Education

Preventive health care, 1999 update: 3. Follow-up after breast cancer

Larissa K.F. Temple, Elaine E.L. Wang, Robin S. McLeod and With the Canadian Task Force on Preventive Health Care
CMAJ October 19, 1999 161 (8) 1001-1008;

Abstract

Objective: To make recommendations to physicians who provide follow-up care for women who have been treated for early-stage breast cancer.

Options: Combination of blood tests, bone scans, liver echography and chest radiography for detection of distant disease; physical examination with or without mammography for detection of contralateral breast cancer; and physical examination with or without mammography for detection of ipsilateral recurrent disease after breast-conserving therapy.

Outcomes: Survival, disease recurrence and quality-of-life measures for distant disease, local recurrence of disease and disease in the contralateral breast.

Evidence: A MEDLINE search for relevant articles published between January 1966 and January 1998 with the MeSH terms "breast neoplasms" and "neoplasm recurrence" (local and distant) with limits to "human" was done. A subsequent MEDLINE search using the MeSH terms "breast neoplasms," "neoplasm recurrence," "local/diagnosis" and "mammography" was done to address issues of mammography. The literature search was reviewed by a medical librarian and 2 breast cancer specialists to ensure completeness.

Benefits, harms and costs: Breast cancer is the most common cancer in Canadian women and is the second leading cause of death after lung cancer. Even with early-stage breast cancer, recurrence after treatment for primary breast cancer is frequent. Traditionally, follow-up has been felt to facilitate early detection and improve survival. Randomized controlled trials (RCTs) have shown that routine screening (blood tests and diagnostic imaging) for distant disease does not alter survival or quality of life over routine physical examination. In an underpowered secondary analysis of RCT data, the detection of contralateral breast cancer did not affect survival. However, there have been no RCTs examining the role of mammography and physical examination and their effect on survival in the detection of contralateral breast cancer. The sensitivity and specificity of mammography after local excision and radiotherapy is unknown. There have been no RCTs examining the role of mammography or physical examination, or both, and their effect on survival in the detection of ipsilateral breast recurrence.

Values: The strength of evidence was evaluated using the methods of the Canadian Task Force on Preventive Health Care. A high value was placed on interventions that changed survival. When evidence was available, high value was also placed on interventions that affected quality of life.

Recommendations: There is good evidence not to include blood work and diagnostic imaging as part of screening for distant disease (grade E recommendation). There is no evidence to suggest that mammography decreases mortality by detecting ipsilateral disease in the conservatively treated breast; however, there is indirect evidence that it may be beneficial (grade C recommendation). There is no direct evidence to suggest that physical examination or mammography, or both, should be used to detect contralateral breast cancer; however, there is indirect evidence that it may be beneficial (grade C recommendation).

Validation: The findings of this analysis were reviewed through an iterative process by the members of the Canadian Task Force on Preventive Health Care.

Sponsors: The Canadian Task Force on Preventive Health Care is funded through a partnership between the Provincial and Territorial Ministries of Health and Health Canada.

Despite earlier detection of breast cancer and changes in breast cancer therapy, recurrence continues to be a problem. The disease recurs even in women with early disease (stage I disease [T1 (<2 cm), N0, M0] or stage II disease [T1, N1, M0; T2 (2-5 cm), N0/N1, M0; or T3 (>5 cm), N0, M0]) (recurrence rate 30%).1 The rate of local recurrence after breast-conserving therapy (local excision and radiation) has been reported in randomized controlled trials (RCTs) to be 6% to 12% at 5 to 10 years.[2–7] Women continue to be at risk for local recurrence for 20 years, and an ipsilateral recurrence develops in 1% to 2% of women every year.[8, 9] With mastectomy, local recurrence is less frequent (4%), but distant disease is more frequent.10 Regardless of local therapy (mastectomy or local excision and radiation), metastatic disease develops in 23% of women with stage I and II breast cancer.[11, 12] In addition to recurrent disease, women who have had breast cancer are at risk for cancer in the contralateral breast. After the first breast cancer, the risk of a new primary breast cancer is 3 to 5 times the risk of a first breast cancer.[13, 14] Large case series have shown a cumulative risk of contralateral breast cancer of 6% to 8%.[15–18]

There is significant variation in both patient expectations and physician practice patterns in the follow-up of women with breast cancer. Early data from a British RCT suggest that women prefer less frequent follow-up,19 whereas data from a US survey suggest that women want very extensive investigations.20 On the one hand, a recent US survey showed that the majority of oncologists would perform blood tests every 3 to 6 months (58%), annual chest radiography (52.1%) and annual mammography (95.9%).21 On the other hand, two UK surveys revealed that few breast cancer specialists (10% to 12%) would order blood tests, chest radiography or bone scans.[22, 23] In this guideline, the role of follow-up in improving survival and quality of life after breast cancer is evaluated to establish evidence-based guidelines.

Methods

Before performing a literature search, we developed the following inclusion criteria: women must have had stage I to III infiltrating ductal adenocarcinoma of the breast; there was no clinical evidence of distant disease at the time of diagnosis; when appropriate, adjuvant therapy, if received, was described; and the women were followed up for at least 5 years.

On consultation with a medical librarian, we performed a MEDLINE search of the English-language literature from January 1966 to January 1998 combining the MeSH headings "breast neoplasms" and "neoplasm recurrence" (local and distant), with limits to "human." To determine the sensitivity of mammography after local excision, we performed a MEDLINE search from 1966 to 1998 combining the MeSH headings "breast neoplasms," "neoplasm recurrence," "local/diagnosis" and "mammography." Reference lists of retrieved articles were reviewed. Two breast cancer specialists were then consulted to ensure the completeness of the literature search.

The evidence was reviewed systematically using the method of the Canadian Task Force on Preventive Health Care (formerly the Canadian Task Force on the Periodic Health Examination).24 The task force of expert clinician/methodologists from a variety of medical specialties used a standardized evidence-based method for evaluating the effectiveness of this intervention (Appendix 1). Procedures to achieve adequate documentation, consistency, comprehensiveness, objectivity and adherence to the task force method were maintained at all stages during review development, the consensus process and beyond.

Manoeuvres

Distant disease

Follow-up for distant disease has included physical examination, blood tests (complete blood count, liver function tests, and determination of calcium and creatinine levels)[25, 26] and diagnostic imaging (chest roentgenography, bone scan and liver ultrasonography).[11, 25, 26]

Local recurrence

There is no method to detect occult local recurrence in a woman after mastectomy. Therefore, local recurrence is detected by physical examination and consists of abnormalities in the incision site or the surrounding skin.

After breast-conserving treatment, local recurrence may be detected by physical examination or mammography, or both. Following surgery and radiation, there are significant changes in the sensitivity and specificity of mammography and physical examination, which have been reported only in case-control and cohort studies (Table 1). Although these studies are plagued with small and highly selected samples, it is evident that 35% to 64% of women who have biopsy of the conserved breast are found to have benign disease, and recurrence is often missed on mammography (25% to 50%) or physical examination (25% to 42%).[27–35] There are no prospective studies addressing the sensitivity and specificity of mammography or physical examination, or both, for the ipsilateral conserved breast.

View this table:

Table 1: Reported sensitivity and specificity of mammography and physical examination for detecting local recurrence of breast cancer

Contralateral breast cancer

The screening characteristics of physical examination with or without mammography have been examined only in the Canadian National Breast Screening Study, in which women aged 50 to 59 years without breast cancer were randomly assigned to yearly physical examination or to yearly physical examination and mammography.[36, 37] The sensitivity and specificity of physical examination were 75% to 100% and 75% to 85% respectively.38 The corresponding values for mammography and physical examination were 81% to 88% and 96.5% to 99.9%.37

Effectiveness of detection and treatment

Distant disease

The role of follow-up in detecting distant disease has been studied in a secondary analysis of 5 RCTs and in 2 RCTs (Table 2).

View this table:

Table 2: Data from randomized controlled trials examining the role of follow-up in the detection of distant disease

Survival

Crivellari and colleagues25 found that among 241 744 blood tests, 6% of the 52% of women with recurrent disease had an elevated alkaline phosphatase level at some point before the metastasis was detected. In the GIVIO RCT, the investigators compared the outcome of women with stage I or II breast cancer who had intensive or conservative clinical follow-up and found that intensive follow-up did not improve the overall survival of the women with recurrent disease (death rate 18% with conservative follow-up and 20% with intensive follow-up).26

Rosselli Del Turco and associates11 compared the 5-year survival rates for women randomly assigned to intensive versus conservative follow-up and found that, although relapse-free survival was shorter in the intensive follow-up group, there was no significant difference in the 5-year death rate between the 2 groups (18.6% v. 19.5%). Interestingly, some women without metastatic symptoms after breast cancer surgery who were assigned to conservative follow-up had diagnostic tests; however, the number of tests in this group (444) was significantly smaller than the number in the intensive follow-up group (8060).

The GIVIO investigators, using a similar protocol, compared the overall survival of 1220 women with stage I to III breast cancer who received intensive follow-up of physical examination, mammography and diagnostic imaging.26 Asymptomatic metastases were identified in 31% of the patients in the intensive follow-up group and in 21% of those in the conservative follow-up group. There was a difference of 1 month in the detection of distant metastasis between the 2 groups, and there was no difference in overall survival or length of survival between the 2 groups.

Quality of life

As a component of the GIVIO trial, the quality of life in the intensive and conservative follow-up groups was compared.26 The health-related quality-of-life assessment was found to have good psychometric properties, and no difference was found in quality of life at 6, 12, 24 or 60 months between the 2 groups. Thus, although there were no negative consequences of screening, the evidence does not suggest that intensive follow-up improves quality of life.

Local recurrence

The survival of women with a local recurrence following local excision has been examined carefully in RCTs (Table 3). In all RCTs, follow-up for the detection of ipsilateral disease has included frequent physical examination and mammography. In this context, despite higher rates of local recurrence, no differences have been found in the survival of women with stage I or II breast cancer treated with either mastectomy or local excision and radiotherapy after 6 and 12 years of follow-up.[2, 7] Although associated with higher local recurrence rates, local excision without radiotherapy has not been shown to increase death rates in 5 RCTs with 5 to 12 years of close follow-up for local recurrence.[2–6] One cohort study has also shown no differences in survival between women who do and those who do not manifest local recurrences after 5 and 10 years.39 In addition, a meta-analysis using individual data for 9709 patients from 10 RCTs comparing various surgical therapies with or without radiotherapy showed that, despite higher local recurrence rates with local excision, overall survival was not affected.40 In summary, local recurrence, if managed appropriately, does not appear to affect overall survival.

View this table:

Table 3: RCTs with level I evidence examining local recurrence and survival after breast-conserving surgery

Because survival does not appear to be affected by local recurrence after breast-conserving therapy in a research setting, it becomes important to evaluate the methods used to detect local recurrence. Although follow-up in the 5 RCTs comparing various surgical treatments with or without radiotherapy was almost complete (0.1% to 1% of subjects lost to follow-up), the follow-up protocol was documented clearly in only 3 of the trials.[3, 4, 12] In these studies, follow-up consisted of frequent physical examination and yearly mammography. No investigators reported the rates of detection with mammography or physical examination, or both, by the physician separately, the stage of lesions detected by the 2 methods, or the differences in surgical therapy or survival based on the 2 methods. Many retrospective series showed that women (76% to 86%) identify their own local recurrences.[8, 13]

Two groups examined retrospectively the stage of the recurrence and method of detection. Abner and collaborators9 analysed a cohort of 1628 women treated for breast cancer between 1967 and 1985. Although the rates of compliance and loss to follow-up are unknown, the authors identified 163 women with ipsilateral recurrence. Histopathological study of 123 mastectomy specimens showed that 99 had invasive, 10 had microinvasive and 14 had noninvasive disease. The 5-year survival rate was significantly higher with noninvasive (including microinvasive) disease than with invasive disease. Although more noninvasive lesions were detected by mammography, as compared with physical examination, there was no significant difference in survival between women with palpable recurrences and those with unpalpable recurrences. Orel and coworkers32 analysed a cohort of 1636 women treated for stage I or II breast cancer and identified 83 women with local recurrence. Physical examination and mammographic information for 72 women showed that 47% had unpalpable lesions. The unpalpable lesions were statistically more likely to be an earlier stage than were the palpable lesions. However, there were no significant differences in the histologic grade of recurrence or the 5-year survival rate between women with palpable lesions and those with unpalpable lesions. Thus, despite some evidence to suggest that mammography detects earlier lesions or those with a more favourable prognosis, these studies do not show any improvement in the survival of women with lesions detected on mammography versus those detected by other means.

There is evidence suggesting that local recurrence can be cured. However, the effect of early detection is unknown. The studies examining the prognostic implications of detection method and stage of detection were retrospective and are subject to both lead and length time biases. The numbers lost to follow-up, referral biases and exclusion criteria were not described.

Contralateral breast cancer

Although screening for primary breast cancer has improved survival,[41–43] one cannot conclude that early detection of contralateral breast cancer will have the same effect. Early detection of contralateral breast cancer has never been the subject of an RCT (Table 4).

View this table:

Table 4: Results from studies examining contralateral (CL) breast cancer

The effect of contralateral breast cancer on survival has been described in a secondary analysis of the National Surgical Adjuvant Breast Project Protocol No. 04, in which the survival of women after either a radical or modified radical mastectomy with or without radiotherapy for stage I or II breast cancer was compared.[10, 46] In a secondary analysis, Fisher and colleagues47 reported on the incidence and survival of women in whom contralateral breast cancer developed. In the project, follow-up of all women, regardless of randomization, included frequent physical examination of the contralateral breast. Of the 1578 women, 4.2% manifested a contralateral breast cancer at 10 years. The metachronous contralateral cancers were smaller than the primary breast cancer (2.4 cm [standard deviation 1.5 cm] v. 3.5 cm [standard deviation 1.8 cm]). Although the possibility of a type II error exists, there was no difference in survival between the women with and those without contralateral breast cancer after 10 years of follow-up.

The role of mammography in the detection of contralateral breast cancer in women who have been previously treated for breast cancer has been examined in 3 retrospective studies. Two studies looked at the frequency of contralateral breast cancer in cohorts of women treated for breast cancer before and after the implementation of mammography for routine follow-up.[44, 45] An increased incidence of both synchronous and metachronous contralateral breast cancer was found after the routine use of mammography. In the third study a cohort of women in a county where both physical examination and mammography were performed was compared with a cohort of women in a county where only physical examination was performed.14 Although the frequency of contralateral breast cancer was identical in the 2 counties, more recurrences were stage I in the women from the county where screening included mammography. All 3 studies contain many methodologic flaws, and the authors did not report the survival rates for women followed before and after the routine use of mammography.

Recommendations

Of the Canadian Task Force on Preventive Health Care (Table 5)

View this table:

Table 5: Recommendations of the Canadian Task Force on Preventive Health Care

  • There is good evidence from well-designed RCTs that there is no difference in survival or quality of life with laboratory or diagnostic screening as compared with physical examination for distant disease.[11, 26] Therefore, laboratory or diagnostic screening, or screening with both methods, for distant disease is not indicated (grade E recommendation).

  • Ipsilateral recurrence after breast-conserving therapy was not shown to affect survival in RCTs comparing various surgical and radiotherapy treatments in which follow-up included frequent physical examination and mammography of all women (level I).[2–7] However, the unique role of early detection in the ipsilateral breast by physical examination and mammography is unknown (grade C recommendation).

  • There is some evidence (level II-3[44, 45] and level II-214) that mammography of the contralateral breast identifies second primary cancers at an earlier stage than does physical examination. However, in an underpowered secondary analysis of an RCT comparing radical mastectomy with modified mastectomy and radiation, contralateral breast cancer, when detected by physical examination, was not shown to affect survival at 10 years (level II-2).47 Screening with yearly mammography and physical examination has been included in the protocols of RCTs and is recommended by experts (level III). Although there is indirect evidence suggesting that there may be a clinical benefit, there is no direct evidence to support the inclusion or exclusion of the manoeuvre in the follow-up of women with breast cancer (grade C recommendation).

Of other bodies

There are no other evidence-based guidelines for appropriate follow-up after breast cancer. Under the auspices of the Italian Ministry of Health and the Italian Research Council, an Italian group of stakeholders met in 1994 and recommended that yearly mammography and physical examination every 3 months be done for the first 2 years, yearly mammography and physical examination every 6 months be done for the next 3 years, and yearly mammography and physical examination be done thereafter.48 Within Canada, a consensus document recommended frequent physical examination and yearly mammography,49 although the authors acknowledged that their recommendations were extrapolated from findings in the general population. Thus, the proposed guidelines differ with respect to the strength of recommendations concerning the role of mammography and physical examination in the follow-up of local recurrence and contralateral breast cancer.

The recommendations for screening with mammography in the general population50 cannot be extrapolated to women who have had breast cancer because all RCTs examining screening have excluded women with previous breast cancer. Although large RCTs[2–5] and a meta-analysis of 16 000 women40 have not shown an increase in death rates with local recurrence, frequent follow-up of the ipsilateral breast and contralateral breast have been part of the follow-up protocol. In addition, although inadequately studied, contralateral breast cancer has not been shown to affect survival. Therefore, although frequent physical examination and mammography have been used in the protocols of RCTs and is recommended by experts, there is no direct evidence to illustrate that early detection of local recurrence or contralateral breast cancer, or both, improves survival in women after breast cancer.

Research agenda

Although new therapies are studied extensively with RCTs, follow-up has not been subjected to the same rigourous examination. As we become more sophisticated in designing RCTs and as therapy for local recurrence evolves, other outcomes may be important in assessing the effectiveness of physical examination with or without mammography. Recurrences detected on mammography may be more amenable to local therapy than those detected by physical examination. Defining the role of follow-up in improving survival will increase our understanding of breast cancer. In addition, evaluating the effect of follow-up on quality of life is an important aspect of health care delivery to women that requires further research.

The Canadian Task Force on Preventive Health Care thanks Dr. Anthony Miller, Faculty of Medicine, University of Toronto, and Dr. Suzanne Fletcher, Harvard Medical School, Boston, for reviewing a draft form of this report. The views expressed in this report are those of the authors and the task force and do not necessarily reflect the positions of reviewers.

Competing interests: None declared.

Appendix 1: Canadian Task Force on Preventive Health Care levels of evidence and grades of recommendations

Levels of evidence

  • I Evidence from at least one well-designed randomized controlled trial

  • II-1 Evidence from well-designed controlled trials without randomization

  • II-2 Evidence from well-designed cohort or case-control analytic studies, preferably from more than one centre or research group

  • II-3 Evidence from comparisons between times or places with or without the intervention; dramatic results from uncontrolled studies could be included here

  • III Opinions of respected authorities, based on clinical experience; descriptive studies or reports of expert committees

Grades of recommendations

  • Good evidence to support the recommendation that the condition or manoeuvre be specifically considered in a periodic health examination (PHE)

  • Fair evidence to support the recommendation that the condition or manoeuvre be specifically considered in a PHE

  • Insufficient evidence regarding inclusion or exclusion of the condition or manoeuvre in a PHE, but recommendations may be made on other grounds

  • Fair evidence to support the recommendation that the condition be specifically excluded from a PHE

  • Good evidence to support the recommendation that the condition or manoeuvre be specifically excluded from a PHE

    • Footnotes

    • *The list of task force members appears at the end of the article.

      This article has been peer reviewed.

      Reprint requests to: Canadian Task Force on Preventive Health Care, Parkwood Hospital, 801 Commissioners Rd. E, London ON N6C 5J1; ctf@ctfphc.org

      Members of the Canadian Task Force on Preventive Health Care Chairman: Dr. John W. Feightner, Professor, Department of Family Medicine, University of Western Ontario, London, Ont. Past chairman: Dr. Richard Goldbloom, Professor, Department of Pediatrics, Dalhousie University, Halifax, NS. Members: Drs. R. Wayne Elford, Professor and Chair of Research, Department of Family Medicine, University of Calgary, Calgary, Alta.; Michel Labrecque, Associate Professor and Director of Research, Department of Family Medicine and Centre hospitalier universitaire de Québec, Laval University, Sainte-Foy, Que.; Robin S. McLeod, Professor, Department of Surgery, Mount Sinai Hospital and University of Toronto, Toronto; Harriet MacMillan, Associate Professor, Departments of Psychiatry and Pediatrics and Centre for Studies of Children at Risk, McMaster University, Hamilton, Ont.; Jean-Marie Moutquin, Professor, Department of Obstetrics and Gynecology and Saint-François d'Assise Research Centre, Laval University, Sainte-Foy, Que.; Christopher Patterson, Professor and Head, Division of Geriatric Medicine, Department of Medicine, McMaster University, Hamilton, Ont.; and Elaine E.L. Wang, Associate Professor, Departments of Pediatrics and Public Health Sciences, Faculty of Medicine, University of Toronto, Toronto. Resource people: Nadine Wathen, Coordinator, and Tim Pauley, Research Assistant, Canadian Task Force on Preventive Health Care, Department of Family Medicine, University of Western Ontario, London, Ont.

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    Preventive health care, 1999 update: 3. Follow-up after breast cancer
    Larissa K.F. Temple, Elaine E.L. Wang, Robin S. McLeod, With the Canadian Task Force on Preventive Health Care
    CMAJ Oct 1999, 161 (8) 1001-1008;
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