- Email: [email protected]
Ultrasound of the breast in the symptomatic and X-ray dense breast
Clinical Radiology (1985) 36, 69 76 © 1985 Royal College of Radiologists
0009-9260/85/365069502.00
Ultrasound of the Breast in the Symptomatic and X-ray Dense Breast P. B. G U Y E R and K. C. D E W B U R Y Department of Radiology, Southampton General Hospital, Tremona Road, Southampton
Our preliminary experience of direct-contact B-scan sonomammography in 500 patients is recorded and is compared with X-ray mammography. The technique has been of considerable value in the radiologically dense breast and, since standard equipment can be used, the practice should become more widespread, in the anticipation that identification and exclusion of malignancy can be increased above that achievable by X-ray mammography alone.
bute the breast tissue evenly over the pectoral muscle and the ipsilateral hand behind the patient's head to tense the breast as much as possible and, thus, reduce contact artefacts. Scans were taken both longitudinally and transversely, at 0.5cm intervals, and at 0.2cm intervals through mass lesions (Harper and Kelly-Fry, 1980; Cole-Beuglet et al., 1981). Aspiration cytology or excision histology was available in 149 patients. RESULTS
In our hospitals, breast imaging plays an integral part in the assessment of patients with breast problems, accounting for one-third of the pre-operative assessment which will determine the type of surgery to be undertaken (Smallwood et al., 1984). An awareness of some of the difficulties in interpretation which occur in X-ray mammography (Teixidor and Kazam, 1977; Martin et al., 1979; Cole-Beuglet et al., 1980; Smallwood et al., 1984) stimulated an assessment of the value of sonomammography. Most previously reported series have employed water-bath techniques (Kobayashi et al., 1974; Harper and Kelly-Fry, 1980; Maturo et al., 1980; Cole-Beuglet et al., 1981; Croll et al., 1982; Jellins et al., 1982; Sickles et al., 1983), only Teixidor and Kazam (1977) and Shepstone et al. (1983) describing direct-contact techniques. We opted to assess a direct-contact technique, using apparatus which was already available for general-purpose Bscanning; we record the result of its use in 500 patients undergoing X-ray mammography. METHODS
X-ray mammography was performed using a Senograph X-ray machine and Kodak minR film. Standard lateral and craniocaudad views were taken in all patients, except those under 35 years without a dominant lump, when lateral views only were obtained initially, with the addition of supero-inferior views if there was radiological evidence of a mass. Sonomammography was undertaken initially in patients referred for breast pain, so that the technique could be established. Once this was achieved, we examined all patients with dense breasts, particularly if there was clinical or radiological evidence of a lump, and as many patients as possible with clinical suspicion of carcinoma. Thus, approximately half the patients referred for X-ray mammography also had breast ultrasound. A Philips B 7100 scanner with a 7.5 MHz transducer was used, employing direct skin contact. Patients were examined in the supine oblique position, the symptomatic side being slightly elevated t o distri-
Five hundred patients with symptomatic breast disease were studied by both X-ray mammography and sonomammography. The diagnostic criteria for the X-ray diagnosis of breast diseases are widely known, but the ultrasound appearances of breast lesions are not universally known, so with each pathology we describe the appearances we have noted using the direct~contact technique. X-ray Mammography
This correctly indicated the presence of malignancy in 55 of the 68 patients with proven malignancy (typical features in 38, incomplete features in 17) and in a further three patients there was asymmetrical breast density as the only indication of malignancy. In three patients a mass was interpreted as benign. In seven patients the X-ray mammograms were negative for malignancy due to breast density (five patients) (Cole-Beuglet et al., 1981) or difficult siting of the tumour (two patients). There were 24 further patients with possible (i.e. false positive) features of malignancy: five with microcalcifications and 19 with an illdefined mass and/or trabecular distortion. Eight of this group also had possible sonographic signs of malignancy (see following section). The remaining 404 patients were normal or showed benign disease. Sonomammography
Carcinoma was present in 68 patients, but was not identified in one patient with Paget's disease of the nipple due to a microscopic tumour. In the remaining 67 patients there were features of a mass in 58 patients, disturbance of the subcutaneous fat in 43 patients, distal attenuation in 34 patients, accentuation in nine patients, mixed distal attenuation and accentuation in 15 patients and distorted trabeculation in 10 patients. These features could be present in varying combinations, 25 patients showing the most frequent appearance of a mixed echoic mass with a surrounding halo of bright echoes and distal attenuation, described as 'a mass within a mass' by Teixidor and Kazam
70
CLINICAL RADIOLOGY
Fig. 1 - Carcinoma. There are two small, hypoechoic niduses (arrowheads) with a surrounding area of bright echoes disrupting the subcutaneous fat. In the deeper tissues there is dense acoustic shadowing (arrow).
Fig. 2 - Carcinoma. No tumour mass is visible, but there is dense acoustic shadowing deep in the breast tissue (arrow). The breast trabeculae are indrawn towards the hyperechoic area (arrowheads), immediately superficial to the shadowing.
71
ULTRASOUND OF THE BREAST
Fig. 3 - Carcinoma. A large, h e t e r o g e n e o u s mass with an irregular posterior margin, variable distal shadowing and quite p r o n o u n c e d edge
shadowing (arrows).
(1977) (Fig. 1). Nine patients had subcutaneous fat disturbance and distal attenuation as the only evidence of malignancy (Fig. 2) (Maturo et al., 1980; Kopans et al., 1982). The other 34 tumours showed variable features (Fig. 3); when visible, the mass was rounded or irregular in shape with poorly defined outlines in all except two patients, when the lesions were rounded and well defined. The internal echo pattern was hypoechoic in 36 of the 58 masses; it was heterogeneous in 22, especially if the tumour was large. Seventeen tumours were 1 cm or less in diameter, the smallest being 5 ram, and these smaller tumours were generally hypoechoic (Fig. 4). Although irregular and ill-defined in outline, 10 of the 58 tumours were rounded in shape, hypoechoic and either without distal effect or with a little accentuation (Maturo et al., 1980) (Fig. 4b). Carcinoma was correctly diagnosed in 62 of the 68 patients with proven malignancy (Table 1); in five patients the lesion was seen and diagnosed as benign and in the remaining patient the tumour was not seen. This patient had a microscopic tumour and Paget's disease of the nipple. In 17 patients, where the X-ray mammogram recorded incomplete features rather than Table 1 - Breast carcinoma (68 patients) X-ray/ultrasound a g r e e m e n t
Ultrasound added information Ultrasound revealed diagnosis Ultrasound less information Ultrasound false negative (Biopsy refused in four other clinicalcarcinomas)
37 17 7 1
6
Table 2 - Sonomammographic misdiagnoses for malignancy
False negative
Fibroadenoma Fibrocystic Cyst Paget's nipple
(6)
3 1 1 l
False positive
Fibroadenoma Fibrocystic Fibroadenosis Papillary adenoma No histology
(12)
2 6 2 1 1
certain malignancy, ultrasound made a firm diagnosis of malignancy. Ultrasound diagnosed carcinoma in the seven patients in whom the lesion could not be seen radiologically due to density or site. There were 12 false positive sonomammograms (Table 2). In one patient no histology was available, but a cyst has been aspirated. There were six patients in whom the histology revealed florid fibrocystic disease (Fig. 5), two with fibroadenosis (Fig. 6) and one with a papillary adenoma. Eight of these 12 patients also had a false positive X-ray mammogram due to the detection of an ill-defined mass lesion and/or trabecular disturbance. There were six patients with carcinoma who were misdiagnosed as having benign lesions by both techniques. One patient had Paget's disease of the nipple, with a microscopic tumour. Three patients, in whom a benign mass was wrongly diagnosed radiologically, were incorrectly considered to have a fibroadenoma sonographically (Fig. 7) (Kobayashi et al., 1974; Cole-Beuglet et al., 1981) and two patients with asymmetrical density on X-ray mammography as the only indication of malignancy were shown to have a
72
CLINICAL RADIOLOGY
localised lesion sonographically, which was diagnosed as a probable cyst in one instance and fibrocystic disease in the other. In addition to the 68 patients with histologically proven carcinoma and 428 patients with clinical or histological benign disease, four patients with carcinoma, clinically and radiologically, refused histological examination. Overall, in breast carcinoma (Table 1) there was radiological and sonographic agreement in 37 patients. Ultrasound confirmed malignancy in 17 patients thought possibly to have malignancy radiologically and revealed malignancy in seven patients in whom the tumour was radiologically invisible. In one patient, ultrasound was less conclusive about malignancy than the X-ray mammogram. Benign breast disease or normal appearances were indicated sonographically in 428 patients (404 radiologically benign and 24 with false positive radiology). There was no difference in the information yield between radiology and ultrasound in 188 patients (Table 3). In 89, ultrasound added further information by revealing additional cysts or fibroadenomas. In 76, ultrasound revealed a diagnosis obscured by X-ray breast density and in 63 patients ultrasound excluded a mass lesion with a palpable lump in an X-ray dense breast. Cysts were sharply defined, particularly on their posterior aspect, and had enhancement deep to the
Table 3 - Benign breast disease (428 patients) X-ray/ultrasound a g r e e m e n t Ultrasound added information Ultrasound revealed diagnosis Ultrasound excluded mass Ultrasound false positive
188 89 76 63 12
(a)
~b) Fig. 4 - (a) X-ray m a m m o g r a m showing a dense breast; a vague, rounded shadow, which was proven to be malignant, is arrowed. (b) Ultrasound scan in the same patient shows an irregular, hypoechoic, rounded shadow with disruption of the subcutaneous fat (arrowheads) and some distal accentuation.
ULTRASOUND OF THE BREAST
73
Fig. 5 - Fibrocystic disease. At least two cysts are present, with sharply defined posterior margins and distal accentuation. On the left side of the abnormal area there is dense acoustic shadowing (arrows) which raised fears of associated malignancy (false positive).
lesion (Fig. 8). They were usually completely transonic, but echoes were sometimes apparent within them due to reverberations, partial volume effect or, possibly, due to the turbidity of the fluid.
A fibroadenoma characteristically produced a homogeneous, echo-containing mass with well defined margins and a good posterior margin (Fig. 9) (ColeBeuglet et al., 1982). There was normally little change
Fig. 6 - Fibroadenosis. There is an extensive hypoechoic area with distal attenuation and some interference with the subcutaneous fat; diagnosed as possible carcinoma, but histology revealed florid fibroadenosis.
74
CLINICAL RADIOLOGY
Fig. 8 - Breast cyst. A hypoechoic mass with well defined posterior margins and distal accentuation; edge shadowing is visible.
Fig. 7 - Carcinoma. A fairly well defined shadow with a slightly heterogeneous echo pattern. There is distal accentuation. Considered to be fibroadenoma, but histologically proven to be carcinoma; in retrospect, the irregular posterior wall (arrowheads) should have led to a diagnosis of malignancy.
in the echo pattern deep to the mass. There may be a hypoechoic halo around the margins of the mass attributable to compressed breast tissue. Fibrocystic disease and fibroadenosis produce variable pictures. Typically, in fibrocystic disease there is a number of small transonic areas with alteration in the surrounding echo pattern, but little distal change; however, occasional distal acoustic shadowing has given rise to a false positive diagnosis (Fig. 5). Patients regarded clinically as having fibroadenosis produced either a normal breast echo pattern, a circumscribed area of brightly reflective breast tissue (Fig. 10) or an area of mixed echo pattern without acoustic shadowing. The smallest lesions identified (both cysts and fibroadenomas) were 3mm in diameter (Fig. 11) (Fields, 1980; Maturo et al., 1980). Microcalcifications have not been visualised, but coarser calcifications give rise to acoustic shadowing. It has been a feature of most palpable mass lesions that it is difficult to avoid producing edge shadows with this direct-contact technique. Aspiration cytology or excision histology was available in the 68 patients with carcinoma and in 81 patients with histologically benign breast disease. The sensitivity for X-ray mammography was 80.9 (55/68) and for sonomammography, 91.2 (62/68); the specificities were 94.4 (404/428) and 97.2 (416/428), respectively.
DISCUSSION The 500 patients described represent approximately half of those referred for breast imaging during the period of the study. Those submitted to sonomammography were mainly those with X-ray dense breasts, or clinical or radiological masses, in whom it was hoped further information might be obtained (Fields, 1980). A recent report from this centre (Smallwood et al., 1984) has shown that, in a series of 99 breast
Fig. 9 - Fibroadenoma. A well circumscribed, echo~containing mass~ mainly homogeneous, with no distal effect.
tumours, radiology positively indicated carcinoma in 87 and suggested it in a further six, an overall accuracy of 94%, which compares with the figures of Cahill et al. (1981). The results in the present study are similar because the 68 patients with carcinoma represent approximately half of those with breast malignancy during the period of the study, the others not being examined sonographically because the tumour was readily visible radiologically, and, thus, the seven radiologically invisible carcinomas and those with asymmetrical density represent about 6% of the total. The 24 radiological false positives were due to possible masses in asymmetrically dense breasts, with or without microcalcifications, and were shown to have no mass lesion on ultrasound. The early sonographic experience was encouraging, all carcinomas being visible, most commonly producing the appearance of a hypoechoic tumour nidus, a surrounding hyperechoic halo ('tissue response' Teixidor and Kazam, 1977; Maturo et al., 1980) and distal acoustic shadowing in varying combinations and degrees. The larger, rounded tumours could be diagnosed by their heterogeneous internal echo pattern alone, even though there might be accentuation of the distal structures, rather than attenuation or no distal effect at all. Medullary carcinoma may produce a more homogeneous internal echo pattern, although we have also seen mixed appearances with this tumour type. The initial experience changed slightly later in the
ULTRASOUND OF THE BREAST
75
Fig. 10 - Fibroadenosis. The central portion of the breast tissue is disorganised by a mixture of predominantly hyperechoic echoes, with smaller areas of hypoechoic shadowing (arrowheads).
Fig. 11 - Cyst. There is a 3mm transonic shadow with distal accentuation in the deepest layers of the breast tissue (arrow). There is also a pronounced duct pattern with hypoechoic shadows radiating from the nipple, indicating a minor degree of duct ectasia.
study when different appearances of malignancy became apparent, resulting in false negative diagnosis in six patients. One of the latter can be disregarded because there was a microscopic tumour in Paget's disease of the nipple, an area which is difficult to image (Harper and Kelly-Fry, 1980). Three masses were diagnosed as fibroadenomas (Teixidor and Kazam, 1977), having fairly well defined margins, a homogeneous, moderately bright echo pattern and either accentuation distally or no change in the distal tissues. The remaining two patients were diagnosed as having a cyst and fibrocystic disease, respectively. In retrospect, the false negative diagnoses of fibroadenoma were clearly incorrect, because the mass outline was ill-defined. The final result was that, apart from the microscopic tumour in Paget's disease of the nipple, all 67 carcinomas were identified, though five were misinterpreted as benign; X-ray mammography indicated carcinoma in 58 of these. The slightly lower yield from radiography might be improved with modern X-ray techniques (Sickles et al., 1983), which we are unable to employ with our present apparatus. The
occurrence of false negative ultrasound findings is recognised by a number of authors (Teixidor and Kazam, 1977; Cole-Beuglet et al., 1981; Croll et al., 1982; Jellins et al., 1982), who record ultrasound accuracy for malignancy varying between 79 and 85%. This contrasts with 100% accuracy claimed by Maturo et al. (1980) and Harper and Kelly-Fry (1980) and also with Sickles et al. (1983), who detected only 58% of carcinomas. The accuracy for carcinoma in our study is 91%. False negative results are due to the overlap between benign and malignant conditions (Cole-Beuglet et al., 1983; Harper et al., 1983), some carcinomas being homogeneous and well defined and some fibroadenomas being heterogeneous and ill-defined. The false positive diagnoses arose due to the occurrence of echoes within a cyst (Cole-Beuglet and Beique, 1975; Crotl et al., 1982), due to reverberations or partial volume effect, and the presence of acoustic shadowing, which was felt to be too strong to be attributed merely to edge shadowing; this can be resolved by cyst puncture during the ultrasound examination. In all instances of false positive diagnosis, the recommendation following imaging was for excision to exclude malignancy, rather than making a firm diagnosis of carcinoma. Edge shadowing occurs frequently in mass lesions as the transducer travels over the margins of the tumour; these edge shadows contribute to what has been referred to as the 'tadpole' sign (Kobayashi et al., 1974), which we have found to be of limited value. The commonest histology in the false positive cases was florid fibrocystic disease, a finding similar to that noted by Harper and Kelly-Fry (1980), Maturo et al. (1980) and Fleischer et al. (1983). The figures for sensitivities of 80.9 for radiology and 91.2 for sonomammography, and respective specificities of 94.4 and 97.2, must be taken with some caution since they result from a selection of patients and the follow-up period is short. However, they do suggest that ultrasound is more informative than X-ray roam-
76
CLINICAL RADIOLOGY
mography, using the techniques we describe, bearing in mind that we do not have the advantage of modern X-ray apparatus. In benign breast disease, sonomammography is of value in investigating areas of varying radiological density. It can more readily identify the nature of any such density and can also detect other lesions not suspected on the radiographs. It has the additional advantage of being able to exclude a circumscribed mass lesion in areas clinically nodular and radiologically dense. In patients considered clinically to have fibroadenosis, we found a varied pattern; some patients produced no change in the echo pattern, others produced focal areas of a predominantly bright echo pattern and others produced a predominantly hypoechoic pattern (Kobayashi et al., 1974; Teixidor and Kazam, 1977; Maturo et al., 1980). Although Harper and Kelly-Fry (1980) say microcalcifications can be seen, this has not been our experience with our direct-contact technique and Maturo et al. (1980) are in agreement with this. In addition, a false suggestion of microcalcifications might be produced by small skin artefacts as the transducer moves over the skin surface. Certainly, it has been possible to see larger calcifications, but these have been of the order of 2-3 mm or larger. Comparing sonomammography with X-ray mammography in this selected series (Tables 1 and 3), it can be seen that the ultrasound is superior (Teixidor and Kazam, 1977; Harper and Kelly-Fry, 1980; Maturo et al., 1982; Fleischer et al., 1983). In malignancy, ultrasound showed 17 radiologically possible carcinomas to be certainly malignant and detected seven carcinomas hidden by breast density (ColeBeuglet et al., 1981) or unsuitably sited for X-ray examination, e.g. in the inferior skinfold or extreme medial aspect of the breast. No tumour mass was missed by ultrasound, apart from the microscopic lesion in Paget's disease, although five lesions were thought likely to represent benign disease (i.e. false negatives). In benign breast disease, ultrasound provided additional information or revealed the diagnosis in 165 patients and excluded a mass lesion in 63 patients (Croll et al., 1982): it can be used to search for a mass in patients with microcalcifications. In its ability to detect small (3mm) lesions, this sonomammographic technique is clearly very sensitive; 16 carcinomas were less than 1 cm in diameter, generally smaller than most other authors have found. However, in the overlap between benign and malignant disease the technique suffers from a lack of specificity; this is less than for X-ray mammography in the X-ray dense breast. Our ultrasound technique causes no discomfort, is free of hazard, as far as is known, and can, therefore, be repeated as necessary. These features have led some authors to recommend it as a suitable first examination for patients under the age of 35 years (Harper and Kelly-Fry, 1980; Jellins et al., 1982; Cole-Beuglet et al., 1983). A significant feature of ultrasound is the time taken to examine each breast (approximately 5 min, depending upon patient morphology) and, because of this and the failure to detect microcalcifications, we cannot recommend this technique as a screening method (Fields, 1980; Cole-Beuglet et al., 1981). The technique is
simple and the equipment used is standard; it should become more widely employed as an adjunct to X-ray mammography (Lees, 1982) and may have to be used with guided biopsy for all apparently benign solid lesions (Teixidor and Kazam, 1977; Cole-Beuglet et al., 1982; Croll et aI., 1982; Cole-Beuglet et al., 1983). REFERENCES Cahill, D. J., Boulter, P. S., Gibbs, N. M. & Price, J. L. (1981). Features of mammographically negative breast tumours. British Journal of Surgery, 68, 882-889. Cole-Beuglet, C. & Beique, R. A. (1975). Continuous ultrasound 13-scanning of palpable breast masses. Radiology, 117, 123-128. Cole-Beugtet, C., Goldberg, B. B., Kurtz, A. B., Patchevsky, A. S., Shaber, G. S. & Rubin, C. S. (1982). Clinical experience with a prototype real-time dedicated breast scanner. American Journal of" Roentgenology, 139, 905-911. Cole-Beuglet, C., Goldberg, B. B., Kurtz, A. B., Rubin, C. S., Patchevsky, A. S. & Shaber, G. S. (1981). Ultrasound mammography: a comparison with radiographic mammography. Radiology, 139, 693-698. Cole-Beuglet, C., Kurtz, A. B., Rubin, C. S. & Goldberg, 13. B. (1980). Ultrasound mammography. Radiologic Clinics of North America, 18, 133-143. Cole-13euglet, C., Soriano, R. Z., Kurtz, A. B. & Goldberg, B. B. (1983). Fibroadenoma of breast - sonomammography correlated with pathology in 122 patients. American Journal of Roentgenology, 140, 369-375. Croll, J., Kotevich, K. & Tabrett, M. (1982). Diagnosis of benign disease and the exclusion of malignancy in patients with breast symptoms. Seminars in Ultrasound, 3, 38-50. Fields, S. I. (1980). Ultrasound mammographic-histopathologic correlation. Ultrasonic Imaging, 2, 150-161. Fleischer, A. C., Muhletaler, C. A., Reynolds, V. H., Machin, J. E., Thieme, G. A., 13undy, A. L., Winfield, A. C. & Everette James, A. (1983). Palpable breast masses: evaluation by highfrcqueney, hand-held real-time sonography and xeromammography. Radiology, 148, 813-817. Harper, A. P. & Kelly-Fry, E. (1980). Ultrasound visualization of the breast in symptomatic patients. Radiology, 137, 465-469. Harper, A. P. & Kelly-Fry, E., Noe, J. S., Bies, J. R. & Jackson, B. P. (1983). Ultrasound in the evaluation of solid breast masses. Radiology, 146, 731-736. Jellins, J., Reeve, T. S., Croll, J. & Kossof, G. (1982). Results of breast echographic examination in Sydney, Australia, 19721979. Seminars in Ultrasound, 3, 58-62. Kobayashi, T., Takatani, O., Hattori, N. & Kimura, K. (1974). Differential diagnosis of breast tumours. Cancer, 33, 940-951. Kopans, D. B., Meyer, J. E. & Steinbock, R. T. (1982). Breast cancer: the appearances as delineated by whole-breast waterbath ultrasound scanning. Journal of Clinical Ultrasound, 10, 313322. Lees, W. R. (1982). Breast ultrasonography. In Ultrasound Annual, ed. Sanders, R. C., pp. 301-320. Raven Press, New York. Martin, J. E., Moskowitz, M. & Milbraith, J. R. (1979). Breast cancer missed by mammography. American Journal of Roentgenology, 132, 737-739. Maturo, V. G., Zusmer, N. R., Gilson, A. J. & Bear, B. (1982). Ultrasonic appearances of mammary carcinoma with a dedicated whole breast scanner. Radiology, 142, 713-718. Maturo, V. G., Zusmer, N. R., Gilson, A. J., Smoak, W. M., Janowitz, W. R., Bear, B. E., Goddard, J. & Dick, D. E. (1980). Ultrasound of the whole breast using a dedicated automated breast scanner. Radiology, 137, 45%463. Shepstone, B. J., Fursdon, P. S. & Lee, E. C. G. (1983). Rapid, routine breast ultrasonoscopy for outpatients (letter). British Journal of Radiology, 56, 69. Sickles, E. A., Filly, R. A. & Callen, P~ W. (1983). Breast cancer detection with sonography and mammography. American Journal of Roentgenology, 140, 843-845. Smallwood, J., Khong, Y., Boyd, A., Guyer, P. 13., Herbert, A., Cooke, T. & Taylor, I. (1984). An assessment of a scoring scheme for the preoperative diagnosis of breast lumps. Annals of the Royal College of Surgeons of England, 66, 267-269. Teixidor, H. S. & Kazam, E. (1977). Combined mammographic and sonographic evaluation of breast masses. American Journal of Roentgenology, 128, 409-417.
0009-9260/85/365069502.00
Ultrasound of the Breast in the Symptomatic and X-ray Dense Breast P. B. G U Y E R and K. C. D E W B U R Y Department of Radiology, Southampton General Hospital, Tremona Road, Southampton
Our preliminary experience of direct-contact B-scan sonomammography in 500 patients is recorded and is compared with X-ray mammography. The technique has been of considerable value in the radiologically dense breast and, since standard equipment can be used, the practice should become more widespread, in the anticipation that identification and exclusion of malignancy can be increased above that achievable by X-ray mammography alone.
bute the breast tissue evenly over the pectoral muscle and the ipsilateral hand behind the patient's head to tense the breast as much as possible and, thus, reduce contact artefacts. Scans were taken both longitudinally and transversely, at 0.5cm intervals, and at 0.2cm intervals through mass lesions (Harper and Kelly-Fry, 1980; Cole-Beuglet et al., 1981). Aspiration cytology or excision histology was available in 149 patients. RESULTS
In our hospitals, breast imaging plays an integral part in the assessment of patients with breast problems, accounting for one-third of the pre-operative assessment which will determine the type of surgery to be undertaken (Smallwood et al., 1984). An awareness of some of the difficulties in interpretation which occur in X-ray mammography (Teixidor and Kazam, 1977; Martin et al., 1979; Cole-Beuglet et al., 1980; Smallwood et al., 1984) stimulated an assessment of the value of sonomammography. Most previously reported series have employed water-bath techniques (Kobayashi et al., 1974; Harper and Kelly-Fry, 1980; Maturo et al., 1980; Cole-Beuglet et al., 1981; Croll et al., 1982; Jellins et al., 1982; Sickles et al., 1983), only Teixidor and Kazam (1977) and Shepstone et al. (1983) describing direct-contact techniques. We opted to assess a direct-contact technique, using apparatus which was already available for general-purpose Bscanning; we record the result of its use in 500 patients undergoing X-ray mammography. METHODS
X-ray mammography was performed using a Senograph X-ray machine and Kodak minR film. Standard lateral and craniocaudad views were taken in all patients, except those under 35 years without a dominant lump, when lateral views only were obtained initially, with the addition of supero-inferior views if there was radiological evidence of a mass. Sonomammography was undertaken initially in patients referred for breast pain, so that the technique could be established. Once this was achieved, we examined all patients with dense breasts, particularly if there was clinical or radiological evidence of a lump, and as many patients as possible with clinical suspicion of carcinoma. Thus, approximately half the patients referred for X-ray mammography also had breast ultrasound. A Philips B 7100 scanner with a 7.5 MHz transducer was used, employing direct skin contact. Patients were examined in the supine oblique position, the symptomatic side being slightly elevated t o distri-
Five hundred patients with symptomatic breast disease were studied by both X-ray mammography and sonomammography. The diagnostic criteria for the X-ray diagnosis of breast diseases are widely known, but the ultrasound appearances of breast lesions are not universally known, so with each pathology we describe the appearances we have noted using the direct~contact technique. X-ray Mammography
This correctly indicated the presence of malignancy in 55 of the 68 patients with proven malignancy (typical features in 38, incomplete features in 17) and in a further three patients there was asymmetrical breast density as the only indication of malignancy. In three patients a mass was interpreted as benign. In seven patients the X-ray mammograms were negative for malignancy due to breast density (five patients) (Cole-Beuglet et al., 1981) or difficult siting of the tumour (two patients). There were 24 further patients with possible (i.e. false positive) features of malignancy: five with microcalcifications and 19 with an illdefined mass and/or trabecular distortion. Eight of this group also had possible sonographic signs of malignancy (see following section). The remaining 404 patients were normal or showed benign disease. Sonomammography
Carcinoma was present in 68 patients, but was not identified in one patient with Paget's disease of the nipple due to a microscopic tumour. In the remaining 67 patients there were features of a mass in 58 patients, disturbance of the subcutaneous fat in 43 patients, distal attenuation in 34 patients, accentuation in nine patients, mixed distal attenuation and accentuation in 15 patients and distorted trabeculation in 10 patients. These features could be present in varying combinations, 25 patients showing the most frequent appearance of a mixed echoic mass with a surrounding halo of bright echoes and distal attenuation, described as 'a mass within a mass' by Teixidor and Kazam
70
CLINICAL RADIOLOGY
Fig. 1 - Carcinoma. There are two small, hypoechoic niduses (arrowheads) with a surrounding area of bright echoes disrupting the subcutaneous fat. In the deeper tissues there is dense acoustic shadowing (arrow).
Fig. 2 - Carcinoma. No tumour mass is visible, but there is dense acoustic shadowing deep in the breast tissue (arrow). The breast trabeculae are indrawn towards the hyperechoic area (arrowheads), immediately superficial to the shadowing.
71
ULTRASOUND OF THE BREAST
Fig. 3 - Carcinoma. A large, h e t e r o g e n e o u s mass with an irregular posterior margin, variable distal shadowing and quite p r o n o u n c e d edge
shadowing (arrows).
(1977) (Fig. 1). Nine patients had subcutaneous fat disturbance and distal attenuation as the only evidence of malignancy (Fig. 2) (Maturo et al., 1980; Kopans et al., 1982). The other 34 tumours showed variable features (Fig. 3); when visible, the mass was rounded or irregular in shape with poorly defined outlines in all except two patients, when the lesions were rounded and well defined. The internal echo pattern was hypoechoic in 36 of the 58 masses; it was heterogeneous in 22, especially if the tumour was large. Seventeen tumours were 1 cm or less in diameter, the smallest being 5 ram, and these smaller tumours were generally hypoechoic (Fig. 4). Although irregular and ill-defined in outline, 10 of the 58 tumours were rounded in shape, hypoechoic and either without distal effect or with a little accentuation (Maturo et al., 1980) (Fig. 4b). Carcinoma was correctly diagnosed in 62 of the 68 patients with proven malignancy (Table 1); in five patients the lesion was seen and diagnosed as benign and in the remaining patient the tumour was not seen. This patient had a microscopic tumour and Paget's disease of the nipple. In 17 patients, where the X-ray mammogram recorded incomplete features rather than Table 1 - Breast carcinoma (68 patients) X-ray/ultrasound a g r e e m e n t
Ultrasound added information Ultrasound revealed diagnosis Ultrasound less information Ultrasound false negative (Biopsy refused in four other clinicalcarcinomas)
37 17 7 1
6
Table 2 - Sonomammographic misdiagnoses for malignancy
False negative
Fibroadenoma Fibrocystic Cyst Paget's nipple
(6)
3 1 1 l
False positive
Fibroadenoma Fibrocystic Fibroadenosis Papillary adenoma No histology
(12)
2 6 2 1 1
certain malignancy, ultrasound made a firm diagnosis of malignancy. Ultrasound diagnosed carcinoma in the seven patients in whom the lesion could not be seen radiologically due to density or site. There were 12 false positive sonomammograms (Table 2). In one patient no histology was available, but a cyst has been aspirated. There were six patients in whom the histology revealed florid fibrocystic disease (Fig. 5), two with fibroadenosis (Fig. 6) and one with a papillary adenoma. Eight of these 12 patients also had a false positive X-ray mammogram due to the detection of an ill-defined mass lesion and/or trabecular disturbance. There were six patients with carcinoma who were misdiagnosed as having benign lesions by both techniques. One patient had Paget's disease of the nipple, with a microscopic tumour. Three patients, in whom a benign mass was wrongly diagnosed radiologically, were incorrectly considered to have a fibroadenoma sonographically (Fig. 7) (Kobayashi et al., 1974; Cole-Beuglet et al., 1981) and two patients with asymmetrical density on X-ray mammography as the only indication of malignancy were shown to have a
72
CLINICAL RADIOLOGY
localised lesion sonographically, which was diagnosed as a probable cyst in one instance and fibrocystic disease in the other. In addition to the 68 patients with histologically proven carcinoma and 428 patients with clinical or histological benign disease, four patients with carcinoma, clinically and radiologically, refused histological examination. Overall, in breast carcinoma (Table 1) there was radiological and sonographic agreement in 37 patients. Ultrasound confirmed malignancy in 17 patients thought possibly to have malignancy radiologically and revealed malignancy in seven patients in whom the tumour was radiologically invisible. In one patient, ultrasound was less conclusive about malignancy than the X-ray mammogram. Benign breast disease or normal appearances were indicated sonographically in 428 patients (404 radiologically benign and 24 with false positive radiology). There was no difference in the information yield between radiology and ultrasound in 188 patients (Table 3). In 89, ultrasound added further information by revealing additional cysts or fibroadenomas. In 76, ultrasound revealed a diagnosis obscured by X-ray breast density and in 63 patients ultrasound excluded a mass lesion with a palpable lump in an X-ray dense breast. Cysts were sharply defined, particularly on their posterior aspect, and had enhancement deep to the
Table 3 - Benign breast disease (428 patients) X-ray/ultrasound a g r e e m e n t Ultrasound added information Ultrasound revealed diagnosis Ultrasound excluded mass Ultrasound false positive
188 89 76 63 12
(a)
~b) Fig. 4 - (a) X-ray m a m m o g r a m showing a dense breast; a vague, rounded shadow, which was proven to be malignant, is arrowed. (b) Ultrasound scan in the same patient shows an irregular, hypoechoic, rounded shadow with disruption of the subcutaneous fat (arrowheads) and some distal accentuation.
ULTRASOUND OF THE BREAST
73
Fig. 5 - Fibrocystic disease. At least two cysts are present, with sharply defined posterior margins and distal accentuation. On the left side of the abnormal area there is dense acoustic shadowing (arrows) which raised fears of associated malignancy (false positive).
lesion (Fig. 8). They were usually completely transonic, but echoes were sometimes apparent within them due to reverberations, partial volume effect or, possibly, due to the turbidity of the fluid.
A fibroadenoma characteristically produced a homogeneous, echo-containing mass with well defined margins and a good posterior margin (Fig. 9) (ColeBeuglet et al., 1982). There was normally little change
Fig. 6 - Fibroadenosis. There is an extensive hypoechoic area with distal attenuation and some interference with the subcutaneous fat; diagnosed as possible carcinoma, but histology revealed florid fibroadenosis.
74
CLINICAL RADIOLOGY
Fig. 8 - Breast cyst. A hypoechoic mass with well defined posterior margins and distal accentuation; edge shadowing is visible.
Fig. 7 - Carcinoma. A fairly well defined shadow with a slightly heterogeneous echo pattern. There is distal accentuation. Considered to be fibroadenoma, but histologically proven to be carcinoma; in retrospect, the irregular posterior wall (arrowheads) should have led to a diagnosis of malignancy.
in the echo pattern deep to the mass. There may be a hypoechoic halo around the margins of the mass attributable to compressed breast tissue. Fibrocystic disease and fibroadenosis produce variable pictures. Typically, in fibrocystic disease there is a number of small transonic areas with alteration in the surrounding echo pattern, but little distal change; however, occasional distal acoustic shadowing has given rise to a false positive diagnosis (Fig. 5). Patients regarded clinically as having fibroadenosis produced either a normal breast echo pattern, a circumscribed area of brightly reflective breast tissue (Fig. 10) or an area of mixed echo pattern without acoustic shadowing. The smallest lesions identified (both cysts and fibroadenomas) were 3mm in diameter (Fig. 11) (Fields, 1980; Maturo et al., 1980). Microcalcifications have not been visualised, but coarser calcifications give rise to acoustic shadowing. It has been a feature of most palpable mass lesions that it is difficult to avoid producing edge shadows with this direct-contact technique. Aspiration cytology or excision histology was available in the 68 patients with carcinoma and in 81 patients with histologically benign breast disease. The sensitivity for X-ray mammography was 80.9 (55/68) and for sonomammography, 91.2 (62/68); the specificities were 94.4 (404/428) and 97.2 (416/428), respectively.
DISCUSSION The 500 patients described represent approximately half of those referred for breast imaging during the period of the study. Those submitted to sonomammography were mainly those with X-ray dense breasts, or clinical or radiological masses, in whom it was hoped further information might be obtained (Fields, 1980). A recent report from this centre (Smallwood et al., 1984) has shown that, in a series of 99 breast
Fig. 9 - Fibroadenoma. A well circumscribed, echo~containing mass~ mainly homogeneous, with no distal effect.
tumours, radiology positively indicated carcinoma in 87 and suggested it in a further six, an overall accuracy of 94%, which compares with the figures of Cahill et al. (1981). The results in the present study are similar because the 68 patients with carcinoma represent approximately half of those with breast malignancy during the period of the study, the others not being examined sonographically because the tumour was readily visible radiologically, and, thus, the seven radiologically invisible carcinomas and those with asymmetrical density represent about 6% of the total. The 24 radiological false positives were due to possible masses in asymmetrically dense breasts, with or without microcalcifications, and were shown to have no mass lesion on ultrasound. The early sonographic experience was encouraging, all carcinomas being visible, most commonly producing the appearance of a hypoechoic tumour nidus, a surrounding hyperechoic halo ('tissue response' Teixidor and Kazam, 1977; Maturo et al., 1980) and distal acoustic shadowing in varying combinations and degrees. The larger, rounded tumours could be diagnosed by their heterogeneous internal echo pattern alone, even though there might be accentuation of the distal structures, rather than attenuation or no distal effect at all. Medullary carcinoma may produce a more homogeneous internal echo pattern, although we have also seen mixed appearances with this tumour type. The initial experience changed slightly later in the
ULTRASOUND OF THE BREAST
75
Fig. 10 - Fibroadenosis. The central portion of the breast tissue is disorganised by a mixture of predominantly hyperechoic echoes, with smaller areas of hypoechoic shadowing (arrowheads).
Fig. 11 - Cyst. There is a 3mm transonic shadow with distal accentuation in the deepest layers of the breast tissue (arrow). There is also a pronounced duct pattern with hypoechoic shadows radiating from the nipple, indicating a minor degree of duct ectasia.
study when different appearances of malignancy became apparent, resulting in false negative diagnosis in six patients. One of the latter can be disregarded because there was a microscopic tumour in Paget's disease of the nipple, an area which is difficult to image (Harper and Kelly-Fry, 1980). Three masses were diagnosed as fibroadenomas (Teixidor and Kazam, 1977), having fairly well defined margins, a homogeneous, moderately bright echo pattern and either accentuation distally or no change in the distal tissues. The remaining two patients were diagnosed as having a cyst and fibrocystic disease, respectively. In retrospect, the false negative diagnoses of fibroadenoma were clearly incorrect, because the mass outline was ill-defined. The final result was that, apart from the microscopic tumour in Paget's disease of the nipple, all 67 carcinomas were identified, though five were misinterpreted as benign; X-ray mammography indicated carcinoma in 58 of these. The slightly lower yield from radiography might be improved with modern X-ray techniques (Sickles et al., 1983), which we are unable to employ with our present apparatus. The
occurrence of false negative ultrasound findings is recognised by a number of authors (Teixidor and Kazam, 1977; Cole-Beuglet et al., 1981; Croll et al., 1982; Jellins et al., 1982), who record ultrasound accuracy for malignancy varying between 79 and 85%. This contrasts with 100% accuracy claimed by Maturo et al. (1980) and Harper and Kelly-Fry (1980) and also with Sickles et al. (1983), who detected only 58% of carcinomas. The accuracy for carcinoma in our study is 91%. False negative results are due to the overlap between benign and malignant conditions (Cole-Beuglet et al., 1983; Harper et al., 1983), some carcinomas being homogeneous and well defined and some fibroadenomas being heterogeneous and ill-defined. The false positive diagnoses arose due to the occurrence of echoes within a cyst (Cole-Beuglet and Beique, 1975; Crotl et al., 1982), due to reverberations or partial volume effect, and the presence of acoustic shadowing, which was felt to be too strong to be attributed merely to edge shadowing; this can be resolved by cyst puncture during the ultrasound examination. In all instances of false positive diagnosis, the recommendation following imaging was for excision to exclude malignancy, rather than making a firm diagnosis of carcinoma. Edge shadowing occurs frequently in mass lesions as the transducer travels over the margins of the tumour; these edge shadows contribute to what has been referred to as the 'tadpole' sign (Kobayashi et al., 1974), which we have found to be of limited value. The commonest histology in the false positive cases was florid fibrocystic disease, a finding similar to that noted by Harper and Kelly-Fry (1980), Maturo et al. (1980) and Fleischer et al. (1983). The figures for sensitivities of 80.9 for radiology and 91.2 for sonomammography, and respective specificities of 94.4 and 97.2, must be taken with some caution since they result from a selection of patients and the follow-up period is short. However, they do suggest that ultrasound is more informative than X-ray roam-
76
CLINICAL RADIOLOGY
mography, using the techniques we describe, bearing in mind that we do not have the advantage of modern X-ray apparatus. In benign breast disease, sonomammography is of value in investigating areas of varying radiological density. It can more readily identify the nature of any such density and can also detect other lesions not suspected on the radiographs. It has the additional advantage of being able to exclude a circumscribed mass lesion in areas clinically nodular and radiologically dense. In patients considered clinically to have fibroadenosis, we found a varied pattern; some patients produced no change in the echo pattern, others produced focal areas of a predominantly bright echo pattern and others produced a predominantly hypoechoic pattern (Kobayashi et al., 1974; Teixidor and Kazam, 1977; Maturo et al., 1980). Although Harper and Kelly-Fry (1980) say microcalcifications can be seen, this has not been our experience with our direct-contact technique and Maturo et al. (1980) are in agreement with this. In addition, a false suggestion of microcalcifications might be produced by small skin artefacts as the transducer moves over the skin surface. Certainly, it has been possible to see larger calcifications, but these have been of the order of 2-3 mm or larger. Comparing sonomammography with X-ray mammography in this selected series (Tables 1 and 3), it can be seen that the ultrasound is superior (Teixidor and Kazam, 1977; Harper and Kelly-Fry, 1980; Maturo et al., 1982; Fleischer et al., 1983). In malignancy, ultrasound showed 17 radiologically possible carcinomas to be certainly malignant and detected seven carcinomas hidden by breast density (ColeBeuglet et al., 1981) or unsuitably sited for X-ray examination, e.g. in the inferior skinfold or extreme medial aspect of the breast. No tumour mass was missed by ultrasound, apart from the microscopic lesion in Paget's disease, although five lesions were thought likely to represent benign disease (i.e. false negatives). In benign breast disease, ultrasound provided additional information or revealed the diagnosis in 165 patients and excluded a mass lesion in 63 patients (Croll et al., 1982): it can be used to search for a mass in patients with microcalcifications. In its ability to detect small (3mm) lesions, this sonomammographic technique is clearly very sensitive; 16 carcinomas were less than 1 cm in diameter, generally smaller than most other authors have found. However, in the overlap between benign and malignant disease the technique suffers from a lack of specificity; this is less than for X-ray mammography in the X-ray dense breast. Our ultrasound technique causes no discomfort, is free of hazard, as far as is known, and can, therefore, be repeated as necessary. These features have led some authors to recommend it as a suitable first examination for patients under the age of 35 years (Harper and Kelly-Fry, 1980; Jellins et al., 1982; Cole-Beuglet et al., 1983). A significant feature of ultrasound is the time taken to examine each breast (approximately 5 min, depending upon patient morphology) and, because of this and the failure to detect microcalcifications, we cannot recommend this technique as a screening method (Fields, 1980; Cole-Beuglet et al., 1981). The technique is
simple and the equipment used is standard; it should become more widely employed as an adjunct to X-ray mammography (Lees, 1982) and may have to be used with guided biopsy for all apparently benign solid lesions (Teixidor and Kazam, 1977; Cole-Beuglet et al., 1982; Croll et aI., 1982; Cole-Beuglet et al., 1983). REFERENCES Cahill, D. J., Boulter, P. S., Gibbs, N. M. & Price, J. L. (1981). Features of mammographically negative breast tumours. British Journal of Surgery, 68, 882-889. Cole-Beuglet, C. & Beique, R. A. (1975). Continuous ultrasound 13-scanning of palpable breast masses. Radiology, 117, 123-128. Cole-Beugtet, C., Goldberg, B. B., Kurtz, A. B., Patchevsky, A. S., Shaber, G. S. & Rubin, C. S. (1982). Clinical experience with a prototype real-time dedicated breast scanner. American Journal of" Roentgenology, 139, 905-911. Cole-Beuglet, C., Goldberg, B. B., Kurtz, A. B., Rubin, C. S., Patchevsky, A. S. & Shaber, G. S. (1981). Ultrasound mammography: a comparison with radiographic mammography. Radiology, 139, 693-698. Cole-Beuglet, C., Kurtz, A. B., Rubin, C. S. & Goldberg, 13. B. (1980). Ultrasound mammography. Radiologic Clinics of North America, 18, 133-143. Cole-13euglet, C., Soriano, R. Z., Kurtz, A. B. & Goldberg, B. B. (1983). Fibroadenoma of breast - sonomammography correlated with pathology in 122 patients. American Journal of Roentgenology, 140, 369-375. Croll, J., Kotevich, K. & Tabrett, M. (1982). Diagnosis of benign disease and the exclusion of malignancy in patients with breast symptoms. Seminars in Ultrasound, 3, 38-50. Fields, S. I. (1980). Ultrasound mammographic-histopathologic correlation. Ultrasonic Imaging, 2, 150-161. Fleischer, A. C., Muhletaler, C. A., Reynolds, V. H., Machin, J. E., Thieme, G. A., 13undy, A. L., Winfield, A. C. & Everette James, A. (1983). Palpable breast masses: evaluation by highfrcqueney, hand-held real-time sonography and xeromammography. Radiology, 148, 813-817. Harper, A. P. & Kelly-Fry, E. (1980). Ultrasound visualization of the breast in symptomatic patients. Radiology, 137, 465-469. Harper, A. P. & Kelly-Fry, E., Noe, J. S., Bies, J. R. & Jackson, B. P. (1983). Ultrasound in the evaluation of solid breast masses. Radiology, 146, 731-736. Jellins, J., Reeve, T. S., Croll, J. & Kossof, G. (1982). Results of breast echographic examination in Sydney, Australia, 19721979. Seminars in Ultrasound, 3, 58-62. Kobayashi, T., Takatani, O., Hattori, N. & Kimura, K. (1974). Differential diagnosis of breast tumours. Cancer, 33, 940-951. Kopans, D. B., Meyer, J. E. & Steinbock, R. T. (1982). Breast cancer: the appearances as delineated by whole-breast waterbath ultrasound scanning. Journal of Clinical Ultrasound, 10, 313322. Lees, W. R. (1982). Breast ultrasonography. In Ultrasound Annual, ed. Sanders, R. C., pp. 301-320. Raven Press, New York. Martin, J. E., Moskowitz, M. & Milbraith, J. R. (1979). Breast cancer missed by mammography. American Journal of Roentgenology, 132, 737-739. Maturo, V. G., Zusmer, N. R., Gilson, A. J. & Bear, B. (1982). Ultrasonic appearances of mammary carcinoma with a dedicated whole breast scanner. Radiology, 142, 713-718. Maturo, V. G., Zusmer, N. R., Gilson, A. J., Smoak, W. M., Janowitz, W. R., Bear, B. E., Goddard, J. & Dick, D. E. (1980). Ultrasound of the whole breast using a dedicated automated breast scanner. Radiology, 137, 45%463. Shepstone, B. J., Fursdon, P. S. & Lee, E. C. G. (1983). Rapid, routine breast ultrasonoscopy for outpatients (letter). British Journal of Radiology, 56, 69. Sickles, E. A., Filly, R. A. & Callen, P~ W. (1983). Breast cancer detection with sonography and mammography. American Journal of Roentgenology, 140, 843-845. Smallwood, J., Khong, Y., Boyd, A., Guyer, P. 13., Herbert, A., Cooke, T. & Taylor, I. (1984). An assessment of a scoring scheme for the preoperative diagnosis of breast lumps. Annals of the Royal College of Surgeons of England, 66, 267-269. Teixidor, H. S. & Kazam, E. (1977). Combined mammographic and sonographic evaluation of breast masses. American Journal of Roentgenology, 128, 409-417.