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International Journal for Quality in Health Care Advance Access originally published online on January 26, 2006
International Journal for Quality in Health Care 2006 18(2):81-86; doi:10.1093/intqhc/mzi100
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International Journal for Quality in Health Care vol. 18 no. 2 © The Author 2006. Published by Oxford University Press on behalf of International Society for Quality in Health Care; all rights reserved

Quality in Practice

Improving cervical cancer prevention in a developing country

Irene Agurto1, Jorge Sandoval2, Maribel De La Rosa3 and Maria Elena Guardado3

1 Pan American Health Organization, Washington, DC, USA, 2 Ministry of Health, El Salvador, San Salvador, 3 Organizacion Panamericana de la Salud, El Salvador, San Salvador

Objective: to enhance the delivery of services, using continuous quality improvement, and an outreach strategy.

Design and setting: pre and post measurements in a Primary Health Care system in El Salvador. Outcome indicators: women screened for the first time in their lifetime, unsatisfactory samples, turnaround time, and follow-up.

Intervention: involvement of policy, service provision and community levels in 4 plan-do-study-act cycles, facilitating linkages between work processes and a quality control group.

Results: 3,408 women screened for the first time in their lifetime in 1 year in regular services; unsatisfactory samples reduced by 1/2; turnaround time reduced by almost 1/3; follow-up increased from 24% (22/90) to 100% (196/196) .146 of the 151 women cytologically defined as low and high-grade squamous intraepithelial lesions (L-HSIL) were confirmed on histology as cervical intraepithelial neoplasia (CIN), while 5 showed benign changes. Of the 43 women classified as having high-grade squamous intraepithelial lesion on cytology, 36 were diagnosed with CIN2 lesions, 7 with CIN3 and 2 were confirmed with invasive carcinoma.

Conclusion: improvements in delivery of screening can be made with few additional resources in the absence of an organized system. We promoted linkages between detection and diagnosis through enhancement of teamwork and functional coordination, which improved follow-up rates. We restored links between screening and reading processes through minor adjustments, which improved the turnaround time of samples. Trained outreach workers created new links between community and health services, identifying women who had never been screened before in their lives and facilitating their access to regular clinic services.

Keywords: quality of Health Care, cervical cancer, practice guidelines, screening, developing countries

Address reprint requests to Irene Agurto, Pan American Health Organization, 525, 23rd St. N.W. Washington, D.C. 20037, USA. E-mail: iagurto{at}yahoo.es

Accepted for publication December 19, 2005.

It has been estimated that 92 136 cervical cancer cases and 37 640 deaths occurred in the Americas in 2000. Latin America and the Caribbean contributed 83.9 and 81.2%, respectively, of the total estimated cancer cases and deaths [1]. Incidence rates for El Salvador were 40.6 per 100 000 women in 2000; age-standardized mortality rate was 15.8 per 100 000 women, which are persistently high along with Nicaragua and Peru [2].

Latin America and the Caribbean have the infrastructure for cervical cancer early detection; however, reductions of the burden of disease have been modest. In Mexico, e.g., in spite of the existence of an early detection program for 20 years, the impact on mortality has been almost none [3].

An organized program should include ensuring the quality, the appropriate analysis of the sample and the timely delivery of results; guidelines that state the priority age group, definitions of abnormalities, frequency of subsequent screens as well as mechanisms to invite women with negative results for re-screening [4,5,6].

Sponsored by the Pan American Health Organization and the Ministry of Health, El Salvador, we used a quality improvement methodology to enhance organizational features of an early detection cytology-based program, employing the updated national prevention guidelines.


   Setting
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 Setting
Objectives
 Study design
 Methodology
 Results
 Discussion
 Acknowledgements
 References
 
El Salvador’s estimated population was 6 000 000 inhabitants in 2002, and 50% of them live in poverty with close to one quarter living in extreme poverty. The public health system covers 80% of the population, and 15% is covered by the social security system, non-governmental organizations and private services. The national public health system in the 14 departments consists of 27 basic comprehensive health systems, each with one or two hospitals, seven clinics and rural health stations. This study was performed in a semi-rural department, with a population of women of 17 550 aged 30–59 years in 2002, and two basic comprehensive health systems each with seven clinics and one hospital and one cytology laboratory serving four other departments.

To improve the national cervical cancer program performance [7,8], the Ministry of Health updated their guidelines. Aspects of these guidelines incorporated in the study are screening women aged 30–59 years every 2 years; prioritizing remote areas and women who have not had a Pap test in their lifetime or who had not had it in the previous 2 years.


   Objectives
Top
 Setting
 Objectives
Study design
 Methodology
 Results
 Discussion
 Acknowledgements
 References
 
To enhance the delivery of services, using continuous quality improvement, and an outreach strategy. Specific objectives include screen the priority population according to the guidelines; improve the quality of test taking; reduce turnaround time; and improve follow-up rates.


   Study design
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 Setting
 Objectives
 Study design
Methodology
 Results
 Discussion
 Acknowledgements
 References
 
The year-long intervention consists of

  1. A baseline study to assess: the capacity of the health providers to undertake changes, skills and procedures, infrastructure, and client satisfaction. We used surveys, expert observations, and program data review.
  2. A continuous quality improvement model: four plan–do–study–act cycles [9] to improve work processes. Participants include 100 health providers (doctors, nurses, and nursing assistants); managerial staff; and one cytology laboratory. National participants include representatives from the policy level, mid-level management, and the national reference laboratory. Activities include analysis of baseline, strategic planning, training, vertical and horizontal coordination, and establishing a quality control group. We performed a mid-term process evaluation and evaluation of outcome indicators.
  3. An outreach strategy: training 100 outreach workers to identify the target population, and facilitating women’s access to screening and follow-up workup. We used an outcome indicator and a survey of women.

Outcome indicators [10] are

  1. Number of women screened for the first time in their lifetime during the intervention.
  2. Number of unsatisfactory samples in relation to total samples, and the reduction of turnaround time for delivering results from and to clinics.
  3. Number of women screened positive followed up with colposcopy in relation to total of women with all positive Pap results.

We measured outcome indicators at two points in time: the first in 2002, before the intervention, and the second in 2003, at the end of the intervention. We compiled the information manually from the clinics’ registry books, the cytology laboratory, and the colposcopy unit (Table 1).


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  		Table 1 Priority areas, improvements, and outcome indicators

 

The Ministry of Health has an ongoing project to address laboratory performance; therefore, quality of the Pap test as done in the local laboratory, although a concern, was not specifically addressed in this study.


   Methodology
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 Objectives
 Study design
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Results
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 Acknowledgements
 References
 
We performed a baseline study in the department, consisting of

  1. A questionnaire to 42 health providers to assess: providers’ performance of the pelvic exam; availability of enough light and supplies; turnaround time of samples; availability of diagnosis and treatment; availability, conditions, and use of supplies to prevent infections; availability of a private space for the pelvic exam and for counseling; interpersonal relationships and relationships with clients.
  2. The evaluation of skills and procedures in 12 clinics using a checklist of 20 items, including, checking risk factors and gynecological status; performance of safety procedures; general health and pelvic exam; use of speculum; performance of Pap; performance of bimanual and rectal exam if indicated; data entry and counseling skills.
  3. A user-satisfaction exit survey (n = 341 women), including perception of access; convenience; courtesy; capacity of staff; information; intention to return to the same clinic and eventual recommendation of the service to friends and family.
  4. Review of program performance data.

We conducted four cycles of plan–do–study–act, consisting of:

  1. Presentation and group discussion of methodology; results of the baseline study; data collection to complete the baseline; introduction of new guidelines. The participants signed a written statement for voluntary participation.
  2. The participants crafted a strategic plan, employing the new guidelines and the baseline evaluation to select the priority areas and propose improvements with the existing resources. They agreed on a quality control group, formed by immediate and intermediate management, chief gynecologist, colposcopist, local and national laboratory representatives, and outreach workers’ supervisors.
  3. The participants tested the improvements, updated the strategic plan, and agreed upon outcome indicators.
  4. The participants and their teams implemented the solutions according to plans. We monitored the project through site visits, conference calls, and written updates. We measured the outcome indicators and discussed the results with the participants.

To identify women who had never been screened in their lifetime, and those who had not been screened in the past 2 years, and facilitate their access to services, we trained the outreach workers in four one-day workshops. Topics included technical information on cervical cancer prevention and new guidelines, gender issues, and behavior change methodologies. We provided them with educational material on cervical cancer prevention developed by PAHO/WHO for use in Latin America. The outreach workers performed a rural census, identified the target population, provided information, and helped women to strengthen their personal networks to overcome access barriers.

To evaluate this strategy, we administered a survey to a random household sample of women aged 30–59 years (n = 265) in the department and to a sample in another similar department, with no intervention (n = 276). We pre-tested the questionnaire and trained university students to collect data. Individuals were randomly selected according to an established procedure. The items include components of the behavioral change and network strengthening methodology; knowledge about cervical cancer; perception of quality of services; visits by outreach workers and its usefulness.


   Results
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 Setting
 Objectives
 Study design
 Methodology
 Results
Discussion
 Acknowledgements
 References
 
The main findings of the baseline study are: at clinic level, insufficient supplies for a Pap smear; poor uptake and loss of samples; slow turnaround time of results (1 month or more), and poor record-keeping and at laboratory level, a reading backlog, and poor quality control [8]. Before the intervention, clinics performed 2446 Pap smears to an undetermined number of women aged 15 years and older. Women rated least favorably the access to services, with an average of 3.7 in a scale of 5.

After the intervention, results were the following: (see Table 2)


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  		Table 2 Summary of intervention from first to second measurement points

 

Number of women aged 30–59 years of age screened for the first time in their lifetime
Local registries were updated to reflect number of women and not number of tests and whether the test was the first or a repeat. A true denominator of the age group has not yet been completed given that there is only a rural census.

Using the guidelines, the services targeted an older age group, and an underserved population, namely women who had never been screened before in their lifetime. According to the laboratory registries, routine services screened 3408 women for the first time in their lifetime in 1 year, and 328 women in mobile clinics.

Women screened for the first time in their lives represent 25.6% of the total population in the age range in the department.

Quality of sample and turnaround time
We were unable to access data at baseline, because the samples were sent to private laboratories with no reporting procedures. The laboratory submitted a special report indicating that when no test-taking training was provided, 41 samples in 6 months were unsatisfactory, and once training had been provided, 14 samples in 6 months were unsatisfactory (no denominator provided in the report).

The time to deliver the samples from the clinics to the laboratory was reduced from an average of 23 days to 9 days. The time to return the samples from the laboratory to the clinics was reduced from an average of 27 days to11 days.

Follow-up
We measured follow-up as number of women colposcoped for low- and high-grade squamous intraepithelial lesion or more.

In 2002, 6 months before the intervention, 90 women with any positive results in the department were referred to colposcopy, and 22 received it. Others either did not attend or did not receive colposcopy in the public system. In 2003, in a 6-month period, 196 women aged 30–59 years screened by conventional cytology, of which 151 were classified as having low-grade squamous intraepithelial lesions; 43 as having high-grade lesions and two cancer. All of these women were biopsied. One hundred and forty-six of the 151 cytologically defined as low- and high-grade squamous intraepithelial lesion were confirmed on histology as CIN1, while five showed benign changes. Of the 43 women classified as having high-grade squamous intraepithelial lesion on cytology, 36 were diagnosed with CIN2 lesions and seven with CIN3. Two women were confirmed with invasive carcinoma (Table 3).


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  		Table 3 Pap test/biopsy results

 

Improved coordination within services, including the outreach workers, increased follow-up workup from 24% (22/90) to almost complete follow-up.

Additionally, survey results indicate that 89% (238) of women in the department consider that their knowledge on cervical cancer prevention had improved, in comparison with 41% (113) in the other department.


   Discussion
Top
 Setting
 Objectives
 Study design
 Methodology
 Results
 Discussion
Acknowledgements
 References
 
Interventions to improve performance of preventive programs have been used in adult immunization, cancer [11], diabetes [9,12], and preventive primary health care services, including Pap smear, mainly in the United States [13]. The USAID Quality Assurance Project has implemented programs in developing and middle income countries [14,15] in the areas of child survival, malaria, HIV/AIDS, family planning, and others.

The improvement of linkages between work processes [16,17] and different levels of involvement of personnel, management, and clients [17] in process improvement are key features of the methodologies most widely employed.

Zapka [17] suggested that cancer care requires a continuum of care starting from risk assessment, primary prevention, screening, detection, diagnosis, treatment, recurrence surveillance, and end of life care. According to this model, following the pioneer study of Taiichi [16], failures occur in the transitions between work processes, which are themselves that set of activities that deliver an end product. Some of the potential failures in the process of care identified by Zapka and addressed by this study lie in the processes of screening, accessing care, and following-up of abnormal results or diagnostic or treatment plan.

To ensure successful transitioning between work processes, the appropriate linkages need to be created, established, and secured to deliver the end product. Most of the organizational features devised in this intervention are aimed at ensuring these links. Linkages between detection and diagnosis, which should have formally been secured by the existing referral and counter referral system, were promoted through enhancement of teamwork, including fostering functional coordination and collaboration. This, in turn, improved the follow-up rates. Links between clinics (screening process) and the public laboratories (reading process) were restored through minor adjustments, such as organizing the collection and delivery of samples and results. This adjustment improved the turnaround time of samples. New links between community and health services were created through trained outreach workers, who identified women who had never been screened before in their lives and facilitated their access to regular clinic services.

The involvement of policy, service provision, and community levels within a common framework during the plan–do–study–act cycles facilitated this intervention, similar to the collaboratives [9]. This built common ground, trust, collaboration and provided a forum for the technical debate of the guidelines. The quality control group supported the everyday implementation and internal monitoring and facilitated linkages among processes.

Resources used include international and national expertise to design, prepare, conduct, monitor, and evaluate the intervention; staff time, particularly to attend workshops and in-service training and redirect current activities; workshop and travel expenses. The central Ministry of Health provided copies of the guidelines. Most of the educational materials are available in Spanish and English, except for the outreach strategy materials. In spite of an initial demand from staff for additional equipment, supplies and training, no investments, or additional purchases, were made. Reducing the use of mobile clinics may have reduced the clinics’ regular costs, but the cost of accessing the routine clinics was not transferred to the users given that the social network approach made travel more affordable and rational. Staff did not receive incentives or benefits, but a survey among participants (not reported here) showed improved job satisfaction, support from top-management, and availability of guidelines, organizational direction, and community resources. Costing of the intervention was initially considered, but not carried out, and would have been an added value for others wishing to replicate the intervention.

Factors that may contribute to the sustainability of the experience include the priority given by the Ministry of Health to the topic and willingness of their officials to discuss with local providers; a bottom-up approach; a quality control group that coincided with the formal leadership; integrating the outreach workers into the core activities; using available resources and materials to fit a low-resource country budget. The Ministry of Health is currently using the methodology to progressively expand their program.

The continuous quality improvement methodology employed is simple enough to be adapted to another setting, and service delivery modalities, but may face the same limitation encountered here, namely, paucity of data. The outreach strategy requires additional input; however, other modalities may be used provided they ensure links with the core activities of health provision.

Most of the components of a successful quality improvement method were included in this intervention, such as organizational change, teamwork, support from top management, and educational material, all of which have proved to increase cancer-screening services [11,19,20]. However, reaching the appropriate mix at the right work processes is a matter that needs attention to local conditions and execution.


   Acknowledgements
Top
 Setting
 Objectives
 Study design
 Methodology
 Results
 Discussion
 Acknowledgements
References
 
The authors acknowledge Dr Sylvia C. Robles, Dr Merle Lewis, Ms Silvana Luciani, Ms Sarah C. White and Dr Torres for their contributions in the preparation of this article. The Bill and Melinda Gates Foundation through the Pan American Health Organization supported this project. Special thanks to Drs Horacio Toro and Eduardo Guerrero, representatives of PAHO/WHO in El Salvador, for their support.


   References
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 Setting
 Objectives
 Study design
 Methodology
 Results
 Discussion
 Acknowledgements
 References
 

  1. Ferlay J, Bray F, Pisani P, Parkin DM. Globocan 2000. In Cancer Incidence, Mortality and Prevalence Worldwide. Lyon, France: IARC Press, 2001.

  2. Pan American Health Organization. A Situational Analysis of Cervical Cancer in Latin America and the Caribbean. Washington, DC: PAHO, 2004.

  3. Lazcano-Ponce EC, Moss S. Alonso de Ruiz P et al. Cervical cancer screening in developing countries: why is it ineffective? The case of Mexico. Arch Med Res 1999; 30: 240–250.[CrossRef][ISI][Medline]

  4. Miller A, Sankaranarayanan R, Bosch X, Sepulveda C. Can screening for cervical cancer be improved, especially in developing countries? Int J Cancer 2003; 107: 337–340.[Medline]

  5. Young J, Ward J. Strategies to improve cancer screening in general practice: are guidelines the answer? Fam Pract 1999; 16: 66–70.[Abstract/Free Full Text]

  6. Adab P, McGhee SM, Yanova J et al. Effectiveness and efficiency of opportunistic cervical cancer screening: comparison with organized screening. Med Care 2004; 42: 600–609.[CrossRef][Medline]

  7. Pan American Health Organization. Cervical Cancer Prevention in El Salvador. Washington, DC: PAHO, 1999.

  8. Pan American Health Organization. Report on the Cytology Laboratories in El Salvador. Washington, DC: PAHO, 2001–2002.

  9. Wagner E, Glasgow R, Davis C et al. Quality improvement in chronic illness care: a collaborative approach. Jt Comm J Qual Improv 2001; 27: 63–80.[Medline]

  10. Marrett LD, Robles S, Ashbury FD, Green B, Goel V, Luciani S. A proposal for cervical screening information systems in developing countries. Int J Cancer 2002; 102 (3): 293–299.[Medline]

  11. Stone E, Morton S, Hulscher M et al. Interventions that increase use of adult immunization and cancer screening services: a meta – analysis. Ann Intern Med 2002; 136: 641–651.[Abstract/Free Full Text]

  12. Wagner E.Population-based management of diabetes care. Patient Educ Couns 1995; 26: 225–230.[CrossRef][ISI][Medline]

  13. Solberg L, Kottke T, Brekke M et al. Failure of a continuous quality improvement intervention to increase the delivery of preventive services. A randomized trial. Eff Clin Pract 2000; 3: 105–115.[Medline]

  14. Quality Assurance Project: http://www.qaproject.org Accessed 2 November 2004.

  15. Smits HL, Leatherman S, Berwick DM. Editorial. Quality improvement in the developing world. Int J Qual Health Care 2002; 14: 439–440.[Free Full Text]

  16. Taiichi O. Toyota Production System: Beyond Large Scale Production. New York: Productivity Press, 1988.

  17. Zapka J, Taplin S, Solberg L, Manos M. A framework for improving the quality of cancer care: the case of breast and cervical cancer screening. Cancer Epidemiol Biomarkers Prev 2003; 12: 4–13.[Abstract/Free Full Text]

  18. Bradley J, Mayfield M, Mehta M, Rukonge A. participatory evaluation of reproductive health care quality in developing countries. Soc Sci Med 2002; 55: 269–282.[CrossRef][ISI][Medline]

  19. Ovretveit J, Bate P, Cleary P et al. Organizational matters. Quality collaboratives: lessons from research. Qual Saf Health Care 2002; 11: 345–351.[Abstract/Free Full Text]

  20. Shortell S, Bennett CH, Byck G. Assessing the impact of continuous quality improvement on clinical practice: what it will take to accelerate progress. Milbank Q 1998; 76: 593–624.[CrossRef][ISI][Medline]


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