IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-24, NO.

4, JULY 1977

347

[51 Tanaka, E., linuma, T. A., "Approaches to Optimal Data Process-

ing in Radioisotope Imaging," Phys. Med. Biol., 15 :603-694, 1970. [6] Knowles, L. G., Kohlenstein, L. C., Schulz, A. G., "Observer Performance as a Measure of 'Goodness' in the Evaluation of Scintigraphic Image Processing," Information Processing in Scintigraphy, U. S. Energy Research and Development Administration, Technical Information Center, Conf.-730687, pp. 15 3-158, 1973. [7] Kuhl, D. E., Sanders, T. D., Edwards, R. Q., and Makler, P. T., "Failure to Improve Observer Performance with Scan Smoothing,"J. Nucl. Med., 13:752-757, 1972. [81 Metz, C. E., Goodenough, D. J., "Failure to Improve Observer Performance with Smoothing: A Rebuttal," J. Nucl. Med.,

[11] Varoutas, P., Nardizzi,

[12]

[131 [141
[15]

[9] Kirch, D. L., Brown, D. W., "Nonlinear Frequency Domain Techniques for Enhancement of Radionuclide Images," Information Processing in Scintigraphy, U. S. Energy Research and Development Administration, Technical Information Center, Conf.730687, 102-114, 1973. [10] Moore, D. J. H. and Parker, D. J., "On Nonlinear Filters Involving Transformation of the Time Variable," IEEE Trans. Information Theory (July 1973), Vol. IT-19, No. 4, pp. 415-422.

14:873-876, 1973.

[161
[17]

[18]

L. and Stokely, E., "Nonlinear Filtering and Boundary Detection for Digital Image Processing," 28th ACEMB, New Orleans, Louisiana, September 1975. Andrews, H. C., "Entropy Considerations in the Frequency Domain," Proceedings of the IEEE, January 1968, pp. 113-114. Golay, M. J. E., "Hexagonal Parallel Pattern Transformations," IEEE Trans. on Computers (August 1969), Vol. C-18, No. 8, pp. 7 33-740. King, R. E., "Digital Image Processing in Radioisotope Scanning," IEEE Transactions on Biomedical Engineering (September 1974), Vol. BME-21, No. 5, pp. 414-416. DeBoor, C., "Bicubic Spline Interpolation," Journal of Mathematics and Physics, Vol. 41, pp. 212-218, 1962. Roberts, L. G., "Machine Perception of Three Dimensional Solids," Optical and Electrooptical Information Processing, by J. J. Tippett et al., M.I.T. Press,Cambridge, Mass., pp. 159-197. Stokely, E., Buja, L. M., Lewis, S. E., Parkey, R. W., et al., "Measurement of Acute Myocardial Infarcts in Dogs with Technetium-99 Stannous Pyrophosphate Scintigrams," J. Nucl. Med., Vol. 17, pp. 1-5, January 1976. Bonte, F. J., Parkey, R. W., Graham, K. D., et al., "A New Method for Radionuclide Imaging of Myocardial Infarcts," Radiology, Vol. 110, pp. 473-474, January 1974.

A Computerized Breast Thermographic Interpreter

MICHAEL NEGIN, MEMBER, IEEE, MARVIN C. ZISKIN, SENIOR MEMBER, AND MARC S. LAPAYOWKER
IEEE,

CHARLES PINER,

Abstract-A computerized breast thermographic interpreter (CBTI) has been developed which outperforms human thermographers on a series of 81 frontal thermograms. The CBTI is composed of feature extraction algorithms followed by linear discriminant classifiers. Human interpretatiois and computer interpretations were compared to a thermographic panel decision and to biopsy findings. In each case, the CBTI performance was better than individual human

from breast cancer has remained essentially constant at 22 per 100,000 female population for the past 40 years [3], [47]. The incidence of this disease increases with age. It is rarely seen before age 30, but its incidence rises rapidly following the menopause. The 5 year survival rate depends on the size of the cancer performance. and metastatic spread existing at the time of diagnosis. Breast The CBTI thus developed has been embedded in a minicomputer cancer found by self-examination results in a 5 year survival (Linc-8) and requires 5 min of minicomputer time to interpret one rate of 45-55% [15], [47]. However, it has been shown that case and issue its findings on a line printer. the use .of methods which aid in the early detection of breast cancer can yield five year survival rates of 80-85% [1, 15]. INTRODUCTION These findings have stimulated research and development of BREAST CANCER is the leading cause of death by cancer techniques which can increase the probability of early in women. In the United States alone, it kills more than detection. 27,000 women each year. One out of every 15 women will at some time develop breast cancer and in spite of new innova- Thermography tions in surgery, radiotherapy, and diagnosis, the death rate Thermography is the science of recording the infrared radiation emitted from the surface of a patient. A thermogram is Manuscript received January 12, 1976; revised March 1, 1976, and therefore a map of the skin temperature of an object or April 9, 1976. This work was supported in part by the National Insti- patient. The use of breast thermograms to detect breast tutes of Health under Grants GM 14548 and GM 54466. M. Negin is with the Biomedical Engineering and Science Program, cancer has been studied by many groups and has been found Department of Electrical Engineering, Drexel University, Philadelphia, to be an imaging modality which can play an important role in PA 19104. screening programs. [13-17], [19], [25], [45]-[46], [48]. M. C. Ziskin, C. Piner, and M. S. Lapayowker are with the Diagnostic Radiology Research Laboratory, School of Medicine, Temple Univer- Although breast thermography has a useful role in screening, sity, Philadelphia, PA 19140. it must be emphasized that breast thermography should never

348

IEEE TRANSACTIONS ON BIOMEDICAL

ENGINEERING, JULY 1977

by the only screening modality used. Furthermore, a positive breast thermogram only indicates suspicion of a breast abnormality and cannot be used for differential diagnosis. The physical principles of thermography have been studied by many investigators [5], [10], [21], [33], [49] -[50]. Many investigators have studied correlations between carcinomas, venous drainage, and temperature [8], [9], [12][13], [29], [30], [31], [36], [38] and have studied variations in thermal patterns [9], [16], [27], [291, [32], [35]. In general, the relationship between tumor size and temperature elevation is not constant, and not all tumors produce a positive scan. Furthermore, unless the tumor is closely related to the underlying skin, there may be no direct relationship between the zone of increased heat and the location of the neoplastic mass [48]. Nevertheless, thermography has been shown capable of detecting some breast cancers that are not detectable by manual examination or mammography and Freundlich et al. [13], have reported the detection of a number of breast cancers as small as 0.1 cm in diameter.

BACKGROUND RE4OVAL
ASSI(qMENT OF "HOT" AREAS

DATA COMPRESSION,

DIVI"UIL.ILL

~~I. I.

PREPROCESSING REDCION
DATA REIlJCIN

FI ND SEPARATE "HOT" REGIONS

TEDPERATR PAYAETER

COMPUTE AREA AND

s
SYMMETRYSHP
WEASURES

GENERATE

GENERATE
<

I. LEStVAL FEATURE T~~~~~~I COWMOSITIN

: PAWNIETERS

Computer Image Analysis in Radiology COMPOUND FEATURE The literature in the field of computer image analysis is COMPOSITIO voluminous, and several excellent review articles have been ;> III . D~IAMNOSIS written [22], [24], [40], [42], [43]. Computers can be CLASSIFY PICI URE used to improve the quality of an image [37], [44], for making specific measurements [7], and for classifying patterns Fig. 1. Breast Thermogram Analysis Block Diagram. [20], [26]. Computers have been applied to the analysis of breast mammograms and xerograms [2], [34], [51] for the detection of breast cancer. The preprocessor and feature extraction stages have been With regard to the quantitative interpretation of breast described in previous publications [38, 57] and will not be thermograms, Barash et al. [6] have shown that the simple described here. The decision maker stage is the critical stage semiquantitative thermographic parameterization improves for this paper and will be emphasized. thermographic sensitivity for detecting breast cancer over the purely subjective reading of thermograms. Revesz and La- Decision Maker payowker [41 ] have suggested that more quantitative thermoThis stage is comprised of two elements, a) compound graphic parameterization will further improve the utility of feature composition and b) picture classification. thermography as a screening aid. Compound Feature Composition: The elemental features Computer quantitation has been considered by numerous are listed in Table I. These features represent some of the investigators and several groups have reported preliminary basic densitometric (temperature) and topological (symmetries, work which demonstrate that computer analysis of thermo- extents, shapes) items of interest in a thermogram. These gramsisfeasible [I1,3S, 39, 52, 53, 56,57]. elemental features were derived based on discussions with thermographers, and a review of the literature which involved COMPUTERIZED THERMOGRAPHY criteria for assessment of thermographic pattern. These The systems used to acquire thermograms in digital format elemental features are not all-inclusive of potential thermohas been described previously by our group [38, 57] and the graphic descriptors, but is a reasonable set of parameters. [57] The elemental features represent basic items of thermoreader is referred to the literature for details of the system. graphic interest but of themselves are not very informative, A brief outline of the major system components is given. since they represent data out of context. The compound parameters, which are combinations of elemental parameters, PROCEDURE the basic aspects of the thermogram in context, and are As shown in Figure 1, the system composed of three sub- place used as the parameters for training a linear discriminant classisystems, as indicated by roman numerals I, II, III. As in most fier. Originally, approximately 100 compound features were pattern analysis systems, these three subsystems can be constructed using logic, intuition, and experience regarding the thought of as: thermographic interpretation criteria. By performing a series I preprocessor or signal conditioner; of studies using frequency histograms of the parameter distriII feature extractor; butions and by computing covariances, all but those shown in III decision maker. Table II were deleted. [38]

NEGIN et al.: COMPUTERIZED BREAST THERMOGRAPHIC INTERPRETER

349

TABLE I ELEMENTAL FEATURES* DESCRIPTION

1. Hottest Focal Area on Left " " Right 2. "' 3. Hottest Region on Left "f " Right 4. 6.

TABLE III PARAMETER CLASSIFICATION RESULTS

Training Set

Nuber of Paraseters

Training Films Normal Abnormal

Performance on

Perfornance on Test Films Norinall.bnorma

9/11 9/15 {(Ot.3%) (60%)

Overall

Perfoormnce
70/81 (86.4%)

Unequivocal* Films

13

(94.30)
26/26 (100%)

33/35

19/20

(95i)

5.
7.

Areolar Temp on Left " " Right

Non-Confusing'
Films

13

(93.31)

14/1S

18/20

(90%)

10/20

(30%.)

(83.9%)

68/81

Reference Temperature

8. Ave. Temp of Left Breast 9. Ave. Temp of Right Breast

10. Ave. Temp of all Hot Regions on Left
11. Ave. Temp of all Hot Regions on Right 12. Total Hot Area on Left " " " 13. Right

*Unequivocal films

are those films where the thermographic Limpression agrees with the biopsy report. 'Non-Confusing" films are those "Unequivocal" films have been which subjectively defined as "easy" films to interpret. **Overall performance is given as the nuemer of correct decisions divided by the total number of cases.

TABLE IV COMPARISON OF COMPUTER AND HUMAN INTERPRETERS

INTERPRETER

14. Horizontal "shift' Between Left and Right Hottest Focal Area
15. Vertical "shift" Between Left and Right Hottest Focal Area 16. Highest p2/A Value on Either Side (Shape Factor) 17. Lowest P2/A Value on Either Side (Shape Factor)

NUBER OF 7APAR ERS

PERFORM ISTNCE ON FILMS 11111 TINER-I MIGRA\PIIC IMUPRESSION AS TRUI115* _______ NO 1R'AL AUNORML

PLERFORM:VNCE CN FTLUE 1I171 BIOPSY RESULTS

AS TRU I *
NORMAl

| ABNOR>L
21/31

Trained on

Computer

42/46

28/35

39/50 74.1%

"Unequivocal Films" Computer 44/46

13 13

86.4%
24/35
83.9%

18. Number of Hot Regions on Left It " " 19. Right

Trained on

43/50
76.7%

19/31

"Non-Confusing Films"

TABLE II COMPOUND PARAMETERS*

nAD)AlkAq'

Hu (Ave. Results of 5

40.2/46
79.0%

23.8/35

36/50
62.2%

14.4/31

Readers)

Individual

TnccCrT)TYT^r)

1. Age
2. 3.

Thereographic "truth" was established by a panel decision.

Difference in hot area extent between left and right breasts. Difference between hottest points on left and right breasts.

*Perforeance

is comnuted as the percent of correct decisions out of the total number of cases.

4. Abs. difference in Temp. between left and right areolar regions.

5. Abs. difference of Ave. temp. between left and right breasts.

6. Abs. difference of highest and lowest P2/A ratio.

7.

Temp. of hottest focal area on either breast, normalized by the reference temp.

8. Largest total hot area on either breast. 9. Temp. of hottest breast, normalized by the reference temp. 10. "Shift" between the Positions of the hottest focal area on the left and right

breast.

11. Abs. difference in number of hot regions between left and right (shifted by 1

region).

12. Abs. difference of hottest focal areas betwveen left and right breasts, normalized by their respective breast temp.
13. Abs. difference between

(temp. of hottest region)-(ave. grid size) of left and right side. (Analogous to a differential heat emission.)

* See reference

57 for detailed discussion.

Picture Classification Training of "Computer Thermographers:" Having established that certain parameters are descriptive of thermograms in effect completes the feature specification problem. The next problem was to establish a classification procedure and then to test it. The classification procedure we used was a linear discriminant procedure [23, 55]. To test the linear discriminant procedure, we subdivided our initial data base into a "training" set and a "test" set. We then established an optimal set of classification coefficients from the training subdivision and then classified the test set to determine the classifier's ability to classify data that it had not seen before. We established several data base subdivisions for training/ testing different classifiers of which two are shown in Table III and Table IV. The training set called Unequivocal Films was comprised of all films where the biopsy report and the thermographic impression agreed. The training set called Non-Confusing Films was based on a set of experiments done by us to determine how difficult a thermogram was to interpret. We distributed our data base to 5 trained thermographic interpreters (3 of whom are

350

IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, JULY 1977

radiologists). Each interpreter was asked to judge each thermogram, and to determine if the thermogram was positively normal, probably normal, probably abnormal, or positively abnormal. Based on the agreement among these five people, a criterion was established to determine how nonconfusing or confusing each film was. In effect, if four or five of the readers agreed on the classification of the film, (and if their decision agreed with biopsy) the film was said to be Non-Confusing. The other films were, of course, said to be confusing. Based on this evaluation, we established the set of non-confusing films for use in training/testing linear discriminant classifiers. The results are shown in Table III and Table IV. In addition to these two "computer thermographers" we imbedded two other CT's which incorporate a decision tree prescreener with each of the two original CT's. The decision tree prescreener permits computer inspection of three parameters individually. This is done because we have found that our best three parameters have certain temperature ranges which are never occupied by completely normal films. For a given film, if one of these three parameters falls in these "abnormal ranges," the film is immediately classified as positive. If none of these three parameters is "abnormal" the linear discriminant program then classifies the thermogram. These four "computer thermographers" can be thought of as representing four different training modalities and biases.

TABLE V
BREAST TEST

COMPUIER THERMOGRAPHER CLASSIFIES BY USING

Unequivocal Training Only

2
3 4

Non-Confusing Training Only

Unequivocal Training and Decision Tree Non-Confusing Training and Decision Tree

thermographic truth, and an average accuracy of 79.0% was obtained. From Table IV, it is seen that the CBTI #2 compares favorably to average human performance. One might question the CBTI #2 performance on the test series (28/40 75%), but considering that the test series represents the confusing films, 28/40 is quite reasonable. Now that the comparisons to thermographic truth have been stated, one needs to consider performance with respect to "tissue truth" or pathology results of the biopsied specimens. These results are also shown in Table IV. Without any retraining or reevaluation of the thermograms by CBTI's or humans, the previous decisions made by CBTI's and humans were simply compared to the biopsy result. These comparisons show that CBTI #2 scored 76.7% and the average human performance was 62.2%. The performance difference of over 14% suggests the possibility that computer scoring RESULTS of thermograms might be better than human scoring. We have Performance of the Computer Thernographers not yet done sufficient studies to verify this possibility. A final point should be made with regard to bias and applicaThe performance of the Computerized Breast Thermographic Interpreters (CBTI's) can be evaluated in several ways. tion of thermographic criteria. It may be true that human and The CBTI's can be compared to human thermographic deci- computer thermographers can be trained to use the same sions or the CBTI's can be compared to tissue pathology. In criteria (i.e., features), in interpreting breast thermograms. fact, since it is sensible to compare the CBTI's to both forms Humans, however, usually have a specific clinical viewpoint or bias which is difficult if not impossible to alter. This of truth, we present both comparisons. As was implied previously, four CBTI's have been designed implies that a given thermographer may consistently underand imbedded in a minicomputer. Table V shows the training or overread films. A computer scheme, however, permits biases of the CBTI's. Since the four CBTI's have similar per- bias shifts by simply changing a threshold of some parameter formances, only one of the CBTI's performances will be pre- or statistic. By this means, a computer's bias can be objecsented in detail. This is done in order to clearly illustrate tively changed to increase the detection rate at an increased the general results which have been ascertained without clut- false positive rate. In certain screening situations, the control tering this presentation with unnecessary detail. Attention that can be excepted on the CBTI's bias may be of crucial will therefore be focused on the CBTI trained on non-confus- importance so that the detection rate can be specified. As an example, one may use CBTI #2. If the reader will look at ing films, i.e., CBTI #2. CBTI #2 vs. Average Human Performance: The training set Table III, a true positive rate of 10/20 (50%) on the test films for the CBTI #2 consisted of the set of "non-confusing" is observed, and a true negative rate of 18/20 (90%) on the films (as defined previously). This training set consisted of 41 test films is observed. By lowering the threshold for abnormalfilms (26 normals and 15 abnormals) (see Table III). After ity or positivity, the true positive rate could be increased, but establishing a set of linear classification coefficients, the CBTI a decrease in the true negative rate would be incurred. Exactly #2 was tested on the remaining 40 films in the series. The where such a threshold for altering true positive and true classifier scored 40/41 on the training set and 28/40 on the negative rate should be placed is dependent on the requiretest set for an overall performance of 68/81 (83.9%o) on the ments of the specific application. The fact that the threshold entire series. Again, refer to Table III for the summary of can be changed to change the performance bias, is of itself a major benefit derivable from computerized thermography. these figures. Table IV presents a comparison of human and CBTI performance. As stated in Table IV, thermographic truth was Virtually Complete System Automation established via a panel decision. Each of the five human At the present time, the computerized system we have thermographers scores was computed and compared to the developed is virtually automatic. After placing the thermo-

NEGIN et al.: COMPUTERIZED BREAST THERMOGRAPHIC INTERPRETER

UATE: 10X03//4
*,******************* ****

351

UATE I 1 0/03//4
BREAST TEST 0
I

I BREAST TLbT s THLNMCGWAP, X 3t43 CUMM~ENT5:

THERMOGRAM 0

iaX. THE PHUbAbILI1Y Ot ABNORMALITY IS SLRtLNIN6 INUICATtS THERmUGRAM IS NtGATIVLI

***************,*********

MULTIPARAMLTtR ANALYSIb mAS PERFURMEU.

CuMMENT3S PERFURMED, MULTIPARAM'tTtR ANALYSIS WAS 75%. THE PRObABILIIY OF ABNOMMALITY IS SCRtENING INUICATtS TmERMOGRAM IS PUSITIVtl

4357

BNtAbT 1EsT 4 a THENMUG1NAM 4 3b43 CUMMENTSI

BREAST IEST o 2 THERMOGRAM a 4357

wAb

PERFURMEU. 3lX, THE FRUHAblLI1Y OF ABNORMALITY IS SLRtELNNG INLICATtS THERMUGRAm AS PRObAbLY NEGATIVE!

MULTIPANAmtTtH ANALYbIb

MULTIPARAMLTtR ANALYbSI WAS PERFURMED, 9fl. THE PROUAMILI1Y OF ABNORMALITY 1S SLRtLNING I)iCATE3 THERMUGRAM IS POSITIVMI
WHEAST TEST 0 3 TiERMUGRAM N 4457 CUMMENTS: BREAST TEmPERATURE OPFCERENCt IS SIGNIFICANT, 99X. THE PROUADILI1Y Of ABNORMALITY 13 SCREENING INDiCATzS THIERMOGRAM 1S POSITIVtE
BREAS1 TEST 0
4

CUMMENTS 3

**** *********w**** *******

BREAST TEST # 3 tHIEMuGkAM 1 3643

MULTIPAkAMLTLR ANALYbIb AAS PERFURMtL). lBX. THE PHOiAbILIXY OP ABNORMALITY IS SLRtE.ING INDICATtS THERMUGkAM IS NLGATIVE!
******** *****************

CuMmEN Tb:

BREAST TEST THERMUGRAM a CUMMENT5;

3b4J

4 4

TmEmRMUGRAM

MULTjPAkAmtTLR ANALYSIS WAS PERFURmEC. 3e X . THE PF OtAdILI1Y U@ ABO4RMALITY IS SLNtLLING INUICATES THENMUGRAM IS PHOBAbLY NEGATIVL:
****** *******************

CUMMENTS3 dRtA*T TEMPERArURE OAFtLRENCt IS SIGNIFICANT, THE PROUAUILIIY OF ABNORMALITY IS 99X, SCREENI1NG INVICATES THERMGURAM 1S POSITIVtE

4457

Fig. 2. Thermographic Analysis Summary.

Fig. 3. Thermographic Analysis Summary.

gram under the TV scanner, the only interaction required by the operator is identification number entry, age entry, and nipple location. Once these parameters have been entered, the computer performs and coordinates all of the feature location, decision analysis, and report generation. The processing of one thermogram requires about 5 min of minicomputer time (Linc-8). This time includes report generation. Of the 5 min of computer time, approximately 2 min is required for picture acquisition.

SUMMARY

Clinical Report Generation For each of the four current computer thermographers, we generate a simplified clinical report. These reports are generated by using the values of the features, the results of the discriminant analysis, and the results of the decision tree prescreening, if applicable. The four minireports are generated by the computer thermographers as defined in Table V. Note in Figure 2 that the results of Test #1 are the same as Test #3, and the results of Test #2 are the same as Test #4. Note also the differences in the COMMENTS among the test results. These differences are attributable to the different way in which the CT's were trained. In Figure 3 one should note that the breast temperature difference is significant (see Comments, Test #3 and #4). This fact alters the form of the report (more comments) and alters the decisions made (note the probabilities of abnormality). This form of the clinical report could, of course, be expanded to include more detailed information if desirable.

A computerized system for the interpretation of breast thermograms has been developed by us. The system has been organized in a standard pattern recognition format using preprocessing stages, feature extraction stages, and a decision stage. The features were defined from thermographic criteria currently in use in breast cancer screening centers. These features were used to design a prototype pattern recognition system for classifying thermograms. The results in Table IV show that the computer thermographic interpreters outperformed the human thermographic interpreters on our test series, with respect to both thermographic impression and biopsy. Based on these results we have imbedded four "computer thermographers" (CT's) in our software. Two of the "computer thermographers" are simple linear discriminant classifiers. One is based on the unequivocal films and the other is based on training on all the non-confusing data. The other two CT's utilize a decision tree approach ~coupled with linear discriminant classifiers.
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1971. [3] "American Cancer Society Policy Statement on the Surgical Treatment of Breast Cancers," CA. 23:341-343, 1973. [4] Barnes, R. Bowling: "Thermography," Annals of the New York Academy of Sciences, 121:34-48, 1964.

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[5] Barnes. R. B.: "Thermography of the Human Body," Science, 140:870-877, 1963. 161 Barash, I. M., Pasternack, B. S., Venet, L., and Wolff, W. I.: "Quantitative Thermography as a Predictor of Breast Cancer," Cancer, 31:769-776, 1973. [7] Becker, N. C., Nettleton, W. J., Megers, P. H., Sweeney, J. W.,
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