493

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Progress in Radiology

L 1
The Evolution of Mammography
Lawrence W. Bassett1 and Richard H. Gold

It was not until the early 1 950s that mammography began tance of comparing images of the right and left breasts by
to gain recognition as a useful diagnostic procedure. Even viewing them side by side. In i933, Lockwood [3] reviewed
then, most radiologists simply considered it a technical ordeal the then-current diagnostic criteria for mammography, and, in
and too specialized to add to their diagnostic procedures. In i938, Gershon-Cohen and Strickler [4] recognized that “a
the i 950s, surgeons and primary-care physicians were only comprehensive knowledge and familiarity of the roentgen
vaguely aware that it was possible to perform a radiographic appearance of the normal breast under all conditions of
examination of the breast. This article traces the evolution of growth and physiologic activity must be acquired by the
mammography through the scientific contributions of those roentgenologist before he can ever hope to make real prog-
who developed, investigated, and improved it, emphasizing ress in the development of the roentgen method of diagnosis
their trenchant articles that appeared in the American Journal in breast neoplasia.” They, therefore, published a report on
of Roentgenology (AJR) over the last 50 years. This retro- variations of the normal mammogram. Otherwise, the litera-
spective was undertaken to provide an understanding not ture of the 1 930s and 1 940s emphasized only the technical
only of the origins of state-of-the art mammography, but also difficulties and limitations of mammography; in fact, from i 938
of the challenges facing mammography then and now. to i 950 the sole mammography article in the AJR was a case
report of extensive posttrauma calcification [5].
In the i950s, Leborgne in Uruguay revitalized interest in
Pioneers In Mammography
mammography with the publication of a series of articles
In 1 9i 3, Salomon, a German surgeon, performed radio- reporting plain breast radiography and duct injection. He used
graphs of 3000 excised breasts, correlating radiographic, nonscreen film and a focus-to-film distance of 60 cm, 20-30
gross, and microscopic anatomy [i ]. Not only did Salomon kVp, 5 mAs for each centimeter of compressed breast thick-
show how highly infiltrating carcinoma could be radiologically ness. Leborgne relied primarily on the cephalocaudal view,
distinguished from circumscribed carcinoma, but he was also which he performed with the patient standing and with “slight
the first to recognize nonpalpable breast cancer on a radio- pressure with the cone on a small cotton pad placed between
graph of a specimen and to report the finding. the cone and the breast so that the least quantity of breast
In the United States, Stafford Warren pioneered the clinical tissue is interposed” (Fig. 2). A large cone was used for a
use of breast radiography when, in i 930, he reported a whole-breast image, and a smaller one was used for a second
stereoscopic technique for mammography (Fig. i). His article image of the area of interest [6]. Most importantly, Leborgne
[2] described and classified the appearances of normal reported the occurrence of carcinomatous microcalcifications
breasts, identifying fatty and glandular types, as well as that, he said, resembled “fine grains of salt”; he detected such
illustrating the changes of pregnancy, mastitis, and benign microcalcifications in about 30% of breast cancers. This sign
and malignant tumors. Warren also emphasized the impor- provided Leborgne an opportunity for detecting carcinomas

Both authors: iris Cantor Mammography Screening Clinic, University of California at Los Angeles School of Medicine, UCLA Department of Radiological
Sciences, UCLA Medical Center, Room B2-1 25, 10833 Le Conte Ave., Los Angeles, CA 90024. Address reprint requests to L. W. Bassett.
AJR 150:493-498, March 1988 036i -803X/88/i 503-0493 C American Roentgen :ay Society
 494 BASSETT AND GOLD AJR:150, March i988

Fig. 1.-1939 mammogram by Staf-

ford Warren. Moving grid diminished
scattered radiation. Technical factors
Included 50-60 kVp, 70 mA, 2’/2-sec
.-..

.‘ exposure,
screens,
dual par-speed
and
Films were viewed
lack
intensifying
of compression.
stereoscoplcally.
Normal examination. Courtesy of Staf-
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ford Warren.

.i

Fig. 2.-Leborgne’s positioning for

cephaiocaudal mammogram. Film lies
in opaque paper envelope under
breast. From Leborgne [6].

I 2

even in the densest breasts. Finally, he performed specimen reported excellent results in imaging the breasts of his first
radiography to localize the calcifications for correlative histo- 1 000 patients [1 i ]. This welcome news overcame the tech-
pathologic study. nical barriers to the widespread use of mammography and
During the 1 950s, Gershon-Cohen and his associates pub- led to the training of radiologists and technologists across the
lished extensively on the malignant and benign abnormalities United States in the performance and interpretation of mam-
that they had identified on mammograms [7-9]. Comparison mograms (Fig. 3A) [i 2]. In February i 965, a Standardization
of their mammographic findings with whole-breast histologic Conference on Mammography, sponsored by an Ad Hoc
sections (1) taught them to recognize the importance of Committee of the American College of Radiology (ACR),
characteristic mammographic findings of benign and malig- produced (1) an agreement on recommended techniques and
nant disease, some of which had been thought to have no dosages and (2) a reproducible technique for diagnostic-
significance, and (2) enabled them to establish reliable diag- quality examinations. The ACR took the leading role in mam-
nostic criteria for carcinoma. Parallel work in Europe, paflic- mography training through its establishment of a Mammog-
ularly in France by Gros and his coworkers, confirmed and raphy Committee chaired by Wendell Scott. With grant sup-
amplified these findings. port from the Cancer Control Branch of the United States
By 1960, however, mammography was employed by only Public Health Service, the committee developed unique teach-
a few radiologists, and dissemination of the method was ing aids and established teaching centers throughout the
hampered by lack of studies showing reliability and reproduc- United States, where interested radiologists and technologists
ibility. In order to aid radiologists hesitant to attempt mam- could spend i week undergoing practical training, with travel
mography, Gershon-Cohen reported on the technical aspects, and living expenses paid by the government [i 3].
emphasizing the importance of high-contrast, nonscreen The evolution of xeromammography provides an excellent
films, collimation, and compression [1 0]. To overcome the example of a successful collaboration between industry and
difficulty in obtaining adequate exposure of both the thinner medicine. The basic physical principles of producing electro-
peripheral and thicker juxtathoracic breast tissues, he rec- static images were known as early as i 777, when Lichtenberg
ommended the “simultaneous exposure of two non-screen made charged patterns visible with charged powder [1 4]. In
films, interposing a thin layer of aluminum 0.5 mm in thickness. 1903, Righi made the first radiograph, using powder devel-
The upper film then reveals good contrast of the thicker opment of an electrostatic image [i 5]. Carlson, in i 937,
portions of the breast and the film covered by the aluminum developed the basic principles of xerography that, in i 950,
foil reveals good contrast of the anterior portions....” evolved into the commercial production of the Xerox copier
The widespread adoption of mammography is primarily for the reproduction of documents [i 6]. In i 952, a study of
attributable to the work of Egan and his coworkers. In i 960, the medical potential of xeroradiography was undertaken by
Egan described a reproducible, high milliamperage-low kilo- Roach and Hilleboe [i 7]. In i 960, Gould et al. [i 8] reported
voltage technique that used industrial film (Fig. 3B), and he on the greater breast image detail that was possible with
 AJR:i50, March i988 EVOLUTION OF MAMMOGRAPHY 495

Radiographic Projections and

Technical Factors

&aniocaudod

(
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1d

Axillary

) I

Fig. 3.-Egan technique.

A, Radiographic projections and technical factors for performing mammog-
INDICATIONS FOR MAMMOGRAPHY
raphy were developed by Egan and taught to radiologists throughout the
united States during the 1960s. From “Mammography,” chart printed by
Eastman Kodak co., Radiography Markets Division, Rochester, NY 14650.
courtesy of Eastman Kodak.
B, Egan mediolateral mammogram showing large cyst. Technical factors -

included 28 kVp, 300 mA, 6-sec exposure, target-film distance 40 in., non-
screen industrial film, courtesy of Robert Egan. .#{149}

xeroradiography. Wolfe began his investigations of xeromam- of cancer” [1 9]. In a 1 962 article [20], Egan reported 53 cases
mography in i 966, using a primitive Xerox radiographic unit. of occult carcinoma identified in 2000 consecutive examina-
Through perseverance and numerous modifications of the tions. He defined an occult carcinoma as “one which remains
equipment, and with the cooperation of the Xerox Company, totally unsuspected following examination by the usual meth-
Wolfe was able to improve image quality and reliability to the ods used to diagnose breast cancer, including an examination
point that in i 97i, the Xerox System 125 became commer- of the breast by an experienced and competent physician. To
cially available. Thus, through advances in both film and qualify for this definition, no symptoms (vague pain, itching,
xeroradiographic applications, mammography was trans- or heaviness) nor signs (nipple discharge, change in breast
formed from an investigative procedure used only in a few contour, or nodules) should be present which would suggest
large institutions to a valuable clinical diagnostic examination a disease process within the organ.” Soon after, Martin et al.
available to all. [21] confirmed the potential of mammography to detect un-
suspected carcinoma in a private-practice setting. Gershon-
Cohen et al. [22]; and Levitan et al. [23] were among those
Mammography for Cancer Screening
who elaborated on the most frequently encountered mam-
In 1958, Kremens, in reporting his results in 1000 mam- mographic sign of nonpalpable breast cancer-microcalcifi-
mograms, included in his list of indications for mammography cations. In 1973, Strax et al. [24] reported the 5-year follow-
“a survey project among healthy women for early detection up results of the Health Insurance Plan of Greater New York
 496 BASSETT AND GOLD AJR:i50, March 1988
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Fig. 4.-Evolution of film mammography with dedicated units.

A, 1969 mammogram performed by Dr. Gros with nonscreen, industrial film, 0.7-mm (nominal) focal spot, molybdenum target at 35-cm source-image
distance, and technical factors of 28 kVp, 40 mA, 4 sec. Normal examination.
B, 1975 mammogram performed with Du Pont Lo-Dose I single-screen/singie-emulsion film combination, 0.7-mm (nominal) focal spot, molybdenum
target, 35-cm source-image distance, and technical factors of 28 kVp, 31 mA, 1 sec. Normal examination.
C, 1987 mediolateral oblique mammogram, performed with Kodak MinR rare-earth screen/OM-single-emulsion film combination, 0.3-mm molybdenum
target, 60-cm source-to-image distance, moving grid, and technical factors of 28 kVp with automatic exposure control, and extended (3-mm) film
processing. To ensure that deeper tissues are imaged, portion of pectoral muscle is included down to level of nipple. carcinoma in axiliary tail, near chest
wall.

randomized, controlled, breast cancer screening study. Com- vanced mammographic imaging. In 1972, the introduction of
pared with the mortality rate of the control group, the mortality a high-definition intensifying screen, held by a vacuum in
rate was reduced by one-third for women who were screened intimate contact with a single-emulsion film, revolutionized
by physical examination and mammography. film mammography (Fig. 46) [27]. The new film-screen com-
bination permitted rapid automatic processing, a shorter ex-
posure, a decrease in motion unsharpness, and a greatly
State of the Art
reduced dosage. Further advances in dedicated film-screen
Advances in technology through the years have ultimately mammography units included the capability to produce mag-
led to a striking improvement in image quality and a dramatic nified images and the use of grids to reduce scattered radia-
reduction in radiation dose. The first completely dedicated tion (Fig. 4C) [28-30].
mammography unit was developed by Gros in France in the Wolfe [31] and Martin [32] popularized xeromammography
middle 1960s (Fig. 4A) [25]. A molybdenum target (0.7-mm (Fig. 5A) through their publications and teaching programs.
focal spot) in place of tungsten heightened the contrast be- Recently, advances in xeromammography have been directed
tween parenchymal, fat, and calcific densities, while a built-in toward reducing surface exposure through the use of in-
compression device decreased scattered radiation and mo- creased aluminum filtration and negative-mode processing
tion artifacts and separated breast structures. According to (Fig. 5B) [33]. Xerox has just introduced a black-liquid-toner
Gershon-Cohen et al. [26], these features significantly ad- development process that provides improved image resolu-
 AJR:150, March i988 EVOLUTION OF MAMMOGRAPHY 497

L . “

1-

.. -
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--;,.. .-

-. 2

A B
Fig. 5.-Evolution of xeromammography.
Because of space limitations, these images were cropped in the editorial office, significantly decreasing the amount of breast tissue actually depicted
in the original images.
A, 1973 positive-mode xeromammogram, Xerox 125 processing system, powder toner, single phase, overhead 1.2-mm tungsten target, 0.5-mm
aluminum filtration, 76-cm source-image distance, and technical factors of 40 kVp and 300 mAs. carcinoma in upper hemisphere.
B, 1978 negative-mode xeromammogram, Xerox 125/6 processing system, powder toner, single phase, overhead 1.2-mm tungsten target, 2.5-mm
aluminum filtration, 80-cm source-image distance, and technical factors of 50 kVp and 200 mAs, Normal examination.
C, 1987 negative-mode xeromammogram, Xerox 175 processing system, black liquid toner, Xerox 120 dedicated unit (three phase), 0.3/0.6-mm
tungsten target, 2.6-mm aluminum filtration, 80-cm source-image distance, technical factors of 48 kvp and 75 mAs, and enhanced photoreceptor sensitivity.
carcinoma in lower hemisphere. courtesy of Xerox Corporation.

tion and broad area contrast, with a corresponding reduction palpable breast lesions [42-45]. Malleable, barbed-tip, self-
in exposure made possible through enhanced photoreceptor retaining wires are less likely to be displaced during mam-
sensitivity (Fig. 5C). mographic compression or at surgery. Special compression
Clinical investigations have failed to reveal a significant devices have been designed to guide needle placement [46],
difference in accuracy between film-screen mammography and researchers continue to develop useful variations in lo-
performed with dedicated equipment and xeromammography calization methods [47-48].
[34]. Although film-screen mammography currently requires In the late 1 970s, the future of breast cancer screening
less radiation than does xeromammography, developments with mammography seemed to be doomed because of public
in both techniques have been characterized by significant fears of radiation-induced carcinoma. However, recent im-
dose reduction compared with previous radiographic methods provements in the ability of mammography to detect early,
[35]. curable cancer, in conjunction with markedly lower radiation
Using state-of-the-art equipment, mammographers have doses, have enabled radiologists to show that the benefits of
learned to identify subtle, indirect signs of breast cancer in its mammography far outweigh the theoretical risks [49-50].
earliest stage, when there is a high likelihood for cure. In
addition to calcifications, these early signs include architec-
Underutilization of Mammography: Responding to the
tural distortion, a developing neodensity, parenchymal asym-
Challenge
metry between right and left breasts, and a unilateral focus
of one or several prominent ducts [36, 37]. Radiologists have In 1 955, Gershon-Cohen and Ingleby [51 ] lamented the
also developed guidelines for managing equivocal findings underutilization of mammography because “periodic roent-
[38]. genographic studies of [ostensibly] normal breasts could be
The detection of more nonpalpable cancers has resulted in is now usually done in patients who accidentally discover the
a need for better methods to locate these lesions before lesions.” Since that time, mammography has progressed to
surgery. In 1 966, Berger et al. [39] recommended preopera- used effectively to detect and care for carcinoma earlier than
tive localization by means of precise descriptions and carefully the point where it is now universally endorsed as the most
prepared diagrams. They also emphasized the importance of effective method for early breast cancer detection [521.
specimen radiography to ensure that the suspicious area was The challenges that face mammography in the future are
removed. Inserting a needle directly into the area of suspicion both difficult and fascinating. They include working toward
and leaving it in place to guide the surgeon proved to be a the ultimate goal of universal screening for all women, training
more accurate method for prebiopsy localization [40]. A dye, an adequate number of qualified personnel to perform and
sometimes mixed with a radiopaque contrast medium, can interpret the mammograms generated by universal screening,
also be injected through the properly placed needle in or near and, finally, further defining the tenuous line that separates
the nonpalpable lesion [41]. More recently, needle/wire mammographically discovered lesions that require biopsy
systems have been developed especially for localizing non- from those that do not.
 498 BASSETT AND GOLD AJR:i50, March 1988

ACKNOWLEDGMENTS Med 1964;92:29-39

24. Strax P. Venet L, Shapiro S. Value of mammography in reduction of
The authors are grateful for the efforts of Jean Chaintreuil and mortality from breast cancer in mass screening. Am J Roontgonol Thor
Dianne A. Lavellee (both of Thomson CGR MediCal Corporation, Radium Nucl Med 1973;1 17:686-689
Columbia, MD) and for the help of Ellen M. Proctor and Paul M. 25. Gros M. Methodologie. J Radiol Eloctrol Med NucI 1967;48:638-655
26. Gershon-Cohen J, Hermel MB, Birsner JW. Advances in mammographic
Chenderlin (both of Xerox Medical Systems, Pasadena, CA).
technique. Am J Roontgonol Radium Thor Nucl Med 1970;108:424-427
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27. Weiss JP, Wayrynen RE. imaging system for low-dose mammography. J
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