the positive predictive value of mammography
TRANSCRIPT
521
The Positive Predictive Value of Mammography
Perspective
Daniel B. Kopans1
Breast cancer is the leading cause of nonpreventable can-cer-associated death among women in the United States. Theprimary purpose of screening asymptomatic, healthy womenfor breast cancer is to diagnose it earlier and in so doingreduce the risk of or delay the onset of death from thisdisease. In addition, detecting cancers when the tumors aresmaller benefits many women by permitting the therapeuticoption of breast preservation.
The importance of mammographic screening is graduallybeing recognized in the United States, and over the pastseveral years, the number of women screened has increased.Mammography has clearly been shown to be quite sensitivein its ability to detect cancer, but frequently it cannot be usedto accurately differentiate benign from malignant lesions [11.Currently, open biopsy is the only accurate way to determinethe benign or malignant basis of a mammographic finding,although fine-needle aspiration cytology and core needle bi-opsy are being explored as alternatives. Preoperative local-ization of clinically occult abnormalities detected by mammog-raphy, followed by excisional biopsy, represents the goldstandard. Because of the lack of morphologic specificity,many biopsies done because of mammographic findings are
being performed for what prove to be benign lesions. In theUnited States, the positive predictive value (PPV) of mam-mography (the number of cancers diagnosed per number ofbiopsies recommended) has ranged from approximately 15%to 30% [2-7]; in the European trials, it ranged from 30% [8]to 75% [9]. Some of the reasons for such discrepancies havebeen discussed [1 0]. Nevertheless, as a consequence of thenumbers of biopsies that are now being done, and the antic-ipated increase in biopsies that are likely to accompany large-
scale screening, the PPV for mammography is under increas-ing scrutiny.
What Is an Appropriate Positive Predictive Value?
Although a biopsy is an extremely safe procedure, � rec-ommendation for a breast biopsy, with the implied possibilityof breast cancer, induces high anxiety in patients. The pro-cedure itself results in a loss of productivity during the surgicaland recuperative time, creates various degrees of surgicaltrauma and cosmetic alteration, and generates increasedcosts for the health care system. It is understandable, anddesirable, that attention be directed toward the reduction ofsurgical procedures for benign changes; however, arriving atan absolute figure for the appropriate PPV is difficult. It isperhaps somewhat ironic that surgeons are now among thecritics of the low PPV for mammographically detected lesions[1 1]. Historically, a low PPV for breast biopsies has long beentolerated. In the era before mammography, when the surgeonwas determining who should have biopsies, the PPV for thebiopsy of palpable lesions was as low as 1 1 % [1 2]. This wastolerated because the presence of a mass was tangibleevidence of possibly malignant disease. The psychologicalimpact of a biopsy done because of clinical findings is inher-ently different from the impact of a biopsy done because ofabnormal mammographic findings. The removal of a palpableabnormality that proves to be benign is not considered un-necessary surgery, because the patient and her physician canrelate directly to the problem. A mammographically detectedlesion, on the other hand, comes as a total surprise to the“healthy” woman and her physician. Its removal must be
Received May 3, 1991; accepted after revision October 14, 1991.
1 Department of Radiology, Massachusetts General Hospital, 32 Fruit St., Boston, MA 02114.
AJR 158:521-526, March 1992 0361-803X/92/1583-0521 0 American Roentgen Ray Society
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completely guided by the radiologist, and when the lesionproves to be benign, it is not unexpected that this would beconsidered “unnecessary” surgery. This qualitative differenceobscures thefact that performing a biopsy ofa palpable lesionis more likely to be unnecessary from a cancer perspective.It has been shown repeatedly that mammographically de-tected cancers are usually at an earlier stage than thosedetected by clinical examination [1 3-1 5]. This revelation notonly serves as a warning that superficial comparisons of PPVmay be misleading but also emphasizes that the appropriatePPv is not an absolute number. When the implications of abiopsy strategy are assessed, PPV cannot be taken out ofcontext but must be evaluated with an understanding of thepopulation in which it occurs. Ultimately, the appropriate PPVdepends on what society considers an acceptable false-negative rate. The decision to perform a biopsy or not followsa receiver operator curve. More cancers will be detected atthe cost of increased falsely positive interpretations. Ulti-mately, if a biopsy were done of everything that was notperfectly normal, the number of cancers diagnosed would bemaximized, but the number of women undergoing unneces-
sary biopsies would likely be unacceptable. Thus, thresholdsfor intervention are set, but no absolute biopsy rates existthat will be universally accepted.
Positive Predictive Value by Itself Can Be Misleading
The same PPV can be found in circumstances with totallydifferent survival implications. It is entirely possible for tworadiologists to interpret mammograms with the same PPV,but one can be affecting the death rate by finding smallcancers, and the other can be intervening when it is too lateto alter the course of the disease. The malignant:benign ratiois relatively meaningless if the threshold criteria used todetermine if a biopsy should be done and the characteristicsof the cancers found by using those criteria are not known.For example, assume that size is the only criterion used toprompt a biopsy, and one radiologist chooses to do biopsiesof lesions that are 1 cm in diameter, whereas another radiol-ogist chooses to wait until a lesion reaches 2 cm. Initially, thefirst radiologist will diagnose more cancers than the second,because both radiologists will be recommending biopsies ofthe 2-cm lesions, but the first radiologist will also be doingbiopsies of the smaller lesions. Once the first radiologist haseliminated the large cancers, he or she will be diagnosinglesions at the same rate (and PPV) as the second radiologist,but at an earlier time in the growth of the lesions (assuminga constant growth rate). Thus, despite the same PPV, thefirst radiologist will more likely have a much greater impacton mortal�ty than the second.
Factors That Influence the Positive Predictive Value
Sensitivity (the number of cancers detected by mammog-raphy divided by the true number of cancers in the populationbeing screened) and specificity (the number of women in thescreened population who do not have breast cancer whosemammograms are interpreted as negative divided by the
number of women who truly do not have breast cancer) givesome indication of the accuracy of a screening program, butthey are not sufficient by themselves. Sensitivity and specific-ity can be misleading, depending on how the “true” numberof cancers in the population is measured, and how the “truly”negative women are determined. One measure might countas “missed cancers” only those that are palpable at the timeof a normal mammogram. A more accurate number wouldinclude those cancers that are diagnosed within 1 year of anormal mammogram (interval cancers).
The significance of a specific PPV should be assessed inthe light of several other factors. Among these is the numberof cancers expected in the particular population beingscreened (prior probability); the percentage of the populationbeing screened for the first time (the prevalence of breastcancer will be higher than the incidence); the size, histologictype, grade, and stage (lymph node involvement) of the can-cers; which cancers are counted as interval lesions; and whatpercentage of the cancers are ductal carcinoma in situ.
Prior Probabillty of Cancer
The incidence of breast cancer increases with age. In anaverage population of women 40-49 years old, the expectedannual incidence is approximately one cancer per 1 000; in apopulation of women 60-70 years old, this rises to two tothree cancers per 1 000. It would be anticipated that the PPVof mammography is likely to be higher in an older populationjust on the basis of this prior probability. In our own recentseries of mammographically detected cancers at the Massa-chusetts General Hospital, the PPV for women age 50 andover was 47%, whereas it dropped to 24% for women under50. Similar results have been found at Mount Sinai Hospitalin New York [1 6]. A higher PPV might be anticipated if thepopulation contains women who are at a higher risk for otherreasons (such as those with a family history of breast cancer)in whom a greater number of cancers will develop each yearper 1 000 women. Understanding this frame of reference isimportant. For example, in a particular population, a PPV of50% may appear successful. If, however, this population hassix to seven cancers per 1 000 women per year, and only fourto five per 1 000 are being found, then the PPV of 50%suggests that the threshold for biopsy may be too high,because cancers are being missed. A lower PPV may bemore desirable if this results in more of the cancers beingdetected earlier.
Percentage of Women Being Screened for the First Time
The PPV is also affected by the percentage of the popula-tion being screened for the first time. Numerous normal andbenign structures may arouse concern when seen mammo-graphically. In the first year of screening, the radiologist isfrequently confronted with potential lesions. These may havebeen present for many years, but in the absence of previousstudies, their significance must be carefully considered, andbiopsy is recommended more frequently. When previous stud-ies are available, the stability of a finding can be assessed,
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and many biopsies can be avoided. Similarly, because thebreast’s appearance is fairly stable over time, a new change,which can be appreciated because of the availability of aprevious study, has a higher probability of being malignant.This phenomenon is reflected in the well-organized Europeantrials, in which the PPV in the first year of screening wassignificantly lower than in the population of women whoreturned for additional screening in subsequent years andthose mammograms could be compared with previous stud-ies.
Size and Stage of Disease
Size and stage of disease are perhaps the most importantfactors in assessing the PPV. Staging permits the comparisonof tumors by classifying them into groups that behave withsome similarity so that prognosis can be estimated and treat-ments chosen and assessed. Survival from breast cancer isdirectly linked to the stage of the cancer at the time ofdetection [1 7]. Women with stage I cancers have a betterthan 90% 5-year survival [1 8]. When axillary nodes are foundto contain tumor or the tumor is larger than 2 cm (stage II),the 5-year survival drops to less than 70%. The prognosis isuniformly poor if metastatic disease is found elsewhere in thebody at the time of diagnosis.
The randomized controlled trials of the Health InsurancePlan of New York [1 9] and the more recent Swedish two-county trial [20] confirmed the validity of survival information.Through the randomization process, and by using mortalityfrom breast cancer as the end point, these trials eliminatedthe effects of lead-time bias and length-bias sampling. Datafrom the Swedish study further revealed that the reduction inmortality associated with screening was due to the earlierstage of the breast cancers detected [21].
As might be expected with an artificial system, staging isimperfect and cannot be used to accurately group cancerswith similar potential. Tumors within the same stage can
behave quite differently. The size of the primary tumor is oneof the most important predictors of future problems. A long-term follow-up of women with stage I cancers diagnosed atSloan-Kettering in New York showed that even within stageI, tumors less than 1 cm in diameter had a more favorableprognosis than those between 1 and 2 cm in diameter [22].A recent study [23] of women whose axillary lymph nodeswere free of cancer also indicated the prognostic importanceof tumor size. In the Swedish trial, when the tumor was lessthan 1 cm in diameter, survival was independent of anotherimportant prognostic indicator, histologic grade (L. Taber,personal communication). Thus, although 1 cm is an artificialthreshold, the detection of invasive lesions smaller than thisseems to have important advantages. Such detection isachievable by mammography and is a reasonable screeninggoal. Among the nonpalpable, screen-detected breast can-cers found between 1978 and 1990 at the MassachusettsGeneral Hospital, 57% of the invasive lesions were less than1 cm in diameter (measured at pathologic examination). In-cluded among the criteria that should be used to assess thesignificance of PPV should be the size of the cancers detected
and, in particular, the percentage of invasive tumors 1 cm orless in diameter. In addition, the percentage of women withlymph nodes that contain cancer should be noted so that the
overall distribution of lesions by size and stage can be deter-
mined.
Interval Cancer Rate
The interval cancer rate, if available, is an important meas-ure of the success of threshold sensitivities. In the BreastCancer Detection Demonstration Project [24], the cancersthat were diagnosed between screenings amounted to almost20% of the total cancers diagnosed in the population. In theMalmo trial [25], interval cancers accounted for almost 30%of the total cancers diagnosed, suggesting a higher thresholdfor biopsy (and perhaps, in part, accounting for the failure inthat trial to, as yet, show a mortality benefit). A comparisonof interval cancer rates gives an indication of the success ofthresholds used for intervention-the higher the interval can-cer rate, the less successful the screen.
A figure that is difficult to obtain in many of the publisheddata is the number of cancers that were interpreted asprobably benign but that grew between screenings and wereultimately diagnosed. These are not counted as interval can-cers because they remained clinically occult despite theirgrowth. A thorough evaluation of biopsy thresholds and PPVshould include this category of clinically occult lesions, ofwhich a diagnosis could have been made sooner but wasdelayed. These should be distinguished from lesions that arevisible in retrospect but were not consciously excluded frombiopsy. In the former case, use of a more aggressive biopsystrategy would affect PPV; in the latter, it would have noaffect as the tumors were not seen to begin with, and,therefore, no opportunity was missed (only double readingcould influence the failure to perceive the lesion).
Percentage of Ductal Carcinoma In Situ
A great deal of controversy still exists about the importanceof ductal carcinoma in situ (DCIS) [26]. Many think that thisis a precursor of invasive breast cancer; others think that inmany women with DCIS, an invasive lesion will never develop.Calcifications are the most common indication of DCIS, but asubstantial overlap occurs between the morphologic charac-teristics of calcifications produced by benign and malignantprocesses. If biopsies are only undertaken when “classic”fine, linear, irregular calcifications of comedocarcinoma arepresent, the PPV will be high, but many other cancers maybe missed. As DCIS may take 1 0 or more years to becomeinvasive, the failure to diagnose these cancers will not beapparent for many years.
In an aggressive screening practice, a significant numberof DCIS cases will be found. In our own practice, as well asin that of Sickles and coworkers [27], 30% of cancers de-tected by mammographic screening are DCIS. Until the nat-ural history of DCIS is better known, we should include thesein the overall breast cancer statistics but classify the lesions
separately.
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Lobular carcinoma in situ is even less well understood, anduntil its true significance is better defined, it should also beclassified separately. Most investigators do not include thislesion in breast cancer statistics.
Improving the Positive Predictive Value
A great deal of anxiety is created by the suggestion of abreast abnormality. Reducing the number of “false alarms” isof primary importance in reducing psychological trauma forthe patient. Surgery also represents various degrees of phys-ical trauma because the surgical approach to these lesionsvaries considerably. Although a breast biopsy can be anextremely safe, outpatient procedure done under local anes-thesia, some patients and surgeons prefer general anes-
thesia, despite the attendant increased risk. In addition, theamount of surgery used and the resulting amount of physicaltrauma sustained by the individual varies widely. Althoughmost of these lesions can be satisfactorily removed in avolume of 5 cm3 or less [28], the reported average amount oftissue removed is more than 40 cm3 [29].
The economic consequences of a breast biopsy cannot be
ignored: the more women screened, the more biopsies rec-ommended. The costs of the needle localization and surgeryare significant. In Chicago in 1 987, the average cost for needlelocalization and open biopsy was $2200 [30]. These costsmust be factored into the overall cost of screening [31] andultimately judged in terms of the best use of health-caredollars.
We should not lose sight of the fact that early diagnosis isthe goal of screening and may save lives. We must alsorecognize the differences between the health care system’sinterests and the advantages and disadvantages for eachwoman as an individual [32]. As we begin to explore newways to reduce the number of open biopsies of benign lesions,we should not overlook the fact that a breast biopsy shouldbe among the safest of surgical procedures and that thestakes are quite high for the woman whose diagnosis may bedelayed by our attempts to reduce the number of procedures.Although physicians prefer to deny the influence of the pres-ent litigious climate, we also cannot overlook the legal con-sequences of a delayed diagnosis [33].
Efforts to improve the PPV should not be limited to mam-mographically detected lesions alone. The challenge shouldalso be to surgeons to develop better approaches to thepalpable breast lesion.
The American College of Radiology with support fromnumerous other societies and the Centers for Disease Controlhas developed reporting and data collection systems to beused by individual practices. It is hoped that both will beadopted by those who provide mammography services. Thereporting system will help standardize the often confusinganalysis of mammograms and, by requiring the radiologist toassign findings into one of five categories, reduce the ambig-uous reports that are prevalent. The data base is importantto help monitor the success of screening and to assist eachpractice in assessing the results of its own program. The PPVfor each practice must be judged in relation to the type of
cancers detected and their size, grade, and stage. Eachpractice should establish guidelines and track the results oftheir biopsy policies. The analysis of mammograms and theresultant recommendation should not be capricious, butshould be based on specific, defined criteria. Thresholds forintervention should be delineated and used consistently. Bymonitoring the results of mammography, specific criteria canbe assessed and thresholds adjusted.
How Will Positive Predictive Value Be Improved?
Experienced interpreters will help improve the PPV. Sickles[27] has shown in his practice that the most experiencedreader has the highest PPV. As more radiologists gain expe-rience, and if they follow up on their patients and learn fromthe results of biopsies, the level of accuracy will improve. Wemust become more sophisticated in our selection of lesionsthat require excision. By organizing our data, as has beendone by Moskowitz [34], it should be possible to developprobabilities for various lesions so that the patient and herphysician can make an informed decision. We, as radiologists,may be willing to follow up a “low-probability” lesion, but itshould be up to the patient to make that decision, and sheneeds the best estimates that we can provide. Women who
are asked to return repeatedly for short-interval follow-up paya psychological penalty because of uncertainty that is sus-tamed over many months. A woman should be offered theoption of certainty provided by a safe, accurate, and imme-diate excision should she so desire.
New techniques must be developed to reduce the traumaand expense needed to accurately determine the nature ofan abnormality. It is time that a modern approach be appliedto breast biopsy. Surgeons have, until recently, been uninter-
ested in rethinking the techniques involved in excising non-palpable breast lesions and have removed far more tissuethan was needed for most lesions. Little has been written in
the surgical literature about technical approaches to thesebiopsies. We can only surmise that the lack of discussionsamong surgeons is due in part to the belief that biopsy ofnonpalpable breast lesions is a fairly simple procedure, yetreports in the literature describing failure to remove lesions,complications from wire transection, excessive tissue re-moval, and complaints about needle positioning belie this. A
fairly common attitude among some surgeons is that a largeamount of tissue can be removed from the breast withoutbeing noticeable. Few surgeons have addressed the questionof how much tissue actually needs to be removed, and howthe amount can be minimized. There is no reason to removea large amount of tissue when a lesion is only marginallysuspicious.
Alternatives to open biopsy, such as fine-needle aspirationcytology and core needle biopsy, are now being explored.Although they should be encouraged, development of newapproaches that do not completely remove the lesion sufferfrom possible sampling error and could potentially result inunfortunate delay in diagnosis in some women. An alternativeis for surgeons and radiologists to develop new approachesto the breast biopsy to improve their techniques, minimize
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the trauma from an excisional procedure, and reduce the costof diagnosis. Complete excision eliminates any question ofsampling error. Improvements in open biopsy can be made.For example, the vagaries of needle localization and guideplacement followed by surgery can be avoided by excisingthe lesion under indirect visualization while the breast is heldin compression in a mammography unit. This could permit thecomplete excision of a lesion with minimum complexity andtrauma. An operating room and all the excess resourcescurrently mobilized would be unnecessary. The size of theincision could be reduced and the volume extracted mini-mized. Such a procedure could be done expeditiously, andby reducing the volume of tissue removed, recuperation wouldbe hastened. The cost of diagnosis would also be reduced.
Alternative approaches to excisional biopsy should be de-veloped. Improved case selection through morphologic analy-sis may reduce the number of benign biopsies. Lesions witha low probability of being malignant would be segregated intoa “probably benign” category and monitored by obtainingmammograms at fixed intervals. In a recent review of lesionsclassified in this fashion, Sickles [35] found that by using aperiodic follow-up instead of biopsy, 1 7 cancers among 3184lesions had a delayed diagnosis. As almost all were still early-stage lesions by the time of ultimate diagnosis, it appearsthat harm likely did not occur from this delay (although twowere stage II). However, the potential problems with thisapproach include the patient’s long period of anxiety, andpoor compliance during the period of careful monitoring mayresult in additional delay in diagnosis. In Sickles’s study, bythe end of the follow-up period, 35% of patients did not returnfor examination.
Fine-needle aspiration cytology and core needle biopsy,although still experimental in the United States, are promisingmethods for further reducing the need for unnecessary openbiopsies. Fine-needle aspiration cytology has had the greatestevaluation, and in some hands it appears to be very accurate[36-38]. It is, however, operator dependent and somewhatof an art. In addition, it requires a highly skilled cytopathologistto interpret the material. Sampling error is a distinct possibility,and because of the vagaries of the technique, each centershould independently establish the efficacy of the procedure[39]. Large-bore core biopsy is likely to become the procedureof choice [40]. Its high degree of mechanization will reducethe learning curve and make it a more transferable technology.The histologic material is more easily interpreted by generalpathologists, and significant complications have not yet beenreported. Sampling errors will likely occur, but delays indiagnosis can be reduced by using the morphologic appear-ance of the lesion on mammograms as well as the coresample [41]. By acting on the more suspicious findings asindicated by the two studies, ultimately, false-negatives canprobably be kept extremely low. Currently, the only negativeconcern that has been voiced has come from pathologists,who fear that given only sections of a lesion, and with theloss of cytologic features that are eliminated during the fixa-tion process, breast cancers may be overdiagnosed whencore biopsy is used. Further demonstration of the efficacy ofthese procedures in various settings is needed before eithercan replace open biopsy.
Other imaging technologies should also be studied. MRimaging holds some promise, and a recent positron emissiontomography study of breast cancer patients had encouragingresults [42].
Conclusions
The “appropriate” PPV for mammography cannot be de-fined in an absolute sense, and an “acceptable” rate willalways be subjective. The factors that contribute to PPV andthat should be included in any discussion of PPV are sum-marized in Table 1.
In order to reduce the cost of screening (human and eco-nomic), the number of cancers diagnosed per biopsy per-
formed should be maximized; but, ideally, this should not bedone at the expense of increased false-negative findings.Although breast cancer is a common malignant disease, itfortunately affects only a small percentage of women eachyear in the large population of women who will be screened.Each case is, therefore, increased in importance.
Several approaches for improving the PPV are available.An improved understanding of morphologic differences be-tween benign and malignant lesions may help reduce thenumber of biopsies of lesions that prove to be benign. Repet-itive screening should be encouraged. Stable findings seenon subsequent mammograms have a low probability of beingcancer.
Fine-needle aspiration and core biopsy should continue tobe explored. These less invasive procedures likely will ulti-mately reduce the number of open biopsies needed for diag-nosis.
The open biopsy itself should be reevaluated. Approachesthat have been used for large, palpable masses in the pastare inappropriate for biopsies that rely on imaging guidance.Any radiologist involved in guiding open biopsies knows thatthe skills of surgeons performing these procedures varywidely. Before accepting a new technique that might result inreduced accuracy and delayed diagnosis, we should try toimprove the gold-standard diagnostic technique of excisional
TABLE 1: Data Needed to Assess the Significance of PositivePredictive Value
Age distribution of the population being screened (other risk factorsshould be monitored if possible)
Number of cancers diagnosed per 1 000 womenSize distribution of the invasive cancers and the percentage less
than 1 cm in diameterHistologic type and grade of cancersPercentage with cancerous nodesInterval cancers (if possible)False-negative mammograms (if possible)
Not visibleSeen but interpreted as benign and followed up (delayed diag-
nosis)Visible in retrospect
Note-Ideally, the positive predictive value should be calculated separately
for women being screened for the first time and for those who have beenscreened before. These data should be tracked separatelyfor ductal carcinomain situ. Lobular carcinoma in situ also should be followed separately and notincluded among the cancer statistics.
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biopsy. Accurate needle localization should be required sothat tissue removal is minimized. New approaches to minimizethe inaccuracies of the open biopsy, such as performing itwith the breast held in the mammography unit, should beexplored. Tissue diagnosis should become a truly minor pro-cedure so that we can aggressively diagnose early cancers,distinguish benign from malignant lesions with greater car-tainty, minimize trauma, and reduce cost.
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