1992, The British Journal of Radiology, 65, 375-383
Magnetic resonance imaging of extracranial head and neck tumours By J . Kabala, MRCP, FRCR, P. Goddard, BSc, M D , FRCR and P. Cook, FRCR Department of Clinical Radiology, Bristol Royal Infirmary, Marlborough Street, Bristol BS2 8HW, UK
(Received 4 July 1991, accepted 4 September 1991) Keywords: MRI, Head neoplasms, Neck neoplasms
Abstract. The role of magnetic resonance imaging (MRI) in the investigation of head and neck tumours (excluding those primarily arising from the central nervous system or orbits) has been investigated. Follow-up data were obtained on 45 scans on 42 patients. MRI provided significant additional information compared with computed tomography (CT) in nine out of 17 (53%) scans performed for staging purposes. In the assessment of 19 patients with suspected tumour recurrence, MRI demonstrated a sensitivity of 100%, a specificity of 80% and an accuracy of 89%.
Direct inspection is the preferred method of examination for the superficial aspects of mucosal lesions of the head and neck. Computed tomography (CT) has developed into an accurate and powerful tool for the assessment of otherwise inaccessible lesions, although inaccuracies of tumour characterization and staging may be found in a significant proportion of cases (Som et al, 1988a; Werber & Lucente, 1989). Magnetic resonance imaging (MRI) has become the modality of choice for the assessment of tumour spread (Byrne et al, 1989; Lloyd & Phelps, 1986; Mandelblatt et al, 1987; Schaefer et al, 1985; Vogl, 1990; Vogl et al, 1988) and offers a number of potential advantages compared with CT. There is generally good contrast between abnormal and normal tissues, including skeletal muscle (Curtin, 1989; Teresi et al, 1987a). Tumours of the head and neck should ideally be displayed in at least two planes and this is routinely achieved with MRI but is considerably more difficult to do with CT. Unlike CT there is an absence of artefact from sharp density steps, for example as caused by dental amalgam or cortical bone. Flowing blood produces a signal void enabling vessels to be clearly distinguished without using intravenous contrast medium (Cross et al, 1989a; Kassel et al, 1989a). A study was undertaken to examine the current role being played by MRI in the investigation of head and neck tumours, excluding those primarily related to the central nervous system and orbits. In particular the accuracy of MRI detection of recurrent tumour and its usefulness in staging tumours compared with CT was examined.
excluding those arising from the central nervous system and orbits) at the Bristol MRI Centre between June 1987 and June 1990 were reviewed. Follow-up data (clinical, pathological and/or operative) were obtained on as many of these patients as possible. The scans were performed with a 0.5 T Picker Vista 2055HP MRI scanner with a surface coil. The following sequences were routinely performed: 1. Coronal Tx -weighted (T1W) spin-echo (time to repeat (TR) 500 ms, time to echo (TE) 26 ms). 2. Coronal short tau inversion-recovery (STIR) (TR 1500 ms, TE 30 ms, time to inversion (TI) 100 ms. 3. Transverse multi-echo-producing proton density (PD) and T2-weighted (T2W) images (TR 1500 ms, TE 30 ms and 80 ms, respectively). Results
Follow-up data were obtained for 45 scans on 42 patients. They can be categorized into four groups according to the clinical problem (Table I). The first two groups (28 scans) were for diagnostic purposes; the third and fourth groups (17 scans) were performed to stage a tumour known to be present. The relevant information on the nine patients in the first group (suspected tumour of unknown nature) is displayed in Table II. In the three cases where neoplasms were not present (the inflammatory salivary
Table I. Clinical indication for MRI scans Clinical problem
Number
Suspected tumour - ? nature Previous tumour - ? recurrent Staging tumour - primary Staging tumour - recurrent
9 19 8 9
Total
45
Subjects and methods
61 scans on 56 patients examined for suspected or confirmed extracranial head and neck tumours (i.e. Address correspondence to J. Kabala, Department of Clinical Radiology, Bristol Royal Infirmary, Marlborough Street, Bristol, UK. Vol. 65, No. 773
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/ . Kabala, P. Goddard and P. Cook Table II. Patients with a suspected tumour of unknown nature
Table IV. Scans performed to determine if tumour has recurred
Condition
Confirmation
MRI positive
Neck lymph node mass (metastatic carcinoma) Bilateral tortuous carotids Childhood developmental tumours Inflammatory salivary gland mass
Excision
Renal cell carcinoma metastasis to angle of mandible
Number
Carcinoma of the laryngopharynx Carcinoma of palate Carcinoma of antrum Chordoma Carcinoma of submandibular gland Carcinoma of floor of the mouth Carcinoma of parotid Nasopharyngeal carcinoma recurrent in neck lymph nodes
Ultrasound Excision 1-year clinical follow-up Excision
Total Table III. Scans performed to determine if tumour has recurred MRI negative
n
Nasopharyngeal Rhabdomyosarcoma Lymphoma Carcinoma Lymphoma of the neck Antral osteosarcoma Total
gland masses and the tortuous carotids), MRI provided the diagnosis. In the remaining six cases in this group, MRI produced elegant images and demonstrated the extent of the lesions accurately but did not provide a specific tissue diagnosis.
(a)
19 scans (Group 2, Table I) were performed to determine if tumour had recurred following treatment. Eight scans showed no recurrence (Table III). There has been no evidence of tumour recurrence after 1-2.5 years follow-up in this group and all these patients have been regarded as true negatives. 11 scans demonstrated recurrent tumour (Table IV). Six of these had histological confirmation of recurrence and three others showed involution of a mass and remission of symptoms with radiotherapy. These nine have been regarded as true positives. The remaining two scans showed lesions that remained static on follow-up MRI examination 4 months later and clinically 8 months later. One patient had been treated for carcinoma of the larynx (Fig. 1), the other for a left submandibular carcinoma. Both patients had undergone surgery and radiotherapy more than 1 year before the first MRI scan. They have both
(b)
Figure 1. (a) Transverse T1W scan (TR 600 ms, TE 26 ms) just below the level of the tracheostomy on a patient treated with surgery and radiotherapy 2 years before this scan. There is asymmetrical thickening of the left wall of the trachea (arrow), (b) The area of tracheal wall thickening (arrow) shows increased signal intensity on the STIR sequence (TR 1500 ms, TE 30 ms, TI 100 ms). A diagnosis of recurrent laryngeal carcinoma was made but appearances remained unchanged on repeat scanning 4 months later and there was no evidence of clinical recurrence 8 months after the initial scan.
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MRI of extracranial head and neck tumours been regarded as false positives. Thus, from these results on a heterogeneous group of 19 scans, the sensitivity of MRI for tumour recurrence was 100% (true positives divided by true positives plus false negatives) and specificity 80% (true negatives divided by true negatives plus false positives) with an overall accuracy of 89% (true positives plus true negatives divided by the total number). The prevalence of recurrence in this group was 47.4%. 17 scans were performed to stage tumours (Table V), nine being cases of recurrent tumour. In eight cases MRI and CT provided equivalent information. In nine cases MRI provided significant additional information, six being on patients with recurrent tumour. In two cases CT missed small lesions involving the maxillary nerve as it emerged from the foramen rotundum (Figs 2, 3), and in one case intracranial spread was indeterminate on CT but delineated on MRI (Fig. 4; the single case in which intravenous Gd-DTPA was employed). In one case the extent of lymph node involvement by a high-grade parotid carcinoma was underestimated by CT (Fig. 5) and in five cases the local extent of the tumour was clearly better seen on MRI than on CT (two parotid tumours, one sublingual carcinoma and two cases of recurrent carcinoma of the larynx; Figs 6, 7). All tumours demonstrated medium signal intensity on the T1W sequence, slightly greater than skeletal muscle, except one case of recurrent sublingual carcinoma (isointense with muscle). On T2W sequences the tumours produced a high signal intensity, between skeletal muscle and fat, except in four cases (one naso-
Table V. Tumours staged with MRI Primary tumours Nasopharyngeal Plasmocytoma Lymphoma Chordoma Parotid carcimona (high grade) Antro-ethmoid Carcinoma Malignant melanoma Recurrent tumours Nasopharyngeal Rhabdomyosarcoma Carcinoma Parotid Carcinoma Lymphangiohaemangioma Laryngopharyngeal carcinoma Antral carcinoma Carcinoma submandibular gland Malignant melanoma recurrent in neck lymph nodes Total
17
pharyngeal plasmocytoma, one low-grade parotid carcinoma, one squamous cell carcinoma recurrent in the parotid and one nasopharyngeal rhabdomyosarcoma) where the tumour produced a very high signal intensity, similar to fat. The appearances of tumour on PD sequences were between that on T1W and T2W
(a) (b) Figure 2. (a) Transverse T2W scan (TR 1500 ms, TE 80 ms) showing recurrent carcinoma lying posteriorly in the left maxillary antrum and extending out of the antrum through the lateral wall (arrow). Note the prior removal of the medial wall of the antrum. (b) Transverse T2W scan (TR 1500 ms, TE 80 ms) showing a second, completely separate deposit along the course of the left maxillary nerve producing left facial pain (arrows). Symptoms remitted following radiotherapy. Vol. 65, No. 773
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Figure 4. Coronal T1W scan (TR 500 ms, TE 26 ms) following gadolinium-DTPA. Heterogeneous-enhancing antro-ethmoid plasmocytoma (arrows) is seen invading through the cribriform plate on the left but without intracerebral invasion.
Figure 3. Coronal STIR scan (TR 1500 ms, TE 30 ms, TI 100 ms) showing high-signal-intensity tumour at the skull base and in the right pterygopalatine fossa (arrows). The patient was complaining of right facial pain in the distribution of the maxillary nerve. Radiotherapy produced remission of symptoms. The histological diagnosis was non-Hodgkin's lymphoma.
sequences, i.e. signal intensity greater than skeletal muscle but considerably less than that from fat. All tumours on the STIR sequence showed a high signal intensity, at least as bright as grey matter, with six tumours producing a very high signal, similar to that from normal nasal mucosa. These six tumours comprised two antral carcinomas, one case of malignant melanoma recurrent in neck lymph nodes and three parotid tumours (one haemangiolymphangioma and two carcinomas). In four patients, tumour was seen at the primary site and in regional lymph nodes (one nasopharyngeal carcinoma, two high-grade parotid carcinomas and one squamous cell carcinoma recurrent in the parotid). The signal intensity from the lymph nodes was similar to that from the primary lesion. Not all patients underwent surgery and even those who were operated on did not necessarily have systematic lymph node excision, so it is not possible to comment on sensitivity and specificity of lymph node detection in this group of patients. There were, however, no known false positives or negatives in this series. 378
Eight patients had sinusitis of the maxillary antra. The signal intensity of the thickened mucosa on the T1W sequence was similar to, or slightly higher than, skeletal muscle (and therefore of virtually identical signal to tumour). On the T2W sequence, however, the signal intensity of inflamed antral mucosa was very high in all cases, similar to fat and nasal mucosa. The appearances on the PD sequence were mid-way between that on the T1W and T2W sequences, generally being of slightly higher signal intensity than tumour. On the STIR sequence, inflamed mucosa was of very high signal intensity, similar to the signal from normal nasal mucosa and again generally of slightly higher signal intensity than tumour. The signal intensity of normal structures are well described in the literature on T1W, PD and T2W sequences (Crawford et al, 1989; Cross et al, 1989b) but not on the STIR sequence. Consequently the following observations relating to signal intensity on the STIR sequence have been made in this series to provide reference points for the discussion of tumour appearances. Nasal mucosa produced a very high signal intensity; grey matter, high signal; major salivary glands, medium to high; skeletal muscle, low; and fat, very low. Discussion
Despite its considerable value as an imaging technique it is doubtful that MRI currently offers any advance over CT in achieving a histological diagnosis for head and neck tumours. Both modalities can make some prediction about the nature of mass lesions based on apparent organ of origin and frequency of occurThe British Journal of Radiology, May 1992
MRI of extracranial head and neck tumours
Figure 5. (a) Coronal TIW (TR 500 ms, TE 26 ms) scan showing a heterogeneous, predominantly medium-signal-intensity carcinoma of the left parotid gland (curved arrow) (lower signal intensity than normal fatty parotid tissue but slightly higher signal intensity than skeletal muscle). Medium-signal-intensity cervical lymph nodes are seen bilaterally. These are more clearly visualized on the STIR sequence (TR 1500 ms, TE 30 ms, TI 100 ms) shown in (b) and (c) (slightly posterior scan). It is interesting to review the lymph node chains seen on the more posterior scan on the TIW sequence (d). The reduced contrast is clearly evident (the lymph node chain on the right is lost against the adjacent skeletal muscle) but the resolution is much improved (note particularly the chain of lymph nodes on the left hand side; curved arrow).
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(b)
Figure 6. (a) CT scan showing a low-density right parotid tumour. The image is markedly degraded by artefact arising from the abrupt density step at cortical bone and at the pharynx, (b) Transverse STIR sequence (TR 1500 ms, TE 30 ms, TI 100 ms) showing high signal intensity from the parotid tumour (vertical straight arrow). Its extent is well defined. Note the strip of normal parotid compressed laterally by the tumour (curved arrow).
Figure 7. (a) Transverse T1W scan (TR 660 ms, TE 26 ms) showing medium- to high-signal-intensity recurrent laryngeal carcinoma (horizontal arrow) invading the muscles of the anterior neck, encasing the right common carotid artery (vertical arrow) and abutting the right internal jugular vein, (b) Contrast-enhanced CT scan of the same patient. The recurrent tumour is indistinguishable from normal muscle and, owing to poor timing of the intravenous contrast, the relationship of tumour to the local vasculature has not been determined. 380
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MRI of extracranial head and neck tumours
rence of specific lesions (Som et al, 1988b; Whyte & Hourihan, 1989). The signal intensity of benign and malignant tumours show considerable overlap and on this criterion only tentative statements at best can be made regarding the aggressive capability of tumours (Byrne et al, 1989; Casselman & Mancuso, 1987; Som et al, 1989a; Teresi et al, 1987a). The major role of MRI is in staging tumours for surgery and radiotherapy and the diagnosis of recurrent tumour (Tabor & Curtin, 1989; Teresi et al, 1989a). In this series MRI provided additional significant information over that provided by CT in nine patients undergoing tumour staging (Figs 2-7). In staging tumours MRI has two advantages over CT: its ability to image in any two or three planes desired, and its superior tissue contrast (Curtin, 1989; Lufkin & Hanafee, 1987; Teresi et al, 1987a). The multiplanar ability of MRI allows complex anatomy and pathology to be well demonstrated. This has been especially noted in the region of the head and neck; for example, demonstration of perineural tumour extension into the skull basal foramina and fossae (Laine et al, 1990; Teresi et al, 1987b, c). This was seen in two patients in this current series (Figs 2, 3). The superior tissue contrast of MRI allows tumour and involved lymph nodes to be differentiated from inflamed mucosa, retained secretions, fibrosis and normal structures, particularly skeletal muscle and blood vessels (Cross et al, 1989b; Kassel et al, 1989b). On CT the attenuation values of these show considerable overlap on unenhanced scans (Som et al, 1988a; Stutley et al, 1989). Although there is some disagreement between reports, tumours in the region of the head and neck are generally described as having the following signal intensities: similar to or just less than skeletal muscle on T1W sequences, higher than skeletal muscle but less than fat {i.e. often similar to the fat-containing major salivary glands) on T2W sequences and somewhere between these on proton density sequences (Casselman & Mancuso, 1987; Som et al, 1987, 1988a, b, 1989a; Vogl et al, 1989). The results in this series parallel those described elsewhere except for the appearances on T1W sequences, where with only one exception (the recurrent sublingual carcinoma isointense with skeletal muscle) the tumours showed a signal intensity slightly greater than skeletal muscle. The STIR sequence used in this current series is not commonly described elsewhere in the American literature although reports of its usefulness for increasing the visibility of malignant lesions can be found (Cobby et al, 1990; Goddard et al, 1988; Shuman et al, 1988). The STIR sequence suppresses fat and is Tx plus T2 weighted. As a result structures containing water produce a high signal. This highlights both tumours and acute inflammatory lesions. In this series most tumours had a high signal on T2W and STIR sequences but only a minority had the very high signal intensity of inflammatory tissue and normal nasal mucosa. Vol. 65, No. 773
For staging tumours the T1W sequence produces excellent demonstration of anatomy, including blood vessels, easily delineated by their signal void. On this sequence tumours are easily differentiated from fat and fatty structures such as the major salivary glands. The T2W and STIR sequences produce better differentiation of tumour from normal muscle, retained secretions and inflammatory lesions (Cross et al, 1989c). The limited numbers with lymph node metastases in this series (four true positives, no known false positives or negatives) do not permit anything more than a tentative comment about the use of MRI for the detection of lymph nodes involved by tumour. Lymph nodes involved by tumour show similar signal intensities to the primary tumour and to inflammatory tumours (Kassel et al, 1989b; Teresi et al, 1989b; van den Brekel et al, 1990). In the upper neck, lymph nodes are generally larger than in the lower neck, presumably because of recurrent inflammation associated with common oropharyngeal and dental ailments. The following criteria for involvement have been suggested: a maximum diameter greater than 1 cm in the lower neck (producing 80% true positives), greater than 1 cm in the upper neck (submandibular and jugulodiagastric regions of the internal jugular nodes) if spherical or in a high-risk group (i.e. known primary carcinoma) but above 1.5 cm in the upper neck if not in a high-risk group (Som, 1987). Any lymph node showing central necrosis (areas of increased signal intensity on a T2W sequence, areas failing to enhance with gadolinium or areas measuring 10-18 HU on CT) can be considered involved and it has been claimed that this is the single most specific feature of metastatic involvement (van den Brekel et al, 1990). There is no doubt that both CT and MRI will miss lymph node micrometastases (Curtin, 1989) and it has been claimed that neither produces a significant increase in accuracy over clinical examination (Feinmesser et al, 1990; Som, 1987; Werber & Lucente, 1989). Van den Brekel et al (1990) have suggested that the accuracy of MRI can be up to 89% with gadolinium, compared with 77-78% for clinical examination. Whether or not a similar accuracy would be achievable using the STIR sequence without gadolinium is not known. Gadolinium enhancement is not required routinely (Vogl et al, 1989) although it can be useful for assessing intracranial extension and meningeal involvement, and may improve differentiation from adjacent inflammatory lesions. Retained secretions will not enhance whereas tumour (and involved lymph nodes) and acutely inflamed tissue will enhance, the latter generally to a greater extent (Robinson et al, 1989; van den Brekel et al, 1990). Many of the centres describing the usefulness of gadolinium are not using the STIR sequence, which to a certain extent fulfills the same function without intravenous contrast, i.e. producing an increase in signal intensity and visibility of tumours and inflammatory tissue. Considering the problem of recurrent tumour, on CT the appearances may be similar to post-radiotherapy or 381
J. Kabala, P. Goddard and P. Cook
post-operativefibrosis.The immediate post-intervention appearances (within 4 months of radiotherapy or surgery) on MRI are similar to inflammation from other causes and to the appearances of inflamed mucosa in the eight patients in whom this was noted in this series (medium signal intensity on the T1W sequence and high on the T2W and STIR sequences). Six months or so after intervention, the signal intensity offibrosisgenererally becomes low on the T1W sequence (a little below that of skeletal muscle) and low to intermediate on the T2W, proton density and STIR sequences (Kassel et al, 1989c; Som et al, 1988a, 1989a). Inspissated secretions could potentially cause problems in delineating sinonasal tumours although, as mentioned above, secretions will not enhance with gadolinium (Dillon et al, 1990). However, even without gadolinium the signal intensity from tumours and sinonasal secretions is generally different. Acute secretions will have low signal intensity on T1W and high signal on T2W sequences owing to a 95% water content. With increasing chronicity the water content falls and the signal intensity becomes medium to high on T1W and high on T2W sequences. Occasionally the protein content exceeds 25% and all water present is bound, producing a very low signal intensity on both T1W and T2W sequences (Som et al, 1989b). Criteria that may suggest tumour recurrence include increased signal intensity on the T2W sequence later than 6 months after intervention, bulky mass beyond the original primary site and obliteration of tissue planes (Kassel et al, 1989c). The last one clearly may also be seen simply as a sequence to the previous intervention. In this series, recurrent tumour always had a signal intensity just above skeletal muscle on the T1W sequence (except one case which was isointense) and a high signal intensity (sometimes very high) on the T2W and STIR sequences. In this series tumour recurrence was diagnosed with a sensitivity of 100% and a specificity of 80%. Two false positives were encountered (Fig. 1). In both these patients the appearances of the suspicious tissue on the T1W sequence (isointense with skeletal muscle in one and less than skeletal muscle in the other) might suggest fibrosis but the increased signal intensity on the T2W and STIR sequences was highly likely to represent an active process, which more than 1 year after surgery or radiotherapy suggested tumour recurrence. It seems from these results that in order to maintain a high sensitivity one has to accept occasional false positives.
Acknowledgments The authors wish gratefully to acknowledge the co-operation and encouragement of the trustees, Dr A. L. T. Beddoe, Dr P. Goddard, Dr C. Johnson and Dr J. L.G. Thomson, and the radiographers, Miss A. Case (Superintendent), Miss Joanne Waring (Deputy Superintendent) and Mrs M. Riley, of the Bristol MRI centre.
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Magnetic resonance imaging of extracranial head and neck tumours By J . Kabala, MRCP, FRCR, P. Goddard, BSc, M D , FRCR and P. Cook, FRCR Department of Clinical Radiology, Bristol Royal Infirmary, Marlborough Street, Bristol BS2 8HW, UK
(Received 4 July 1991, accepted 4 September 1991) Keywords: MRI, Head neoplasms, Neck neoplasms
Abstract. The role of magnetic resonance imaging (MRI) in the investigation of head and neck tumours (excluding those primarily arising from the central nervous system or orbits) has been investigated. Follow-up data were obtained on 45 scans on 42 patients. MRI provided significant additional information compared with computed tomography (CT) in nine out of 17 (53%) scans performed for staging purposes. In the assessment of 19 patients with suspected tumour recurrence, MRI demonstrated a sensitivity of 100%, a specificity of 80% and an accuracy of 89%.
Direct inspection is the preferred method of examination for the superficial aspects of mucosal lesions of the head and neck. Computed tomography (CT) has developed into an accurate and powerful tool for the assessment of otherwise inaccessible lesions, although inaccuracies of tumour characterization and staging may be found in a significant proportion of cases (Som et al, 1988a; Werber & Lucente, 1989). Magnetic resonance imaging (MRI) has become the modality of choice for the assessment of tumour spread (Byrne et al, 1989; Lloyd & Phelps, 1986; Mandelblatt et al, 1987; Schaefer et al, 1985; Vogl, 1990; Vogl et al, 1988) and offers a number of potential advantages compared with CT. There is generally good contrast between abnormal and normal tissues, including skeletal muscle (Curtin, 1989; Teresi et al, 1987a). Tumours of the head and neck should ideally be displayed in at least two planes and this is routinely achieved with MRI but is considerably more difficult to do with CT. Unlike CT there is an absence of artefact from sharp density steps, for example as caused by dental amalgam or cortical bone. Flowing blood produces a signal void enabling vessels to be clearly distinguished without using intravenous contrast medium (Cross et al, 1989a; Kassel et al, 1989a). A study was undertaken to examine the current role being played by MRI in the investigation of head and neck tumours, excluding those primarily related to the central nervous system and orbits. In particular the accuracy of MRI detection of recurrent tumour and its usefulness in staging tumours compared with CT was examined.
excluding those arising from the central nervous system and orbits) at the Bristol MRI Centre between June 1987 and June 1990 were reviewed. Follow-up data (clinical, pathological and/or operative) were obtained on as many of these patients as possible. The scans were performed with a 0.5 T Picker Vista 2055HP MRI scanner with a surface coil. The following sequences were routinely performed: 1. Coronal Tx -weighted (T1W) spin-echo (time to repeat (TR) 500 ms, time to echo (TE) 26 ms). 2. Coronal short tau inversion-recovery (STIR) (TR 1500 ms, TE 30 ms, time to inversion (TI) 100 ms. 3. Transverse multi-echo-producing proton density (PD) and T2-weighted (T2W) images (TR 1500 ms, TE 30 ms and 80 ms, respectively). Results
Follow-up data were obtained for 45 scans on 42 patients. They can be categorized into four groups according to the clinical problem (Table I). The first two groups (28 scans) were for diagnostic purposes; the third and fourth groups (17 scans) were performed to stage a tumour known to be present. The relevant information on the nine patients in the first group (suspected tumour of unknown nature) is displayed in Table II. In the three cases where neoplasms were not present (the inflammatory salivary
Table I. Clinical indication for MRI scans Clinical problem
Number
Suspected tumour - ? nature Previous tumour - ? recurrent Staging tumour - primary Staging tumour - recurrent
9 19 8 9
Total
45
Subjects and methods
61 scans on 56 patients examined for suspected or confirmed extracranial head and neck tumours (i.e. Address correspondence to J. Kabala, Department of Clinical Radiology, Bristol Royal Infirmary, Marlborough Street, Bristol, UK. Vol. 65, No. 773
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/ . Kabala, P. Goddard and P. Cook Table II. Patients with a suspected tumour of unknown nature
Table IV. Scans performed to determine if tumour has recurred
Condition
Confirmation
MRI positive
Neck lymph node mass (metastatic carcinoma) Bilateral tortuous carotids Childhood developmental tumours Inflammatory salivary gland mass
Excision
Renal cell carcinoma metastasis to angle of mandible
Number
Carcinoma of the laryngopharynx Carcinoma of palate Carcinoma of antrum Chordoma Carcinoma of submandibular gland Carcinoma of floor of the mouth Carcinoma of parotid Nasopharyngeal carcinoma recurrent in neck lymph nodes
Ultrasound Excision 1-year clinical follow-up Excision
Total Table III. Scans performed to determine if tumour has recurred MRI negative
n
Nasopharyngeal Rhabdomyosarcoma Lymphoma Carcinoma Lymphoma of the neck Antral osteosarcoma Total
gland masses and the tortuous carotids), MRI provided the diagnosis. In the remaining six cases in this group, MRI produced elegant images and demonstrated the extent of the lesions accurately but did not provide a specific tissue diagnosis.
(a)
19 scans (Group 2, Table I) were performed to determine if tumour had recurred following treatment. Eight scans showed no recurrence (Table III). There has been no evidence of tumour recurrence after 1-2.5 years follow-up in this group and all these patients have been regarded as true negatives. 11 scans demonstrated recurrent tumour (Table IV). Six of these had histological confirmation of recurrence and three others showed involution of a mass and remission of symptoms with radiotherapy. These nine have been regarded as true positives. The remaining two scans showed lesions that remained static on follow-up MRI examination 4 months later and clinically 8 months later. One patient had been treated for carcinoma of the larynx (Fig. 1), the other for a left submandibular carcinoma. Both patients had undergone surgery and radiotherapy more than 1 year before the first MRI scan. They have both
(b)
Figure 1. (a) Transverse T1W scan (TR 600 ms, TE 26 ms) just below the level of the tracheostomy on a patient treated with surgery and radiotherapy 2 years before this scan. There is asymmetrical thickening of the left wall of the trachea (arrow), (b) The area of tracheal wall thickening (arrow) shows increased signal intensity on the STIR sequence (TR 1500 ms, TE 30 ms, TI 100 ms). A diagnosis of recurrent laryngeal carcinoma was made but appearances remained unchanged on repeat scanning 4 months later and there was no evidence of clinical recurrence 8 months after the initial scan.
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MRI of extracranial head and neck tumours been regarded as false positives. Thus, from these results on a heterogeneous group of 19 scans, the sensitivity of MRI for tumour recurrence was 100% (true positives divided by true positives plus false negatives) and specificity 80% (true negatives divided by true negatives plus false positives) with an overall accuracy of 89% (true positives plus true negatives divided by the total number). The prevalence of recurrence in this group was 47.4%. 17 scans were performed to stage tumours (Table V), nine being cases of recurrent tumour. In eight cases MRI and CT provided equivalent information. In nine cases MRI provided significant additional information, six being on patients with recurrent tumour. In two cases CT missed small lesions involving the maxillary nerve as it emerged from the foramen rotundum (Figs 2, 3), and in one case intracranial spread was indeterminate on CT but delineated on MRI (Fig. 4; the single case in which intravenous Gd-DTPA was employed). In one case the extent of lymph node involvement by a high-grade parotid carcinoma was underestimated by CT (Fig. 5) and in five cases the local extent of the tumour was clearly better seen on MRI than on CT (two parotid tumours, one sublingual carcinoma and two cases of recurrent carcinoma of the larynx; Figs 6, 7). All tumours demonstrated medium signal intensity on the T1W sequence, slightly greater than skeletal muscle, except one case of recurrent sublingual carcinoma (isointense with muscle). On T2W sequences the tumours produced a high signal intensity, between skeletal muscle and fat, except in four cases (one naso-
Table V. Tumours staged with MRI Primary tumours Nasopharyngeal Plasmocytoma Lymphoma Chordoma Parotid carcimona (high grade) Antro-ethmoid Carcinoma Malignant melanoma Recurrent tumours Nasopharyngeal Rhabdomyosarcoma Carcinoma Parotid Carcinoma Lymphangiohaemangioma Laryngopharyngeal carcinoma Antral carcinoma Carcinoma submandibular gland Malignant melanoma recurrent in neck lymph nodes Total
17
pharyngeal plasmocytoma, one low-grade parotid carcinoma, one squamous cell carcinoma recurrent in the parotid and one nasopharyngeal rhabdomyosarcoma) where the tumour produced a very high signal intensity, similar to fat. The appearances of tumour on PD sequences were between that on T1W and T2W
(a) (b) Figure 2. (a) Transverse T2W scan (TR 1500 ms, TE 80 ms) showing recurrent carcinoma lying posteriorly in the left maxillary antrum and extending out of the antrum through the lateral wall (arrow). Note the prior removal of the medial wall of the antrum. (b) Transverse T2W scan (TR 1500 ms, TE 80 ms) showing a second, completely separate deposit along the course of the left maxillary nerve producing left facial pain (arrows). Symptoms remitted following radiotherapy. Vol. 65, No. 773
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Figure 4. Coronal T1W scan (TR 500 ms, TE 26 ms) following gadolinium-DTPA. Heterogeneous-enhancing antro-ethmoid plasmocytoma (arrows) is seen invading through the cribriform plate on the left but without intracerebral invasion.
Figure 3. Coronal STIR scan (TR 1500 ms, TE 30 ms, TI 100 ms) showing high-signal-intensity tumour at the skull base and in the right pterygopalatine fossa (arrows). The patient was complaining of right facial pain in the distribution of the maxillary nerve. Radiotherapy produced remission of symptoms. The histological diagnosis was non-Hodgkin's lymphoma.
sequences, i.e. signal intensity greater than skeletal muscle but considerably less than that from fat. All tumours on the STIR sequence showed a high signal intensity, at least as bright as grey matter, with six tumours producing a very high signal, similar to that from normal nasal mucosa. These six tumours comprised two antral carcinomas, one case of malignant melanoma recurrent in neck lymph nodes and three parotid tumours (one haemangiolymphangioma and two carcinomas). In four patients, tumour was seen at the primary site and in regional lymph nodes (one nasopharyngeal carcinoma, two high-grade parotid carcinomas and one squamous cell carcinoma recurrent in the parotid). The signal intensity from the lymph nodes was similar to that from the primary lesion. Not all patients underwent surgery and even those who were operated on did not necessarily have systematic lymph node excision, so it is not possible to comment on sensitivity and specificity of lymph node detection in this group of patients. There were, however, no known false positives or negatives in this series. 378
Eight patients had sinusitis of the maxillary antra. The signal intensity of the thickened mucosa on the T1W sequence was similar to, or slightly higher than, skeletal muscle (and therefore of virtually identical signal to tumour). On the T2W sequence, however, the signal intensity of inflamed antral mucosa was very high in all cases, similar to fat and nasal mucosa. The appearances on the PD sequence were mid-way between that on the T1W and T2W sequences, generally being of slightly higher signal intensity than tumour. On the STIR sequence, inflamed mucosa was of very high signal intensity, similar to the signal from normal nasal mucosa and again generally of slightly higher signal intensity than tumour. The signal intensity of normal structures are well described in the literature on T1W, PD and T2W sequences (Crawford et al, 1989; Cross et al, 1989b) but not on the STIR sequence. Consequently the following observations relating to signal intensity on the STIR sequence have been made in this series to provide reference points for the discussion of tumour appearances. Nasal mucosa produced a very high signal intensity; grey matter, high signal; major salivary glands, medium to high; skeletal muscle, low; and fat, very low. Discussion
Despite its considerable value as an imaging technique it is doubtful that MRI currently offers any advance over CT in achieving a histological diagnosis for head and neck tumours. Both modalities can make some prediction about the nature of mass lesions based on apparent organ of origin and frequency of occurThe British Journal of Radiology, May 1992
MRI of extracranial head and neck tumours
Figure 5. (a) Coronal TIW (TR 500 ms, TE 26 ms) scan showing a heterogeneous, predominantly medium-signal-intensity carcinoma of the left parotid gland (curved arrow) (lower signal intensity than normal fatty parotid tissue but slightly higher signal intensity than skeletal muscle). Medium-signal-intensity cervical lymph nodes are seen bilaterally. These are more clearly visualized on the STIR sequence (TR 1500 ms, TE 30 ms, TI 100 ms) shown in (b) and (c) (slightly posterior scan). It is interesting to review the lymph node chains seen on the more posterior scan on the TIW sequence (d). The reduced contrast is clearly evident (the lymph node chain on the right is lost against the adjacent skeletal muscle) but the resolution is much improved (note particularly the chain of lymph nodes on the left hand side; curved arrow).
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(b)
Figure 6. (a) CT scan showing a low-density right parotid tumour. The image is markedly degraded by artefact arising from the abrupt density step at cortical bone and at the pharynx, (b) Transverse STIR sequence (TR 1500 ms, TE 30 ms, TI 100 ms) showing high signal intensity from the parotid tumour (vertical straight arrow). Its extent is well defined. Note the strip of normal parotid compressed laterally by the tumour (curved arrow).
Figure 7. (a) Transverse T1W scan (TR 660 ms, TE 26 ms) showing medium- to high-signal-intensity recurrent laryngeal carcinoma (horizontal arrow) invading the muscles of the anterior neck, encasing the right common carotid artery (vertical arrow) and abutting the right internal jugular vein, (b) Contrast-enhanced CT scan of the same patient. The recurrent tumour is indistinguishable from normal muscle and, owing to poor timing of the intravenous contrast, the relationship of tumour to the local vasculature has not been determined. 380
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MRI of extracranial head and neck tumours
rence of specific lesions (Som et al, 1988b; Whyte & Hourihan, 1989). The signal intensity of benign and malignant tumours show considerable overlap and on this criterion only tentative statements at best can be made regarding the aggressive capability of tumours (Byrne et al, 1989; Casselman & Mancuso, 1987; Som et al, 1989a; Teresi et al, 1987a). The major role of MRI is in staging tumours for surgery and radiotherapy and the diagnosis of recurrent tumour (Tabor & Curtin, 1989; Teresi et al, 1989a). In this series MRI provided additional significant information over that provided by CT in nine patients undergoing tumour staging (Figs 2-7). In staging tumours MRI has two advantages over CT: its ability to image in any two or three planes desired, and its superior tissue contrast (Curtin, 1989; Lufkin & Hanafee, 1987; Teresi et al, 1987a). The multiplanar ability of MRI allows complex anatomy and pathology to be well demonstrated. This has been especially noted in the region of the head and neck; for example, demonstration of perineural tumour extension into the skull basal foramina and fossae (Laine et al, 1990; Teresi et al, 1987b, c). This was seen in two patients in this current series (Figs 2, 3). The superior tissue contrast of MRI allows tumour and involved lymph nodes to be differentiated from inflamed mucosa, retained secretions, fibrosis and normal structures, particularly skeletal muscle and blood vessels (Cross et al, 1989b; Kassel et al, 1989b). On CT the attenuation values of these show considerable overlap on unenhanced scans (Som et al, 1988a; Stutley et al, 1989). Although there is some disagreement between reports, tumours in the region of the head and neck are generally described as having the following signal intensities: similar to or just less than skeletal muscle on T1W sequences, higher than skeletal muscle but less than fat {i.e. often similar to the fat-containing major salivary glands) on T2W sequences and somewhere between these on proton density sequences (Casselman & Mancuso, 1987; Som et al, 1987, 1988a, b, 1989a; Vogl et al, 1989). The results in this series parallel those described elsewhere except for the appearances on T1W sequences, where with only one exception (the recurrent sublingual carcinoma isointense with skeletal muscle) the tumours showed a signal intensity slightly greater than skeletal muscle. The STIR sequence used in this current series is not commonly described elsewhere in the American literature although reports of its usefulness for increasing the visibility of malignant lesions can be found (Cobby et al, 1990; Goddard et al, 1988; Shuman et al, 1988). The STIR sequence suppresses fat and is Tx plus T2 weighted. As a result structures containing water produce a high signal. This highlights both tumours and acute inflammatory lesions. In this series most tumours had a high signal on T2W and STIR sequences but only a minority had the very high signal intensity of inflammatory tissue and normal nasal mucosa. Vol. 65, No. 773
For staging tumours the T1W sequence produces excellent demonstration of anatomy, including blood vessels, easily delineated by their signal void. On this sequence tumours are easily differentiated from fat and fatty structures such as the major salivary glands. The T2W and STIR sequences produce better differentiation of tumour from normal muscle, retained secretions and inflammatory lesions (Cross et al, 1989c). The limited numbers with lymph node metastases in this series (four true positives, no known false positives or negatives) do not permit anything more than a tentative comment about the use of MRI for the detection of lymph nodes involved by tumour. Lymph nodes involved by tumour show similar signal intensities to the primary tumour and to inflammatory tumours (Kassel et al, 1989b; Teresi et al, 1989b; van den Brekel et al, 1990). In the upper neck, lymph nodes are generally larger than in the lower neck, presumably because of recurrent inflammation associated with common oropharyngeal and dental ailments. The following criteria for involvement have been suggested: a maximum diameter greater than 1 cm in the lower neck (producing 80% true positives), greater than 1 cm in the upper neck (submandibular and jugulodiagastric regions of the internal jugular nodes) if spherical or in a high-risk group (i.e. known primary carcinoma) but above 1.5 cm in the upper neck if not in a high-risk group (Som, 1987). Any lymph node showing central necrosis (areas of increased signal intensity on a T2W sequence, areas failing to enhance with gadolinium or areas measuring 10-18 HU on CT) can be considered involved and it has been claimed that this is the single most specific feature of metastatic involvement (van den Brekel et al, 1990). There is no doubt that both CT and MRI will miss lymph node micrometastases (Curtin, 1989) and it has been claimed that neither produces a significant increase in accuracy over clinical examination (Feinmesser et al, 1990; Som, 1987; Werber & Lucente, 1989). Van den Brekel et al (1990) have suggested that the accuracy of MRI can be up to 89% with gadolinium, compared with 77-78% for clinical examination. Whether or not a similar accuracy would be achievable using the STIR sequence without gadolinium is not known. Gadolinium enhancement is not required routinely (Vogl et al, 1989) although it can be useful for assessing intracranial extension and meningeal involvement, and may improve differentiation from adjacent inflammatory lesions. Retained secretions will not enhance whereas tumour (and involved lymph nodes) and acutely inflamed tissue will enhance, the latter generally to a greater extent (Robinson et al, 1989; van den Brekel et al, 1990). Many of the centres describing the usefulness of gadolinium are not using the STIR sequence, which to a certain extent fulfills the same function without intravenous contrast, i.e. producing an increase in signal intensity and visibility of tumours and inflammatory tissue. Considering the problem of recurrent tumour, on CT the appearances may be similar to post-radiotherapy or 381
J. Kabala, P. Goddard and P. Cook
post-operativefibrosis.The immediate post-intervention appearances (within 4 months of radiotherapy or surgery) on MRI are similar to inflammation from other causes and to the appearances of inflamed mucosa in the eight patients in whom this was noted in this series (medium signal intensity on the T1W sequence and high on the T2W and STIR sequences). Six months or so after intervention, the signal intensity offibrosisgenererally becomes low on the T1W sequence (a little below that of skeletal muscle) and low to intermediate on the T2W, proton density and STIR sequences (Kassel et al, 1989c; Som et al, 1988a, 1989a). Inspissated secretions could potentially cause problems in delineating sinonasal tumours although, as mentioned above, secretions will not enhance with gadolinium (Dillon et al, 1990). However, even without gadolinium the signal intensity from tumours and sinonasal secretions is generally different. Acute secretions will have low signal intensity on T1W and high signal on T2W sequences owing to a 95% water content. With increasing chronicity the water content falls and the signal intensity becomes medium to high on T1W and high on T2W sequences. Occasionally the protein content exceeds 25% and all water present is bound, producing a very low signal intensity on both T1W and T2W sequences (Som et al, 1989b). Criteria that may suggest tumour recurrence include increased signal intensity on the T2W sequence later than 6 months after intervention, bulky mass beyond the original primary site and obliteration of tissue planes (Kassel et al, 1989c). The last one clearly may also be seen simply as a sequence to the previous intervention. In this series, recurrent tumour always had a signal intensity just above skeletal muscle on the T1W sequence (except one case which was isointense) and a high signal intensity (sometimes very high) on the T2W and STIR sequences. In this series tumour recurrence was diagnosed with a sensitivity of 100% and a specificity of 80%. Two false positives were encountered (Fig. 1). In both these patients the appearances of the suspicious tissue on the T1W sequence (isointense with skeletal muscle in one and less than skeletal muscle in the other) might suggest fibrosis but the increased signal intensity on the T2W and STIR sequences was highly likely to represent an active process, which more than 1 year after surgery or radiotherapy suggested tumour recurrence. It seems from these results that in order to maintain a high sensitivity one has to accept occasional false positives.
Acknowledgments The authors wish gratefully to acknowledge the co-operation and encouragement of the trustees, Dr A. L. T. Beddoe, Dr P. Goddard, Dr C. Johnson and Dr J. L.G. Thomson, and the radiographers, Miss A. Case (Superintendent), Miss Joanne Waring (Deputy Superintendent) and Mrs M. Riley, of the Bristol MRI centre.
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