Diagnostic value of nailfold capillaroscopy to systemic sclerosis with Raynaud s phenomenon: a preliminary study
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1 Formosan Journal of Rheumatology 2009;23:37-42 Original Article Diagnostic value of nailfold capillaroscopy to systemic sclerosis with Raynaud s phenomenon: a preliminary study Po-Chang Wu, Min-Nung Huang,3, Song-Chou Hsieh, Chia-Li Yu,2 Division of Allergy, Immunology and Rheumatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan 2 Graduate Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan 3 GPILS-Molecular Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, USA Objective: To analyze the sensitivity, specificity, positive predictive value, and negative predictive value of nailfold capillaroscopy to systemic sclerosis with Raynaud s phenomenon. Methods: The database of the National Taiwan University Hospital was searched for patients with Raynaud s phenomenon who had been given a nailfold capillaroscopy examination between 2007 and The medical records were reviewed. Results: The medical records of a total of 33 patients were obtained from the database and the sensitivity and specificity of a scleroderma pattern for systemic sclerosis were 84.62% and 75%, respectively. The positive predictive value and negative predictive value of a scleroderma pattern for systemic sclerosis were 68.75% and 88.24%, respectively. Conclusion: This study is unique in measuring semi-quantitative and qualitative parameters of the nailfold vasculature for systemic sclerosis. The sensitivity, specificity, positive predictive value, and negative predictive value of scleroderma pattern for systemic sclerosis are demonstrated. Key words: Nailfold capillaroscopy, Raynaud s phenomenon, sensitivity, specificity, systemic sclerosis Introduction Raynaud s phenomenon (RP) is one of the early clinical manifestations of diffuse connective tissue diseases (DCTD), such as systemic sclerosis (SSc), mixed connective tissue disease (MCTD), systemic lupus erythematosus (SLE), and dermatomyositis (DM)/ polymyositis (PM), and nailfold capillaroscopy (NC) enables an in vivo assessment of the morphology of Corresponding author:chia-li Yu M.D., Ph.D. Division of Allergy, Immunology and Rheumatology, Department of Internal Medicine, National Taiwan University Hospital. No. 7, Chung Shan South Rd., Taipei 00, Taiwan Tel: ext 650 or 6570, Fax: chialiyu@ntu.edu.tw Received: May 2, 2009 Revised: May 5, 2009 Accepted: August 4, 2009 cutaneous capillaries, and has been used for evaluating patients with RP []. NC distinguishes primary and secondary RP due to, connective tissue diseases (CTD) []. A typical normal NC pattern demonstrates hairpin capillaries, arranged in parallel with each other. In 973, Maricq et al recognized massive capillary dilatation in scleroderma-dermatomyositis [2], and in 980, they identified scleroderma spectrum disorders, including classic scleroderma, MCTD and DM, because of their indistinguishable NC findings [3]. In 996, Kabasakal et al. described and quantified the morphological characteristics of different forms of CTD, thus enhancing the value of NC [4], and in 2000, Cutolo et al. classified NC patterns of scleroderma into 3 major patterns, namely early, active and late [5], which are now considered to be useful in assessing the appearance and progression of sclerodermic micro-angiopathy [5]. The 37
2 Nailfold capillaroscopic patterns in scleroderma detection of mega-capillaries in patients with RP has a good predictive value for the subsequent development of a scleroderma spectrum disorder [6], and Blockmans et al. studied the predictive value of NC in the diagnosis of CTD [7], concluding the sensitivity of the presence of mega-capillaries in different forms of CTD as follows: diffuse systemic sclerosis: 00%, limited cutaneous systemic sclerosis: 73%, MCTD: 56%, and DM: 86%. The positive predictive value (PPV) of the presence of mega-capillaries for a scleroderma spectrum disorder (SSD) was 63.5% and the negative predictive value (NPV) of a normal capillaroscopy was 96.7%. It was, thus, concluded that NC can be utilized to rule out SSD [7]. However, so far, no study has illustrated the sensitivity, specificity, positive predictive value, and negative predictive value of scleroderma pattern (by the classification of Cutolo et al.) for systemic sclerosis. Therefore we addressed this issue in a retrospective study. Materials and Methods Patients and subjects The database of National Taiwan University Hospital was searched for patients who had received an NC examination between 2007 and 2008 and, after a careful review of the medical records, patients without RP were excluded. Finally, 33 patients were recruited for this study, and they were examined by physicians blind to the clinical information. Clinical and laboratory data collection Clinical data relating to RP was obtained from the medical records, including the duration of RP, NC patterns, age, gender, laboratory data at NC examination, patients final diagnosis, and associated clinical conditions (such as smoking, diabetes ). Nailfold capillaroscopy techniques An observation of nailfold capillaries was performed on all patients by an in vivo NC (Fig. ). Each patient stayed inside the examination room for a minimum of 5 minutes before the nailfold was examined and the room temperature was C. The epithelium was made transparent by adding a drop of immersion oil, and images were generated by lens providing a magnification of 200, and a charged-coupled device (CCD) camera giving high-resolution images of pixels. The capillaries in the distal row were observed, and a mm graticule was imaged along with each finger to allow for quantification of the capillary density and width (CapiScope, KK Research Technology LTD UK). At least 4 fingers on each hand were examined, and a minimum of 4 photo-micrographs were taken of each patient. All capillary examinations were performed by clinicians to whom the clinical information of each individual not to be provided. Vascular loops were estimated to be of normal width (<25 µm) [4], widened (>50 µm) [6], or giant (>25 µm). Distinctive morphological alterations were recorded along with their average count, and these were classified as few (<4 altered capillaries/mm), moderate (4~6 altered capillaries/mm), or frequent (>6 altered capillaries/mm) [8]. The nailfold bleeding/finger was classified as grade (punctate hemorrhages >2/finger), grade 2 (punctate hemorrhages >2/finger), or grade 3 (confluent areas of hemorrhage) [4], and the avascularity of the capillary bed was classified as grade ( 2 discrete areas of vascular deletion), grade 2 (>2 discrete areas of vascular deletion), or grade 3 (large avascular areas) [4]. These morphological descriptions and quantifications were adapted from two previous studies conducted by Kabasakal et al. [4] and Dolezalova et al. [9]. Interpretation of the nailfold capillaroscopy findings A typical normal NC pattern shows hairpin capillaries, arranged parallel with each other, and the early scleroderma pattern (Scl-early) is defined by a few (<4 altered capillaries/mm) giant capillaries, a few capillary hemorrhages (grade ), relatively wellpreserved capillary distribution without obvious loss of capillaries [5]. The active scleroderma pattern (Sclactive) is defined by frequent (>6 altered capillaries/ mm) giant capillaries, frequent capillary hemorrhages (grade 2 or 3), a moderate loss (20-30%) of capillaries (grade 2), mild disorganization of the capillary architecture, and absent or mildly ramified capillaries Figure. Nailfold capillaroscopy 38
3 Wu et al Figure 2. Representation of the normal NC pattern (A) and the three scleroderma patterns (B, C and D). A: Normal nailfold capillaroscopic pattern: hairpin capillaries (arrows) arranged in a parallel fashion to each other; B: Early scleroderma pattern: few giant capillaries (arrow), relatively well-preserved capillary distribution, and no evident loss of capillaries; C: Active scleroderma pattern: frequent giant capillaries (arrows); D: Late scleroderma pattern: absent giant capillaries, severe loss of capillaries (arrows) with extensive avascular areas, and disorganization of the normal capillary array. [5]. The late scleroderma pattern (Scl-late) is defined by an irregular enlargement of the capillaries, few or absent giant capillaries and hemorrhages, severe loss (50-70%) of capillaries with extensive avascular areas (grade 3), disorganization of the normal capillary array, and ramified/bushy capillaries [5] (Fig. 2). Statistical analysis The results were expressed as means ± standard deviation (SD), and the sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of scleroderma pattern for SSc, were calculated. Results Demographics and clinical characteristics of patients The data of a total of 33 patients with RP was analyzed, 3 of whom had been diagnosed with SSc and 20 with non-scleroderma. The non-scleroderma diagnoses included SLE, PM/DM, MCTD, primary Sjögren's syndrome, anti-phospholipid syndrome (APS), undifferentiated connective tissue disease (UCTD), and a number of other diagnoses. A summary of the demographic details and clinical characteristics of these patients is shown in Table. Table. Demographics and clinical characteristics of the patients examined SSc (n = 3) Non-scleroderma a (n = 20) Age (years) ± ± 7.44 Gender (M:F) 3:0 2:8 Smoking 2 Alcohol 0 0 Diabetes 0 Duration of RP (months) ± ± ANA titer ( :320) 2/3 7/20 Abbreviations: SSc = systemic sclerosis; RP = Raynaud s phenomenon; SLE = systemic lupus erythematosus; PM/DM = polymyositis/dermatomyositis; MCTD = mixed connective tissue disease; APS = anti-phospholipid syndrome; UCTD = undifferentiated connective tissue disease; ANA = antinuclear antibody test; M: male; F: female a The non-scleroderma diagnoses included SLE, PM/DM, MCTD, primary Sjögren's syndrome, APS, UCTD, and a number of other diagnoses. Patients final diagnoses and nailfold capillaroscopic patterns The diagnoses and results of NC of these 33 patients are shown in Table 2, from which it can be seen that (84.62%) of the 3 patients with SSc demonstrated a scleroderma pattern and 2 exhibited other patterns. In the 20 patients with non-scleroderma diagnoses, 5 presented with a scleroderma pattern and 5 (75%) demonstrated other patterns. Sensitivity and specificity of a capillaroscopic pattern for diagnosing corresponding diseases The sensitivity, specificity, PPV, and NPV of scleroderma pattern for SSc were calculated (Table 3), and the results indicate that the sensitivity and specificity of a scleroderma pattern for SSc were 84.62% and 75%, respectively. The PPV and NPV of a scleroderma pattern for SSc were 68.75% and 88.24%, respectively. Table 2. Capillaroscopic patterns and corresponding clinical diagnoses NC pattern SSc Non-scleroderma a Total numbers Scleroderma 5 6 Early Active Late Not Scleroderma Total numbers Abbreviations: NC = nailfold capillaroscopy a The non-scleroderma diagnoses included SLE, PM/DM, MCTD, primary Sjögren's syndrome, APS, UCTD, and a number of other diagnoses. 39
4 Nailfold capillaroscopic patterns in scleroderma Table 3. Sensitivity, specificity, PPV, and NPV of scleroderma pattern for SSc Sensitivity (%) Specificity (%) PPV (%) NPV (%) Abbreviations: SSc = systemic sclerosis; PPV = positive predictive value; NPV = negative predictive value Discussion Our study is unique in measuring the semiquantitative and qualitative parameters of the nailfold vasculature for systemic sclerosis. This morphological description and quantification were modified from two previous studies conducted by Kabasakal et al. [4] and Dolezalova et al. [9]. These parameters are advantageous for the classification of a specific nailfold capillaroscopic pattern. The definition and classification of a scleroderma pattern were adapted from previous research conducted by Cutolo [5]. Although several studies have shown a good predictive value [7,0] and prognostic role [6,] of NC in patients with RP over the past three decades, these focused mainly on morphological (such as giant loops or micro-hemorrhages ) and quantitative changes (such as area of avascularity or number of mega-capillaries ) of connective tissue diseases. In 980, Maricq et al. attempted to determine the specificity of a scleroderma pattern. However, they discovered that this pattern could also be seen in related disorders, such as MCTD, and dermatomyositis but rarely in SLE (only of 60 patients studied) [3]. Due to their indistinguishable NC findings, they suggested scleroderma spectrum disorders, including classic scleroderma, MCTD, and dermatomyositis [3]. The sensitivity of a scleroderma pattern for SSc was 82% [3]. However, the specificity of a scleroderma pattern was undetermined, since there was no definite classification and quantification of the nailfold capillaroscopic pattern. In 996, Kabasakal et al. described and quantified the morphological characteristics of different forms of CTD [4]. In addition, in the year 2000, Cutolo et al. re-classified NC patterns of scleroderma into three major patterns, namely early, active and late [5]. However, no study was conducted to demonstrate the sensitivity and specificity of scleroderma patterns for SSc, and our study is the first one to address this issue. The sensitivity and specificity of a scleroderma pattern for SSc were found to be 84.62% and 75%, respectively. In 996, Blockmans et al. suggested the sensitivity of the presence of mega-capillaries for different forms of CTD was as follows: diffuse systemic sclerosis: 00%, limited cutaneous systemic sclerosis: 73%, MCTD: 56%, and DM: 86% [7]. They reported the single parameter (mega-capillaries) of the nailfold vasculature with high sensitivity and high NPV (96.7%). However, the PPV of the presence of mega-capillaries for a scleroderma spectrum disorder (SSD) was low (63.5%) [7]. Our research addressed the scleroderma patterns for SSc, and demonstrated a superior specificity, and the overall sensitivity of the three scleroderma patterns for SSc was also high (84.62%). The PPV and NPV of the scleroderma pattern for SSc were 68.75% and 88.24%, respectively. The limitation of our study is the relatively low case numbers of SSc, which could potentially cause an inaccurate statistical evaluation. With higher case numbers, such a calculation would be more reliable and thus, we hope to investigate more cases in future studies. In conclusion, our results demonstrate the usefulness of semi-quantitative parameters for the classification of a scleroderma pattern, as well as confirm the high diagnostic value of NC in SSc. Acknowledgements The authors deeply appreciated Dr. Wen-Hsiang Wu for his statistical assistance. Reference. Mannarino E, Pasqualini L, Fedeli F, Scricciolo V, Innocente S. Nailfold capillaroscopy in the screening and diagnosis of Raynaud's phenomenon. Angiology 994;45: Maricq HR, LeRoy EC. Patterns of finger capillary abnormalities in connective tissue disease by "wide-field" microscopy. Arthritis Rheum 973;6: Maricq HR, LeRoy EC, D'Angelo WA, Medsger TA Jr, Rodnan GP, Sharp GC, et al. Diagnostic potential of in vivo capillary microscopy in scleroderma and related disorders. Arthritis Rheum 980;23: Kabasakal Y, Elvins DM, Ring EF, McHugh NJ. Quantitative nailfold capillaroscopy findings in a population with connective tissue disease and in normal healthy controls. Ann Rheum Dis 996;55: Cutolo M, Sulli A, Pizzorni C, Accardo S. Nailfold videocapillaroscopy assessment of microvascular damage in systemic sclerosis. J Rheumatol 2000;27: Zufferey P, Depairon M, Chamot AM, Monti M. Prognostic significance of nailfold capillary microscopy in patients with Raynaud's phenomenon and scleroderma-pattern abnormalities. A six-year follow-up study. Clin Rheumatol 992;:
5 Wu et al 7. Blockmans D, Beyens G, Verhaeghe R. Predictive value of nailfold capillaroscopy in the diagnosis of connective tissue diseases. Clin Rheumatol. 996;5: Cutolo M, Pizzorni C, Tuccio M, Burroni A, Craviotto C, Basso M, et al. Nailfold videocapillaroscopic patterns and serum autoantibodies in systemic sclerosis. Rheumatology 2004;43: Dolezalova P, Young SP, Bacon PA, Southwood TR. Nailfold capillary microscopy in healthy children and in childhood rheumatic diseases: a prospective single blind observational study. Ann Rheum Dis 2003;62: Meli M, Gitzelmann G, Koppensteiner R, Amann-Vesti BR. Predictive value of nailfold capillaroscopy in patients with Raynaud's phenomenon. Clin Rheumatol 2006;25: Ingegnoli F, Boracchi P, Gualtierotti R, Lubatti C, Meani L, Zahalkova L, et al. Prognostic model based on nailfold capillaroscopy for identifying Raynaud's phenomenon patients at high risk for the development of a scleroderma spectrum disorder: PRINCE (prognostic index for nailfold capillaroscopic examination). Arthritis Rheum 2008;58:
6 Nailfold capillaroscopic patterns in scleroderma 甲褶鏡應用於全身性硬化症合併雷諾氏現象的診斷價值 初步研究報告 吳柏樟 黃閔農 謝松洲,2 余家利 國立台灣大學附設醫院內科部風濕免疫科 2 國立台灣大學醫學院分子醫學研究所 目的 : 研究甲褶鏡用於全身性硬化症診斷上的敏感性 特異性 陽性預測值 以及陰性預測值 方法 : 我們搜尋臺大醫院資料庫中, 從西元 2007 年到 2008 年中, 有雷諾式現象並接受甲褶鏡檢查的病例, 分析其在全身性硬化症的診斷經驗 結果 :33 位病患符合有雷諾式現象並接受甲褶鏡檢查的病例進行分析研究 甲褶鏡用於全身性硬化症診斷上的敏感性為 84.62%; 特異性為 75%; 陽性預測值為 68.75%; 陰性預測值為 88.24% 結論: 臨床上有雷諾式現象的病例, 使用甲褶鏡檢查, 其在全身性硬化症上的診斷價值相當高 關鍵詞 : 甲褶鏡 雷諾式現象 敏感性 特異性 全身性硬化症 42
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