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Ultrasonic examination of the thyroid gland
REVIEWS
Ultrasonic
Examination
of the Thyroid Gland
Possibilities and Limitations
L. G. THIJS, M.D. J. D. WIENER, Ph.D. Amsterdam, The Netherlands
In 440 patients with various thyroid disorders scintiphotography and ultrasonography were carried out. For ultrasonic examination both the A-mode and B-mode display technics were employed. Included in the study were 324 patients with hypofunctioning solitary nodules; a histopathologic dlagnosis could be obtained in 151 of these. The method proved to be especially valuable for differentiating between solid and cystic nodules. This is of practical importance because completely cystic nodules are nearly always benign and may be treated by thin needle puncture with aspiration of the cyst fluid. In addition, ultrasonography is of some value in making a better functional classification of nodules, better estimating the size of the thyroid and in the follow-up of patients with various thyroid disorders who are under treatment or untreated. Differentiating between benign and malignant solid nodules was not possible with the technic used. The examination can be safely carried out in pregnancy. The limitations of the technic are discussed. As early as 1955 Howry and co-workers [l] predicted that, concerning the use of ultrasound, “the method will probably outline areas of different density, such as adenomas and cystic degenerations within the thyroid gland. A series of such pictures at different levels makes it possible to determine the volume of the gland.” Donald [2] actually showed that visualization of the thyroid by means of ultrasound was possible. However, Yamakawa and Naito [3] were supposedly the first to practice this technic. Since then, several reports on this subject have appeared [4-191. Although these investigations differed in many respects concerning, e.g.,
equipment and performance, the conclusions were surprisingly similar. Now, 20 years after Howry’s paper, it seems worthwhile to reassess the clinical value of diagnostic ultrasound in evaluating thyroid gland pathology on the basis of our own experience and relevant data from the literature.
MATERIALS AND METHODS From the Department of Internal Medicine, Free University Hospital, Amsterdam, The Netherlands. Requests for reprints should be addressed to Dr. L. G. Thijs. Department of Internal Medicine, Free University Hospital, De Boelelaan 1117, Amsterdam 101 I, The Netherlands. Manuscript accepted July 25, 1975.
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Included in this study were 440 patients who were referred of Nuclear
Medicine
of our Department
tion and for thyroid scanning.
Ultrasonic
for the evaluation investigations
to the section of thyroid func-
were
carried
out
with the Diasonograph (Type NE 4101, Nuclear Enterprises Ltd.), provided with a 2.5 MHz transducer. The examination was always performed with the patient in the sitting position after scintiphotography
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ULTRASONIC EXAMINATION OF THE THYROID GLAND-THUS.
WIENER
palpation of the gland [ 181. Both the A-mode and B-mode display technics were employed with a variable sensitivity as an essential
part of the procedure.
The examination was started with a B-scan at low sensitivity, using the compound scanning technic [20], which produced a cross section through the neck in a transversal plane. This procedure was repeated at higher sensitivities. After completion of the B-scans, A-scans were made at low and high sensitivity at regions of interest, e.g., nodules. Both low and high sensitivity settings of the apparatus were empirically found [ 171. At high sensitivity, cystic lesions remained echo-free, whereas solid nodules were completely filled up by echoes. Thyroid function was assessed with standard technics, including ‘311-uptake studies. A diagnosis was made on clinical, laboratory and scintiphotographic evidence. A histopathologic diagnosis was obtained in 199 patients who were either operated on or subjected to biopsy.
%. -
d RL
T
LL
s
.&’ t b
RESULTS Figure 1 shows a normal thyroid gland for reference. Both lobes and sometimes also the isthmus appeared on the B-scan at low sensitivity as an echofree area between the neighboring structures which gave rise to distinct echoes. The anterior wall of the
trachea, the skin, the cervical spine, the vascular sheaths and sometimes the sternomastoid muscle were visible. With rising sensitivities, echoes also appeared within the thyroid. Hypofunctioning Solitary Nodules (324 patients). nodules were outlined on Solitary hypofunctioning the B-scan at low sensitivity in almost all cases. In a solid nodule, echoes sometimes appeared at intermediate sensitivity: at high sensitivity, these nodules were generally completely filled up, whereas cystic nodules remained echo-free both on the A- and on the B-scan (Figures 2 to 6). In a partially cystic nodule, echoes were absent in part of the nodule on the A- and on the B-scan at high sensitivity (Figure 4). In cystic nodules the structures behind the cyst were readily discernible even at low sensitivity. The absorption of ultrasonic energy in cystic lesions was apparently less than in solid lesions. Calcified lesions produced strong echoes at low sensitivity (Figure 3). A pathologic diagnosis was obtained in 151 patients. In Table I the gross pathologic findings are compared with the preoperative ultrasonic diagnosis. The diagnosis was correct in 19 of 21 simple cysts, l
in 82 of 90 solid nodules, but in only 22 of 40 partially cystic nodules. To obtain the best results, we found it essential to combine the A-mode and B-mode technics. With the
In most cases it cannot be ascertained whether these nodules were hypofunctioning or actually nonfunctioning (see “Comments”). For the sake of simplicity, the term “hypofunctioning” is used throughout this text. l
1
e
Figure 1. Normal thyroid g/and. a, B-scan at low sensitivity; b, scintiphoto, the arrows indicate markers on thyroid cartilage and sternal notch. The dashed line represents the level where the ultrasonic examination was carried out; c, B-scan at intermediate sensitivity; d, B-scan at high sensitivity; e, schematic representation of (a): RL = right lobe, LL = left lobe, T = anterior wall trachea, S = skin, VB = vertebral body, V = vascular sheath.
B-scan at low sensitivity, the nodule could be depicted and its localization in relation to the surrounding structures established. At high sensitivity, places with “filling defects” could be detected, and the place and direction of the A-scan chosen more accurately. The A-scan is only one-dimensional, but in general it gave more detailed information about the inner structures of the nodule. Therefore, the diagnosis solid or cystic was best made by the A-scan at high sensitivity (Figure 5).
TABLE I
Comparison of Preoperative Ultrasonic Diagnosis and Gross Pathologic Findings UltrasonicDiagnosis
Pathologic Diagnosis Solid Mixed solid-cystic Cystic Total
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Partially Cystic Cystic
Uncertain
Total
Solid
(no.)
(no.)
(no.)
90 40
82 15
2 22
:::
6 3
21 151
9;’
1 25
19 19
1 10
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e
b
C
f
Figure 2. Solid coid nodule in the left lobe; pathologic examination: colloid nodule. a-c, B-scan at low, intermediate and high sensitivity, respective/y; d, A-scan at low sensitivity in the direction indicated in (a) as a dotted line; E emission signal; e, A-scan at h@h sensitivity; f, schematic representation of (a): N = nodule; g, scintiphoto, the circle indicates the place of the palpated nodule.
‘5cm’
With correct calibration of the apparatus, the depth of a nodule could be measured from the ultrasonogram at low sensitivity. When a nodule either
scintiphoto, ultrasonography of this lobe (Figure 8).
appeared on the scintiphoto as an isoactive (“warm”) area (24 patients), or was not delineated at all (16 patients), ultrasonography usually disclosed its presence and proved that it was in fact hypofunctioning per unit volume, because it was thicker than the extranodular normal thyroid tissue (Figure 6). Palpated nonfunctioning nodules situated mainly outside the functioning thyroid tissue, e.g., in thyroglossal remnants, cannot be visualized by scintiphotography. By means of ultrasonography, their presence could be ascertained, their size measured and their cystic or solid nature established (12 patients). Finally, the size of nodules could be measured repeatedly in course of time, and changes in size could be noted in an objective way (Figure 7). Hyperfunctioning Nodules (41 patients). Solitary hyperfunctioning (“hot”) nodules, either with or without functional suppression of normal thyroid tissue, could be visualized by ultrasonic scanning as well. They presented in the same way as hypofunctional nodules, their acoustic properties apparently being similar. In case of complete suppression of the normal lobe, which therefore failed to appear on the
in diffuse nontoxic goiter, the enlarged lobes and isthmus were depicted at low sensitivity. At higher sensitivities, finely dispersed discrete echoes were reflected from the interior of the gland; at high sensitivity, the whole gland was filled up (Figure 9). Sometimes, only low amplitude echoes appeared on the A-scan at high sensitivity. Multinodular Goiter (31 patients). In many patients with toxic or nontoxic goiter, the B-scan showed the
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Diffuse Goiter (35 patients).
disclosed the presence In Graves’ disease and
thyroid to be much more enlarged than was apparent from palpation or scintiphoto alone (Figure 10). A preoperative ultrasonogram was of value for the surgeon. Echoes from calcified sensitivities.
within the gland, sometimes arising areas, were visible at relatively low
Thyroiditis (nine patients).
The gland was depicted on the B-scan at low sensitivity: this was of importance in patients with De Quervain’s subacute thyroiditis in its acute phase, when radionuclide uptake was not enough to produce adequate scintiphotos (Figure 11). In patients with Hashimoto’s thyroiditis, the method provided no additional information, except that extension of the gland could be better eval-
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f C
Figure 3. Large simple cyst of the right lobe. a-c, B-scan at low, intermediate and h@h sensitivity, respectively. The nodule clearly remains echo-free; d, scintiphoto; e, A-scan at low sensitivity; f, A-scan at high sensitivity, showing absence of echoes in the nodule; g, schematic representation of (a); C = calcified area in the cyst wail; h, crosssection through the operative specimen at the level of investigation.
T
LL
S
h
uated. The method was of some value in the followup of these patients. COMMENTS
Clinical Value.
RL(N)
In common with others [6-141, we believe that the most important contribution of ultrasonography to clinical thyroidology lies in differentiating between solid and cystic solitary hypofunctioning nodules. In our series, simple cysts and solid nodules were correctly diagnosed in 90 per cent of the cases; on the other hand, only 22 of 40 partly cystic lesions were diagnosed as such (Table I). However, in all but five of the incorrectly classified cases, the diameter of the cystic lesion was less than 1.5 cm. In
our experience, cystic lesions under 1.0 to 1.5 cm in diameter cannot be detected with this method. Differentiating between solid and cystic nodules is of practical importance because completely cystic nodules only very rarely harbor malignancy [2 I]. We found no malignancy in any of the cystic nodules, but malignancy was found in four (10 per cent) of the partially cystic and in 21 (23 per cent) of the solid nodules. All four malignant, partly cystic nodules were described as cystic degenerations of the tumor. Cystic or hemorrhagic degeneration in larger thyroid masses, either benign or malignant, is not rare [lo]. Although use of the A-scan for differentiating between cystic and solid nodules has been described
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RL(N)
T
LL
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S
WIENER
e
b
Figure 4. Colloid nodule with central cystic degeneration in the right lobe. a, B-scan at low sensitivity; b, schematic representation of (a); c, B-scan at high sensitivity showing a small echo-free area within the nodule; d, operative specimen (right lobe); e, A-scan at low sensitivity; f, A-scan at high sensitivity, showing a central cystic area: g, scintiphoto.
d
[9. IO], most investigators use the B-scan for this purpose [4,6,8,12,13,15]. In common with Rasmussen et al. [ 71, we obtained the best results when the A-mode and B-mode technics were combined (see “Results”). In our hands, differentiating between malignant and benign solid nodules, as suggested by some investigators [4,5], was not possible. This is in agreement with the experience of other workers, who used conventional technics [6,11,15]. Recently, two reports have appeared on the use of gray scale echography for differentiating benign from malignant solid thyroid nodules, with promising results [22,23]. The pattern seen within malignant nodules was described as one of low amplitude, sparse and disordered echoes at standard sensitivity. In our limited series of malignant nodules, low amplitude echoes were observed on the A-scan as well, but not in all cases. Besides, a similar phenomenon was seen in 100
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patients with subacute and chronic thyroiditis and in patients with Graves’ disease. Therefore, the results with the gray scale technic must await further confirmation with larger series of patients. Further differentiation as to histologic type within the group of benign solid nodules proved equally impossible in our series. The practical consequences of our results are that purely cystic lesions may be treated by thin needle puncture with aspiration and cytologic examination of the cyst fluid, thereby obviating the need for an operation. Several investigators have reported satisfactory results with this policy [ 15,24,25]. Besides, the cause of a rapid enlargement of a nodule can be evaluated by this method as hemorrhage produces a (partially) cystic pattern [ 111. In all nonpurely cystic nodules, especially completely solid hypofunctioning nodules, a substantial risk of malignancy exists, figures ranging roughly from IO to 30 per cent in operated series [21,26-301. Patients in this group may
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nodule
VB
e
b
Figure 5. Follicular carcinoma in the right lobe. a-b, B-scan at low and high sensitivity; c, schematic representation of (a); d-e, A-scan at low and high sensitivity; 1, scintiphoto. From the B-scan at high sensitivity a central cystic degeneration in the nodule may be presumed, but the A-scan at high sensitivity clearly shows that the nodule is solid.
WIENER
RL(N)T
LL
S
C
a
Figure 6. Large solid colloid nodule in the right lobe presenting on the scintiphoto as a warm area. a-c, B-scan at low, intermediate and high sensitivity, respectively; d-e, A-scan at low and high sensitivity; f, schematic representation of (a); g, scintiphoto. Combination of B-scan and scintiphoto proves the nodule to be hypofunctioning per unit volume. January 1976
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7. Hypofunctioning nodule in the right lobe. a, B-scan at low sensitivity; b, schematic representation of (a); c, scintiphoto. The examination was repeated 2 years later (d-f); d, B-scan at low sensitivity; e, schema tic representation of (d); f, scintiphoto. As can be seen the nodule has increased in size. The patient was operated upon and the pathologic diagnosis was papillary carcinoma. Note: B-scans at high sensitivi-
Figure b
ty (proving nodule to be solid) not shown here.
_I
a
Flgure 8. Toxic nodule of the left lobe. a-c, B-scan at low, intermediate and high sensitivity; d-e, A-scan at low and f, schematic represenhigh sensitivity tation of (a); g, scintiphoto. The suppressed right lobe is cfearly visible on the B-scan and not on the scintiphoto.
be selected
for surgery
by relevant
clinical criteria
[151. Measuring the depth of a nodule is not possible by any method other than ultrasonography [9,10, 16,181. As the scintiphoto is only a two-dimensional representation of the spatial distribution of the radionuclide in the gland, adding the third dimension by means of ultrasonography may lead to a better functional classification of nodules. By combining both
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technics, scintigraphically isoactive or nondelineated nodules may be shown to be hypofunctioning per unit volume [ 181. Whether in such a case the activity seen on the scintiphoto at the site of the nodule is contained in the nodule itself or mainly stems from normal tissue overlying the nodule [31] cannot be determined in this way; in the latter case, the “isoactive” nodule may even be completely nonfunctioning (similarly, a scintigraphically hypofunctioning nodule
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may actually be nonfunctioning). Addition of ultrasonography to scintiphotography thus sensibly improves the recognition of hypofunctioning nodules. Measuring the size of nodules repeatedly in patients left untreated is of great importance, as growth of a hypofunctioning noncystic nodule is an absolute indication for operation. Besides, documenting the size of nodules in patients receiving suppressive therapy is useful [ 11,181. Palpation has been shown to be rather inaccurate in this respect [32]. In patients with hyperfunctioning nodules, ultrasonography may disclose the presence of a suppressed contralateral lobe [6,16,18]. This obviates the need for a repeat scintiphoto after the administration of thyroid stimulating hormone, although, strictly speaking, ultrasonography does not prove that this suppressed tissue is able to function. Furthermore, cystic degeneration within a hyperfunctioning nodule [33,34], although often suspected from the scintiphoto, can be proved only by ultrasonography [16,35]; the clinical implication of such a finding is uncertain. Finally, the method may be of some value in follow-up of patients with hyperfunctioning nodules who are left untreated. Theoretically this technic offers the possibility of a better estimation of thyroid weight, which is of importance in radioiodine therapy for Graves’ disease [6,10,16]. However, Hansen et al. [ 361 and Leclere et al. [37] have shown that with the presently available equipment the technic is far from satisfactory in this respect. Both groups of investigators agree that volume measurements of cysts appear feasible. In patients with nontoxic goiter receiving suppressive therapy, ultrasonographic measurements of goiter size can be used in the follow-up [ 371. Finally, ultrasonography can be helpful in cases in which scintiphotography is impossible, gives poor results (as in iodine contamination) or is contraindicated (as in pregnancy). The size of a nodule or of the thy-
WIENER
c
&we 9. Graves ’ disease. a-c, B-scan at low, intermedi ate and high sensitivity, respectively; d-e, A-scan at low and high sensitivity; f, schematic representation of (a): g, scintiphoto.
-l
nodule
roid as a whole can be measured in these cases [6,16], and the solid or cystic nature of a nodule can be determined.
Limitations of the Method. The method has its limitations, which are partly inherent to the technic itself. In a few cases in our series, it was not possible to depict the gland or a nodule properly, especially its lateral border. This might be due to the fact that the transducer only detects objects that are hit perpendicularly by the ultrasonic beam, which in the complex anatomy of the neck is not always the case. In our experience, the use of the compound scanning technic reduces the number of failures. Secondly, the ultrasonogram only gives information about one transversal plane. Of course, the investigation can be carried out at several transversal
e RL
TN
LL
S
f
J Figure 10. Toxic multinodular goiter. a-c, B-scan at low, intermediate and high sensitivity, respectively. At (b) many irregular echoes are visible and at (c) small areas remain echo-free. d-e, A-scan at low and high sensitivity; f, schematic representation of (a); g, scintiphoto.
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c
S
RL
T
Figure II. Subacute thyroid& (De Quervain) in its acute phase (a, c, e) and after recovery (b, 4 f). a, B-scan at low sensitivity: b, B-scan at low sensitivity two months later; c, schematic representation of (a); d, schematic representatfon of (b); e, scintiphoto showing absence of uptake; f, scintiphoto two months later. Note: B-scans at high sensitivity not shown.
LL
b
Finally, artifacts sometimes may give rise to confusing pictures. In our experience, the main source of artifacts in direct contact scanning is caused by losing skin contact, which should be avoided. Besides, areas of calcification may reflect most of the ultrasonic energy, thereby causing a more or less echofree area behind these structures. Other sources of artifacts have been discussed by Robinson et al.
or other planes, but this is more time-consuming. Sometimes, however, this procedure is desirable and gives ancillary information. Thirdly, the spatial resolution of the technic is limited in that nodules smaller than 1 cm in diameter escape detection [ 4,151. Neither can cystic lesions, not surpassing 1.0 cm in diameter, be detected in larger nodules. Use of transducers with higher frequencies and a narrower beam may improve the resolution. Apart from that, it is sometimes very difficult to ascertain whether a nodule is completely or only partially cystic. Combination with the scintiphoto is always necessary to compare the size of the hypofunctioning area with the size of the cystic part on the ultrasonogram. Even then, this distinction is not
CONCLUSIONS
always possible. We found failure to detect cysts to be sometimes attributable to the presence of blood clots or other solid material in the cyst. In the fourth place, the ultrasonogram at low sensitivity shows the thyroid tissue as a whole in the plane selected and, strictly speaking, a distinction between normal thyroid tissue and nodules is impossible, unless the nodule is surrounded by a distinct capsule or harbors calcified areas. At high sensitivity, this dis-
Diagnostic ultrasound is a safe, reliable and easily repeatable noninvasive method that may give valuable additional information in clinical thyroid investigation. It can differentiate with a reasonably high degree of accuracy between cystic and solid nodules. This is by far its most important contribution, because cystic nodules are nearly always benign. It should be
tinction can only be made when the acoustic properties of the nodule clearly differ from those of normal thyroid tissue, which in our experience is only the case in cystic lesions. In the fifth place, from the ultrasonogram per se there is no certainty that a depicted nodule actually is a thyroid nodule. Cysts from nonthyroidal origin, e.g., branchiogenic cysts, may show the same ultrasonic characteristics as thyroidal cysts. Also, nonthyroidal solid nodules, like parathyroid tumors, glomus tumors and lymph nodes, possess acoustic properties similar to those of thyroidal solid nodules. The method has not been useful with substernal thyroid masses [ 111. 104
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[381. From our experience we conclude that diagnostic ultrasound is a valuable, but only additional, diagnostic tool, not replacing other established methods.
stressed that with the conventional technic differentiating between benign and malignant solid nodules is not possible. It adds a third dimension to the two-dimensional scintiphoto which may lead to a better functional classification of nodules and improves the detection of hypofunctioning nodules. It may disclose the presence of the suppressed lobe in case of a toxic nodule. In Graves’ disease the method may be of value for a better estimation of thyroid weight. In multinodular goiter the extension of the gland can be better evaluated when ultrasonography is
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ULTRASONIC EXAMINATICN OF THE THYRCUI GLAND-THUS, WIENER
carried out in combination with palpation and scintiphotgraphy. lt offers the possibility to follow the size of a nodule or the thyroid as a whole in course of time in an objective way, independent of the functional status. It may visualize nonfunctioning thyroid nodules, situated mainly outside the normal thyroid configuration
and therefore not visible on the scintiphoto. Besides, the size of such nodules can be measured and their solid or cystic nature established. When scintiphotography is not possible or gives poor results (pregnancy. exogenous iodine contamination) ultrasonography may be carried out with the advantages mentioned.
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evaluation of hypofunctioning thyroid nodules (abstract). lsr J Med Sci 8: 1879, 1972. Donald I: Ultrasonics in obstetrtcs. Br Med Bull 24: 71, 1968. Melliere D, Massin JP. Calmettes C, Chigot JP, Savoie JC, Gamier H: Le risque de malignite des nodules frokls thyroidbns. A propos de 607 cas op&s. Presse M&i 78: 311,197O. Cracker EF, McLaughlin AF, Kossoff 0, Jellins J: The gray scale echographic appearance of thyroid malignancy. J Clin Ultrasound 2: 305, 1974. Taylor KJW, Carpenter DA, Barrett JJ: Gray scale uitrasonography in the diagnosis of thyrokl swellings. J Clin UC trasound 2: 327, 1974. Crile G Jr: Treatment of thyroid cysts by aspiration. Surgery 59: 210. 1966. Miller JM. Zafar SU: The cystic thyrok! nodule: recognition and management. Programme of the 46th Annual Meeting of the American ThyroM Association, Chicago, September 20-23,1972. Koutras DA, Liiadas D, Sfontouris J, Messaris G, Statherou PK: A study of 408 cotd thyroid nodules in a country with endemic goitre. Nucl-Med (Stuttgt) 7: 165. 1968. Cassano C: Thyroid tumours: diagnostic and therapeutic problems. Folia Endocrinol (Roma) 21: 655, 1968. Jackson IMD, Thomson JA: The relationshlp of carcinoma to the single thyroid nodule. Br J Surg 54: 1907, 1967. Psarras A, Papadopoubs SN, Livadas D, Pharmakeotis AD, Koutras DA: The single thyroid nodule. Br J Surg 59: 39. 1972. Perimutter M, Slater SL. Attii J: Method for preoperative differentiation between the benign and the possibly malignant solitary nontoxic thyrold nodule. J Clin Endocrinoi 14: 672, 1954. Miller JM, Hamburger Ji, Mellinger RC: The thyroid scintii gram. Ii. The CON nodule. Radblosy 85: 702, 1965. Mortensen JD, Woolner LB, Bennett WA: Gross and mkroscopic findings in clinically normal thyroid glands. J Ciin Endocrinol 15: 1270, 1955. Silverstein GE, Burke G, Cogan R: The natural history of the autonomous hyperfunctioning thyrokl nodule. Ann Intern Med 67: 539, 1967. Decourt,J, Savoie JC, de Gennes JL. Jungers P: L’adenome thyrokiien toxique, a la IumPe des explorations par I’iode radioactif. Sem Hbp Paris 38: 3317, 1962. Blum M, Nocero Jr MA: Spontaneous resolution of a euthyroM autonomous nodule of the thyroid. Am J Med Sci 264: 49.1972. Hansen JM, Kampmann J, Madsen SN, Sotgaard S, Grytter C. Rasmussen SN: Determination of thyrokl volume by ultrasonic scanning (abstract). Endocrinobgii Experirnentalis 8: 223. 1974 Leclere J. Bertrand A, Thouvenot P, Vaillant D: Mesure du volume thy&&n a I’akie des ultrasons. Ann Endocrinol (Paris) 35: 48, 1974. Robinson DEG, Kossoff G, Garrett WJ: Artefacts in uitrasonic echoscopic visualization. Uftrasonics 4: 186, 1966.
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18. Schiebler GL, Van Mieron LHS, Krovetz LJ: Diseases of the tricuspid valve, chap 2. Heart Disease in Infants, Children and Adolescents (Moss AJ, Adams F, eds), Baltimore, Williams & Wilkins, 1968. For book references
For periodical
references:
22. Theologides A, Kennedy BJ: Toxoplasmic myocarditis and pericarditis. Am J Med 47: 169, 1969.
(with chapter):
(without
13. Berne E: Principles York, Oxford University Authors are responsible erences.
chapter):
of Group Treatment, Press, 1966, p 26.
for the accuracy
New
of the ref-
preparation of illustrations and tables Illustrations must be black and white glossy prints or professional drawings in india ink; they should be unmounted. The name of the lead author and the title of the article should be typed on a label and affixed to the back of each illustration; the top should be indicated. Reference to all illustrations should be inserted in the text in consecutive order. Legends for the illustrations should be typed, double spaced, on a separate sheet with numbers corresponding to those on the photographs or drawings. They should not be attached to the pictures.
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reprints Price schedules and order mailed to each contributor.
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106
January 1976
10019
The Am&can
Journal ol Medklno
Voluma 60
Ultrasonic
Examination
of the Thyroid Gland
Possibilities and Limitations
L. G. THIJS, M.D. J. D. WIENER, Ph.D. Amsterdam, The Netherlands
In 440 patients with various thyroid disorders scintiphotography and ultrasonography were carried out. For ultrasonic examination both the A-mode and B-mode display technics were employed. Included in the study were 324 patients with hypofunctioning solitary nodules; a histopathologic dlagnosis could be obtained in 151 of these. The method proved to be especially valuable for differentiating between solid and cystic nodules. This is of practical importance because completely cystic nodules are nearly always benign and may be treated by thin needle puncture with aspiration of the cyst fluid. In addition, ultrasonography is of some value in making a better functional classification of nodules, better estimating the size of the thyroid and in the follow-up of patients with various thyroid disorders who are under treatment or untreated. Differentiating between benign and malignant solid nodules was not possible with the technic used. The examination can be safely carried out in pregnancy. The limitations of the technic are discussed. As early as 1955 Howry and co-workers [l] predicted that, concerning the use of ultrasound, “the method will probably outline areas of different density, such as adenomas and cystic degenerations within the thyroid gland. A series of such pictures at different levels makes it possible to determine the volume of the gland.” Donald [2] actually showed that visualization of the thyroid by means of ultrasound was possible. However, Yamakawa and Naito [3] were supposedly the first to practice this technic. Since then, several reports on this subject have appeared [4-191. Although these investigations differed in many respects concerning, e.g.,
equipment and performance, the conclusions were surprisingly similar. Now, 20 years after Howry’s paper, it seems worthwhile to reassess the clinical value of diagnostic ultrasound in evaluating thyroid gland pathology on the basis of our own experience and relevant data from the literature.
MATERIALS AND METHODS From the Department of Internal Medicine, Free University Hospital, Amsterdam, The Netherlands. Requests for reprints should be addressed to Dr. L. G. Thijs. Department of Internal Medicine, Free University Hospital, De Boelelaan 1117, Amsterdam 101 I, The Netherlands. Manuscript accepted July 25, 1975.
96
January 1976
Included in this study were 440 patients who were referred of Nuclear
Medicine
of our Department
tion and for thyroid scanning.
Ultrasonic
for the evaluation investigations
to the section of thyroid func-
were
carried
out
with the Diasonograph (Type NE 4101, Nuclear Enterprises Ltd.), provided with a 2.5 MHz transducer. The examination was always performed with the patient in the sitting position after scintiphotography
The American Journal of Medlcine
Volume 60
and after careful
ULTRASONIC EXAMINATION OF THE THYROID GLAND-THUS.
WIENER
palpation of the gland [ 181. Both the A-mode and B-mode display technics were employed with a variable sensitivity as an essential
part of the procedure.
The examination was started with a B-scan at low sensitivity, using the compound scanning technic [20], which produced a cross section through the neck in a transversal plane. This procedure was repeated at higher sensitivities. After completion of the B-scans, A-scans were made at low and high sensitivity at regions of interest, e.g., nodules. Both low and high sensitivity settings of the apparatus were empirically found [ 171. At high sensitivity, cystic lesions remained echo-free, whereas solid nodules were completely filled up by echoes. Thyroid function was assessed with standard technics, including ‘311-uptake studies. A diagnosis was made on clinical, laboratory and scintiphotographic evidence. A histopathologic diagnosis was obtained in 199 patients who were either operated on or subjected to biopsy.
%. -
d RL
T
LL
s
.&’ t b
RESULTS Figure 1 shows a normal thyroid gland for reference. Both lobes and sometimes also the isthmus appeared on the B-scan at low sensitivity as an echofree area between the neighboring structures which gave rise to distinct echoes. The anterior wall of the
trachea, the skin, the cervical spine, the vascular sheaths and sometimes the sternomastoid muscle were visible. With rising sensitivities, echoes also appeared within the thyroid. Hypofunctioning Solitary Nodules (324 patients). nodules were outlined on Solitary hypofunctioning the B-scan at low sensitivity in almost all cases. In a solid nodule, echoes sometimes appeared at intermediate sensitivity: at high sensitivity, these nodules were generally completely filled up, whereas cystic nodules remained echo-free both on the A- and on the B-scan (Figures 2 to 6). In a partially cystic nodule, echoes were absent in part of the nodule on the A- and on the B-scan at high sensitivity (Figure 4). In cystic nodules the structures behind the cyst were readily discernible even at low sensitivity. The absorption of ultrasonic energy in cystic lesions was apparently less than in solid lesions. Calcified lesions produced strong echoes at low sensitivity (Figure 3). A pathologic diagnosis was obtained in 151 patients. In Table I the gross pathologic findings are compared with the preoperative ultrasonic diagnosis. The diagnosis was correct in 19 of 21 simple cysts, l
in 82 of 90 solid nodules, but in only 22 of 40 partially cystic nodules. To obtain the best results, we found it essential to combine the A-mode and B-mode technics. With the
In most cases it cannot be ascertained whether these nodules were hypofunctioning or actually nonfunctioning (see “Comments”). For the sake of simplicity, the term “hypofunctioning” is used throughout this text. l
1
e
Figure 1. Normal thyroid g/and. a, B-scan at low sensitivity; b, scintiphoto, the arrows indicate markers on thyroid cartilage and sternal notch. The dashed line represents the level where the ultrasonic examination was carried out; c, B-scan at intermediate sensitivity; d, B-scan at high sensitivity; e, schematic representation of (a): RL = right lobe, LL = left lobe, T = anterior wall trachea, S = skin, VB = vertebral body, V = vascular sheath.
B-scan at low sensitivity, the nodule could be depicted and its localization in relation to the surrounding structures established. At high sensitivity, places with “filling defects” could be detected, and the place and direction of the A-scan chosen more accurately. The A-scan is only one-dimensional, but in general it gave more detailed information about the inner structures of the nodule. Therefore, the diagnosis solid or cystic was best made by the A-scan at high sensitivity (Figure 5).
TABLE I
Comparison of Preoperative Ultrasonic Diagnosis and Gross Pathologic Findings UltrasonicDiagnosis
Pathologic Diagnosis Solid Mixed solid-cystic Cystic Total
January 1976
Partially Cystic Cystic
Uncertain
Total
Solid
(no.)
(no.)
(no.)
90 40
82 15
2 22
:::
6 3
21 151
9;’
1 25
19 19
1 10
The Amerkan Journalof Medklne
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ULTRASONG
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WIENER
e
b
C
f
Figure 2. Solid coid nodule in the left lobe; pathologic examination: colloid nodule. a-c, B-scan at low, intermediate and high sensitivity, respective/y; d, A-scan at low sensitivity in the direction indicated in (a) as a dotted line; E emission signal; e, A-scan at h@h sensitivity; f, schematic representation of (a): N = nodule; g, scintiphoto, the circle indicates the place of the palpated nodule.
‘5cm’
With correct calibration of the apparatus, the depth of a nodule could be measured from the ultrasonogram at low sensitivity. When a nodule either
scintiphoto, ultrasonography of this lobe (Figure 8).
appeared on the scintiphoto as an isoactive (“warm”) area (24 patients), or was not delineated at all (16 patients), ultrasonography usually disclosed its presence and proved that it was in fact hypofunctioning per unit volume, because it was thicker than the extranodular normal thyroid tissue (Figure 6). Palpated nonfunctioning nodules situated mainly outside the functioning thyroid tissue, e.g., in thyroglossal remnants, cannot be visualized by scintiphotography. By means of ultrasonography, their presence could be ascertained, their size measured and their cystic or solid nature established (12 patients). Finally, the size of nodules could be measured repeatedly in course of time, and changes in size could be noted in an objective way (Figure 7). Hyperfunctioning Nodules (41 patients). Solitary hyperfunctioning (“hot”) nodules, either with or without functional suppression of normal thyroid tissue, could be visualized by ultrasonic scanning as well. They presented in the same way as hypofunctional nodules, their acoustic properties apparently being similar. In case of complete suppression of the normal lobe, which therefore failed to appear on the
in diffuse nontoxic goiter, the enlarged lobes and isthmus were depicted at low sensitivity. At higher sensitivities, finely dispersed discrete echoes were reflected from the interior of the gland; at high sensitivity, the whole gland was filled up (Figure 9). Sometimes, only low amplitude echoes appeared on the A-scan at high sensitivity. Multinodular Goiter (31 patients). In many patients with toxic or nontoxic goiter, the B-scan showed the
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1976
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Journal
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Diffuse Goiter (35 patients).
disclosed the presence In Graves’ disease and
thyroid to be much more enlarged than was apparent from palpation or scintiphoto alone (Figure 10). A preoperative ultrasonogram was of value for the surgeon. Echoes from calcified sensitivities.
within the gland, sometimes arising areas, were visible at relatively low
Thyroiditis (nine patients).
The gland was depicted on the B-scan at low sensitivity: this was of importance in patients with De Quervain’s subacute thyroiditis in its acute phase, when radionuclide uptake was not enough to produce adequate scintiphotos (Figure 11). In patients with Hashimoto’s thyroiditis, the method provided no additional information, except that extension of the gland could be better eval-
Volume 60
ULTRASONIC EXAMINATION OF THE THYROID GLAND-THUS,
WIENER
f C
Figure 3. Large simple cyst of the right lobe. a-c, B-scan at low, intermediate and h@h sensitivity, respectively. The nodule clearly remains echo-free; d, scintiphoto; e, A-scan at low sensitivity; f, A-scan at high sensitivity, showing absence of echoes in the nodule; g, schematic representation of (a); C = calcified area in the cyst wail; h, crosssection through the operative specimen at the level of investigation.
T
LL
S
h
uated. The method was of some value in the followup of these patients. COMMENTS
Clinical Value.
RL(N)
In common with others [6-141, we believe that the most important contribution of ultrasonography to clinical thyroidology lies in differentiating between solid and cystic solitary hypofunctioning nodules. In our series, simple cysts and solid nodules were correctly diagnosed in 90 per cent of the cases; on the other hand, only 22 of 40 partly cystic lesions were diagnosed as such (Table I). However, in all but five of the incorrectly classified cases, the diameter of the cystic lesion was less than 1.5 cm. In
our experience, cystic lesions under 1.0 to 1.5 cm in diameter cannot be detected with this method. Differentiating between solid and cystic nodules is of practical importance because completely cystic nodules only very rarely harbor malignancy [2 I]. We found no malignancy in any of the cystic nodules, but malignancy was found in four (10 per cent) of the partially cystic and in 21 (23 per cent) of the solid nodules. All four malignant, partly cystic nodules were described as cystic degenerations of the tumor. Cystic or hemorrhagic degeneration in larger thyroid masses, either benign or malignant, is not rare [lo]. Although use of the A-scan for differentiating between cystic and solid nodules has been described
January 1976
The American Journal of Medlclne
Volume 60
S9
ULTRASONIC
EXAMINATION
RL(N)
T
LL
OF THE THYROID GLAND-THIJS,
S
WIENER
e
b
Figure 4. Colloid nodule with central cystic degeneration in the right lobe. a, B-scan at low sensitivity; b, schematic representation of (a); c, B-scan at high sensitivity showing a small echo-free area within the nodule; d, operative specimen (right lobe); e, A-scan at low sensitivity; f, A-scan at high sensitivity, showing a central cystic area: g, scintiphoto.
d
[9. IO], most investigators use the B-scan for this purpose [4,6,8,12,13,15]. In common with Rasmussen et al. [ 71, we obtained the best results when the A-mode and B-mode technics were combined (see “Results”). In our hands, differentiating between malignant and benign solid nodules, as suggested by some investigators [4,5], was not possible. This is in agreement with the experience of other workers, who used conventional technics [6,11,15]. Recently, two reports have appeared on the use of gray scale echography for differentiating benign from malignant solid thyroid nodules, with promising results [22,23]. The pattern seen within malignant nodules was described as one of low amplitude, sparse and disordered echoes at standard sensitivity. In our limited series of malignant nodules, low amplitude echoes were observed on the A-scan as well, but not in all cases. Besides, a similar phenomenon was seen in 100
January 1976
The American Journal of Medicine
patients with subacute and chronic thyroiditis and in patients with Graves’ disease. Therefore, the results with the gray scale technic must await further confirmation with larger series of patients. Further differentiation as to histologic type within the group of benign solid nodules proved equally impossible in our series. The practical consequences of our results are that purely cystic lesions may be treated by thin needle puncture with aspiration and cytologic examination of the cyst fluid, thereby obviating the need for an operation. Several investigators have reported satisfactory results with this policy [ 15,24,25]. Besides, the cause of a rapid enlargement of a nodule can be evaluated by this method as hemorrhage produces a (partially) cystic pattern [ 111. In all nonpurely cystic nodules, especially completely solid hypofunctioning nodules, a substantial risk of malignancy exists, figures ranging roughly from IO to 30 per cent in operated series [21,26-301. Patients in this group may
Volume 60
ULTRASONIC EXAMINATION OF THE THYROID GLAND-THUS,
nodule
VB
e
b
Figure 5. Follicular carcinoma in the right lobe. a-b, B-scan at low and high sensitivity; c, schematic representation of (a); d-e, A-scan at low and high sensitivity; 1, scintiphoto. From the B-scan at high sensitivity a central cystic degeneration in the nodule may be presumed, but the A-scan at high sensitivity clearly shows that the nodule is solid.
WIENER
RL(N)T
LL
S
C
a
Figure 6. Large solid colloid nodule in the right lobe presenting on the scintiphoto as a warm area. a-c, B-scan at low, intermediate and high sensitivity, respectively; d-e, A-scan at low and high sensitivity; f, schematic representation of (a); g, scintiphoto. Combination of B-scan and scintiphoto proves the nodule to be hypofunctioning per unit volume. January 1976
The American Journal of Medicine
Volume SO
101
I ILTRASONIC
EXAMINATION
OF
THE
THYROID GLAND-THUS. WIENER
7. Hypofunctioning nodule in the right lobe. a, B-scan at low sensitivity; b, schematic representation of (a); c, scintiphoto. The examination was repeated 2 years later (d-f); d, B-scan at low sensitivity; e, schema tic representation of (d); f, scintiphoto. As can be seen the nodule has increased in size. The patient was operated upon and the pathologic diagnosis was papillary carcinoma. Note: B-scans at high sensitivi-
Figure b
ty (proving nodule to be solid) not shown here.
_I
a
Flgure 8. Toxic nodule of the left lobe. a-c, B-scan at low, intermediate and high sensitivity; d-e, A-scan at low and f, schematic represenhigh sensitivity tation of (a); g, scintiphoto. The suppressed right lobe is cfearly visible on the B-scan and not on the scintiphoto.
be selected
for surgery
by relevant
clinical criteria
[151. Measuring the depth of a nodule is not possible by any method other than ultrasonography [9,10, 16,181. As the scintiphoto is only a two-dimensional representation of the spatial distribution of the radionuclide in the gland, adding the third dimension by means of ultrasonography may lead to a better functional classification of nodules. By combining both
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technics, scintigraphically isoactive or nondelineated nodules may be shown to be hypofunctioning per unit volume [ 181. Whether in such a case the activity seen on the scintiphoto at the site of the nodule is contained in the nodule itself or mainly stems from normal tissue overlying the nodule [31] cannot be determined in this way; in the latter case, the “isoactive” nodule may even be completely nonfunctioning (similarly, a scintigraphically hypofunctioning nodule
Volume 60
ULTRASONIC EXAMINATION OF THE THYROID GLAND-THUS,
may actually be nonfunctioning). Addition of ultrasonography to scintiphotography thus sensibly improves the recognition of hypofunctioning nodules. Measuring the size of nodules repeatedly in patients left untreated is of great importance, as growth of a hypofunctioning noncystic nodule is an absolute indication for operation. Besides, documenting the size of nodules in patients receiving suppressive therapy is useful [ 11,181. Palpation has been shown to be rather inaccurate in this respect [32]. In patients with hyperfunctioning nodules, ultrasonography may disclose the presence of a suppressed contralateral lobe [6,16,18]. This obviates the need for a repeat scintiphoto after the administration of thyroid stimulating hormone, although, strictly speaking, ultrasonography does not prove that this suppressed tissue is able to function. Furthermore, cystic degeneration within a hyperfunctioning nodule [33,34], although often suspected from the scintiphoto, can be proved only by ultrasonography [16,35]; the clinical implication of such a finding is uncertain. Finally, the method may be of some value in follow-up of patients with hyperfunctioning nodules who are left untreated. Theoretically this technic offers the possibility of a better estimation of thyroid weight, which is of importance in radioiodine therapy for Graves’ disease [6,10,16]. However, Hansen et al. [ 361 and Leclere et al. [37] have shown that with the presently available equipment the technic is far from satisfactory in this respect. Both groups of investigators agree that volume measurements of cysts appear feasible. In patients with nontoxic goiter receiving suppressive therapy, ultrasonographic measurements of goiter size can be used in the follow-up [ 371. Finally, ultrasonography can be helpful in cases in which scintiphotography is impossible, gives poor results (as in iodine contamination) or is contraindicated (as in pregnancy). The size of a nodule or of the thy-
WIENER
c
&we 9. Graves ’ disease. a-c, B-scan at low, intermedi ate and high sensitivity, respectively; d-e, A-scan at low and high sensitivity; f, schematic representation of (a): g, scintiphoto.
-l
nodule
roid as a whole can be measured in these cases [6,16], and the solid or cystic nature of a nodule can be determined.
Limitations of the Method. The method has its limitations, which are partly inherent to the technic itself. In a few cases in our series, it was not possible to depict the gland or a nodule properly, especially its lateral border. This might be due to the fact that the transducer only detects objects that are hit perpendicularly by the ultrasonic beam, which in the complex anatomy of the neck is not always the case. In our experience, the use of the compound scanning technic reduces the number of failures. Secondly, the ultrasonogram only gives information about one transversal plane. Of course, the investigation can be carried out at several transversal
e RL
TN
LL
S
f
J Figure 10. Toxic multinodular goiter. a-c, B-scan at low, intermediate and high sensitivity, respectively. At (b) many irregular echoes are visible and at (c) small areas remain echo-free. d-e, A-scan at low and high sensitivity; f, schematic representation of (a); g, scintiphoto.
January 1976
The American Journal of Medicine
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ULTRASONIC
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WIENER
c
S
RL
T
Figure II. Subacute thyroid& (De Quervain) in its acute phase (a, c, e) and after recovery (b, 4 f). a, B-scan at low sensitivity: b, B-scan at low sensitivity two months later; c, schematic representation of (a); d, schematic representatfon of (b); e, scintiphoto showing absence of uptake; f, scintiphoto two months later. Note: B-scans at high sensitivity not shown.
LL
b
Finally, artifacts sometimes may give rise to confusing pictures. In our experience, the main source of artifacts in direct contact scanning is caused by losing skin contact, which should be avoided. Besides, areas of calcification may reflect most of the ultrasonic energy, thereby causing a more or less echofree area behind these structures. Other sources of artifacts have been discussed by Robinson et al.
or other planes, but this is more time-consuming. Sometimes, however, this procedure is desirable and gives ancillary information. Thirdly, the spatial resolution of the technic is limited in that nodules smaller than 1 cm in diameter escape detection [ 4,151. Neither can cystic lesions, not surpassing 1.0 cm in diameter, be detected in larger nodules. Use of transducers with higher frequencies and a narrower beam may improve the resolution. Apart from that, it is sometimes very difficult to ascertain whether a nodule is completely or only partially cystic. Combination with the scintiphoto is always necessary to compare the size of the hypofunctioning area with the size of the cystic part on the ultrasonogram. Even then, this distinction is not
CONCLUSIONS
always possible. We found failure to detect cysts to be sometimes attributable to the presence of blood clots or other solid material in the cyst. In the fourth place, the ultrasonogram at low sensitivity shows the thyroid tissue as a whole in the plane selected and, strictly speaking, a distinction between normal thyroid tissue and nodules is impossible, unless the nodule is surrounded by a distinct capsule or harbors calcified areas. At high sensitivity, this dis-
Diagnostic ultrasound is a safe, reliable and easily repeatable noninvasive method that may give valuable additional information in clinical thyroid investigation. It can differentiate with a reasonably high degree of accuracy between cystic and solid nodules. This is by far its most important contribution, because cystic nodules are nearly always benign. It should be
tinction can only be made when the acoustic properties of the nodule clearly differ from those of normal thyroid tissue, which in our experience is only the case in cystic lesions. In the fifth place, from the ultrasonogram per se there is no certainty that a depicted nodule actually is a thyroid nodule. Cysts from nonthyroidal origin, e.g., branchiogenic cysts, may show the same ultrasonic characteristics as thyroidal cysts. Also, nonthyroidal solid nodules, like parathyroid tumors, glomus tumors and lymph nodes, possess acoustic properties similar to those of thyroidal solid nodules. The method has not been useful with substernal thyroid masses [ 111. 104
January 1976
The American Journal of Medicine
[381. From our experience we conclude that diagnostic ultrasound is a valuable, but only additional, diagnostic tool, not replacing other established methods.
stressed that with the conventional technic differentiating between benign and malignant solid nodules is not possible. It adds a third dimension to the two-dimensional scintiphoto which may lead to a better functional classification of nodules and improves the detection of hypofunctioning nodules. It may disclose the presence of the suppressed lobe in case of a toxic nodule. In Graves’ disease the method may be of value for a better estimation of thyroid weight. In multinodular goiter the extension of the gland can be better evaluated when ultrasonography is
Volume 60
ULTRASONIC EXAMINATICN OF THE THYRCUI GLAND-THUS, WIENER
carried out in combination with palpation and scintiphotgraphy. lt offers the possibility to follow the size of a nodule or the thyroid as a whole in course of time in an objective way, independent of the functional status. It may visualize nonfunctioning thyroid nodules, situated mainly outside the normal thyroid configuration
and therefore not visible on the scintiphoto. Besides, the size of such nodules can be measured and their solid or cystic nature established. When scintiphotography is not possible or gives poor results (pregnancy. exogenous iodine contamination) ultrasonography may be carried out with the advantages mentioned.
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LISHER. STATEMENTS CONTAINED THEREIN ARE THE RESPONSIBILITY OF THE AUTHOR. THE PUBLISHER RESERVES COPYRIGHT AND RENEWAL ON ALL PUBLISHED MATERIAL AND SUCH MATERIAL MAY NOT BE REPRODUCED IN ANY FORM WITHOUT THE WRITTEN PERMISSION OF THE PUBLISHER.
preparation of manuscripts Manuscripts should be typed on one side of the sheet, double-spaced, on white bond paper, 81/z by 11 inches, with margins of 1 inch. The original and a duplicate (preferably a Xerox copy) of the manuscript and illustrations should be sent to the Editor at 666 Fifth Ave., New York, N.Y. 10019. Title page should inclulde full name, degrees and affiliation of all authors, arrd the name and address of person to whom requests for reprints should be addressed.
All manuscript pages and tables should be numbered consecutively in the upper right hand corner with page number and name of lead author, e.g., 2. Smith The number of manuscript pages, the number of illustrations and the number of tables should be indicated at the bottom of the covering letter.
preparation of bibliography Bibliographic references should be listed numerically on a separate sheet (not in footnotes) as referred to in text and should be typed in accordance with the style and abbreviations used by Index Medicus with the following exceptions: use only the first page in a journal article citation and list all authors rather than three plus “et al.” Examples follow:
For book references
18. Schiebler GL, Van Mieron LHS, Krovetz LJ: Diseases of the tricuspid valve, chap 2. Heart Disease in Infants, Children and Adolescents (Moss AJ, Adams F, eds), Baltimore, Williams & Wilkins, 1968. For book references
For periodical
references:
22. Theologides A, Kennedy BJ: Toxoplasmic myocarditis and pericarditis. Am J Med 47: 169, 1969.
(with chapter):
(without
13. Berne E: Principles York, Oxford University Authors are responsible erences.
chapter):
of Group Treatment, Press, 1966, p 26.
for the accuracy
New
of the ref-
preparation of illustrations and tables Illustrations must be black and white glossy prints or professional drawings in india ink; they should be unmounted. The name of the lead author and the title of the article should be typed on a label and affixed to the back of each illustration; the top should be indicated. Reference to all illustrations should be inserted in the text in consecutive order. Legends for the illustrations should be typed, double spaced, on a separate sheet with numbers corresponding to those on the photographs or drawings. They should not be attached to the pictures.
Tables should be typed on separate sheets, with table number and title at the top of each sheet. Symbols for units should be confined to column headings. Abbreviations should be kept to a minimum and those used should be explained. All vertical rules should be omitted. The publisher allows a fixed amount towards the reproduction of illustrations and tables. Charges in excess of this amount must be assumed by the authors. The Editor reserves the right to limit the number of illustrations and/or tables.
reprints Price schedules and order mailed to each contributor.
cards
for
reprints
are
The American Journal of Medicine 666 Fifth Avenue, New York, N.Y.
106
January 1976
10019
The Am&can
Journal ol Medklno
Voluma 60