MSCT Pulmonary Manifestations and Complications of Long Standing Sarcoidosis
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1 Med. J. Cairo Univ., Vol. 83, No. 1, March: 1-9, MSCT Pulmonary Manifestations and Complications of Long Standing Sarcoidosis YOUSSRIAH Y. SABRI, M.D.; IMAN M. HAMDY, M.D.; IRENE SABRY, M.D. and AHMED A. BAZ, M.Sc. The Department of Radiology, Thoracic Imaging Unit, Faculty of Medicine, Cairo University Abstract Background: Sarcoidosis is a multisystem chronic inflammatory condition of unknown etiology. It is known to have mediastinal lymphadenopathy and parenchymal perilymphatic distribution of its granulomas. In long standing cases, however, fibrosis and honey combing described as fibrocystic changes with classic broncho-centric and upper zonal predilection are recognized. Mycetoma is a reported complication of fibrocystic sarcoidosis. Multi-slice computed tomography (MSCT) especially high-resolution technique (high resolution computed tomography, HRCT) play a very important role in diagnosing pulmonary manifestations and detect the possible complications of long standing sarcoidosis. Aim of the Work: The purpose of this study is to depict the pulmonary parenchymal changes and the possible complications in long standing sarcoidosis and to explore the role of MSCT/HRCT in its diagnosis. Patients and Methods: This study included 23 cases 20 females and 3 males, age range 45 to 62 years old (average years). Cases were referred to the Radiology Department Kasr Al-Aini for MSCT/HRCT assessment of the chest. All patients were known cases of sarcoidosis with duration of illness ranging from five to seventeen years (5-17 years), all were subjected to thorough clinical evaluation, laboratory assessment. CT chest (with high resolution technique) done to all patients using MDCT (Toshiba- Aquillion, 64 detectors). Results: In this study multi-slice and high resolution computed tomography (MSCT with high resolution technique; HRCT) detected various CT chest signs in long standing sarcoidosis patients. Key Words: Multi-slice computed tomography High resolution technique Long standing sarcoidosis. Introduction SARCOIDOSIS is a multisystem disorder of unknown cause that is characterized by the presence of non caseating granulomas and the proliferation of epithelioid cells [1]. Correspondence to: Dr. Youssriah Y. Sabri, The Department of Radiology, Thoracic Imaging Unit, Faculty of Medicine, Cairo University Although sarcoidosis can affect patients of any age, sex, or race, it typically affects adults less than 40 years old, and the incidence peaks in the 3rd decade of life, classically more in women than in men [2]. The diagnosis of sarcoidosis is commonly established based on clinical and radiological findings that are supported by histological findings [3]. The histological hallmark of sarcoidosis is non caseous granuloma [4]. Fibrotic changes usually begin at the periphery of a granuloma and extend centrally, leading to complete fibrosis and hyalinization, or both [5]. The upper lobes of the lung are most severely affected [6]. Vascular involvement is observed in more than half of patients with sarcoidosis who undergo an open lung biopsy or autopsy study [7]. The clinical signs and symptoms are non specific and include fatigue, general malaise, weight loss, and less commonly fever [3]. The characteristic radiological findings associated with sarcoidosis have been well described and the findings include bilateral hilar lymphadenopathy and parenchymal abnormalities [8]. Multiple small nodules in a perilymphatic distribution along with irregular thickening of the interstitium are typical CT findings of sarcoidosis [3]. The clinical course varies; nearly two-thirds of patients with sarcoidosis generally remain stable or experience a remission within a decade after diagnosis, with few or no consequences thereafter [8,9]. However, approximately 20% of patients develop chronic disease leading to pulmonary fibrosis [10]. Less than 5% of patients die of sarcoidosis; death from sarcoidosis is usually the result of extensive and irreversible lung fibrosis with respiratory failure or cardiac or neurological 1
2 2 MSCT Pulmonary Manifestations & Complications involvement [11]. Sarcoidosis-associated pulmonary hypertension (SAPH) has been reported by several groups [12,13]. More than 40 years ago, Siltzbach developed a sarcoidosis staging system based on the pattern of plain chest radiographic findings [3] The Siltzbach classification system defines the following five stages of sarcoidosis in plain chest radiography: Stage 0, with a normal appearance at chest radiography; stage 1, with lymphadenopathy only; stage 2, with lymphadenopathy and parenchymal lung disease; stage 3, with parenchymal lung disease only; and stage 4, with pulmonary fibrosis [7]. Computed tomography added a great value in establishing diagnosis, staging and detection of complications of long standing thoracic sarcoidosis, sometimes giving more anatomic and pathological details that were undetectable by conventional plain radiography. High resolution technique (HRCT) demonstrates normal and abnormal lung interstitium and morphologic characteristics of both localized and diffuse parenchymal abnormalities; in this regard, HRCT is clearly superior to plain radiographs and conventional CT. A role for high resolution computed tomography (HRCT) exists when patients present with atypical clinical or radiographic findings, for detection of complications, or in the context of a normal radiograph but clinical disease suspicion,thus changing the staging with plain radiography [6,14-17]. Parenchymal fibrotic changes: In most patients, sarcoid granulomas resolve with time [8]. However, in an estimated 20% of patients, fibrosis becomes more prominent over time, producing CT and radiographic findings of linear opacities, traction bronchiectasis, and architectural distortion (displacement of fissures and broncho-vascular bundles). Fibrosis is seen predominantly in the upper and middle zones, in broncho-centric pattern or in patchy distribution [18]. Extensive interstitial fibrosis can cause pulmonary arterial hypertension and resultant right side heart failure [19]. Fibrotic changes may manifest as conglomerate masses with broncho-centric distribution associated with marked traction bronchiectasis [20]. These processes are usually seen predominantly in the central and upper lung. Again, this distribution is typical of sarcoidosis but can also be seen in tuberculosis and silicosis. Extensive calcification may be encountered within fibrotic granulomas [3]. Fibrotic cysts, bullae, and paracicatricial emphysema represent advanced-stage sarcoidoses which are irreversible changes [21]. Fibrotic and cystic lesions typically involve the upper and middle lung zones and follow the large airways in a peri-hilar distribution [22]. Posterior displacement of the main or upper-lobe bronchus and volume loss (particularly in the upper lobes) are characteristic features of chronic fibrosis [3] see Tables (1,2). Honeycomb-like cysts in patients with sarcoidosis are most commonly distributed in the subpleural regions of the middle and upper lung zones, whereas the lung bases are usually spared [23]. Occasionally this pattern of fibrocystic change is seen in the lower lung zones, an atypical location that may cause pulmonary sarcoidosis to be mistaken for idiopathic pulmonary fibrosis [24,25]. The formation of mycetomas is a wellrecognized complication of long standing sarcoidosis [26]. Fungal balls may develop when preexisting bullae and cysts (typically in the upper lobes) are colonized by saprophytic fungi, usually Aspergillus species [27]. Aim of the work: The purpose of this study is to depict the pulmonary parenchymal changes and the possible developed complications in long standing sarcoidosis and to explore the role of MSCT using the high resolution technique (HRCT) in its diagnosis. Patients and Methods This study included 23 cases 20 females and 3 males, age range 45 to 62 years old (average years). Referred to the Radiology Department Kasr Al-Aini at the period from , till All patients were already known to be cases of sarcoidosis with duration of illness ranging from five to seventeen years (5-17 years), all were subjected to thorough clinical evaluation, laboratory assessment. CT chest (with high resolution technique) was done to all patients using MDCT (Toshiba-Aquillion, 64 detectors). Thirteen out of them were under therapy by corticosteroids for periods ranging from five years to fifteen years and were coming for follow-up. All patients had progressive dyspnea and dry cough while two patients had hemoptysis. Inclusion criteria: Known cases of long standing sarcoidosis.
3 Youssriah Y. Sabri, et al. 3 Exclusion criteria: Recent onset of sarcoidosis. Methods: Thorough clinical evaluation and laboratory assessment. CT chest done to all patients using multi-detector computed tomography MDCT (ToshibaAquillion, 64 detectors). High-resolution CT was done in all patients for detection of chronic pulmonary parenchymal changes (Figs. 1-7), see Table (3). Pulmonary function tests: Done to all patients and showed restrictive changes in 20 patients, mixed changes in two patients and no appreciable changes in one patient. Results This study included 23 cases with sarcoidosis. HRCT chest results showing different parenchymal lesions, their distribution as well as the fibrotic changes Tables (4,5). Table (3): Helical HRCT protocol for Toshiba aquilion multislice 64 channels CT scanner at Kasr Al-Aini Hospital. Preparation: Not needed. IV contrast: Not needed. CT scanning: CT scan examinations are performed using Toshiba Aquilion multislice 64 channels. The examination is done in supine position. A scout is taken with 120kV and 120mA, and then helical scanning is done in caudo-cranial direction to minimize respiration artifacts. Using 64 detector row. Slice thickness 1.0mm. Pitch 1.5:1. Speed (mm/rotation) 7.5mm. Detector configuration 64x1. Beam collimation 5mm. Interval 5mm. Gantry tilt 0.0. FOV depends on the patients body built, but is about 35cm. kv 120. ma Total exposure time 7 seconds during breath hold in inspiration. Table (1): Pulmonary manifestations and complications of chronic sarcoidosis at high-resolution CT [3]. Morphological changes Fibrotic changes: Bronchocentric fibrosis, reticular opacities, architectural distortion, traction bronchiectasis, bronchiolectasis, volume loss. Table (4): Parenchymal lesions; number and percentage in studied cases. Lesion Upper-Lobe fibrotic changes Fibrocystic/ emphysema/ honey combing Architecture distortion Mycetoma Fibrocystic changes: Cysts, bullae, blebs, emphysema, No. of cases honeycomb-like opacities. % of cases 60.8% 30.4% 69.5% 8.7% Mycetoma, aspergilloma. Distribution of changes Bilateral predominant: Upper-and middle-zone locations of parenchymal abnormalities with broncho-centric distribution of fibrotic changes. Rarely: Unilateral. Basal predominance. Table (5-a): Bilaterality Distribution of parenchymal lesions. No. of cases % of cases Bilateral with rather symmetry % Unilateral predominance 2 8.7% Table (2): Irreversible abnormalities of pulmonary sarcoidosis at high-resolution CT [3]. Honeycomb-like opacities, cysts, bullae, emphysema. Architectural distortion. Traction bronchiectasis, bronchiolectasis. Volume loss in upper lobes, retraction of hila. Mycetoma (in 10% of patients with end-stage sarcoidosis and a preexisting cavity). Table (5-b): Zonal distribution of parenchymal lesions (fibrotic changes). Upper and mid zonalpredilection Mid and lower zonal Broncho-centric fibrotic changes Diffuse No. of cases 21 None Fibrosis % of cases 91.39% 0% 100% 100%
4 4 MSCT Pulmonary Manifestations & Complications Fig. (1a,b): Female patient 55 years old with chronic sarcoidosis, HRCT (axial and coronal images) showing broncho-centric fibrosis in both lungs more on the right side (arrows). Fig. (2a,b): Female patient 32 years old with sarcoidosis, HRCT (axial and sagittal images) showing broncho-centric fibrosis in both lungs more on the right side with reduced volume of the right upper lobe. Prominent interlobular septa are seen on the right upper lobe anterior segment with a nodule seen in the left upper lobe posterior segment (arrow). Fig. (3a,b): Female patient 40 years old with sarcoidosis, HRCT (axial and coronal images) showing broncho-centric fibrosis (arrows) in both lungs and right upper lobar honeycombing (asterisk).
5 Youssriah Y. Sabri, et al. 5 (c) Fig. (4a-d): Female patient 40 years old known case of sarcoidosis coming for followup. Axial post IV contrast enhanced CT (mediastinal and lung windows). Mediastinal window shows right paratracheal, bilateral hilar and subcarinal lymphadenopathy, with punctuate calcification (arrows). Lung window (d) shows bilateral upper lobar nodules with bilateral upper lobar fibrosis (curved arrows). (d) (c) (d) Fig. (5a-d): Female patient 55 years old known case of sarcoidosis coming for follow-up. High resolution CT in axial, coronal and sagittal planes showing bilateral upper lobe fibrosis, volume loss with honeycombing (asterisk), multiple fibrocysts, and thickened distorted fissures (curved arrow).
6 6 MSCT Pulmonary Manifestations & Complications (c) Fig. (6a-c): Female patient 40 years old known case of sarcoidosis coming for follow-up after an attack of hemoptysis. High resolution CT in (a,b) coronal and sagittal planes (a,b) showing left cavitary lesion with mycetoma (curved arrow), and bibasal fibrosis with traction bronchiectasis. (c) Mediastinal window (c) shows bilateral hilar lymphadenopathy (arrows). (c) Fig. (7a-d): 52 year old male patient with eight yearhistory of sarcoidosis, CT in axial plane (lung window) (a,b) showing bilateral upper lobar fibrosis (arrows) with a left upper lobe cavity and mycetoma (open arrow). Mediastinal window (c,d) shows mediastinal and bilateral axillary lymph nodes (curved arrows). (d) Discussion Sarcoidosis is a multisystem chronic inflammatory condition of unknown etiology in which lung and the mediastinal lymph nodes affection is most common, being seen in approximately 90% of patients [1,3] and accounts for most of the morbidity and mortality associated with the condition [28]. Plain films as a preliminary study is usually done with no evident changes detected in early stages or very subtle parenchymal changes, yet, it was helpful in staging of the disease process [29]. Computed tomography has a great value in establishing diagnosis of thoracic sarcoidosis. The rapid adoption of multi slice computed tomography (MSCT) technology testifies to its advantages over single slice computed tomography (SSCT). The principal basis of its advantages can be stated as follows: MSCT allows large anatomic ranges to be scanned while simultaneously producing both
7 Youssriah Y. Sabri, et al. 7 thin and thick slices and consequently results in lowered image noise. HRCT can demonstrate normal and abnormal lung interstitium and morphologic characteristics of both localized and diffuse parenchymal abnormalities; in this regard, HRCT is clearly superior to plain radiographs and conventional CT. A role for high resolution computed tomography (HRCT) exists when patients present with atypical clinical or radiographic findings, detection of complications, or in the context of a normal radiograph but clinical disease suspicion is still present. If biopsy is required, then HRCT can be utilized to guide clinicians to potential highyield sites for transbronchial or surgical lung biopsy; this was also ensured by Hawtin et al., Whitten et al., Taguchi and Anno, Flohr et al., Bartz and Stern [6,14-17]. All of our patients were already known to be cases of long standing sarcoidosis with duration of illness ranging from five to seventeen years (5-17 years). In our study the broncho-centric fibrotic changes were found in all patients (100%); compared to 20% found in Abehsera et al., [30], this could be attributed to that our study was concerned with chronic patients of sarcoidosis where irreversible pulmonary parenchymal architecture distortion supervened with permanent fibrotic and cicatricial changes. Their study was concerned with reversible and irreversible parenchymal changes. Thus, likelihood of early and reversible fibrotic changes were less expected to be seen in our study, on the other hand chronic fibrotic sequale were more prevalent in our targeted sample (chronic and complicated cases). Co-existence of pulmonary chronic fibrotic as well as fibro cystic changes and mediastinal lymphadenopathy (Figs. 4,6,7) was found in five of our patients (21.7%), this agrees with Criado et al., and Koyama et al., that Siltzbach classification stands only for plain radiography, while MSCT has changed this concept [3,9]. Honeycombing (Table 4) is less common compared to other interstitial lung diseases, and if seen, tends to distribute sub-pleurally in the mid-upper zone, sparing the bases [31]. In our study, honeycombing, (Figs. 3,5) was found in seven of our patients (30.4%) and was supleural and predominantly upper lobar in distribution, this was also described by Abehsera et al., [30] and by Nishino et al., [31]. In the review of 80 consecutive patients with pathologically proven sarcoidosis and radio- graphic evidence of pulmonary fibrosis the honeycomb pattern was seen in 23 patients (29%) [30,31]. According to Koyama et al., [9] pulmonary sarcoid nodules rarely manifest with cavitation (in <3% of patients with parenchymal opacities). In our study fibrocysts, traction bronchiectasis and blebs were found in seven of our patients (Figs. 3,5) (30.4%); putting such findings in the chronic sequale of the disease process, this goes with Muller et al., describing similar changes in long standing sarcoidosis patients [24]. Mycetoma formation was noted in 1-3% by Muller et al., and Hours et al., [24,25]. In our study only two patients had mycetoma (8.7%); a higher incidence in the current study, dealing with the long standing sarcoidosis with fibrocystic changes but not early or non complicated cases, pointing to that it was atypical parenchymal manifestation of chronic sarcoidosis; actually considering it as a remote complication of long standing fibrocystic sarcoidosis (Figs. 6,7). Regarding the disease process distribution [Tables (5a-b)]: Bilateral fairly symmetric distribution was noted in twenty one of our cases (91.39%), with the broncho-centric distribution found in all patients (100%) Figs. (1-7), while unilateral predominance was noted in two of our patients (8.7%), this greatly matches with the literature considering bilaterality and rather symmetry of the disease distribution found in more than 90% of patients and the unilateral predominance of distribution considered an uncommonly encountered finding, (Fig. 4) [3]. For interstitial pattern of disease distribution, upper and mid zonal predilection was depicted in twenty one of our patients (91.3%) this goes with that found by Nishino et al., and was not found in mid/lower zonal or bi basal regions individually as a separate distribution pattern [31]. Fibrotic changes were noted as diffuse changes in all of our patients (100%), while in the upper and mid-zones in twenty one out of them (91.3%), Fig. (5), while in only one patient (4.3%); these changes were present predominantly in the basal zones. Extensive calcification may be encountered within fibrotic granulomas [3]. However, in our study it was found in one patient (4.3%), being smaller and non-extensive, Fig. (4).
8 8 MSCT Pulmonary Manifestations & Complications Conclusion: Long standing sarcoidosis with chronic irreversible fibrotic and fibrocystic changes have a classic broncho-centric distribution with classic predominant upper lobar distribution. This could be well demonstrated by multi-slice CT using the high resolution technique. Honeycombing in long standing sarcoidosis is classically subpleural and upper lobar. Mycetoma is a rare but recognizable complication of chronic sarcoidosis. References 1- COLBY T.V. and CARRINGTON C.B.: Infiltrative lung disease in Thurlbeck W.M., ed. Pathology of the lung. Stuttgart: Thieme Medical, , RYBICKI B.A., IANNUZZI M.C., FREDERICK M.M., et al.: Familial aggregation of sarcoidosis: A case-control etiologic study of sarcoidosis (ACCESS). Am. J. Respir. Crit. Care Med., 164 (11): , CRIADO E., MARCELO SÁNCHEZ, JOSÉ RAMÍREZ, et al.: Radio. Graphics, 30: , WEINBERGER S.E., GOLDMAN L. and AUSIELLO D.: Cecil Textbook of Medicine. Sarcoidosis. 23 rd ed. Philadelphia, Pa.: Saunders Elsevier, Chap. 95, BAUGHMAN R.P., CUVLER D.A. and JUDSON M.A.: Concise review in pulmonary AJR and Critical Care Medicine, Vol. 183 No. 4: pp , HAWTIN K.E., RODDIE M.E., MAURI F.A. and COP- LEY S.J.: Pulmonary sarcoidosis: The Great Pretender Clinical Radiology, 65 (8): , DRAKE W. and NEWMAN L.S.: Sarcoidosis. In: Mason R.J., Broaddus V.C., Martin Tr., et al.: Eds. Murray and Nadel s Textbook of Respiratory Medicine. 5 th ed. Philadelphia, Pa.: Saunders Elsevier, Chap. 59, PARK H.J., JUNG J.I., CHUNG M.H. et al.: Typical and Atypical Manifestations of Intrathoracic Sarcoidosis Korean J. Radiol., 10 (6): , KOYAMA T., UEDA H., TOGASHI K., UMEOKA S., KATAOKA M. and NAGAI S.: Radiologic manifestations of sarcoidosis in various organs. Radio. Graphics, 24 (1): , JUDSON M.A., BAUGHMAN R.P., THOMPSON B.W., TEIRSTEIN A.S., TERRIN M.L., ROSSMAN M.D., et al.: Two year prognosis of sarcoidosis: The ACCESS experience. Sarcoidosis Vasc. Diffuse Lung Dis., 20: , IANNUZZI M.C., RYBICKI Ba. and TEIRSTEIN A.S.: Sarcoidosis. N. Engl. J. Med., 357: , BAUGHMAN R.P., ENGEL P.J., TAYLOR L. and LOW- ER E.E.: Survival in sarcoidosis associated pulmonary hypertension: The importance of hemodynamic evaluation. Chest, 138: , DIAZ-GUZMAN E., FARVER C., PARAMBIL J. and CULVER D.A.: Pulmonary hypertension caused by sarcoidosis. Clin. Chest Med., 29: , WHITTEN C.R., KHAN S., MUNNEKE G.J., et al.: A diagnostic approach to mediastinal abnormalities. Radio. Graphics, 27: , TAGUCHI K. and ANNO H.: High temporal resolution for multi-slice helical computed tomography. Med. Phys., 27: , FLOHR T., STIERSTORFER K., BRUDER H., SIMON J., POLACIN A. and SCHALLER S.: Image reconstruction and image quality evaluation for multi detector-slice CT scanner. Med. Phys., 30: , BARTZ R.R. and STERN E.J.: Airways obstruction in patients with sarcoidosis: Expiratory CT scan findings. J. Thorac. Imaging, 15 (4): , KIM E.A., LEE K.S., JOHKOH T., et al.: Interstitial lung diseases associated with collagen vascular diseases: Radiologic and histopathologic findings. Radio. Graphics, 22 (Spec. No.): S151-S165, SULICA R., TEIRSTEIN A.S., KAKARLA S., NEMANI N., BEHNEGAR A. and PADILLA M.L.: Distinctive clinical, radiographic, and functional characteristics of patients with sarcoidosis-related pulmonary hypertension. Chest, 128: , KIM J. S., MULLER N.L., PARK C.S. et al.: Cylindrical bronchiectasis: Diagnostic findings on thin-section CT. AJR Am. J. Roentgenol., 168: , WEBB R.W., MÜLLER N.L. and NAIDICH D.P.: Illustrated glossary of high-resolution computed tomography terms. In: Webb W.R., Muller N.L., Naidich D.P., editors. High-resolution CT of the lung. Philadelphia: Lippincott Williams & Wilkins, p , NAGASHIMA O., TAKAHASHI K., SUZUKI T., MIURA K., SATO K., MURAMATSU M., et al.: An elderly case of sarcoidosis with multiple pulmonary cysts [Article in Japanese]. Nihon Kokyuki Gakkai Zasshi, 43 (6): 370-4, GRANT L.A., BABAR J. and GRIFFIN N.: Cysts, cavities, and honeycombing in multisystem disorders: Differential diagnosis and findings on thin-section CT. Clin. Radiol., 64 (4): , MULLER N., FRASER R., LEE K., et al.: Miscellaneous pulmonary diseases. In: Muller N., Fraser R., Lee K. (Eds) Diseases of the lung. Radiologic and pathologic correlations, 1st edn. Lippincott, Philadelphia, pp , HOURS S., HILARIO NUNES, MARIANNE KAM- BOUCHNER, et al.: Pulmonary Cavitary Sarcoidosis Clinico-Radiologic Characteristics and Natural History of a Rare Form of Sarcoidosis Medicine, Vol. 87, No. 3: , INOUE K., MATSUYAMA W., HASHIGUCHI T., et al.: Expression of vascular endothelial growth factor in pulmonary aspergilloma. Intern. Med., 40 (12): , LACHKAR S., DOMINIQUE S., THIBERVILLE L., NOUVET G. and GENEVOIS A.: Aspergillosis and sarcoidosis. Rev. Mal. Respir., 24: , BAUGHMAN R.P., LOWER E.E. and DU BOIS R.M.: Sarcoidosis. Lancet, 361: , 2003.
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