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W4246374977 abstract "CancerVolume 80, Issue 8 p. 1432-1437 Original ArticleFree Access Breast carcinoma stage in relation to time interval since last mammography† A registry-based study First published: 20 November 2000 https://doi.org/10.1002/(SICI)1097-0142(19971015)80:8<1432::AID-CNCR10>3.0.CO;2-6Citations: 4 † Presented in part at the Annual Meeting of the International Association of Cancer Registries, Rio de Janeiro, Brazil, October 30-November 1, 1995. AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Abstract BACKGROUND In the Romagna Region of Italy, mammography screening for breast carcinoma (BC) was implemented as a routine practice in the regular healthcare system. The Romagna Cancer Registry evaluated the effects of self-selection for mammography on the stage of BC at the time of presentation. METHODS Of the 851 invasive BC cases registered in 1989-1991, tumor size (T) was documented for 790 (93%) and lymph node status (N) for 681 (80%). Mammography experience was determined by cross-checks with the radiology files in the area. The Mantel-Haenszel chi-square test stratified by age was used to evaluate the difference in the proportion of advanced BC between subsets of patients diagnosed at increasing time intervals since their most recent mammography and those with no previous examination. RESULTS The incidence of T2+/N1+ (T2 or worse and/or lymph node positive) BC was 71% among patients without previous mammography. No advantage was observed for patients diagnosed within 6-12 months of their last mammography (69%). A marked advantage was associated with intervals varying between 12-23 months (45%; P < 0.001) and between 24-35 months (43%; P < 0.001). For longer intervals, the proportion of T2+/N1+ disease stabilized at 56%. For patients with any interval > 5 years (range, 5-22 years; median, 11 years) the relative stage advantage was significant (P = 0.013). CONCLUSIONS The stage pattern of patients diagnosed with BC 5-22 years after their last mammography suggests that even if health-aware women who volunteered for screening stop undergoing regular mammography, they present for a relatively prompt diagnosis in the event they develop BC. Cancer 1997; 80:1432-7. © 1997 American Cancer Society. According to current concepts, cancer registries should be actively and directly involved in strategies for cancer control.1 In particular, the adoption by a cancer registry of a central role in the evaluation of interventions against cancer at the population level is consonant with the basic functions of cancer registration.1, 2 Among the potential areas of application, mammography screening for breast carcinoma (BC) appears to be a priority. In many Western countries, mammography screening has been implemented as a routine practice in the regular healthcare system. Descriptive reports as well as analytic studies have considered the effects of routine mammography on the incidence of BC.3-9 However, these observations have provided only indirect information regarding the benefits and disadvantages of this practice.10 In particular, they have not focused on the adverse implications of the inevitable self-selection of women who are health-aware, educated, and motivated.11 This remains the outstanding adverse feature of routine mammography practice and needs to be addressed specifically.12 The current study was conducted by the cancer registry that covers the Romagna region of Italy (Romagna Cancer Registry [RTRO]). The authors examined mammography use as observed in the routine healthcare system and evaluated the effect of self-selection for mammography on the stage of disease at diagnosis in a series of incident BC cases. Background The determinants of self-selection for mammography have been the subject of several studies,13, 14 one of which was from the Romagna area.15 The major implications of self-selection are known. Women who volunteer for mammography screening are more likely to present promptly if they develop BC symptoms.11 The outcome for these women, even in the absence of mammography screening, is expected to be better than that of the general population.12, 16 In the evaluation of screening trials this prognostic selection bias is adjusted for. Its misleading effect on the impact of routine mammography use is uncontrolled.12 The trials of mammography screening consistently have shown an association between detection status and the stage of BC. The frequency of lesions > 2 cm in size,17, 18 of those with positive lymph nodes,16 and of those classified as Stage II (American Joint Committee on Cancer Staging System) or worse19 is low among the screen-detected patients and high among those who refuse mammography, with intermediate values among the interval cases. By contrast, the stage of BC in patients with irregular attendance (and, thus, long time intervals since their last mammogram) rarely has been addressed. The Utrecht screening project provided data on the T classification of BC cases diagnosed over a 8-year period among women who responded only to the first invitation.18 The proportion of T2+ cases (20% among screen-detected tumors) increased rapidly during the first 2 years since mammography (35-45%) and after 3 years equaled that observed in the nonresponse group (60%). Rationale and Objective In the current study, the frequency of advanced disease20 among the registered BC patients who had undergone at least one mammography prior to diagnosis was stratified based on the time interval since the most recent examination and was compared with that observed among individuals with no previous examination. The primary objective was to evaluate the advantage in stage distribution for the BC patients diagnosed at least 5 years after their most recent mammogram. In the absence of regularly repeated mammography, any stage advantage for this subset of patients compared with those with no previous examination was assumed to reflect their tendency to present promptly for diagnosis. The rationale was that the previous self-selection for mammography screening and a rapid self-referral for diagnosis both were related to proactive health behavior. The second goal of the current study was to evaluate the advantage associated with shorter intervals since the most recent mammography. MATERIALS AND METHODS Cases Methods, organization, and incidence data of the RTRO have been reported in detail elsewhere.21, 22 All cases (n = 851; mean and median age, 62 years; standard deviation, 13 years; range, 27-92 years) of invasive BC (International Classification of Diseases for Oncology [ICD-O] 174) registered in the female population (approximately 270,000) of the districts of Ravenna, Faenza, Lugo, and Forlì between 1989 and 1991 were considered. Patients with in situ carcinoma (n = 41) were not included in the study. The average annual age-standardized (world standard population) incidence rate of invasive BC was 64.8 per 100,000 women. Tumor Size and Lymph Node Status Details on the size of the primary tumor (T) and the lymph node status (N) of cases of BC reported to the RTRO routinely are collected but not computerized. The data on T and N for the 851 study cases were abstracted from the original histologic, clinical, and mammographic report sheets stored in the paper archives of the Registry. T and N data were classified retrospectively according to the American Joint Committee on Cancer staging system.23 T classification was documented for 790 cases (93%). For 712 of these (90%), the pathologic measurement was obtained. For the other 78 cases, the greater T classification was used, whether measured on physical examination (n = 59) or mammogram (n = 19). N was classified based only on the postsurgical data (pN) and was determined for 681 cases (80%). Among these, the number of the lymph nodes examined was available for 594 cases (87%). Only 5 cases (<1%) had <6 lymph nodes examined. The availability of the number of lymph nodes was the same for those BC patients with a previous mammography as for those without a previous mammography (87% for both groups). The (20%) 170 cases with unknown lymph node status were comprised of 146 patients who did not undergo axillary lymph node dissection and 24 patients with missing data. The authors grouped the study cases into three broad TN categories: T1N0 (tumor ≤ 2 cm in greatest dimension with no regional lymph node metastasis; n = 274 or 32%), T2+ and/or N1+ (tumor > 2 cm in greatest dimension and/or presence of regional lymph node metastasis, abbreviated as T2+/N1+ in the text; n = 477 or 56%), and unclassified (any other TN pattern as well as the death certificate only cases; n = 100 or 12%). Mammography Experience In the study area, the overwhelming majority of mammographies are performed in two general radiology departments and two breast clinics of the National Health Service. The two-view technique is systematically employed. In the study period, spontaneous attendance was considerable. As a rule, 2-year intervals between negative tests were advised. However, the actual frequency of repeat screening mammograms as well as the patient age at baseline examination were uncontrolled. In three of the four districts of the area, the authors conducted a telephone survey (district of Lugo) and two independent archive-based inquiries (districts of Ravenna and Forlì) and found that 37% of women age 40-49 years and 30% of those age 50-69 years had undergone a mammography over a 24-month period (unpublished data). For BC cases diagnosed in the 1980s, the Romagna region was characterized by a greater age-standardized 5-year relative survival rate (85%) than that observed in the other areas of Italy covered by cancer registration (range, 68%-78%).24 The names of all study cases were cross-checked with the files of each of these four institutions. For all BC cases identified, the date of all mammograms was recorded. The first relevant mammography dated back to 1968. Currently implemented in clinical settings, screening or preventive mammography was not recognized as a specific diagnostic area. Access modalities were the same as for the clinical mammography performed in the diagnostic work-up of symptomatic diseases. As a major correlate, the presence or absence of subjective symptoms were not systematically recorded, with the exception of incomplete and nonstandard notations. In contrast, information regarding the presence and the date of previous mammography was available for all study cases and was absolutely objective. Although mammograms taken during the 6 months prior to diagnosis could be either diagnostic (in response to symptoms) or screening mammograms, previous screening mammography was defined as any examination performed at least 6 months prior to the date of BC registration. The time interval since the most recent examination was classified according to the following categorization (in months): 6-11, 12-23, 24-35, 36-59, and 60+. Data Analysis The Mantel-Haenszel chi-square test stratified by age was used to assess the difference in the proportion of T2+, N1+, and T2+/N1+ lesions between BC cases without previous mammography (reference category) and those registered at increasing time intervals since the most recent mammography. Differences in the distribution by number of lymph nodes (those examined and those positive) were evaluated with the Wilcoxon rank sum test. P values < 0.05 were considered significant. RESULTS Table 1 addresses the frequency of cases classified as T2+ according to previous mammography experience. Such lesions accounted for 54% of patients with no previous mammography. In comparison with this reference category, no advantage in tumor size was observed among cases diagnosed within 1 year of the most recent examination. A significant advantage was associated with a 12-35-month interval. Cases diagnosed at least 5 years since last mammography showed a nonsignificantly lower proportion of T2+ tumors. Table 1. T Distribution by Pattern of Previous Screening Mammography Experience T2+ cases MX No. of mos since MX Total no. of cases No. of T1 cases No. % P valuea No 484 222 262 54 Referent Yes 6-11 39 18 21 54 NS 12-23 78 58 20 26 < 0.001 24-35 56 45 11 20 < 0.001 36-59 43 26 17 40 NS 60+ 90 51 39 43 NS Total 306 198 108 35 < 0.001 MX: previous mammography; NS: not significant. a P values are for the Mantel-Haenszel chi-square test stratified by age (10-year age groups). Table 2 shows the frequency of lymph node involvement (N1+) and the number of positive lymph nodes. The advantage associated with the presence of at least one previous mammography was less pronounced. The frequency of lymph node involvement was significantly lower only for cases diagnosed 12-23 months since the last mammogram. Similarly, there was an overall tendency toward a reduced number of positive lymph nodes but statistical significance was restricted to cases diagnosed 36-59 months since the previous mammogram. Table 2. N Distribution and Number of Positive Lymph Nodes by Pattern of Previous Screening Mammography Experience N1 + cases No. of positive lymph nodes MX No. of mos since MX Total no. of cases No. % P valuea Median (range) P valueb No 397 177 45 Ref 4 (1-24) Ref Yes 6-11 37 16 43 NS 5 (1-13) NS 12-23 73 25 34 0.047 3 (1-21) NS 24-35 53 18 34 NS 1 (1-22) NS 36-59 44 20 46 NS 2 (1-10) 0.026 60+ 77 29 38 NS 3 (1-10) NS Total 284 108 38 0.029 3 (1-22) 0.029 MX: previous mammography; NS: not significant; ref: referent. a Mantel-Haenszel chi-square test stratified by age (10-year age groups). b Wilcoxon rank sum test. Table 3 addresses the protective effect of previous mammography on the proportion of T2+/N1+ cases. The advantage was more evident for all subgroups with the exception of cases diagnosed within 1 year of the most recent mammogram. For the cases diagnosed between 12-35 months since the last mammography the decrease in the proportion of advanced lesions was significant. For longer intervals, the proportion increased but stabilized at a lower level (56%) than that observed in the reference category. For the selected subset of cases diagnosed at least 5 years since last mammogram (range, 5-22 years, median, 11 years) the advantage was found to be significant (P = 0.013). Table 3. TN Distribution by Pattern of Previous Screening Mammography Experience T2+/N1+ cases MX No. of mos since MX Total no. of cases No. of T1N0 cases No. % P valuea No 455 134 321 71 Referent Yes 6-11 39 12 27 69 NS 12-23 75 41 34 45 < 0.001 24-35 53 30 23 43 < 0.001 36-59 43 19 24 56 NS 60+ 86 38 48 56 0.013 Total 296 140 156 53 < 0.001 MX: previous mammography; NS: not significant. a P values are for the Mantel-Haenszel chi-square test stratified by age (10-year age groups). DISCUSSION The published analyses of the relationship between incidence trends and mammography utilization3-9 have suggested that the practice of routine screening mammography has major epidemiologic effects. However, it has been pointed out that only evidence concerning modes of BC detection demonstrates the relationship between incidence trends and mammography utilization.10 Although the current study is not a substitute for a formal evaluation of the impact of mammography on mortality, the authors showed that the combined evaluation of TN status and the mammography-to-diagnosis interval of incident BC cases can provide direct information regarding the effect of routine screening on a population basis. As a major limitation of the current data set, the lack of information regarding the clinical status at diagnosis (asymptomatic vs. symptomatic) made it impossible to distinguish the true screening mammograms from clinical mammograms among those performed in the 6 months before surgical treatment. The latter thus were excluded and the analysis was restricted to the time interval since the previous mammogram. The potential biases within each subgroup of cases need to be discussed specifically. The primary objective of the current study was to evaluate the stage pattern of patients diagnosed with BC > 5 years since their last mammogram. Although the nonsignificant advantage observed for T and N alone highlighted the limited power of the study, the authors found that such patients had a lower frequency of T2+/N1+ lesions compared with those who never volunteered for mammography screening. It should be remembered that the median interval since previous mammography was 11 years. This suggests that those cases were unlikely to be accounted for by a rescreening mammogram and that the stage advantage was related mainly to a rapid self-referral for clinical diagnosis. The current study's observations provide a population-based confirmation of the self-selection of health-aware women for screening, although indirectly.11-13, 16 Even in the event these women stop undergoing mammography, behavioral factors responsible for previous self-selection will lead them to present for a relatively prompt diagnosis if they develop BC.11 This observation was expected. It should be considered carefully that self-selection is the promoting factor (not merely a bias) for routine screening. The selective effect is inherently stronger among true self-referred women than those in high attendance centralized programs based on invitation. To the authors' knowledge, only a report from the Utrecht screening project18 addressed the stage distribution associated with irregular attendance, providing figures comparable to those presented here. That study included data on cases diagnosed over an 8-year period among women who responded only to the first invitation and failed to participate in subsequent screens. The frequency of T2+ cases was low (20%) for screen-detected tumors, increased rapidly (35-45%) for cases observed in the first 2 years since previous mammogram, and equaled that observed in the nonresponse group (60%) for cases diagnosed from the third year on. In Romagna, the relative advantage for BC patients who stopped undergoing regular mammography screening decreased at the third year but stabilized thereafter at a favorable level. The basic health awareness of self-selected screenees appears to be the only determinant of stage that can be assumed to be constant enough to account for the observed long term stability. As a second goal of the study, the authors assessed the stage distribution of cases diagnosed 12-36 months since the last mammography compared with those women with no previous mammography. The observed advantage was an approximate indicator of the relative benefit associated with periodic mammography screening of asymptomatic women in Romagna. Because the mammography experience and detection mode of cases were categorized based solely on the presence and date of the previous examination, two potential implications must be considered: 1) cases with no previous mammogram also could include a minority of small asymptomatic lesions detected at first examination, and 2) cases diagnosed 12-36 months since the last mammography also could include a minority of cases surfacing clinically. However, the majority of BC diagnoses made within that interval almost certainly were due to a rescreening mammogram. Moreover, it is worth noting that the combined effect of these potential biases (if any) was comprised of an underestimation of the relative protection associated with mammography as repeated at appropriate intervals. In the Swedish Two-County screening trial,17 the T2+ cases accounted for 22% of those detected on second and subsequent screens. In an age-comparable subset of cases from the current series the frequency of T2+ cases among those diagnosed 12-36 months after last mammogram was 23% (data not shown). BC cases registered 6-12 months after the last mammogram did not show any improvement compared with patients with no previous examination. Cases diagnosed within 6-12 months were probably accounted for by interval carcinomas (i.e., mammogram negative diseases with a high growth rate as well as cases with a false-negative mammography report). In fact, in most screening trials the interval cases showed a better stage distribution compared with patients who refused mammography.16-19 This suggests the presence in the 6-12 months group of a third subset of cases with a poor stage pattern (i.e., patients with a dubious mammogram who were recommended for a repeat examination within 6 months and were diagnosed after a longer [and unacceptable] delay). Incidentally, this raises the question of the adequacy of follow-up actions for a dubious mammogram. The lack of fail safe systems has caused follow-up failures for abnormal smears to became one of the most frequent inefficiencies in routine screening for cervical carcinoma.25 Such shortcomings also may occur in mammography practice. The current study pointed out some of the conflicting effects of routine mammography practice at the population level. Although patients who returned for periodic mammography screening at 12-36-month intervals showed a markedly lower frequency of advanced BC compared with patients who never volunteered for screening, it also was confirmed that health-aware women spontaneously undergoing mammography were at a lower risk of advanced stage BC, even in the absence of regular examinations. Whenever clinical radiology services are not in charge of evaluating the effects of mammography on a population basis, the cancer registry should take the responsibility of promoting the implementation of essential models for the surveillance of routine mammography use.1, 2 This study confirms that an active intervention of the registry in this important area of cancer control is feasible. Acknowledgements The Romagna Cancer Registry and Collaborators (members of analysis and writing committee indicated by*): Dino Amadori, M.D.,* Lauro Bucchi, M.D.,* Fabio Falcini, M.D.,* Oriana Nanni, S.D.,* Carlo Cordaro, B.D., Stefania Giorgetti, T.A., Marina Marchini, T.A., Carlo Milandri, M.D., Manuela Montanari, B.D., Silvia Salvatore, T.A., Monica Serafini, B.D., and Rosa Vattiato, T.A. (Romagna Cancer Registry, Medical Oncology Department, Luigi Pierantoni Hospital, Forlì, Italy); Ruggero Ridolfi, M.D., Patrizia Gentilini, M.D., and Donata Casadei Giunchi, M.D. (Medical Oncology Department, Luigi Pierantoni Hospital, Forlì, Italy); Luca Saragoni, M.D. (Pathology Department, Luigi Pierantoni Hospital, Forlì, Italy); Gianfranco Buzzi, M.D., Carlo Naldoni, M.D., and Patrizia Bravetti, M.D. (Center for Cancer Prevention, St. Maria delle Croci Hospital, Ravenna, Italy); Giuseppe Lanzanova, M.D. (Pathology Department, St. Maria delle Croci Hospital, Ravenna, Italy); Anselmo Piatesi, M.D. (Radiology Department, Umberto I Hospital, Lugo, Italy); Giorgio Cruciani, M.D. (Oncology Service, Umberto I Hospital, Lugo, Italy); Paolo Lorenzini, M.D. (Pathology Department, Umberto I Hospital, Lugo, Italy); Gian Enea Zarabini, M.D., (Radiology Department, Degli Infermi Hospital, Faenza, Italy); Giorgio Gambi, M.D., and Flavia Foglietta, M.D. (Oncology Service, Degli Infermi Hospital, Faenza, Italy); and Mirella Aldi, M.D. (Pathology Department, Degli Infermi Hospital, Faenza, Italy). 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Tumori 1997; 83: 39- 425. 25 Elwood JM, Cotton RE, Johnson J, Jones GM, Curnow J, Beaver MW. Are patients with abnormal cervical smears adequately managed? BMJ 1984; 289: 891- 4. Citing Literature Volume80, Issue815 October 1997Pages 1432-1437 ReferencesRelatedInformation" @default.
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