Magnetic resonance imaging (MRI) and dynamic MRI evaluation of extranodal non-Hodgkin lymphoma in oral and maxillofacial regions
Hidenobu Matsuzaki, DDS,a
Marina Hara, DDS,b
Yoshinobu Yanagi, DDS,c
Jun-ichi Asaumi, DDS, DMSci,d
Naoki Katase, DDS, PhD,e
Teruhisa Unetsubo, DDS, PhD,b
Miki Hisatomi, DDS, PhD,f
Hironobu Konouchi, DDS, PhD,c
Toshihiko Takenobu, DDS, PhD,b
and Hitoshi Nagatsuka, DDS, PhD,g
Objective.The purpose of this study was to evaluate the diagnostic value of magnetic resonance imaging (MRI), especially dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI), in extranodal non-Hodgkin lymphoma (NHL) of oral and maxillofacial regions.
Study design.Thirteen cases with extranodal NHL were examined using MRI. T1-weighted images (T1WI) and T2-weighted images (T2WI) or short TI inversion recovery (STIR) images were obtained in all cases. Contrast-enhanced images and DCE- MRI were acquired in 10 and 7 cases, respectively. On DCE-MRIs, we analyzed the parameters as follows: contrast index at maximal contrast enhancement (CImax), maximum contrast index (CI) gain/CImax ratio, and washout ratios (WR300, WR600, and WR900) at 300, 600, and 900 seconds after contrast medium injection.
Results.The signal intensity of all lesions was hypointense to isointense on T1WIs and showed variable contrast enhancement patterns. On T2WIs and STIR images, the signal intensity was isointense to hyperintense in almost all cases. Analysis of DCE- MRI parameters in extranodal NHLs resulted in the identification of 4 types of CI curves according to CImax and WR: (1) CImax greater than 2.0 and WR900greater than 40%, (2) CImax greater than 2.0 and WR900less than 40%, (3) CImax less than 1.5 and WR900greater than 40%, and (4) CImax less than 1.5 and WR900greater than 40%.
Conclusions.The signal intensities on MRI were not specific to extranodal NHL and resembled those of other tumor types.
When CImax was less than 1.5 or WR900 was less than 40%, these parameters contributed to diagnosis in extranodal NHLs.
(Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:126-133)
Malignant lymphomas are divided into non-Hodgkin and Hodgkin groups, and approximately 40% of non- Hodgkin lymphomas (NHLs) arise at extranodal sites outside the lymphoid system.1
The most common sites of extranodal NHL in the oral region are the palate and maxilla.2-7
The common clinical symptom is mass for- mation with or without ulceration, and the radiological sign of lesions involving the jawbone is diffuse bone resorption, similar to those of periodontal inflamma- tion, osteomyelitis, and other malignant tumors.3-10
Some authors have reported the existence of various magnetic resonance (MR) findings for extranodal NHL
of the head and neck region and nonspecific signal characteristics.11-15
It has been reported that the time versus signal- intensity curve, which uses the parameters of dynamic contrast-enhanced magnetic resonance imaging (DCE- MRI), is useful for diagnosis of some lesions.16-29
Furthermore, using the calculated values from param- eters of DCE-MRI, such as the contrast index (CI) curve, might make it possible to investigate the char- acteristics of lesions and contribute to diagnosis.15,30-37
We reported that the CI of malignant lymphomas (in- cluding nodal lymphomas in the head and neck region) have characteristic values and maximum CI values that are useful for distinguishing malignant lymphomas from oral squamous cell carcinomas.15,35
In the present study, we retrospectively evaluated magnetic resonance imaging (MRI) studies of extran- odal NHL of oral and maxillofacial regions. Further- more, we evaluated the diagnostic value of the param- eters of CI curves on DCE-MRI.
MATERIAL AND METHODS Patients
Twenty-six patients were histopathologically diag- nosed with extranodal NHL in our hospital between April 1993 and December 2009. Of these patients, we
aAssistant Professor, Department of Oral Diagnosis and Dentomax- illofacial Radiology.
bResearch Fellow, Department of Oral and Maxillofacial Radiology.
cSenior Assistant Professor, Department of Oral Diagnosis and Den- tomaxillofacial Radiology.
dProfessor, Department of Oral and Maxillofacial Radiology.
eAssistant Professor, Department of Oral Pathology and Medicine.
fAssistant Professor, Department of Oral and Maxillofacial Radi- ology.
gProfessor, Department of Oral Pathology and Medicine.
Received for publication Apr 2, 2011; returned for revision Jul 19, 2011; accepted for publication Jul 29, 2011.
© 2012 Elsevier Inc. All rights reserved.
2212-4403/$ - see front matter doi:10.1016/j.tripleo.2011.07.038
evaluated the records of 13 who underwent MR exam- ination with or without contrast medium enhancement in this retrospective study. This study was approved by our institutional review board (No. 232). The patients were 5 men and 8 women with a mean age of 66.5 years (age range, 44-79 years) (Table I).
MRI study protocol
The MR examination was performed using a 1.5-T unit with a head or head-neck coil. T1-weighted images (T1WI) were acquired with a spin-echo sequence using parameters of 500 to 660/15 ms (repetition time/echo time [TR/TE]). T2-weighted images (T2WI) with fat suppression, for 9 cases, or short TI inversion recovery (STIR) images, for 4 cases, were acquired with a turbo–
spin-echo sequence, using parameters of 2800 to 3000/90 to 105 ms (TR/TE) for T2WIs and 4500, 6100/60/140 ms (TR/TE/inversion time [TI]) for STIR images. Patient images were taken in both the axial and coronal planes.
In 10 patients, contrast-enhanced T1WIs (CE- T1WIs) with fat suppression were acquired using the same parameters as the unenhanced T1WIs after the administration of contrast medium. In this study, we used 2 types of contrast medium, gadopentetate dime- glumine (Gd-DTPA) and gadodiamide hydrate (Gd- DTPA-BMA). For 7 of these 10 patients, we performed dynamic contrast-enhanced MRI (DCE-MRI) with the conditions described as follows.
The first series of DCE-MRIs was acquired using 3-dimensional fast imaging with a steady-state preces- sion sequence using the following parameters: TR 5
ms; TE 2 ms; flip angle 25°; 16 partitions for a 48-mm slab resulting in an effective thickness of 3 mm; and a 250 ⫻ 188-mm rectangular field of view and 256 ⫻ 192 matrix resulting in a 0.98 ⫻ 0.98-mm pixel size.
The first series of DCE-MRI was composed of 21 consecutive scans (17, 14, and 12 consecutive scans for 3 cases, respectively) at 1-second intervals (the acqui- sition time for each scan was 14 seconds). Total scan time of this series was 180 to 315 seconds. Before the second scan, 0.2 mL/kg contrast medium was admin- istered intravenously for 6 seconds at a rate of approx- imately 2.0 mL per second with manual injection. CE- T1WIs were acquired after the acquisition of the first series of DCE-MRIs in these 7 patients. In another 3 patients without DCE-MRIs, CE-T1WIs were acquired immediately after administration of the contrast me- dium.
Second and third series of DCE-MRIs were acquired at approximately 600 to 800 seconds and 900 to 1200 seconds (only at 800 seconds for 1 case) after the administration of contrast medium. Two consecutive scans were applied for the second and third series of DCE-MRIs, resulting in a total scan time of 30 seconds.
Evaluation of MR images
The MR images in 13 cases were retrospectively eval- uated for tumor size and signal characteristics. Regard- ing the signal intensity (SI), the signal from the mus- culature was interpreted as isointense on T1WI, and the signal from the cerebrospinal fluid was interpreted as hyperintense on T2WI and STIR images. In 9 cases
8* 79 F Palate DLBCL 23⫻ 20 ⫻ 10 Homo Iso — — Nearly homo Iso Homo L
9* 58 F BM FL 15⫻ 7 ⫻ 10 Nearly homo Hypo-Iso — — Nearly homo Iso-Hyper Hetero L 10† 74 F UG DLBCL 53⫻ 50 ⫻ 37 Nearly homo Hypo-Iso Nearly homo Iso-Hyper — — Hetero M-H
11* 68 F Maxilla DLBCL 39⫻ 40 ⫻ 32 Homo Iso — — Hetero Iso-Hyper Hetero L
12† 73 F Palate MALT 22⫻ 21 ⫻ 16 Nearly homo Hypo-Iso Nearly homo Iso-Hyper —— Nearly homo L
13 68 F Palate FL 18⫻ 12 ⫻ 9 Homo Iso Nearly homo Hypo-Iso — — — —
MRI, magnetic resonance imaging; Loc, location; WI, weighted image; CE, contrast-enhanced; DE, degree of enhancement by contrast medium;
BM, buccal mucosa; UG, upper gingiva; MaxS, maxillary sinus; DLBCL, diffuse large B-cell lymphoma; MALT, mucosa-associated lymphoid tissue; ATLL, adult T-cell leukemia/lymphoma; FL, follicular lymphoma; Homo, homogenous; Hetero, heterogeneous; Hypo, hypointense; Iso, isointense; Hyper, hyperintense; L, low; M, moderate; H, high; —, not performed.
*Cases that underwent dynamic contrast-enhanced MRI.
†Cases with contrast enhancement.
with CE-T1WI, we evaluated the degree of contrast medium enhancement as low to high.
Analysis of DCE-MRI parameters
In 7 cases with DCE-MRIs, we created CI curves using dynamic images to evaluate the flow pattern of contrast medium into the tumor mass. The region of interest (ROI) was drawn to include the maximal region of the tumor mass using the cursor on the monitor. The mean SI on the ROI of each lesion was calculated using a workstation (Synapse Vincent, Fujifilm, Medical Co., Tokyo, Japan). The CI was calculated using the formula CI ⫽ (SI [postcontrast] – SI [precontrast])/SI (precon- trast). The CI was plotted on a time course to obtain the CI curves. We evaluated the maximum CI gain (CI- gain), the maximum CI (CImax), and the CIgain/CImax ratio for the DCE-MRI parameters. The CIgain was considered to indicate the maximum gradient on the upslope phase of the enhancement curve as CIgain indicates the difference in the CI between 2 consecutive images. The CImax was considered to represent the max- imum amplitude of enhancement. The washout ratio (WR300
, and WR900
), expressed as a percentage, was defined as follows: CImax – CI300s
/ CImax ⫻ 100(%), where CI300s
, and CI900s
represent the CIs at 300, 600, and 1200 seconds after the administration of contrast medium, respectively.
, and CI900s
were calculated by obtained or linearly interpolated SIs at 315, 615, and 1215 sec- onds. The calculation with the linearly interpolated method uses the formula: y ⫽ ya
) / (xb
) ⫻ (x – xa
), where y is the SI to be obtained, x is the time to be obtained, (x, y) is the point to be obtained between point A and point B, point A ⫽ (xa
), and point B ⫽ (xb
ⱕ x ⱕ xb
. The parameters of CI curves are summarized in Figure 1.
MR findings (size and characteristics of SI) The MR findings of all cases are summarized in Table I. The mean greatest dimension of the tumor was 34.2 mm (range: 18-59 mm). On T1WIs, all cases had ho- mogeneous or nearly homogeneous SIs that were hy- pointense or isointense (Figures 2, A, and 3, A). On T2WIs (n ⫽ 9) and STIR images (n ⫽ 4), almost all cases had nearly homogeneous SIs that were isointense or hypointense (Figures 2, B, and 3, B). On the CE- T1WIs of 10 cases, almost all cases had (nearly) ho- mogeneous SIs, although the degree of enhancement was variable (Figures 2, C, and 3, C).
The CI curves and the DCE-MRI parameters, calcu- lated from a dynamic series, are shown in Figure 4 and Table II. The CI curves of 2 cases, upper gingiva and maxilla, increased rapidly, reaching a CImax of less than 1.2 at 120 to 165 seconds. After that, the CI curves showed a nearly sustained plateau until 600 seconds, and gradually decreased to 1200 seconds. The WR300
values of these cases were less than 20% and 30%, respectively. In the case of the maxillary sinus, the CI curve was similar to those of the upper gingiva and maxilla in the early phase, but showed a greater decrease in the late phase. In this case, the WR300
was less than 20%, but the WR900
was 48.6%, higher than those of the previous 2 cases. The CIgain of these 3 cases was less than 1.0, and the CIgain/CImax ratio was 40% to 55%.
The CI curves of the other 4 cases (palate, 2;
buccal mucosa, 2) increased rapidly, reaching a CI-
max greater than 2.0 at 30 to 120 seconds. The
CIgain of these 4 cases was greater than 1.5, and theFigure 1. CI curves constructed with DCE-MRI (left) and CI curve parameter definitions (right). The CI-gain was considered to indicate the maximum gradient on the upslope phase of the enhancement curve, as the CI-gain indicates the difference in the CI between 2 consecutive images. The WR300, WR600, and WR900, expressed as percentage, was defined as follows: CImax – CI300s,600s,900s/CImax⫻ 100(%), where CI300s, CI600s, or CI900sis the CI at 300, 600, or 900 seconds after contrast medium administration.
CIgain/CImax ratio was 60% to 85%. In these 4 cases, the WR300
was higher than 20%, and the WR600
of 3 cases was higher than 40%. In only 1 case of the palate, the WR600
and 35.1%, respectively.
Malignant lymphoma is the second most common ma- lignancy in the head and neck region, although its morbidity rate is not high.38-41
The occurrence rate of extranodal NHL is reported to be approximately 40%, and the most common site in the head and neck region is Waldeyer’s ring.1,8,42-48
Only 3.0% to 9.5% of ex- tranodal NHL arises in the oral region, and its most common sites are the palate and maxilla.1-7,42,44
In the cases of extranodal NHL involving the jawbone, the typical radiological finding is diffuse bone resorption, similar to that of periodontal inflam- mation and other malignant tumors.3-10
Thus, there is no specific radiological finding for this lesion. Oth- erwise, when malignant lymphoma arises at the para- nasal sinus, computed tomography (CT) images of- ten show specific findings: namely, the tumor
permeates the wall without aggressive bony destruc- tion.11,39,49-52
In NHL of the oral region, such as the jawbone and palate, this finding is not observed as often. Furthermore, in cases arising from soft tissue locally, it is difficult to diagnose NHL by conven- tional radiographs and CT images.
Generally, the soft tissue contrast resolution of MRI is superior to that of CT; however, MRIs of extranodal lymphoma in the head and neck region have been reported to show variable homogeneity and SI of tumor on both T1WIs and T2WIs.12-15
The degree of enhance- ment on CE-T1WIs has been reported to be even more variable; therefore, characterizing this lesion by MRI is difficult. Our results are consistent with previous arti- cles, including our own.12-15
Otherwise, in the analysis of DCE-MRI parameters, 2 characteristic patterns of CI curves, relating to the value of CImax and WR, were observed. In the first pattern, extranodal NHLs of the oral region were placed in 2 groups by the value of CImax; one group (n ⫽ 4) showed CImax over 2.0, whereas the other (n ⫽ 3) showed CImax less than 1.5. The lesions with CImax greater than 2.0 arose from the buccal mucosa or palate;
Figure 2. Case 5: A 58-year-old man. A, Axial T1WI shows a mass (arrow) with nearly homogeneous isointensity at the right upper gingiva (TR/TE⫽ 660/15). B, On T2WI, the lesion (arrow) appears with nearly homogeneous isointensity to hyperintensity (TR/TE⫽ 3000/90). C, On CE-T1WI, the tumor (arrow) shows moderate to high homogeneous enhancement.
Figure 3. Case 8: A 79-year-old woman. A, The mass (arrow) of the right hard palate shows homogeneous isointensity on coronal T1WI (TR/TE ⫽ 660/15). B, The STIR image shows the lesion (arrow) with nearly homogeneous isointensity (TR/TE ⫽ 4500/60). C, On CE-T1WI, there is low homogeneous enhancement in the lesion (arrow).
in contrast, the cases with lower CImax arose from the upper gingiva, maxilla, and maxillary sinus. We previ- ously reported that CImax of NHLs tended to be less than 2.0, a different outcome from that in the present study.15,35
Our previous articles, however, included 10 nodal lymphoma lesions in 5 patients and 17 lesions in 8 patients overall, and this might have led to the dif- ferences in outcome between the past studies and the present study.15,35
In the previous results for extranodal lymphomas only, the CImax values of 5 lesions were all greater than 2.0 or close to 2.0 and that of another lesion was 1.37. Furthermore, the sites of lesions were the palate (1 case, CImax ⫽ 4.24), buccal mucosa (3 cases, CImax ⫽ 1.97, 1.93, and 1.37), and orbit (2 cases, CImax ⫽ 2.33 and 1.97). The association of lesions with high CImax values with the palate and
buccal mucosa is consistent with the findings of the present study.35
On the other hand, we reported that the CImax of oral squamous cell carcinomas (SCCs) was 2.59 to 2.88, with no relationship between the CImax and the site of lesions.35-37
The conflicting results of NHL and SCC can be interpreted 2 ways. Focusing on the present study, the degree of enhancement of extranodal NHLs might differ by site, unlike oral SCCs.35-37
Another inter- pretation is that the present study might have yielded a lopsided outcome because of the small number of patients.
The second pattern we found related to washout of the contrast medium; extranodal NHLs could be di- vided into 2 groups by the WR at 900 seconds. The WR900
of 1 group (1 palate, 1 buccal mucosa, 1 max- illary sinus) was greater than 40%, with a WR600
value greater than 50% in 1 case; this means that CI curvesFigure 4. The CI curves of 3 cases (cases 5, 6, and 11) increased rapidly, reaching a CImax less than 1.2 at 120 to 165 seconds.
After that, in 2 cases (cases 5 and 11), the CI curves showed a nearly sustained plateau until 600 seconds, and gradually decreased to 1200 seconds. In case 6, the CI curve decreased more sharply than the previous 2 cases in the late phases. The CI curves of the other 4 cases (cases 2, 4, 8, and 9) also increased rapidly, reaching a CImax greater than 2.0 at 30 to 120 seconds. The CI curves in 3 of these cases (cases 2, 4, and 9) showed a gradual decrease until 600 seconds, and then a sustained plateau to 1200 seconds.
In case 8, the CI curve continued its gradual decrease to 1200 seconds.
Table II. CImax, Tmax.
, CIgain, CIgain/CImax ratio, and WR300-900
in 7 patients
Case Loc Pathology
CImax Tmax. CIgain CIgain/CImax ratio WR300 WR600 WR900
2 Palate DLBCL 2.03 90s 1.66 81.6% *50.1% 51.2% 52.2%
4 BM MALT 2.21 120s 1.79 81.0% *35.7% 45.7% 49.3%
5 UG DLBCL 1.19 165s 0.63 52.7% *14.5% 21.5% 23.6%
6 MaxS DLBCL 1.32 120s 0.55 41.5% *17.9% 39.7% 47.3%
8 Palate DLBCL 2.99 90s 1.87 62.6% 25.4% 29.6% 35.1%
9 BM FL 2.51 30s 1.92 76.6% 42.7% 51.3% —
11 Maxilla DLBCL 1.08 120s 0.59 54.5% 7.0% 8.4% 18.1%
CI, contrast index; DCE-MRI, dynamic contrast-enhanced magnetic resonance imaging; WR, washout ratio; BM, buccal mucosa; DLBCL, diffuse large B-cell lymphoma; FL, follicular lymphoma; Loc, location; MALT, mucosa-associated lymphoid tissue; MaxS, maxillary sinus; UG, upper gingiva.
*The cases using measurement value of DCE-MRI to calculate WR.
enhancement on CE-T1WIs differed from study to study because of the different intervals between con- trast medium injection and imaging.12-15
In 4 cases in this study, we used interpolated values instead of mea- sured values to calculate WR600
using 21 consecutive scans of DCE-MRIs, because no other clin- ical data were available retrospectively. In the calcula- tion of WRs at each time by the linear interpolation method, we used 2 values anteroposterior to the tar- geted time. Although the interpolated values might not be accurate, we thought they were reasonable estimates for consideration of the clinical WRs.
We could not evaluate our cases histopathologically because almost all specimens were taken by biopsy, not total extirpation. Several authors reported that DCE- MRI is useful for discrimination between benign and malignant disease, and the enhancement pattern of DCE-MRI has a relationship with tumor angiogene- sis.28,29,36,37,53-56
We also reported that the DCE-MRI parameters of oral SCC, particularly with the CIgain/
CImax ratio, were correlated with the microvessel den- sity (MVD) estimated by CD34.36
This positive corre- lation in oral SCC means that the more rapidly the CI curve increases, the higher the intratumor MVD of SCC becomes. By mechanically extrapolating the results of oral SCC into extranodal NHLs in this study, the cases with high CIgain/CImax ratios might have higher MVD than the cases with low ratios. Still, the enhancement pattern of both cases with high and low CIgain/CImax ratios showed rapid increase, and the pattern of washout was divided into 2 types: rapidly decreasing and gradually decreasing. Our results suggested that factors other than MVD might affect the enhancement pattern of extranodal NHLs of nonepithelial tumors, unlike that of oral SCCs.
We were unable to study the histopathological types of NHLs because the number of patients in our study was too small for such an evaluation. We at least confirmed, however, that the enhancement patterns of diffuse large B-cell lymphoma appeared to be variable.
In conclusion, the SIs on MRI are not specific to extranodal NHL and resemble those for other tumors of the oral and maxillofacial regions. Although the DCE- MRI parameters also lack a characteristic pattern, le- sions in which CImax is less than 1.5 or WR900
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