Nuclear Medicine Communications:
Comparison between sarcoidosis and IgG4-related disease by whole-body 67Ga scintigraphy
Ishii, Shirou; Miyajima, Masayuki; Sakuma, Kotaro; Kikuchi, Ken; Shishido, Fumio
Fukushima Medical University Hospital, Department of Radiology, Fukushima Medical University, Fukushima, Japan
Correspondence to Shirou Ishii, PhD, MD, Fukushima Medical University Hospital, Department of Radiology, 1, Hikarigaoka, Fukushima, Japan Tel: +81 24 547 1111; fax: +81 24 549 3789; e-mail: email@example.com
Received August 7, 2012
Accepted September 7, 2012
Purpose: The aim of this study was to compare uptake lesions in sarcoidosis and IgG4-related disease through gallium-67 (67Ga) scintigraphy to differentiate between the two diseases.
Materials and methods: Whole-body 67Ga scintigraphy findings of 27 patients with sarcoidosis and 16 with IgG4-related disease were reviewed between 2005 and 2011 at our hospital.
Results: In the case of patients with sarcoidosis, significant accumulation of 67Ga was observed in the lacrimal gland in the case of 26 patients (96%), in mediastinal lymph nodes (LNs) in 23 (85%), in pulmonary hilar LNs in 21 (78%), in the parotid gland in 10 (38%), in supraclavicular LNs in eight (30%), in muscles in seven (26%), in the lung in five (18%), in inguinal LNs in four (15%), in submandibular LNs in two (7%), and in the heart, spleen, kidney and para-aorta in one patient (4%). In patients with IgG4-related disease, abnormal uptake was detected in the pulmonary hilar LNs in 12 patients (75%), in the lacrimal gland in 10 (62%), in the pancreas in 10 (62%), in the parotid gland in six (37%), in the submandibular gland in six (37%), in the para-aorta in three (19%), in the lung in three (19%), in mediastinal LNs in two (12%), and in the kidney in the case of two patients (12%). Asymmetrical accumulation in the submandibular gland was observed in three of six patients (50%) with IgG4-related disease and in none of the two patients (0%) with sarcoidosis. Significant differences were observed in the uptake ratio of the lacrimal gland, the submandibular gland, supraclavicular LNs, mediastinal LNs, pancreas, and muscle between the two groups (P<0.05).
Conclusion: 67Ga scintigraphy was useful in differentiating between the two diseases. Uptake in mediastinal LNs, in supraclavicular LNs, and in the muscle was specific to sarcoidosis, whereas uptake in the pancreas and in the submandibular gland indicated IgG4-related disease.
IgG4-related disease is a newly recognized systemic autoimmune disease that includes Mikulicz’s disease, retroperitoneal fibrosis, autoimmune pancreatitis (AIP), and sclerotic cholangitis 1–6. IgG4-related disease is characterized by IgG4-positive plasma cells and T-lymphocyte infiltration in various organs such as the pancreas, the bile duct, the gallbladder, the salivary gland, the retroperitoneum, and the kidney, lungs, and prostate 1–4. It commonly occurs in elderly men but its exact incidence is unknown 1. Clinical manifestations of this disease depend on the lesion involved and a soft tissue mass could be observed in the various organs on imaging study 7–9. Because IgG4-related disease responds well to steroid therapy, its accurate diagnosis is important for appropriate treatment and avoidance of unnecessary surgery 1–6.
Sarcoidosis is characterized by noncaseous epithelioid cell granulomas, which involve multiple organs such as mediastinal, pulmonary hilar, and peripheral lymph nodes (LNs) as well as the lungs, liver, spleen, muscle, skin, eyes, and parotid glands 10–14. Both IgG4-related disease and sarcoidosis are benign systematic diseases with overlapping infiltrating lesions.
Differential diagnosis between these diseases is sometimes difficult and coincidental occurrence of both diseases has been reported 15–17. In gallium-67 (67Ga) scintigraphy, both entities have been reported to demonstrate uptake in pulmonary hilar LNs, lungs, and the salivary gland 8,9,18,19. Further, it has been reported that previously undiagnosed suspected sarcoidosis may include cases of unrecognized IgG4-related disease 17,20.
We previously reported 67Ga scintigraphic findings in cases of IgG4-related disease 9. The present report describes the difference in accumulation sites between these two diseases using 67Ga scintigraphy.
Materials and methods
We retrospectively investigated 1650 consecutive patients who underwent gallium scintigraphy at our hospital between January 2005 and December 2011. Of them, 16 patients with IgG4-related disease and 27 with sarcoidosis who underwent 67Ga scintigraphy before steroid therapy were enrolled in this study.
Diagnosis of IgG4-related disease was based on the presence of elevated serum IgG4 (>135 mg/dl), a combination of histopathological features including lymphocyte and IgG4-positive cell infiltration, and specific organ involvement (pancreas, salivary grand, lacrimal gland, biliary duct, retroperitoneum) 21. Eleven patients were diagnosed as having AIP according to the Japanese Pancreas Society criteria 22. Three patients were diagnosed by histopathology of dense infiltration of IgG4-positive cells: in the submandibular LN in one patient and in the lacrimal glands in the other two. Involvement of other organs was also observed in all three patients on computed tomography (CT) examination. CT images, laboratory data, and clinical examination showed two patients to have elevated IgG4 and involvement of salivary glands; biliary duct involvement was also observed in one patient. Elevation of serum IgG4 was confirmed in all patients, and all but two showed good response to steroid therapy. One patient with AIP underwent partial resection of the pancreas without subsequent corticosteroid therapy. Another patient with sialadenitis and cholangitis was followed up without steroid therapy. Pancreatic cancer was excluded by biopsy or resection in all patients with AIP.
Diagnosis of sarcoidosis was based on the pathology report, on the basis of examination of the adenopathy lesion by transbronchial lung biopsy, neck LN biopsy, or skin biopsy. Four patients who were clinically suspected of having sarcoidosis without pathological findings were excluded from this study.
67Ga citrate imaging
Whole-body 67Ga imaging was performed 48–72 h after intravenous administration of 74 MBq 67Ga citrate (Fujifilm RI Pharma, Tokyo, Japan). Anterior and posterior views of the whole body were obtained on an E.CAM (Siemens Medical Systems, Chicago, Illinois, USA) using two-headed cameras equipped with a middle-energy, parallel-hole collimator at a scan speed of 10 cm/min, matrix of 512×1024, energy discrimination set to 92 keV±20%, and 185 keV±20% consideration of the 67Ga photopeaks.
Visual analysis of the 67Ga planar images was performed by two radiologists with 10 and 7 years of experience in nuclear medicine. Readers were unaware of CT scan findings, the accompanying reports, clinical information, and diagnosis pertaining to whether the findings confirmed sarcoidosis or IgG4-related disease. Images were evaluated independently and the final decision was made by consensus. Accumulation in the lacrimal gland, salivary gland, lung, supraclavicular LNs, mediastinal LNs, pulmonary hilar LNs, pancreas, kidney, muscle lesions, and para-aortic lesions was evaluated, as well as other lesions with abnormal uptake. Uptake in the parotid gland and submandibular gland was evaluated to determine which gland showed a stronger uptake. Asymmetry of accumulation was also assessed.
Statistical analysis was performed using SPSS software for windows (17.0; SPSS Inc., Chicago, Illinois, USA). Age was presented as mean±SD. The Mann–Whitney U-test was used to compare the ages of patients in the IgG4-related disease and sarcoidosis groups. The χ2-test was used to analyze the sex ratio and accumulation sites of the two groups. Differences between the groups were considered significant when P value was less than 0.05.
The Fukushima Medical University local research ethics committee approved this study.
The patient population of the IgG4-related disease group comprised 14 men and two women, ranging in age from 47 to 80 years (mean age±SD, 62.5±9.9 years). Patients belonging to the sarcoidosis group comprised 14 men and 13 women, ranging in age from 23 to 77 years (54.7±16.9 years).
In patients with sarcoidosis, significant accumulation of 67Ga was observed in the lacrimal gland in the case of 26 patients (96%), in mediastinal LNs in 23 (85%), in pulmonary hilar LNs in 21 (78%), in the parotid gland in 10 (38%), in supraclavicular LNs in eight (30%), in the muscle in seven (26%), in the lungs in five (18%), in inguinal LNs in four (15%), in submandibular LNs in two (7%), and in the heart, spleen, kidney and para-aorta in one patient (4%).
In patients with IgG4-related disease, abnormal uptake was detected in the pulmonary hilar LNs in the case of 12 patients (75%), in the lacrimal gland in 10 (62%), in the pancreas in nine (56%), in the parotid gland in six (37%), in submandibular LNs in six (37%), in the para-aorta in three (19%), in the lung in three (19%), in mediastinal LNs in two (12%), and in the kidney in two patients (12%).
Asymmetrical accumulation in the parotid gland was observed in two of six patients (33%) with IgG4-related disease and in three of 10 patients (30%) with sarcoidosis.
Asymmetrical accumulation in the submandibular gland was observed in three of six patients (50%) with IgG4-related disease and in none of the two patients with sarcoidosis (0%).
Of the patients with IgG4-related disease, seven demonstrated parotid and/or submandibular gland uptake. 67Ga scintigraphy showed stronger uptake in the submandibular gland than in the parotid gland in three patients. Uptake in the parotid gland was stronger than in the submandibular in two patients and at the same level in another two. Of patients with sarcoidosis, 10 demonstrated parotid and/or submandibular gland uptake. Uptake in the parotid gland was stronger than that in the submandibular gland in eight patients, and parotid gland accumulation was at the same level of submandibular gland accumulation in two.
There were significant differences in age and sex ratio between the two groups (P<0.05). Significant difference was also observed in the uptake ratio of the lacrimal gland, the submandibular gland, supraclavicular LNs, mediastinal LNs, the pancreas, and muscle (P<0.05). There were no significant differences in the uptake ratio of the parotid gland, pulmonary hilar LNs, lungs, heart, spleen, kidney, para-aorta, and inguinal LNs (Table 1).
67Ga scintigraphy has been used to diagnose and evaluate the extent of sarcoidosis and monitor patients after treatment 11,13,23. Uptake in the intrathoracic LNs and in both lacrimal and salivary glands called Lambda and Panda signs is useful in diagnosing sarcoidosis; however, accumulation in the lacrimal and salivary glands and in hilar LNs has also been observed in patients with IgG4-related disease 9,12,13,18,19,23. Indeed, this study found overlapping accumulation sites in many organs in sarcoidosis and IgG4-related disease. Until now, similar therapies have been used for both sarcoidosis and IgG4-related disease 1,4,10. However, the rate of cardiac death is high in patients with sarcoidosis and hence differentiation between sarcoidosis and IgG4-related disease is important from the viewpoint of prognosis, patient management, and disease conception 10,24,25.
Sarcoidosis typically affects adults less than 40 years of age; however, there is a second peak incidence in women over 50 years of age in Japan 14,26,27. However, AIP, the most common type of IgG4-related disease, occurs mostly in older men 1,4. This predilection almost corresponds with the results of the present study, in which significant differences were observed in age and sex ratio between sarcoidosis and IgG4-related disease.
Accumulation in the submandibular glands was observed with significant difference in six of 16 patients (37%) with IgG4-related disease compared with two of 27 patients (7%) with sarcoidosis. Uptake in the parotid gland was observed in three patients (37%) with IgG4-related disease and in 10 patients (38%) with sarcoidosis, with no significant difference. Asymmetrical accumulation in the submandibular gland was observed in three of six patients (50%) with IgG4-related disease and in no patient (0%) with sarcoidosis. In cases with IgG4-related disease, 67Ga scintigraphy showed stronger uptake in the submandibular gland than in the parotid gland in three patients. Uptake in the parotid gland was stronger than in the submandibular in two patients and at the same level in two others. However, in cases with sarcoidosis, there was no patient whose uptake in the submandibular gland was stronger than that in the parotid gland. This asymmetric uptake and high accumulation in submandibular glands rather than in parotid glands are characteristic findings of IgG4-related disease (Fig. 1). There are also other diseases with salivary gland uptake, such as chronic sialadenitis and Sjogren’s syndrome; it is important to exclude these diseases 23.
Accumulation in the pulmonary hilar LNs was observed in 21 patients (78%) with sarcoidosis and in 12 patients (75%) with IgG4-related disease. This finding was observed in both diseases in high frequency with no significant difference. In contrast, uptake in the mediastinal LNs and supraclavicular LNs was observed with significant differences in 23 (85%) and eight patients (30%) with sarcoidosis and in two (12%) and no patients (0%) with IgG4-related disease, respectively. Uptake in the mediastinal LNs and supraclavicular LNs indicates sarcoidosis. Although we did not conduct a quantitative assessment in this study, accumulation in pulmonary hilar LNs in patients with sarcoidosis was more intense compared with that in patients with IgG4-related disease (Figs 1–3).
It has been reported that simultaneous uptake called Lambda and Panda signs is specific for patients with sarcoidosis 12,19. Although the Panda sign and simultaneous uptake in hilar LNs were observed in one patient, this characteristic simultaneous uptake of Lambda and Panda signs was not observed in patients with IgG4-related disease in this study. This finding was observed in six of 27 patients (22%) with sarcoidosis in the present study.
Uptake in muscle was not observed in patients with IgG4-related disease but was observed in seven patients (26%) with sarcoidosis, with significant difference. Uptake in muscle in the lower leg was seen in six patients and in the shoulder and four limbs in one. Asymptomatic muscle involvement has been reported to occur in 50–80% of patients with sarcoidosis 28. None of our patients had symptoms of muscle involvement (Fig. 2).
Abnormal uptake in the heart, spleen, and inguinal LNs was not observed in patients with IgG4-related disease but was observed in one (4%), one (4%), and four (15%) sarcoidosis patients, respectively. Although the accumulation rates of these organs were low and a significant difference was not observed between the two groups, they are important clues for differential diagnosis, determination of optimum biopsy site, and assessment of the involved lesion. In particular, cardiac involvement may lead to fatal outcome and needs immediate investigation and therapy 24,25 (Fig. 3).
Uptake in the pancreas due to AIP was observed in 56% of patients with IgG4-related disease but in no patient with sarcoidosis. This finding is useful in differentiating sarcoidosis from IgG4-related disease. However, this might not be an absolute finding because pancreatic sarcoidosis and uptake of FDG in the pancreas were reported; hence, uptake of 67Ga in the pancreas may be observed 29–31. Determination of accumulation of 67Ga in the pancreas using only planar imaging is sometimes difficult because of overlapping regions such as the transverse colon, unless an apparently high uptake is observed in the middle to left abdominal region. If pancreatic uptake is suspected, a single-photon emission computed tomography (SPECT) scan, or reference to other modalities such as CT or MRI, may be needed (Fig. 4).
Uptake in the lacrimal gland is well observed in cases of both sarcoidosis and IgG4-related disease with no significant difference. Although both diseases can involve the lacrimal gland, it is sometimes difficult to differentiate from physiological uptake unless very strong uptake or laterality is observed. Determination of the level of accumulation requires experience, and diagnosis using only this finding is difficult.
Lung and renal involvement has been reported in both diseases. However, a significant difference was not observed between the two diseases in this study with respect to accumulation at either site 8,32–38. Lung parenchymal lesion is common in sarcoidosis compared with IgG4-related disease but the uptake rate in the lung parenchyma in sarcoidosis was lower in the present study 14,27,32–34.
To date, no study has reported a comparison between sarcoidosis and IgG4-related disease using 67Ga scintigraphy. Many reports on sarcoidosis and a few on AIP on the usefulness of 67Ga or 18F-FDG PET in the evaluation of the two diseases have been published 8,9,11,13,18,37–41. The results of studies comparing the ability of 18F-FDG PET and 67Ga in the detection of sarcoidosis have suggested that 18F-FDG PET can detect more involved lesions 37,38. This is considered to be a limitation of using only planar 67Ga imaging because of its lower spatial resolution and overlap of organs. A combination of SPECT and CT for evaluation may improve the detection of involved lesions.
18F-FDG PET might contribute to a clearer differential diagnosis of both diseases. Evaluation by 18F-FDG PET or 67Ga scintigraphy has the advantage of evaluating the whole body – that is, not only lesions in the body trunk but also diseases of the head, neck, and four limbs simultaneously. Indeed, most muscle lesions were difficult to detect by routine CT, and, as symptomatic muscle involvement is uncommon, muscle examination by MRI is rarely carried out 28.
The retrospective nature of the study and the small number of cases studied contribute to the limitations of the study. Immunohistochemical findings for IgG4 were not available for all patients. Further, because histopathological verification was not obtained for each lesion showing accumulation, there is no proof that the uptake lesion was involved in sarcoidosis or IgG4-related disease. Several diagnostic criteria and terms defining IgG4-related disease have been proposed but none have been established 1–6,42. We used one of the proposed criteria for IgG4-related disease; however, other criteria might be adopted internationally in the immediate future. We assessed only whole-body planar images. More lesions can be detected by SPECT imaging.
Lesions of both sarcoidosis and IgG4-related disease that show accumulation may overlap in many organs. Uptake in mediastinal LNs, supraclavicular LNs, and muscles is highly specific to sarcoidosis, whereas uptake in the pancreas and submandibular gland, especially asymmetrical uptake in the submandibular gland, indicates IgG4-related disease. The differential diagnosis between the two diseases is important from the viewpoint of prognosis and patient management.
Conflicts of interest
There are no conflicts of interest.
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autoimmune pancreatitis; 67Ga scintigraphy; IgG4; Mikulicz’s disease; sarcoidosis
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