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1
Department of Radiology and Cancer Biology, Nagasaki University School of
Dentistry, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan.
2
Department of Radiology, Nagasaki University School of Medicine, Nagasaki
852-8501, Japan.
3
General Electric Yokogawa Medical Systems, 4-7-127 Asahigaoka, Hino 191-8503,
Japan.
Received June 28, 2001;
accepted after revision October 1, 2001.
Address correspondence to T. Nakamura.
Abstract
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SUBJECTS AND METHODS. A diffusion-weighted single-shot spin-echo type of echoplanar MR imaging was performed on the parotid or submandibular glands, or both, in 36 healthy subjects, 20 patients with Sjögren's syndrome, and six patients with sialoadenitis. The apparent diffusion coefficient of the salivary gland was calculated using two b factors (b = 500 and 1,000 sec/mm2).
RESULTS. The apparent diffusion coefficient was lower in the parotid glands (0.28 x 10-3 mm2/sec) than that of the submandibular glands (0.37 x 10-3 mm2/sec). The apparent diffusion coefficient was increased in sialoadenitis, whereas it decreased with abscess formation. The apparent diffusion coefficients of the parotid glands in patients with Sjögren's syndrome correlated with the salivary flow rates but not with the sialographic gradings of the glands. We also found a correlation of the decreases in apparent diffusion coefficients with the severity of gland damage as assessed on T1-weighted MR images.
CONCLUSION. Diffusion-weighted echoplanar MR imaging may reveal diseased states of the salivary glands.
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ADC can be defined by the following equation:
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The salivary glands are secretory organs, where various molecules are conveyed into the saliva-producing cells (acinar cells) via the capillary network, and the saliva is moving in the small ductal termination surrounded by acinar cells and is then secreted into the lumen of the excretory ductal system [3]. The secretory process is an isotonic water transport, in which the major active process is a sodium transport from the intracellular to the intercellular space. As a result, an isotonic, high-sodium, low-potassium fluid is formed and secreted into the striated ducts. This fluid is further modified mainly in the striated ducts where reabsorption of sodium chloride occurs in excess of water.
These movements of molecules and water represent the main function of the salivary glands. Within the gland, alterations in blood perfusion also occur in response to various stimuli. Therefore, such a process is altered in the diseased states of the salivary glands—for example, in sialoadenitis and Sjögren's syndrome. We applied the diffusion-weighted echoplanar MR imaging technique to the salivary gland imaging in normal and diseased states.
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The study protocol was approved by the institutional review board, and informed consent was obtained from all subjects.
MR Imaging
Initially, axial T1-weighted MR images (TR/TE, 600/14; number of
excitations, 2) of the parotid and submandibular glands were obtained by a
1.5-T MR imager (Signa Horizon LX 1.5T CV/NV; General Electric Medical
Systems, Milwaukee, WI) using a conventional spin-echo sequence. Axial
fat-suppressed T2-weighted MR images (3,200/96; number of excitations, 2) were
also obtained by a fast spinecho sequence. The section thickness was 5 mm. The
MR imaging was performed with a matrix of 256 x 224, a field of view of
24 cm2, and an interslice gap of 1 mm. We did not use contrast
enhancement.
Then, axial diffusion-weighted MR images (10,000/99) of the parotid and submandibular glands were obtained by a single-shot spin-echo type of echoplanar MR imaging sequence (General Electric Yokogawa Medical Systems, Tokyo, Japan) using a neurovascular array coil. The section thickness was 5 mm. The MR imaging was performed with a matrix of 160 x 128, a field of view of 24 cm2, and an interslice gap of 1 mm. The sequence was repeated for two values of the motion-probing gradients (b = 500 and 1,000 sec/mm2). To increase the signal-to-noise ratio, we repeated the sequence four times for each image (number of excitations, 4).
Diffusion-Weighted MR Image Analysis
As previously mentioned, the ADC was given by the following formula:
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In advance, we performed a pilot study on a single volunteer (a 25-year-old woman) using b factors of 300, 500, and 1,000. The pilot study showed that b factors of 500 and 1,000 provided satisfactory diffusion-weighted MR images of the parotid and submandibular glands, and these b factors efficiently suppressed the perfusion factors involved in the ADC (Fig. 1A,1B,1C). Therefore, in the present study, we used b factors of 500 and 1,000.
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Analysis was performed in regions of interest placed in the glands. Each region of interest was placed manually in the gland parenchyma on all slices that contained the gland, and measurements were averaged for a single gland. Each region of interest was variable so that it included as much of the gland as possible. The gland regions that contained large vessels, such as the retromandibular vein in the parotid gland, were not analyzed. Measurements obtained from bilateral glands were averaged in normal subjects and patients with Sjögren's syndrome.
MR Imaging Gradings of Sjögren's Syndrome
Based on the obtained T1-weighted MR images, we classified the parotid
glands into four grades (G1-G4) as previously described in the literature
[4]; a gland with a higher
grade was classified as being more severely affected. For measurements of the
signal intensity of the parotid glands, regions of interest were defined in
the gland. Signal intensities were determined in each gland and also in the
neighboring masseter muscle and air. Because signal intensity was not an
absolute measurement, we determined its relative value in two tissues by
calculating the signal-intensity ratio as follows:
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Salivary Flow Rate Test
The salivary flow rate of patients with Sjögren's syndrome was
quantified in 19 of the 20 patients by Saxon's test and expressed as grams per
2 min. A sterile gauze was placed in a screw-topped 50 mL plastic tube (Blue
Max; Falcon Labware, Oxnard, CA), and the dry gauze and tube were weighed.
After preexisting oral fluid was removed, saliva was collected by having
patients chew vigorously on the gauze for exactly 2 min (one bite per second).
The salivary flow rate was determined by subtracting the original weight from
the weight obtained after chewing.
Sialography
Sialography of the parotid gland was performed on 19 of the 20 patients
with Sjögren's syndrome using the nonionizing contrast medium iopamidol
(Iopamiron; Schering AG, Berlin, Germany). The sialographic staging of
Sjögren's syndrome was determined on the basis of the lateral views,
according to criteria developed by Rubin and Holt
[5]. Sialographic results were
classified into stage 1 (punctate), stage 2 (globular), stage 3 (cavitary), or
stage 4 (destructive).
Statistical Analysis
Significance in correlations between the ADCs and the salivary flow rate or
the MR stagings of the parotid glands in patients with Sjögren's syndrome
was assessed by Spearman's rank correlation test using commercially available
statistical software (StatView 4.51; Abacus Concepts, Berkeley, CA).
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Sialoadenitis
Of the four patients with sialoadenitis of the submandibular glands
resulting from sialolithiasis, three patients showed increased ADCs of the
affected glands relative to the opposite healthy glands
(Table 1). In one patient,
inflammatory and healthy submandibular glands showed similar levels of ADCs.
In the parotid glands with sialoadenitis, we could identify the
high-signal-intensity areas on fat-suppressed T2-weighted gland images,
suggestive of the abscess formation. We performed contrast-enhanced CT on
these patients to distinguish abscess from cellulitis in the parotid glands.
In these patients, CT showed ring enhancement with a central low attenuation
area characteristic of abscess. Thus, we calculated ADCs of such abscess areas
separately from the remaining portions of the parotid glands. In a 70-year-old
woman, we confirmed abscess in the gland at surgery. In the nonabscess
edematous lesions, the ADCs were higher than those in the opposite healthy
glands (Table 1). However, the
abscess formation was associated with decreased ADCs even lower than those of
the healthy glands (Fig.
4A,4B,4C,
Table 1).
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Sjögren's Syndrome
Salivary gland dysfunction in Sjögren's syndrome is characterized by
progressive impairment in the production and excretion of the saliva due to
acinar destruction by autoimmunized lymphocytes. Therefore, we first examined
whether the ADC of the parotid gland was correlated with the progressive
impairment in salivary flow rate. Because it is difficult to differentiate the
salivary flows from the parotid glands and from the other salivary glands, we
compared the ADC of the parotid gland and the total salivary flow rate as
determined by Saxon's test. As shown in Figures
5A,5B,5C
and 6, the ADC of the parotid
gland was correlated with the impairment of the salivary flow function (ADC =
0.0000759 x In [salivary flow rate] + 0.0002162, r = 0.75,
p = 0.0064).
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These findings suggested that the degrees of gland damage in Sjögren's syndrome may correlate with the ADC. Furthermore, when the parotid glands in patients with Sjögren's syndrome were classified into four grades on the basis of T1-weighted MR images, the ADCs were significantly lower in the glands at higher (more severe) grades (p = 0.0030) (Fig. 7). However, no unidirectional correlation was found between the sialographic staging and the ADCs of the parotid glands. Sialography showed that the patients with Sjögren's syndrome comprised 10 patients at stage 1, three patients at stage 2, three patients at stage 3, and three patients at stage 4. In the early to mid stages (stages 1-3), the ADC was gradually increased, whereas in the advanced stage (stage 4) of sialography, the ADCs were markedly decreased (Fig. 8).
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Normal Glands
The parotid gland is purely serous, whereas the submandibular gland is a
mixed gland composed of serous and mucous acini
[3]. The parotid gland contains
an abundant amount of adipose tissue that occupies about a half of the gland
parenchyma. In contrast, adipose tissue is not a substantial component of the
parenchyma of the submandibular gland. Hence, the differences in gland
components may lead to the differences in the ADCs of the parotid and
submandibular glands. In fact, diffusion-weighted MR imaging efficiently
differentiated cysts containing fluid with different viscosity
[6]. However, increases in the
amount of adipose tissue in the breast were reported to be associated with
decreases in the ADC [7].
Therefore, lower ADCs of the parotid glands relative to the submandibular
glands may be a balance of the viscosity of the saliva present in the gland
acini and the ductal system and the amount of adipose tissue in the gland
parenchyma.
Sialoadenitis
Sialoadenitis resulting from sialolithiasis in the submandibular glands was
basically characterized by a combination of decreased signal intensities on
T1-weighted images and increased intensities on fat-suppressed T2-weighted
images, a combination of increased signal intensities on T1-weighted images
and decreased or unchanged intensities on fatsuppressed T2-weighted images, or
no apparent change on T1- or T2-weighted images
[8].
In the present study, all of the submandibular glands affected by sialoadenitis caused by sialolithiasis revealed the first type of MR imaging features (decreased signal intensities on T1-weighted images and increased intensities on T2-weighted images). These glands were frequently associated with clinical symptoms such as pain and swelling and were histopathologically characterized by active inflammation with extensive infiltration of inflammatory mononuclear cells. We found that the ADC was higher in such glands with sialoadenitis than that of the opposite healthy glands of each patient. These findings may indicate that increases in the ADC reflect the edematous states of the gland with sialoadenitis.
However, one of these patients with sialoadenitis, who presented with more severe clinical symptoms such as pain and swelling of the gland compared with the other three patients, was associated with an ADC similar to that of the opposite healthy gland. One possible explanation is that in severely affected glands with sialoadenitis, the damaged glands may contain protenaceous contents from dead cells that may increase the viscosity of the extracellular water contents. A preceding report described that brain abscesses showed restricted diffusion likely due to the presence of viscous pus [9], supporting the previously mentioned notion.
Interestingly, in this context, the abscess formation in the parotid glands was associated with decreased ADCs, probably reflecting decreased water mobility due to increased viscosity (accumulating pus) of the lesion. Therefore, the submandibular glands displaying an ADC at similar levels to the healthy counterpart may be a result of a balance between an edematous low-viscosity component and a puslike high-viscosity component of inflammation. Collectively, the present findings suggest that the inflammatory states of the glands influence the ADC of the gland with sialoadenitis. This notion seems provocative and deserves further evaluation.
Sjögren's Syndrome
The salivary glands affected by Sjögren's syndrome were characterized
histopathologically by the infiltration of mononuclear leukocytes and
destruction of gland acini, and the glands were also characterized by varying
degrees of fat deposition, which may replace most of the gland parenchyma in
the latest phase of the disease
[4,
10]. This senario was
correlated with the observed changes in the ADC, which decreased with the
severity of the salivary dysfunction.
The changes in ADC were also decreased correlatively with the severity of the gland damage as assessed by signal intensity ratios of the glands on T1-weighted images. The inflammatory glands and the glands affected by Sjögren's syndrome share common histopathologic features such as inflammatory mononuclear cell infiltrations, but the ADCs of those glands were distinct. The glands with sialoadenitis displayed increased ADCs, whereas the glands with Sjögren's syndrome were associated with decreased ADCs. This change may be attributed to the states of extracellular water in these glands. In the glands affected by Sjögren's syndrome, extensive edema may not coexist with infiltrating inflammatory mononuclear cells [8].
Sialography of the salivary glands with Sjögren's syndrome shows punctate to cavitary staining patterns [5], which were pathognomonic features of the disease. However, in the present study population, sialographic gradings of the parotid glands did not correlate with changes in the ADCs of the glands. One of the most likely explanations for these findings may be that, at the end-stage (destructive), the parotid gland is almost completely replaced by fat tissue, and thus the ADC is markedly decreased because of a severe decrease in the amount of fluid in the gland. In contrast, in the gland at the cavitary stage, the fluid is still preserved in the cystic cavity, and thus the ADC is higher than those in the glands at milder stages (punctate and globular). A previous report showed that T2-weighted MR imaging features of the parotid glands at the end-stage of Sjögren's syndrome displayed signal intensity levels similar to those at earlier stages of the disease [4], consistent with the present findings. However, in the present study, saliography was performed on small numbers of patients at each stage. Large numbers in each group might have shown something slightly different from the present findings. Collectively, these findings imply that diffusion-weighted MR imaging monitored the water or molecular diffusion in the gland parenchyma, whereas sialography simply detected the ductal changes in the glands.
In the present study, we took advantage of echoplanar imaging, which allows rapid imaging of the body, avoiding motion artifacts. The disadvantages of echoplanar imaging are low signal-to-noise ratios and high susceptibility artifacts. We attempted to increase the signal-to-noise ratios by repeating the sequence four times for each image. However, the problem of high-susceptibility artifacts remained, which may be serious when imaging head and neck diseases because of dental amalgams.
In conclusion, we determined the ADCs of the salivary glands using diffusion-weighted echoplanar MR imaging to clarify that the parotid glands possessed lower ADCs compared with the submandibular glands. We also found that the ADCs characteristically changed in the glands with sialoadenitis (edematous glands or abscess) or Sjögren's syndrome. These changes in ADCs may be due to changes in the extra-cellular water content and its viscosity in the gland parenchyma.
Taken together, the present findings suggest that the ADCs obtained by the diffusion-weighted MR imaging of the salivary glands could provide useful information about extra-cellular water in the gland parenchyma, which is distinct from that of the ductal changes in the diseased glands, as obtained by sialography.
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