Concise report. Calcinosis in systemic sclerosis: subsets, distribution and complications RHEUMATOLOGY
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1 RHEUMATOLOGY Rheumatology 2016;55: doi: /rheumatology/kew193 Advance Access publication 30 May 2016 CLINICAL SCIENCE Concise report Calcinosis in systemic sclerosis: subsets, distribution and complications Francesca Bartoli 1, Ginevra Fiori 1, Francesca Braschi 1, Laura Amanzi 1, Cosimo Bruni 1, Jelena Blagojevic 1, Silvia Bellando-Randone 1, Laura Cometi 1, Carolina de Souza Mueller 1,2, Serena Guiducci 1, Laura Rasero 3, Francesco Epifani 4, Daniel E. Furst 5 and Marco Matucci-Cerinic 1 Abstract Objective. To retrospectively analyse the features of calcinosis in a cohort of SSc patients. Methods. Charts of SSc patients attending the Ulcer Unit of the Rheumatology Department, University of Florence and presenting a clinical suspicion of calcinosis were considered in the study. Data on clinical history, including recent skin changes, and clinical examination of all areas with suspected calcinosis, radiological imaging of the calcinotic area, demographics and SSc-related organ involvement and pain measured by a visual analogue scale were recorded. Results. In 52 of 112 SSc patients, a total of 316 calcinoses were recorded and were divided into visible and palpable {154 [47.4%], clustered according to their macroscopic features as mousse [49 (31.8%)] and stone [105 (68.2%)]} and non-visible but palpable {162 [52.6%]: net [5 (3%)], plate [22 (13.8%)] and stone [135 (83.2%)]}. The X-ray-based classification of all calcinoses, both visible and non-visible, was as follows: stone, 289 (91.4%); net, 12 (3.8%) and plate, 15 (4.8%). Skin ulcers complicated 154 of 316 calcinoses (48.7%). Mousse calcinosis was associated with pulmonary arterial hypertension, the stone subset was suggestive of pulmonary involvement and justified further investigation and the net subset was the slowest to heal. Conclusion. Our data indicate that calcinosis may be classified in SSc as mousse, stone, net and plate according to its clinical and X-ray features. This classification awaits validation for a possible use in clinical practice and to support early treatment and prevention of complications. Key words: calcinosis, systemic sclerosis Rheumatology key messages. Different subsets of calcinoses associate with different organ involvement in SSc.. Calcinoses should be assessed in SSc as at risk for developing ulcers and infection. 1 Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Florence, Florence, Italy, 2 Serviço de Reumatologia, University Hospital of Curitiba, Paraná, Brazil, 3 Department of Public Health and 4 Interinstitutional Department of Didactic, Azienda Ospedaliero-Universitaria Careggi, University of Florence, Florence, Italy and 5 Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA Submitted 23 July 2015; revised version accepted 8 March 2016 Correspondence to: Bartoli Francesca, Department of Experimental Clinical Medicine, Division of Rheumatology, University of Florence, Villa Monna Tessa, Viale Pieraccini 18, Firenze, Italy. francesca.bartoli19@gmail.com Introduction Calcinosis is a frequent problem in SSc. Boulman et al. [1] classified soft tissue calcifications as calcareous metastasis, tumoural calcification, dystrophic calcification, idiopathic calcification and calciphylaxis. In SSc, calcinoses were classified as dystrophic calcification, characterized by normal levels of calcium and phosphorus in tissues affected by hypoxia, deficient vascularization and/or structural damage [1 3], but no specific classification was proposed. The aim of our work was to retrospectively analyse the main features of calcinosis in a cohort of SSc patients and! The Author Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please journals.permissions@oup.com
2 Calcinosis in systemic sclerosis FIG. 1Visible and palpable calcinosis on clinical examination (A) Mousse, (B) stone calcinosis on knee provoking an ulcer and (C) finger with small stones. On X-ray examination: (D) net calcinosis of the calf and (E) stone calcinosis of the fingers. to describe subsets, body area distribution and secondary complications. Patients and methods The clinical charts of SSc patients attending the Ulcer Unit of the Division of Rheumatology (University of Florence) from January 2004 to August 2010 were reviewed. Clinical history with reports of any signs and/or symptoms raising suspicion for calcinosis (new visible or self-palpable formations in the skin and subcutaneous tissues, pain, sensation of foreign body into the soft tissues, functional impairment and new skin ulcers) were considered as inclusion criteria. According to our practice, patients were always submitted to a systematic clinical evaluation. First, a visual evaluation was performed to identify evident calcinoses. If this was negative, a systematic palpation was made in the following areas: finger, wrist, forearm, elbow, iliac crest, knee patella and areas around the knee. According to reported clinical examination of the areas, with skin and soft tissue alterations raising the suspicion for calcinosis and performed by the same SSc expert rheumatologist, calcinoses were clinically classified as visible and palpable, if there was evidence of palpable skin and soft tissue alteration with white calcareous material also leaking through the damaged skin, and non-visible but palpable, if there was an alteration of skin and soft tissues detectable only by palpation, without skin lesions. These calcinoses were also classified according to their shape and consistency on palpation into mousse (characterized by soft consistency and white, cream-like material) (Fig. 1A), net (palpable as a diffuse thin network), plate (palpable as large uniform and flat agglomerate) and stone (palpable as a single stone or agglomerates of multiple stones of hard consistency) (Fig. 1B and C). In both cases, when calcinoses were either evident or palpable, according to our clinical practice, X-ray of the involved area was performed in order to confirm calcinosis. Both these evaluations were recorded in the data sheet, together with the X-ray images, which were reviewed by an SSc expert rheumatologist. Calcinoses were classified according to their X-ray morphology into net (calcium deposits forming a network) (Fig. 1D), plate (calcium deposits arranged in a plate), stone (calcium deposits forming small, round aggregates) and mousse (Fig. 1E). Calcinoses and data on their characteristics and their complications (such as skin ulcers, infection and fistulas), routinely recorded in the charts, were extracted in a separate data sheet. If present, the following characteristics were recorded for skin ulcers: localization, dimensions (area in
3 Francesca Bartoli et al. square millimetres), wound bed (re-epithelialization, granulation tissue, fibrin, wet or dry necrosis, eschar and gangrene), exudates (low, high, pus), edges of the lesions (regular or irregular), perilesional skin (normal or inflamed), oedema and time to healing. Moreover, data on fistulas, signs of infection (as inflamed perilesional skin, purulent exudates and pain) and pain [measured by a visual analogue scale (VAS)] were also obtained from the charts. This study received approval from the institutional review board of the University Hospital of Careggi and all patients gave informed consent for data recording and management. The following features were recorded: age, gender, disease subset, RP and SSc duration (from the onset of the first non-rp symptom), modified Rodnan skin score, presence of ulcers, tendon friction rubs, clinically evident joint synovitis confirmed by US with power Doppler evaluation, capillaroscopic pattern and autoantibody pattern (positivity of ANA, ACA, anti-topoisomerase and anti-rna polymerase antibody), as well as gastro-oesophageal symptoms (defined by the presence of symptomatic gastro-oesophageal reflux, alteration on oesophageal manometry and/or esophagogastroduodenoscopy and/or X-ray modification) [4], lung involvement (defined as evidence of interstitial lung disease on CT, supported by a restrictive pattern on pulmonary function tests), pulmonary arterial hypertension (suspected on echocardiography and confirmed by right heart catheterization) and scleroderma renal crisis (defined as new-onset systemic hypertension associated with a decrease in estimated glomerular filtration rate >30 ml/min). Statistical analysis The association between calcinosis and the above mentioned features were tested through chi-squared test using SPSS software (version 17; IBM, Armonk, NY, USA). The results were expressed as mean (S.D.). Results were considered significant for P-values <0.05. Results A total of 112 SSc patients were eligible for the study. In 52/112 patients [50 females, mean age 63.5 years (S.D.11); 6 dssc and 46 lssc, mean disease duration 9.5 years for lssc and 12 years for dssc], calcinoses were confirmed radiologically; for clinical features of the study population, see Table 1. On clinical examination, a total of 316 calcinoses were found. Of these, 154 (47.4%) were visible and palpable [49 (31.8%) were classified as mousse and 105 (68.2%) as stone] and 162 (52.6%) were palpable only [5 of them (3%) were classified as net and were detected in the lower limbs only while 22 (13.8%) were classified as plate and 135 (83.2%) were classified as stone]. Both plate and stone could be found in any part of the body. All clinically suspected calcinoses were confirmed in by X-ray (100% of concordance). Patients without visible or palpable calcinoses were not systemically investigated with X-rays. In fact, no routine systemic radiological programme is employed, to avoid X-ray overload. No radiologically incidentally found calcinosis was observed TABLE 1 Clinical features of study population Parameter during data collection, as imaging is routinely performed only on patients with clinical findings. Calcinoses were then classified according to their morphology on X-ray examination into net [12 (3.8%)] (Fig. 1D), plate [15 (4.8%)] and stone/mousse [289 (91.4%)] (Fig. 1E). Skin ulcers complicating calcinosis Prevalence Age, mean (S.D.), years 63.5 (11) Gender, n Female 50 Male 2 Subset, n (%) Limited 46 (88.4) Diffuse 6 (11.6) RP duration, mean (S.D.), years 15.3 (8.7) Disease duration, mean (S.D.), years 9.5 (6.5) Autoantibodies, n (%) ACA 38 (73) Scl70 13 (25) ANA 52 (100) Videocapillaroscopy, n (%) Early 8 (15) Active 31 (60) Late 13 (25) mrss, mean (S.D.) (9.3) Digital ulcers, n (%) 8 (15.3) Joint synovitis, n (%) 3 (5.7) Tendon friction rubs, n (%) 4 (7.7) Gastro-oesophageal 43 (82.7) involvement GERD, n (%) Interstitial lung disease, n (%) 29 (55.7) Pulmonary arterial hypertension, n (%) 13 (25) History of scleroderma renal crisis, n (%) 0 (0) mrss: modified Rodnan skin score. Skin ulcers developed in 154/316 calcinosis areas (48.7%). Ulcers developed in 76% of lssc patients and in 50% of dssc patients, without a significant difference (P = 0.32). The 154 skin ulcers with calcinosis were found on the hand (64.9%), knee (11%), hip (5.4%), upper arm (5.2%), pretibial region (3.9%), elbow (3.9%), foot (3.2%), wrist (1.5%) and abdomen (1%). The mean size of skin ulcers was 48.2 mm 2 (S.D. 24.3). In our patients, the presence of calcium deposits in soft tissue was almost always accompanied by local inflammatory reaction, oedema and inflammation of the surrounding skin (80%). Local inflammatory reaction was found in 80% of the hip calcinosis, 75% of hand, 70% of knee, 75% of elbow and rarely in other areas. Clinical examination of the ulcers was compatible with granulation tissue that was always present and had jagged edges. The ulcers derived from the net form of calcinosis took the longest to heal [mean 140 days (S.D. 22.3)], while stone calcinosis took the shortest time [30 days (S.D. 12)]
4 Calcinosis in systemic sclerosis Skin ulcers were complicated by infection, developed in 62.3% of ulcerated calcinosis areas at the level of the wrist, hip, pretibial area, knee and elbow; and fistulas, as a complication of skin ulcers secondary to calcinosis, developed in only two patients (1.3%), in the knee and forearm. Anatomic distribution of calcinosis Calcinosis areas were found more often in the hand (periungual areas and finger tips, 65.2%), knee/patella (10.5%) and hip (6.7%). They were also found in the arm, elbow, foot, wrist, abdomen, pretibial (only one patient, an agglomerate of stones), iliac crest and intergluteal area (only one patient, plate). According to the radiological subsets, net calcinoses were all present in the lower limbs [12/12 (100%)], while plate calcinoses were distributed between the intergluteal area [8/15 (53%)], iliac crest [6/15 (40%)] and patella [1/15 (7%)]. Mousse/stone calcinoses were located mostly on the fingers [225/289 (78%)] and less frequently on the elbows [44/289 (15%)] and knees [20/289 (7%)]. Pain In the area of calcinosis, almost every patient complained of pain, being influenced by localization, size, the morphology of the calcium deposits and the presence of infection. Pain was recorded (on a VAS) in all areas affected by calcinosis: it was higher in the knee [72 mm (S.D. 22)] and elbow [70 mm (S.D. 28)] and less intense in the fingertips [49 mm (S.D. 18)]. Mousse calcinosis caused more intense pain [64 mm (S.D. 22)] than a single stone [49 mm (S.D. 21)]. Correlation with clinical features Calcinosis developed after 9.5 years (S.D. 6) of disease onset in lssc and after 12 years (S.D. 4.7) in dssc. Moreover, we found that patients with stone calcinosis had a higher prevalence of lung involvement than patients with mousse calcinosis ( 2 = 5.380, P = 0.020), while pulmonary arterial hypertension was significantly more frequent in patients with mousse calcinosis ( 2 = 4.524, P = 0.033). None of the other clinical or instrumental features showed a correlation with calcinosis subset. Discussion The presence of calcinoses significantly affects the quality of life of SSc patients but, to date, no extensive or comprehensive clinical studies addressing this complication, its classification and treatment in SSc are available. In practice, it is not uncommon that the fortuitous identification of subcutaneous calcium deposits occurs when X- rays are requested for other purposes. Our retrospective study allowed us to identify features that may be relevant in clinical practice. In our population, calcinoses were more frequent (46%) than reported in the literature, where <40% of patients with lssc had calcinosis [5, 6]. This discrepancy may be due to the fact that our Ulcer Unit is entirely devoted to SSc ulcers, including calcinosis and related complications, thus causing a possible overestimation of the prevalence of calcinoses and their risk of ulcerations. In addition, there are no data in the literature on the incidence of ulcers secondary to calcinosis, although these ulcers were frequently detected in our patients (48.7%). This clearly suggests that when calcinosis is found, strict follow-up is needed, especially due to the high risk of infection and fistulisation. The present results confirm the previous data of our group showing a long time to heal for calcinosis-derived digital ulcers compared with spontaneous digital ulcers; in fact, the high prevalence of infection, observed in both lesions, was associated with a negative effect on the healing process. In the present cohort, the level of pain was lower than previously observed, likely because not all calcinoses were associated with ulceration, which, in fact, significantly increases the perception of pain [7]. To our knowledge, this is the first study showing an association between subsets of calcinoses and clinical manifestations of SSc, which might be linked to hypoxia, a potential cause of the calcinosis formation [1]. In the literature, a severity index to classify calcinosis is available that divides them into four grades according to size and depth: only radiological evidence, not palpable (first grade), multiple small palpable areas (second grade), larger palpable areas and more numerous calcifications (third grade) and large areas with large deposits with or without ulceration (fourth grade) [8]. However, this classification has never been used in clinical practice or in clinical trials. In SSc, where calcinosis is common, a simple classification may be useful and may link the morphological and/or X-ray features to prognosis and treatment. Our analysis showed that a classification and subsetting stemming from either a clinical and/or X-ray evaluation of the features of calcinosis may be usefully employed in clinical practice. In fact, we described and confirmed different subsets of calcinoses, clinically and/or radiologically. Due to the high impact on quality of life and functionality in SSc patients, early identification of calcinoses is of paramount importance for a rapid decision on best management (i.e. excision, physical activity). However, the clinical approach with palpation remains the most important tool for early identification, while X-rays remain the reference tool to confirm and classify the subset. The use of a total-body X-ray screening to detect non-clinical and asymptomatic calcinoses is not warranted, to limit the radiation exposure [9] and evolution to cancer [10]. On the basis of the results derived from clinical and X-ray evidence, we propose classifying SSc calcinoses into four subsets: mousse, which is always visible and does not need an X-ray; net, which is usually palpable and not usually visible; plate, which may be visible and/ or palpable; and stone, which may be visible and/or palpable (all need investigation with X-rays). In conclusion, calcinosis is a frequent complication in SSc and it may be classified into four clinical subsets by observation and palpation and with the fundamental help of X-rays. Our proposed classification should be applied
5 Francesca Bartoli et al. to larger cohorts of patients in everyday clinical settings to confirm and validate our data. Funding: No specific funding was received from any bodies in the public, commercial or not-for-profit sectors to carry out the work described in this article. Disclosure statement: D.E.F. has received grants/research support from AbbVie, Actelion, Amgen, Bristol-Meyers Squibb, Gilead, GlaxoSmithKline, National Institutes of Health (NIH), Novartis, Pfizer, Roche/Genentech and UCB; has acted as a consultant for AbbVie, Actelion, Amgen, BMS, Cytori, Janssen, Gilead, GlaxoSmithKline, NIH, Novartis, Pfizer, Roche/Genentech and UCB and has participated in the speakers bureau (CME only) with AbbVie, Actelion and UCB. All other authors have declared no conflicts of interest. References 1 Boulman N, Slobodin G, Rozenbaum M, Rosner I. Calcinosis in rheumatic diseases. Semin Arthritis Rheum 2005;34: AAVV. Sunderkotter C. Skin involvement. In: Hachulla E, Czirják L, eds. EULAR Textbook on Systemic Sclerosis BMJ 2013: Ward M, Curé J, Schabel S et al. Symptomatic spinal calcinosis in systemic sclerosis (scleroderma). Arthritis Rheum 1997;40: Xin-Ping T, Zhang X. Gastrointestinal complications of systemic sclerosis. World J Gastroenterol 2013;19: Steen VD, Ziegler GL, Rodnan GP, Medsger TA. Clinical and laboratory associations of anticentromere antibody in patients with progressive systemic sclerosis. Arthritis Rheum 1984;27: Chamberlain AJ, Walker NPJ. Successful palliation and significant remission of cutaneous calcinosis in CREST syndrome with carbon dioxide laser. Dermatol Surg 2003;29: Amanzi L, Braschi F, Fiori G et al. M. Digital ulcers in scleroderma: staging, characteristics and sub-setting through observation of 1614 digital lesions. Rheumatology 2010;49: Berger RG, Featherstone GL, Raasch RH, McCartney WH, Hadler NM. Treatment of calcinosis universalis with lowdose warfarin. Am J Med 1987;83: Picano E, Semelka R, Ravenel J, Matucci-Cerinic M. Rheumatologic diseases and cancer: the hidden variable of radiation exposure. Ann Rheum Dis 2014;73: Picano E, Matucci-Cerinic M. Unnecessary radiation exposure from medical imaging in the rheumatology patient. Rheumatology 2011;50:
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