population (35–60 years)/target population. Target population was 40% of the eligible population for whom government funding was available.
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Table 2 Cervical cytology results by year of screening, 2005–2009.a Fiscal year of screening Pap smear result
2005
Inadequate Normal LSIL HSIL Cancer Total
2924 399 663 1814 1141 214 405 756
2006 (0.7) (98.5) (0.4) (0.3) (0.1) (100.0)
4616 572 565 5645 3541 614 586 981
2007 (0.8) (97.5) (1.0) (0.6) (0.1) (100.0)
2008
6136 834 159 8834 5116 845 855 090
(0.7) (97.6) (1.0) (0.6) (0.1) (100.0)
4390 628 560 5524 2994 687 642 155
2009 (0.7) (97.9) (0.9) (0.5) (0.1) (100.0)
2925 623 038 5436 2914 560 634 873
2005–2009 (0.5) (98.1) (0.9) (0.5) (0.1) (100.0)
20 991 3 057 985 27 253 15 706 2920 3 124 855
(0.7) (97.9) (0.9) (0.5) (0.1) (100.0)
Abbreviations: HSIL, high-grade squamous intraepithelial lesions; LSIL, low-grade squamous intraepithelial lesions; Pap, Papanicolaou. a Values are given as number (percentage).
was recorded for the year 2005, Table 1 also includes the age-specific totals for the period 2006–2009. Except for the over 60-year-old age group, the numbers of women screened were evenly distributed across the different age strata. More than one-quarter of the eligible women were screened. However, because government funding for the screening program targeted 40% of the eligible population, the compliance to screening (which was based on the targeted women) was 69.2% during the period 2006–2009 (Table 1). Pap smear results by year of screening are given in Table 2. Tests results were normal in most cases (97.9%). Among the remaining women screened, 20 991 (0.7%) had inadequate smears; 27 253 (0.9%) had LSIL; 15 706 (0.5%) had HSIL; and 2920 (0.1%) had features of invasive cancer. “Inadequate” or “unsatisfactory” smears indicated a poor-quality smear with 1 or more of the following attributes: inadequate numbers of squamous or endocervical cells; poorly preserved and/or fixed smears; and presence of obscuring elements such as blood, inflammation cells, and other debris. Pap smear results by age at screening are given in Table 3. LSIL, HSIL, and cancerous lesions were similar across the age strata. In the 35–60-year-old targeted population, LSIL was detected in 0.8%–0.9%, while 0.4%–0.7% had HSIL on cytology. Although repeat smears were advised for those women with inadequate smears, this information was not captured in the database. Of the 2 719 099 Pap smears processed, results were reported within 1 week from receiving the smears for 572 738 women (21.1%); between 1 and 2 weeks for 547 723 (20.1%); between 3 and 4 weeks for 713 185 (26.2%); between 1 and 3 months for 693 208 (25.5%); and after 3 months for 192 245 (7.1%) (data not shown). Follow-up of women with positive test results was not well documented in the screening program. Of the 45 879 women detected with precancerous or cancerous lesions eligible for colposcopy, information was included in the database for only 3814 (8.3%). Treatment information was recorded for 240 women with precancerous lesions and referral information for 148 women with cancer. Approximately 500 000 smears were taken annually as part of the opportunistic cytology screening provided by private practitioners and private hospitals during 2005–2009 (i.e. outside the present
program). The results of national sample surveys of women aged 35–59 years that were conducted in 2005 and 2007 indicated that 37.7% and 71.9% of women had undergone a Pap smear in the preceding 5 years; in 2007, the frequency ranged from 66.7% in Bangkok to 78.8% in the northern region of Thailand. These surveys were conducted independently from the present study. 4. Discussion Phase 1 of the Thai cervical cancer screening program has shown that it is feasible to provide cytology services through the existing healthcare system. Two-thirds of women targeted had a cytology screen, although data on follow-up investigations for women with positive test results were inadequately documented. For more than 60% of the women screened, Pap smears results were reported within 1 month of collection. Approximately 4 million cervical smears were taken as part of the opportunistic screening during 2005–2009 and it is quite likely both these activities (i.e. smears taken in the screening program [current study] and smears taken by private doctors and private hospitals) have increased the overall coverage. This finding is substantiated by the fact that 71.9% of the women surveyed as part of the 2007 national sample survey reported having undergone a Pap smear in the preceding 5 years [11]. Encouraged by the outcomes of the present study, phase 2 was initiated in 2010 with the aim of screening 13 million women aged 30–60 years over 5 years. Nonetheless, there remains much to be improved in the program and in the way data are captured. Information about referral, adherence to referral, colposcopy, and management of precancerous lesions was not fully captured in the database owing to lack of regular feedback from the colposcopy services and hospitals involved to the program organizers. As a consequence, the proportion of women undergoing colposcopy, biopsy, and treatment after a positive test result cannot be reported, indicating a major lapse in assessing the entire range of process measures in the present phase of the screening program. Efforts are underway to ensure complete capture of colposcopy and treatment information in the next phase of the program, along with utilization of cancer registry data in evaluating the outcomes. Another
Table 3 Cervical cytology results by age at screening, 2006–2009.a Pap smear result Age at screen, y
Inadequate
b 35 35–39 40–44 45–49 50–54 55–60 > 60 Total
2145 2557 2873 2824 2714 4000 954 18 067
Normal (0.5) (0.6) (0.6) (0.6) (0.7) (0.9) (1.1) (0.7)
409 589 427 710 473 765 452 106 385 118 424 631 85 403 2 658 322
LSIL (98.0) (98.1) (97.9) (97.7) (97.6) (97.6) (96.6) (97.8)
4898 3833 4367 4341 3708 3423 869 25 439
HSIL (1.2) (0.9) (0.9) (0.9) (0.9) (0.8) (1.0) (0.9)
1311 1920 2631 2934 2616 2391 762 14 565
Cancer (0.3) (0.4) (0.5) (0.6) (0.7) (0.5) (0.9) (0.5)
Abbreviations: HSIL, high-grade squamous intraepithelial lesions; LSIL, low-grade squamous intraepithelial lesions; Pap, Papanicolaou. a Values are given as number (percentage).
79 164 360 436 483 721 463 2706
Total (b 0.1) (b 0.1) (0.1) (0.1) (0.1) (0.2) (0.5) (0.1)
418 022 436 184 483 996 462 641 394 639 435 166 88 451 2 719 099
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limitation is that a large number of women outside the target age range (35–60 years) underwent a Pap test because screening was not denied to any woman who requested it. Furthermore, monetary incentives for undergoing a Pap smear may have also contributed to obtaining smears from women under 35 years and those over 60 years. Information on screening coverage is an important input measure when monitoring and evaluating cervical cancer screening programs. Before the initiation of the present pilot project, screening coverage in Thailand was poor, with one-third of women reporting previously undergoing a Pap smear in cross-sectional surveys [4,12–14]. It is not clear what proportion of women with abnormal smears received diagnosis and treatment in the present study. A study by Thinkhamrop et al. found that 41% of women with abnormal tests were lost to follow-up. The primary reason given for non-attendance was poor communication: 36% of non-participants did not receive the appropriate letter informing them of the results; 10% did not understand the information provided in the letter; 5% received a letter stating that their test was normal; and 14% believed that their test result was not serious [15]. A secondary reason for non-attendance involved travel-related issues. Previous studies have shown that risk of invasive cancer decreased with increasing frequency of having a Pap smear; that a history of previous Pap smear was protective; and that the risk of cervical cancer increased with the interval since the previous Pap smear [14,16–18]. One-third of women in Khon Kaen province had never been screened for cervical neoplasia according a survey conducted in 2000 [12]. Half of the women in a cohort study involving 16 000 women in Khon Kaen province had undergone no prior screening and many screen-positive women did not have further investigation and treatment [13]. Population-based cancer registries provide a useful source of cancer incidence data for evaluating the outcome of cancer screening programs. Such registries were organized in Chiang Mai, Khon Kaen, Songkhla, Bangkok, and Lampang during the period 1986–1993 [3]. Population-based cancer registration has been organized in 20 Thai provinces since 2005; such registration has since been extended to cover 15 additional provinces where the Pap smear and VIA screenand-treat programs are functioning. An extensive cancer registration network will facilitate evaluation of these 2 screening programs in terms of trends in cervical cancer incidence and the negative predictive value of negative screens by linking the screening and cancer registration databases. New developments in cervical cancer screening are being taken into account for possible future applications in Thailand. Increasing evidence suggests that testing for the presence of human papillomavirus (HPV) is a more objective and effective approach than cytology. Furthermore, tests negative for HPV have a high negative predictive value for high-grade precancerous and cancerous cervical lesions [19,20]. Rapid, simple, affordable, yet accurate HPV tests designed for use in low-resource settings will soon be available [21]. As a consequence, Thailand may consider a national screening policy of primary HPV testing of women older than 30 years with cytology triage of HPV-positive women once affordable HPV tests become commercially available. The present study has provided invaluable experience in organizing and expanding cervical cancer prevention services. The necessary infrastructure, human resources, expertise, and information systems have been established so that a program based on objective testing,
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such as HPV testing with cytology or VIA triage, may be successfully implemented in Thailand. Conflict of interest The authors have no conflicts of interest. References [1] Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. GLOBOCAN 2008: Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10. Published 2010. http://globocan.iarc.fr. [2] Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, et al. Cancer Incidence in Five Continents, Vol. IX. IARC Scientific Publications No. 160. Lyon: International Agency for Research on Cancer; 2007. [3] Khuhaprema T, Attasara P, Srivatanakul P, Sriplung H, Wangnon S, Sumitsawan Y. Cancer in Thailand 2001–2003. Bangkok: National Cancer Institute; 2010. [4] Ministry of Public Health. The Survey Report of Behavioural Risk Factors of Noncommunicable Diseases and Injuries in Thailand, 2005. Nonthaburi: MOPH; 2008. [5] Deerasamee S, Srivatanakul P, Sriplung H, Hong-Ngam A, Tansuwan T, Nilvachararung S, et al. Prevention and early detection of cervical cancer in Nakornpanom Province: implementation of a model demonstration project for the control of cervical cancer in Thailand. Int J Cancer 2002;100(Suppl. 13):97. [6] Deerasamee S, Srivatanakul P, Sriplung H, Nilvachararung S, Tansuwan U, Pitakpraiwan P, et al. Monitoring and evaluation of a model demonstration project for the control of cervical cancer in Nakhon Phanom province, Thailand. Asian Pac J Cancer Prev 2007;8(4):547–56. [7] Gaffikin L, Blumenthal PD, Emerson M, Limpaphayom K. Safety, acceptability, and feasibility of a single-visit approach to cervical-cancer prevention in rural Thailand: a demonstration project. Lancet 2003;361(9360):814–20. [8] United Nations Statistics Division. UNdata – a data access system to UN databases. http://data.un.org/Data.aspx?q=maternal+mortality&d=MDG&f=seriesRowID% 3a553. Accessed April 18, 2012. [9] United Nations Statistics Division. UNdata – a data access system to UN databases. http://data.un.org/Data.aspx?q=infant+mortality+rate&d=MDG&f=seriesRowID% 3a562. Accessed April 18, 2012. [10] Sellors JW, Sankaranarayanan R. Colposcopy and Treatment of Cervical Intraepithelial Neoplasia: A Beginners' Manual. IARC Non serial publication. Lyon: International Agency for Research on Cancer; 2003. [11] Ministry of Public Health. The Survey Report of Behavioural Risk Factors of Noncommunicable Diseases and Injuries in Thailand, 2007. Nonthaburi: MOPH; 2008. [12] Kritpetcharat O, Suwanrungruang K, Sriamporn S, Kamsa-Ard S, Kritpetcharat P, Pengsaa P. The coverage of cervical cancer screening in Khon Kaen, northeast Thailand. Asian Pac J Cancer Prev 2003;4(2):103–5. [13] Sriamporn S, Parkin DM, Pisani P, Suwanrungruang K, Pengsaa P. Behavioural risk factors for cervical cancer from a prospective study in Khon Kaen, Northeast Thailand. Cancer Detect Prev 2004;28(5):334–9. [14] Sriamporn S, Khuhaprema T, Parkin M. Cervical cancer screening in Thailand: an overview. J Med Screen 2006;13(Suppl. 1):S39–43. [15] Thinkhamrop J, Lumbiganon P, Jitpakdeebodin S. Loss to follow-up of patients with abnormal Pap smear: magnitude and reasons. J Med Assoc Thai 1998;81(11): 862–5. [16] Chichareon S, Herrero R, Muñoz N, Bosch FX, Jacobs MV, Deacon J, et al. Risk factors for cervical cancer in Thailand: a case-control study. J Natl Cancer Inst 1998;90(1): 50–7. [17] Thomas DB, Ray RM, Koetsawang A, Kiviat N, Kuypers J, Qin Q, et al. Human papillomaviruses and cervical cancer in Bangkok. I. Risk factors for invasive cervical carcinomas with human papillomavirus types 16 and 18 DNA. Am J Epidemiol 2001;153(8):723–31. [18] Wangsuphachart V, Thomas DB, Koetsawang A, Riotton G. Risk factors for invasive cervical cancer and reduction of risk by 'Pap' smears in Thai women. Int J Epidemiol 1987;16(3):362–6. [19] Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial. Lancet Oncol 2010;11(3):249–57. [20] Sankaranarayanan R, Nene BM, Shastri SS, Jayant K, Muwonge R, Budukh AM, et al. HPV screening for cervical cancer in rural India. N Engl J Med 2009;360(14): 1385–94. [21] Qiao YL, Sellors JW, Eder PS, Bao YP, Lim JM, Zhao FH, et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol 2008;9(10):929–36.