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Quality assurance in follow-up and initial treatment for screening mammography programs in 22 countries

CARRIE N. KLABUNDE, HÉLÈNE SANCHO-GARNIER, STEPHEN TAPLIN, STEINAR THORESEN, NORIAKI OHUCHI, RACHEL BALLARD-BARBASH
DOI: http://dx.doi.org/10.1093/intqhc/14.6.449 449-461 First published online: 1 December 2002

Abstract

Objective. To describe the quality assurance activities related to follow-up evaluation of abnormal screening mammograms and subsequent initial treatment of women determined to have breast cancer for the screening programs represented in the International Breast Cancer Screening Network (IBSN).

Design. Analysis of data from a survey that included questions about screening program policies, standards, and procedures for follow-up of women with abnormal mammograms, as well as the data and measures that programs use to assess the adequacy of follow-up and initial treatment.

Setting and participants. IBSN representatives in 23 countries completed a comprehensive questionnaire between May and December 1998.

Results. Two-thirds of IBSN countries reported that they have a written policy or guidelines for follow-up of an abnormal mammogram; 64% require accreditation of the cytology or pathology laboratories that analyze breast specimens, or subject pathology laboratories to external audits. Of the 22 activities and measures related to quality of follow-up and initial treatment that we examined, all countries had in place at least half of them, although countries were more likely to have implemented activities and measures related to data collection and evaluation than to processes of care.

Conclusions. Population-based screening mammography programs cannot achieve the goal of reducing breast cancer mortality if women with abnormal mammograms do not receive appropriate, timely follow-up and initial treatment. This study shows that IBSN countries vary in their implementation of procedures and measures to assure the quality of follow-up and initial treatment for women with abnormal screening mammograms. There is more emphasis on collecting and evaluating data than establishing mechanisms to ensure that the processes of care for follow-up and initial treatment are of high quality.

  • breast cancer
  • follow-up
  • mammography
  • quality assurance
  • screening
  • treatment

Clinical trial evidence demonstrating breast cancer mortality reductions in asymptomatic women receiving mammography has prompted many countries to establish population-based screening mammography programs [1]. While the ultimate goal of such programs is to achieve reductions in breast cancer mortality comparable to those established in clinical trials, this goal will not be realized if a high proportion of women in the target population do not attend for screening, and if women with abnormal screening mammograms do not receive appropriate and timely follow-up and initial treatment [26]. Population-based programs also must carefully monitor the outcomes associated with diagnostic follow-up of abnormal mammograms to ensure that women are not being subjected to unnecessary invasive procedures (e.g. fine-needle aspiration cytology, core biopsy, open biopsy) [2]. Moreover, several countries have begun to examine the impact of their population-based programs on breast cancer mortality [711]. Because mortality reduction can be attributable to screening as well as to receipt of state-of-the-art treatment, countries engaging in such evaluation require comprehensive data on all aspects of the breast cancer early detection continuum, from screening to follow-up of abnormal results and treatment of identified breast cancers. For these reasons, population-based screening mammography is best viewed as a process that extends beyond the mammography examination itself to include follow-up of women with abnormal results and, if cancer is detected, assessment of treatment received (Figure 1). Furthermore, evaluation of program performance and impact requires data on cancer outcomes which ideally are obtained through access to a high-quality cancer registry operating within the geographic region targeted by the screening program [2].

Figure 1

Diagram of the screening mammography process, including follow-up and treatment. Adapted with permission from Klabunde et al. [15].

Defined as a system of procedures, checks, audits, and corrective actions to ensure that health services and reporting activities are of the highest achievable quality [12], quality assurance is crucial in achieving optimal screening program benefit. In recognition of this vital role, the International Breast Cancer Screening Network (IBSN), a voluntary consortium of 25 countries with population-based breast cancer screening programs, undertook an assessment of the scope of quality assurance activities for screening mammography across member countries in 1998. The goal of the IBSN is to obtain and analyze data on the policies, administration, performance, and outcomes of population-based breast cancer screening. Descriptions of the organization, funding, coverage policies, and operating procedures for the screening programs in IBSN countries have been published elsewhere [13,14]. The quality assurance assessment consisted of four major components: organization of quality assurance, technical quality control, quality assurance in follow-up and initial treatment, and quality assurance for data collection systems. Each component is summarized in a separate paper [1517]. This report describes the quality assurance activities related to follow-up diagnostic evaluation of abnormal screening mammograms and subsequent initial treatment of women determined to have breast cancer for the screening programs represented in the IBSN. Both the extent to which quality assurance activities include processes of care and the collection and evaluation of data are considered. The assessment covers the major themes of organization of screening, assuring quality in the follow-up of abnormal screening mammograms, and accessibility of data on initial treatment and tumor characteristics.

Methods

A working group comprised of IBSN representatives from eight countries was formed in October 1997 to develop and implement the quality assurance assessment. Between November 1997 and April 1998, the working group constructed a comprehensive questionnaire designed to assess the following aspects of screening mammography quality assurance: organization of quality assurance; site visits and accreditation; quality control; quality assurance for data systems; quality assurance in follow-up and initial treatment; and program performance and impact measures. Existing screening mammography guidance documents addressing quality assurance [2, 1820] were consulted in the development of the questionnaire. The section on quality assurance in follow-up and initial treatment included questions about program policies, standards, and procedures in general, as well as those specific to surgical evaluation, cytology, and pathology. Items asking about calculation of measures to evaluate the adequacy of follow-up and access to data on treatment and tumor characteristics also were included. Thus, the questionnaire section on quality assurance in follow-up and initial treatment covered activities related to both processes of care and the collection and evaluation of data.

Questionnaire drafts were reviewed by working group members and experts in screening mammography and questionnaire design. The finalized questionnaire was mailed in late May 1998 to IBSN representatives in the 23 countries participating in the IBSN at that time. Representatives from countries with organized screening programs and opportunistic screening (i.e. screening occurring outside of organized programs) were asked to respond for the quality measures of their organized programs. Representatives from countries with multiple organized screening programs were asked to provide, if possible, a summary response that reflected the majority of programs. Because the United States does not have an organized national or regional screening program comparable to those found in many European and other countries with more centralized health care systems, the questionnaire was sent to a representative from the National Cancer Institute (NCI) who is responsible for a program of surveillance research focusing on community-based screening mammography within a multi-region, organized mammography registry system [21]. Thus, data for the United States reflect a diverse subset of health care facilities engaged in screening mammography and contributing data on mammography practice and outcomes to a centralized statistical center. Investigators in this mammography registry system are evaluating mammography performance and outcomes within defined populations, an objective common to all of the screening programs represented in the IBSN. While the facilities providing data to the registry system are not a census of all facilities, they are generally representative of screening mammography practice in the United States and cover diverse geographical regions in the country.

Completed questionnaires were received from all 23 countries. Data were coded and entered into a Microsoft Access database. Responses were reviewed by the working group in October 1998. After clarification of missing or unclear responses by re-contacting each country’s IBSN representative as needed, responses were finalized in December 1998. Because the Republic of Ireland was in the process of developing a new national breast cancer screening program after concluding a pilot program, Ireland’s response is excluded from this report due to incomplete data.

Comparisons were made between seven countries with population-based screening programs that are national in scope and 13 countries with screening programs that are more locally organized. In some cases, these are pilot programs that eventually may be expanded to encompass a larger geographical area within the country. For example, data provided for Japan reflect the pilot program in Miyagi prefecture; implementation of a national screening mammography program began in Japan in 2000. Data for Germany are included in this report, although it should be noted that a population-based screening program was in the planning and implementation stages in Germany at the time of the survey. As described above, data for the United States represent an organized mammography registry system, and are summarized separately.

Nearly all of the countries with organized screening mammography programs also have opportunistic screening. However, because few of these countries collect or assess data on opportunistic screening, it is impossible to summarize opportunistic screening practice. Therefore, most countries are not able to examine cancer outcomes among women who are diagnosed outside of organized screening programs. In this assessment, we report data obtained from organized screening programs and registries, the only data currently available for international comparisons of screening mammography practice.

Results

Characteristics of the screening mammography programs in the 22 responding countries are displayed in Table 1. All countries except Belgium and the United States reported having one or more organized programs designed to screen a designated target population in a systematic fashion. The Belgian program represented in this paper covers the city of Brussels and the region of Wallonia; an organized, population-based screening program encompassing all of Belgium began implementation in 2001. As indicated by the number of programs, mammography facilities, X-ray units, and the proportion of the target population reached, screening programs vary considerably in size and scope. Furthermore, a variety of approaches to implementing quality assurance for these programs is evident, with nine countries doing so on a national basis, seven subnationally, and four using a combined national/subnational approach. In two countries (Belgium and Uruguay), screening mammography quality assurance is the responsibility of the individual mammography facilities. All but three countries (Belgium, Greece, and Hungary) have established linkages between screening program and cancer registry data, an important requirement for assessing program performance and impact [6]. In about half of these countries, though, the linkage is not fully computerized.

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Table 1

Organization of screening mammography programs represented in the International Breast Cancer Screening Network, 1998

Assuring quality in the follow-up of abnormal screening mammograms

Sixteen countries (73%) reported that the screening mammography program is responsible for carrying out the follow-up diagnostic evaluation of an abnormal mammogram (Table 2). In the six countries in which screening mammography programs do not have this responsibility (Israel, The Netherlands, Belgium, Canada, Uruguay, United States), women with an abnormal mammogram are either referred to dedicated assessment centers or to their primary physician for further evaluation. Fifteen countries (68%) indicated that they have a written policy or guideline that delineates the steps to be taken to ensure follow-up of an abnormal mammogram. Fourteen countries (64%) have established standards for the percentage of all screening mammograms that are deemed to be abnormal; these standards range from 5–7% for all screens, 2–10% for first screens, and 1–7% for subsequent screens. Slightly over half (55%) of the countries have a specified time limit for follow-up of an abnormal mammogram; the time limit varied from 1 week (Denmark, Norway) to 1 month (Belgium, Spain, Greece, Japan, Uruguay). Five countries (23%) have established standards for a minimum percentage of abnormal mammograms that should have follow-up with fine needle aspiration, core biopsy, or open biopsy; of these countries, only Norway specifies standards for all three procedures.

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Table 2

Follow-up of abnormal screening mammogram results by screening mammography programs represented in the International Breast Cancer Screening Network, 1998

All countries reported having a set procedure for initiating surgical evaluation of women with abnormal mammograms (Table 3). Requiring the woman with an abnormal screen to contact the surgeon’s office to arrange evaluation is a more commonly used procedure (13 countries) than direct contact of the surgeon’s office by screening program staff (11 countries) or direct evaluation by a surgeon in the screening program (seven countries). Furthermore, as can be seen in Table 3, some countries use more than one mechanism for initiating surgical evaluation. In all countries, open biopsies are performed by surgeons, and in two, physicians other than surgeons also perform open biopsies: Uruguay (radiologists) and the United States (family physicians in certain rural areas). Five countries (23%) indicated that physicians who perform open biopsies are required to have certification in this procedure.

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Table 3

Standards and procedures for surgical evaluation in the screening programs represented in the International Breast Cancer Screening Network, 1998

Fourteen countries (64%) require accreditation of the cytology or pathology laboratories that analyze breast specimens, or subject pathology laboratories to periodic external audits (Table 4). Four countries (Australia, Netherlands, United Kingdom, United States) have all three of these quality assurance mechanisms in place; seven (Belgium, Denmark, Portugal, Sweden, Greece, Hungary, Japan) require accreditation of cytology and pathology laboratories but not external audits of pathology laboratories; two (Spain, Germany) subject pathology laboratories to periodic external audits; and one (Uruguay) requires accreditation of pathology laboratories. The remaining eight countries (Finland, Iceland, Israel, Luxembourg, Canada, France, Italy, Norway) do not have quality assurance requirements specific to cytology and pathology laboratories. All countries, however, indicated that screening programs have access to cytology and pathology data on breast lesions, and all but one (Portugal) reported that screening program staff must actively obtain these data, although in about two-thirds of the countries, cytology and pathology reports are also routinely forwarded to the screening program, thereby somewhat lessening the program’s data collection burden.

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Table 4

Standards review and accessibility of cytology and pathology data for the screening mammography programs represented in the International Breast Cancer Screening Network, 1998

Countries reported that screening programs use a variety of measures and procedures to evaluate the adequacy of follow-up to an abnormal mammogram (Table 5). All countries calculate and monitor a recall rate for their programs. Seventeen (77%) convene multi-disciplinary case conferences to review abnormal screening mammograms that subsequently are determined to be breast cancer, with 14 of these including a radiologist, pathologist, and surgeon in the case conference. Seventeen (77%) actively assess a benign-to-malignant biopsy ratio, while the remaining five countries indicated that they have the data to do so although they do not currently assess this measure. Thirteen countries (59%) assess the sensitivity of screening mammography, with another six reporting that they could calculate this measure although they do not do so at present. Sixteen countries (73%) specify a target breast cancer detection rate, and all but one (Uruguay) assess the rate of interval cancers. Seventeen (77%) conduct radiological reviews of interval cancers.

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Table 5

Measures and procedures for evaluating adequacy of follow-up within the screening mammography programs represented in the International Breast Cancer Screening Network, 1998

Access to data on initial treatment and tumor characteristics

Eighteen of the 22 countries (82%) indicated that they are able to access data on surgery, radiation therapy, chemotherapy, hormonal therapy, tumor size, and lymph node involvement for women with abnormal mammograms who are diagnosed with breast cancer (Table 6). However, in nearly half of these countries (44%), access to data on adjuvant therapy (i.e. radiation therapy, chemotherapy, hormonal therapy) was reported to be with at least some difficulty. Only one country (Belgium) indicated that the screening program does not obtain data on either initial treatment or tumor characteristics. Two countries (United Kingdom, Canada) obtain data on surgery but not adjuvant therapy, while three (Finland, Canada, Denmark) do not obtain data on nodal involvement.

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Table 6

Access to data on initial treatment and tumor characteristics for the screening programs represented in the International Breast Cancer Screening Network, 1998

Of the 21 countries that reported having access to data on surgery, all but three (Finland, Portugal, Hungary) indicated that screening program staff actively seek these data, although about half of the countries noted that surgical reports are also routinely forwarded to the screening program. Among the countries that obtain data on tumor characteristics (i.e. assessments of tumor size and nodal status), pathological analysis was more often cited as the source of these data than was clinical assessment.

Discussion

Quality assurance involves an ongoing process of monitoring health services to ensure the provision of appropriate care that contributes to desired outcomes [22]. In screening mammography, population-based programs strive to demonstrate a reduction in breast cancer mortality in the screened population by attempting to identify a high proportion of the breast cancer extant in the target population, optimize the rates of referral for follow-up diagnostic evaluation, and detect a high proportion of breast cancers with small tumor size and no nodal involvement [23]. Attainment of these goals necessitates careful attention to the processes of care involved in screening delivery, as well as the collection and evaluation of data on screening delivery and outcomes. In particular, programs must ensure not only high standards for screening but also that women with abnormal mammograms receive appropriate and timely follow-up diagnostic evaluation and, if cancer is detected, high-quality treatment.

We assessed the extent to which the quality assurance activities of the screening mammography programs represented in the IBSN extend to follow-up of abnormal mammograms and, when breast cancer is identified, initial treatment. We examined approximately 22 different activities and measures addressing procedures and processes for follow-up of abnormal mammograms, and data collected on follow-up and initial treatment to facilitate evaluation of screening outcomes and program impact. Results show that all countries have in place at least half of the quality assurance activities and measures considered in this evaluation, although there is variation in the extent to which these mechanisms have been implemented. For example, four countries (Israel, Luxembourg, Belgium, Canada) have implemented approximately half of the activities and measures, while nine countries (Finland, Iceland, Netherlands, Denmark, France, Italy, Hungary, Uruguay, United States) have about two-thirds in place and another nine (Australia, United Kingdom, Norway, Portugal, Spain, Germany, Sweden, Greece, Japan) have implemented three-quarters or more. Countries with nationally organized screening programs did not appear to be more likely to have implemented these mechanisms than did countries with programs that were organized more locally.

Most countries, however, appeared to place greater emphasis on quality assurance activities for follow-up and initial treatment that involve the collection and evaluation of data than the implementation of mechanisms addressing processes of care. We considered that nine of the mechanisms reflected such processes of follow-up care as having time limits for investigation of abnormal results, requiring accreditation or external audits of cytology and pathology laboratories, and conducting case conferences to review abnormalities that are subsequently determined to be breast cancer. Another nine concerned collection of data on follow-up of abnormal screening mammograms such as assessing the recall rate, benign-to-malignant biopsy ratio, cancer detection rate, and interval cancer rate. On average, countries reported having five of the processes of care measures and seven of the data collection measures in place. This finding may reflect differences in screening program organization, as programs in slightly over one-quarter of the countries reported not having responsibility for carrying out the follow-up of an abnormal mammogram. It may also be an indication of the influence of quality assurance guidance documents, especially the European Guidelines for Quality Assurance in Mammography Screening [2], which place greater emphasis on the data that programs should collect to monitor follow-up and initial treatment than on specifying activities for ensuring high-quality processes of care in follow-up and initial treatment.

However, it is important to point out that we do not know which quality assurance mechanisms are associated with optimal screening mammography program performance. Furthermore, because the questionnaire that comprised the data source for this report covered multiple aspects of screening mammography quality assurance, we were limited in the number of items that could be included on the topic of quality assurance in follow-up and initial treatment. For example, monitoring the recall rate is at best an indirect means of assessing whether women with abnormal mammograms receive appropriate follow-up and initial treatment. A ‘time to follow-up’ or ‘lost to follow-up’ measure might be more informative. The rate of screen-detected, in situ breast cancers is also an important measure of program performance; however, these measures were not captured in our assessment. Likewise, we did not evaluate whether and how individual countries respond when screening mammography programs do not adhere to defined quality standards.

Three countries appear to be particularly comprehensive in their implementation of quality assurance mechanisms related to follow-up and initial treatment. Australia reported having all but one of the indicators considered in this evaluation in place. Norway responded that it has implemented all of the measures with the exception of accreditation of cytology and pathology laboratories and external auditing of pathology laboratories. The United Kingdom is noteworthy because, despite the size and considerable complexity of this national program, it too has implemented nearly all of the quality assurance aspects we considered. All three countries have developed quality assurance guidelines specific to their screening programs [15,19,20]. The United Kingdom has been particularly active in this regard, having published separate sets of guidelines addressing quality assurance for cytology, pathology, and surgical services [2426]. It should be noted that Canada has recently initiated efforts to develop and monitor quality assurance standards specific to follow-up and treatment [27].

Quality assurance in follow-up and treatment is integral to the goal of demonstrating a reduction in breast cancer mortality attributable to population-based screening programs. As stated in the European Guidelines [2], ‘a high quality screening program can only lead to a long-term mortality reduction if the treatment of women detected at screening is of equally high quality’. Activities and measures that most programs should have in place to evaluate program impact on mortality include monitoring the cancer detection rate, interval cancer rate, recall rate, benign to malignant biopsy ratio, and size and nodal status of screen-detected tumors [23]. Furthermore, the most efficient means of accessing the cancer outcomes data necessary for such an evaluation usually requires linkage to a cancer registry located in the region targeted by the screening program. The results of the IBSN quality assurance assessment reported here and in a previous paper [16] suggest that only about one-quarter of IBSN countries have screening programs that have been operating for a time period of sufficient length, and with procedures and data of sufficient comprehensiveness to permit such evaluation. Australia, The Netherlands, the United Kingdom, Sweden, and the United States (through the Breast Cancer Surveillance Consortium) are among these countries. A few of these countries have begun to publish the results of their efforts to evaluate screening program impact on breast cancer mortality [11,2829].

In summary, this study shows that IBSN countries vary in their implementation of procedures and measures to assure the quality of follow-up and initial treatment for women with abnormal screening mammograms. Most of the countries give greater attention to collecting and evaluating data on follow-up and initial treatment than to establishing mechanisms to ensure that the processes of care for follow-up and initial treatment are of high quality. We anticipate, however, that as more countries begin to assess the long-term impact of their population-based programs, they will increase their activities related to this integral component of the breast cancer early detection continuum.

Acknowledgments

The following IBSN members and collaborators contributed data to this study: P. Jha, B. Chapple, Australia; A. Grivegnée, Belgium; F. Bouchard, Canada; E. Lynge, Denmark; M. Hakama, Finland; H. Sancho-Garnier, J. Stines, France; L. von Karsa, Germany; I. Garas, A. Linos, E. Riza, Greece; E. Szabò, A. Petrànyi, Hungary; B. F. Sigfússon, Iceland; J. Buttimer, Ireland; G. Rennert, Israel; E. Paci, E.. Gentile, M Rosselli del Turco, Italy; N. Ohuchi, Japan; A. Scharpantgen, Luxembourg; M. Broeders, R. Holland, J. Hendricks, K. Siekman, J. Fracheboud, H. de Koning, The Netherlands; G. Skare, Norway; V. Rodrigues, Portugal; N. Ascunce, Spain; H. Malmquist, G. Svane, Sweden; S. Moss, J. Cooke, J. Patnick, United Kingdom; G. Pou, Uruguay; R. Ballard-Barbash, S. Taplin, B. Yankaskas, E. Hendrick, W. Barlow, USA. IBSN Quality Assurance Working Group members are: Rachel Ballard-Barbash (NCI, IBSN Chair), Françoise Bouchard (Canada), Mary Codd (Ireland), Andre Grivegnée (Belgium), Edward Hendrick (USA), Carrie Klabunde (NCI, Study Coordinator), Gonzalo Pou (Uruguay), Vitor Rodrigues (Portugal), Hélène Sancho-Garnier (France), Astrid Scharpantgen (Luxembourg), and Stephen Taplin (USA). The authors wish to thank Cindy Mattingly and James Cucinelli of Information Management Services, Inc. (Silver Spring, MD, USA) for expert assistance with questionnaire design and database programming. Funding for this study was provided by the NCI (Bethesda, MD, USA).

Footnotes

  • Address reprint requests to Carrie Klabunde, NCI/DCCPS/ARP, Health Services and Economics Branch, EPN Room 4005, 6130 Executive Boulevard, Bethesda, MD 20892-7344, USA. E-mail: ck97b{at}nih.gov

References

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