Top

Published in:

01-09-2019 | Systemic Sclerosis | Review Article

Practical issues in assessing nailfold capillaroscopic images: a summary

Authors: Abdolamir Karbalaie, Zahra Emrani, Alimohammad Fatemi, Mahnaz Etehadtavakol, Björn-Erik Erlandsson

Published in: Clinical Rheumatology | Issue 9/2019

Abstract

Nailfold capillaroscopy (NC) is a highly sensitive, safe, and non-invasive technique to assess involvement rate of microvascularity in dermatomyositis and systemic sclerosis. A large number of studies have focused on NC pattern description, classification, and scoring system validation, but minimal information has been published on the accuracy and precision of the measurement. The objective of this review article is to identify different factors affecting the reliability and validity of the assessment in NC. Several factors can affect the reliability of the examination, e.g., physiological artifacts, the nailfold imaging instrument, human factors, and the assessment rules and standards. It is impossible to avoid all artifacts, e.g., skin transparency, physically injured fingers, and skin pigmentation. However, minimization of the impact of some of these artifacts by considering some protocols before the examination and by using specialized tools, training, guidelines, and software can help to reduce errors in the measurement and assessment of NC images. Establishing guidelines and instructions for automatic characterization and measurement based on machine learning techniques also may reduce ambiguities and the assessment time.

Paxton D, Pauling JD (2018) Does nailfold capillaroscopy help predict future outcomes in systemic sclerosis? A systematic literature review. Semin Arthritis Rheum 48(3):482–494. https://doi.org/10.1016/j.semarthrit.2018.02.005 CrossRefPubMed

Herrick AL, Cutolo M (2010) Clinical implications from capillaroscopic analysis in patients with Raynaud’s phenomenon and systemic sclerosis. Arthritis Rheumatism 62(9):2595–2604. https://doi.org/10.1002/art.27543 CrossRefPubMed

Berks M, Dinsdale G, Murray A, Moore T, Manning J, Taylor C, Herrick AL (2018) Automated structure and flow measurement—a promising tool in nailfold capillaroscopy. Microvasc Res 118:173–177. https://doi.org/10.1016/j.mvr.2018.03.016 CrossRefPubMedPubMedCentral

Ghizzoni C, Sebastiani M, Manfredi A, Campomori F, Colaci M, Giuggioli D, Ferri C (2015) Prevalence and evolution of scleroderma pattern at nailfold videocapillaroscopy in systemic sclerosis patients: clinical and prognostic implications. Microvasc Res 99:92–95. https://doi.org/10.1016/j.mvr.2015.03.005 CrossRefPubMed

Shirshin EA, Gurfinkel YI, Matskeplishvili ST, Sasonko ML, Omelyanenko NP, Yakimov BP, Lademann J, Darvin ME (2018) In vivo optical imaging of the viable epidermis around the nailfold capillaries for the assessment of heart failure severity in humans. J Biophotonics 11(9):e201800066. https://doi.org/10.1002/jbio.201800066 CrossRefPubMed

Emrani Z, Karbalaie A, Fatemi A, Etehadtavakol M, Erlandsson BE (2017) Capillary density: an important parameter in nailfold capillaroscopy. Microvasc Res 109:7–18. https://doi.org/10.1016/j.mvr.2016.09.001 CrossRefPubMed

Gurfinkel YI, Sasonko M, Priezzhev A (2015) Digital capillaroscopy as important tool for early diagnostics of arterial hypertension. Paper presented at the Saratov Fall Meeting 2014, Russian Federation,

Hughes M, Moore T, O’leary N, Tracey A, Ennis H, Dinsdale G, Murray A, Roberts C, Herrick AL (2015) A study comparing videocapillaroscopy and dermoscopy in the assessment of nailfold capillaries in patients with systemic sclerosis–spectrum disorders. Rheumatology 54(8):1435–1442. https://doi.org/10.1093/rheumatology/keu533 CrossRefPubMed

Mazzotti N, Bredemeier M, Brenol C, Xavier R, Cestari T (2014) Assessment of nailfold capillaroscopy in systemic sclerosis by different optical magnification methods. Clin Exp Dermatol 39(2):135–141. https://doi.org/10.1111/ced.12254 CrossRefPubMed

10.

Hofstee HM, Serne EH, Roberts C, Hesselstrand R, Scheja A, Moore TL, Wildt M, Manning JB, Vonk Noordegraaf A, Voskuyl AE, Herrick AL (2012) A multicentre study on the reliability of qualitative and quantitative nail-fold videocapillaroscopy assessment. Rheumatology (Oxford) 51(4):749–755. https://doi.org/10.1093/rheumatology/ker403 CrossRef

11.

Smith V, Beeckman S, Herrick AL, Decuman S, Deschepper E, De Keyser F, Distler O, Foeldvari I, Ingegnoli F, Müller-Ladner U (2016) An EULAR study group pilot study on reliability of simple capillaroscopic definitions to describe capillary morphology in rheumatic diseases. Rheumatology 55(5):883–890. https://doi.org/10.1093/rheumatology/kev441 CrossRefPubMed

12.

Gutierrez M, Bertolazzi C, Tardella M, Becciolini A, M DIC, Dottori M, Grassi W, De Angelis R (2012) Interreader reliability in assessment of nailfold capillary abnormalities by beginners: pilot study of an intensive videocapillaroscopy training program. J Rheumatol 39(6):1248–1255. https://doi.org/10.3899/jrheum.111299 CrossRefPubMed

13.

Murray AK, Vail A, Moore TL, Manning JB, Taylor CJ, Herrick AL (2012) The influence of measurement location on reliability of quantitative nailfold videocapillaroscopy in patients with SSc. Rheumatology 51(7):1323–1330. https://doi.org/10.1093/rheumatology/kes007 CrossRefPubMed

14.

Karbalaie A, Etehadtavakol M, Abtahi F, Fatemi A, Emrani Z, Erlandsson B-E (2018) Image enhancement effect on inter and intra-observer reliability of nailfold capillary assessment. Microvasc Res 120:100–110. https://doi.org/10.1016/j.mvr.2018.06.005 CrossRefPubMed

15.

Cutolo M, Trombetta AC, Melsens K, Pizzorni C, Sulli A, Ruaro B, Paolino S, Deschepper E, Smith V (2018) Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: proof of principle and validation in systemic sclerosis. Microcirculation 25(4):e12447. https://doi.org/10.1111/micc.12447 CrossRefPubMed

16.

Karbalaie A, Abtahi F, Fatemi A, Etehadtavakol M, Emrani Z, Erlandsson BE (2017) Elliptical broken line method for calculating capillary density in nailfold capillaroscopy: proposal and evaluation. Microvasc Res 113:1–8. https://doi.org/10.1016/j.mvr.2017.04.002 CrossRefPubMed

17.

Nivedha R, Brinda M, Suma K, Rao B (2016) Classification of nailfold capillary images in patients with hypertension using nonlinear SVM. In: 2016 International conference on Circuits, Controls, Communications and Computing (I4C). IEEE, 1–5

18.

Suma K, Indira K, Rao B (2017) Fuzzy logic based classification of nailfold capillary images in healthy, hypertensive and diabetic subjects. In: 2017 International Conference on Computer Communication and Informatics (ICCCI), Coimbatore, IEEE, pp 1–5

19.

Berks M, Tresadern P, Dinsdale G, Murray A, Moore T, Herrick A, Taylor C (2014) An automated system for detecting and measuring nailfold capillaries. Med Image Comput Comput Assist Interv 17(Pt 1):658–65

20.

Cutolo M, Herrick AL, Distler O, Becker MO, Beltran E, Carpentier P, Ferri C, Inanc M, Vlachoyiannopoulos P, Chadha-Boreham H, Cottreel E, Pfister T, Rosenberg D, Torres JV, Smith V, Investigators CAPS (2016) Nailfold videocapillaroscopic features and other clinical risk factors for digital ulcers in systemic sclerosis: a multicenter, prospective cohort study. Arthritis Rheumatology 68(10):2527–2539. https://doi.org/10.1002/art.39718 CrossRefPubMed

21.

Baran U, Shi L, Wang RK (2015) Capillary blood flow imaging within human finger cuticle using optical microangiography. J Biophotonics 8(1–2):46–51. https://doi.org/10.1002/jbio.201300154 CrossRefPubMed

22.

Sangiorgi S, Manelli A, Congiu T, Bini A, Pilato G, Reguzzoni M, Raspanti M (2004) Microvascularization of the human digit as studied by corrosion casting. J Anat 204(2):123–131. https://doi.org/10.1111/j.1469-7580.2004.00251.x CrossRefPubMedPubMedCentral

23.

Sørensen LT, Jørgensen S, Petersen LJ, Hemmingsen U, Bülow J, Loft S, Gottrup F (2009) Acute effects of nicotine and smoking on blood flow, tissue oxygen, and aerobe metabolism of the skin and subcutis. J Surg Res 152(2):224–230CrossRefPubMed

24.

Roizen MF (2004) The RealAge makeover: take years off your looks and add them to your life! HarperCollins, New York

25.

Ingegnoli F, Zeni S, Gerloni V, Fantini F (2005) Capillaroscopic observations in childhood rheumatic diseases and healthy controls. Clin Exp Rheumatol 23(6):905–911PubMed

26.

Allen PD, Taylor CJ, Herrick AL, Moore T Image analysis of nailfold capillary patterns from video sequences. In: International Conference on Medical Image Computing and Computer-Assisted Intervention, 1999. Springer, Berlin, Heidelberg, pp 698–705. https://doi.org/10.1007/10704282_76

27.

Lin K-M, Cheng T-T, Chen C-J (2009) Clinical applications of nailfold capillaroscopy in different rheumatic diseases. J Int Med Taiwan 20(3):238–247

28.

Etehad Tavakol M, Fatemi A, Karbalaie A, Emrani Z, Erlandsson B-E (2015) Nailfold capillaroscopy in rheumatic diseases: which parameters should be evaluated? Biomed Res Int 2015:1–17. https://doi.org/10.1155/2015/974530 CrossRef

29.

Darrigade A, Vedie A, Gauthier C, Cario-André M, Taieb A, Truchetet M, Constans J, Seneschal J (2016) Pigmented skin patches without scleroderma as a predominant clinical symptom revealing systemic sclerosis. Clin Exp Dermatol 41(4):379–382. https://doi.org/10.1111/ced.12752 CrossRefPubMed

30.

Shore AC (2000) Capillaroscopy and the measurement of capillary pressure. Br J Clin Pharmacol 50(6):501–513CrossRefPubMedPubMedCentral

31.

Ingegnoli F, Boracchi P, Gualtierotti R, Biganzoli EM, Zeni S, Lubatti C, Fantini F (2010) Improving outcome prediction of systemic sclerosis from isolated Raynaud’s phenomenon: role of autoantibodies and nail-fold capillaroscopy. Rheumatology 49(4):797–805. https://doi.org/10.1093/rheumatology/kep447 CrossRefPubMed

32.

Mazzullo M, Miceli GM, Adamo A, Amato S (2014) Capillaroscopy. In: Enzo B, Howard IM, Klaus-Peter W (eds) Non invasive diagnostic techniques in clinical dermatology. Springer, pp 127–134. https://doi.org/10.1007/978-3-642-32109-2

33.

Ingegnoli F (2014) SP0142 How to select the most appropriate capillaroscopic device: pros and cons. Ann Rheum Dis 75(Suppl 2):35. https://doi.org/10.1136/annrheumdis-2016-eular.6383

34.

Moore TL, Roberts C, Murray AK, Helbling I, Herrick AL (2009) Reliability of dermoscopy in the assessment of patients with Raynaud’s phenomenon. Rheumatology 49(3):542–547CrossRefPubMed

35.

Maricq HR (1981) Widefield capillary microscopy. Technique and rating scale for abnormalities seen in scleroderma and related disorders. Arthritis Rheumatism 24(9):1159–1165. https://doi.org/10.1002/art.1780240907 CrossRefPubMed

36.

Andrade LEC, Gabriel A Jr, Assad RL, Ferrari AJL (1990) Atra E panoramic nailfold capillaroscopy: a new reading method and normal range. In: Seminars in arthritis and rheumatism, vol 1. Elsevier, pp 21–31

37.

Dinsdale G, Moore T, O’Leary N, Berks M, Roberts C, Manning J, Allen J, Anderson M, Cutolo M, Hesselstrand RJ Mr (2017) Quantitative outcome measures for systemic sclerosis-related microangiopathy–reliability of image acquisition in nailfold capillaroscopy. Microvasc Res 113:56–59

38.

Dinsdale G, Moore T, O’Leary N, Tresadern P, Berks M, Roberts C, Manning J, Allen J, Anderson M, Cutolo MJM (2017) Intra-and inter-observer reliability of nailfold videocapillaroscopy—a possible outcome measure for systemic sclerosis-related microangiopathy, vol 112, pp 1–6

39.

Sekiyama JY, Camargo CZ, Andrade LEC, Kayser C (2013) Reliability of widefield nailfold capillaroscopy and videocapillaroscopy in the assessment of patients with Raynaud’s phenomenon. Arthritis Care & Research 65(11):1853–1861. https://doi.org/10.1002/acr.22054 CrossRef

40.

Wildt M, Wuttge D, Hesselstrand R, Scheja A (2012) Assessment of capillary density in systemic sclerosis with three different capillaroscopic methods. Clin Exp Rheumatol 30(2):S50–S54PubMed

41.

Dogan S, Akdogan A, Atakan N (2013) Nailfold capillaroscopy in systemic sclerosis: is there any difference between videocapillaroscopy and dermatoscopy? Skin Res Technol 19(4):446–449PubMed

42.

Dinsdale G, Peytrignet S, Moore T, Berks M, Roberts C, Manning J, Allen J, Anderson M, Cutolo M, Hesselstrand R (2018) The assessment of nailfold capillaries: comparison of dermoscopy and nailfold videocapillaroscopy. Rheumatology 57(6):1115–1116. https://doi.org/10.1093/rheumatology/key018 CrossRefPubMed

43.

Parker MJ, Oliffe MT, McGill NW (2018) An evaluation of two novel capillaroscopy techniques in suspected scleroderma-spectrum disorders: a single-centre cross-sectional study. Mod Rheumatol 28(4):676–680. https://doi.org/10.1080/14397595.2017.1404179 CrossRefPubMed

44.

Ingegnoli F, Ughi N, Dinsdale G, Orenti A, Boracchi P, Allanore Y, Foeldvari I, Sulli A, Cutolo M, Smith V (2017) An international SUrvey on non-iNvaSive tecHniques to assess the mIcrocirculation in patients with RayNaud’s phEnomenon (SUNSHINE survey). Rheumatol Int 37(11):1879–1890CrossRefPubMed

45.

Chojnowski MM, Felis-Giemza A, Olesińska M (2016) Capillaroscopy–a role in modern rheumatology. Reumatologia 54(2):67–72CrossRefPubMedPubMedCentral

46.

Wu C, Lin K, Chung B (2007) A study of image quality analysis for a cutaneous capillary imaging system. J Med Biol Eng 27(3):110

47.

Weekenstroo HH, Cornelissen BM, Moens HJB (2015) Green light may improve diagnostic accuracy of nailfold capillaroscopy with a simple digital videomicroscope. Rheumatol Int 35(6):1069–1071CrossRefPubMed

48.

Dobrev H (2007) Capi text V. 1--data analysis software for nailfold skin capillaroscopy. Folia Med 49(3–4):84–87

49.

Hulley SB, Cummings S, Browner W, Grady D, Newman T (2007) Designing clinical research. 3rd edn. Lippincott Williams & Wilkins, Philadelphia

50.

Burghardt GM, Bartmess-LeVasseur JN, Browning SA, Morrison KE, Stec CL, Zachau CE, Freeberg TM (2012) Perspectives–minimizing observer bias in behavioral studies: a review and recommendations. Ethology 118(6):511–517CrossRef

51.

Mitchell ML, Jolley JM (2012) Research design explained, vol 1. 8th edn. Cengage learning. Wadsworth, CA

52.

Rodriguez-Reyna TS, Bertolazzi C, Vargas-Guerrero A, Gutiérrez M, Hernandez-Molina G, Audisio M, Roverano S, de Urizar MG, Coto JFD, Velasco BEH (2019) Can nailfold videocapillaroscopy images be interpreted reliably by different observers? Results of an inter-reader and intra-reader exercise among rheumatologists with different experience in this field. Clin Rheumatol 38(1):205–210. https://doi.org/10.1007/s10067-018-4041-2

53.

Karbalaie A (2018) Novel analysis toolkit for capillaroscopic images: development and clinical evaluation. comprehensive summary. KTH Royal Institute of Technology, US, AB

54.

Maldonado G, Guerrero R, Paredes C, Ríos C (2017) Nailfold capillaroscopy in diabetes mellitus. Microvasc Res 112:41–46. https://doi.org/10.1016/j.mvr.2017.03.001 CrossRefPubMed

55.

Kayser C, Sekiyama JY, Próspero L, Camargo CZ, Andrade L (2013) Nailfold capillaroscopy abnormalities as predictors of mortality in patients with systemic sclerosis. Clin Exp Rheumatol 31(2 Suppl 76):103–108PubMed

56.

Cutolo M, Sulli A, Smith V (2013) How to perform and interpret capillaroscopy. Best Pract Res Clin Rheumatol 27(2):237–248. https://doi.org/10.1016/j.berh.2013.03.001 CrossRefPubMed

57.

Dinsdale G, Roberts C, Moore T, Manning J, Berks M, Allen J, Anderson ME, Cutolo M, Hesselstrand R, Howell K (2018) Nailfold capillaroscopy—how many fingers should be examined to detect abnormality? Rheumatology 58(2):284–288. https://doi.org/10.1093/rheumatology/key293 CrossRef

58.

Cutolo M, Melsens K, Herrick AL, Foeldvari I, Deschepper E, De Keyser F, Distler O, Ingegnoli F, Mostmans Y, Müller-Ladner U (2018) Reliability of simple capillaroscopic definitions in describing capillary morphology in rheumatic diseases. Rheumatology 57(4):757–759. https://doi.org/10.1093/rheumatology/kex460 CrossRefPubMed

59.

Karbalaie A, Fatemi A, Etehadtavakol M, Abtahi F, Emrani Z, Erlandsson B-E (2016) Counting capillaries in nailfold capillaroscopy: state of the art and a proposed method. In: 2016 IEEE EMBS Conference on Biomedical Engineering and Sciences (IECBES). IEEE, pp 170–174

60.

Faggioli P, Tamburello A, Sciascera A, Gilardi AG, Mazzone A (2015) Nailfold videocapillaroscopy in internal medicine. Italian Journal of Medicine 9(3):234–242CrossRef

61.

Ingegnoli F, Gualtierotti R, Lubatti C, Zahalkova L, Meani L, Boracchi P, Zeni S, Fantini F (2009) Feasibility of different capillaroscopic measures for identifying nailfold microvascular alterations. Semin Arthritis Rheum 38(4):289–295. https://doi.org/10.1016/j.semarthrit.2007.10.008 CrossRefPubMed

62.

Lambova SN, Muller-Ladner UJ Crr (2018) Nailfold capillaroscopy of fingers and toes-variations of normal. 14 (1):28–35. https://doi.org/10.2174/1573397113666170726120344

63.

Manfredi A, Sebastiani M, Cassone G, Pipitone N, Giuggioli D, Colaci M, Salvarani C, Ferri C (2015) Nailfold capillaroscopic changes in dermatomyositis and polymyositis. Clin Rheumatol 34(2):279–284CrossRefPubMed

64.

Sulli A, Secchi ME, Pizzorni C, Cutolo M (2008) Scoring the nailfold microvascular changes during the capillaroscopic analysis in systemic sclerosis patients. Ann Rheum Dis 67(6):885–887. https://doi.org/10.1136/ard.2007.079756 CrossRefPubMed

65.

Furtado RN, Pucinelli ML, Cristo V, Andrade LE, Sato E (2002) Scleroderma-like nailfold capillaroscopic abnormalities are associated with anti-U1-RNP antibodies and Raynaud’s phenomenon in SLE patients. Lupus 11(1):35–41. https://doi.org/10.1191/0961203302lu144oa CrossRefPubMed

66.

Gronenschild E, Muris D, Schram M, Karaca Ü, Stehouwer C, Houben A (2013) Semi-automatic assessment of skin capillary density: proof of principle and validation. Microvasc Res 90:192–198. https://doi.org/10.1016/j.mvr.2013.08.003 CrossRefPubMed

67.

Berks M, Dinsdale G, Murray A, Moore T, Herrick A, Taylor C (2016) Improved diagnosis of systemic sclerosis using nailfold capillary flow. In: Ourselin S, Joskowicz L, Sabuncu MR, Unal G, Wells W (eds) Medical image computing and computer-assisted intervention -- MICCAI 2016 : 19th International Conference, Athens, Greece, October 17-21, 2016, Proceedings, vol 3, pp 344–352

Title: Practical issues in assessing nailfold capillaroscopic images: a summary
Authors: Abdolamir Karbalaie
Zahra Emrani
Alimohammad Fatemi
Mahnaz Etehadtavakol
Björn-Erik Erlandsson
Publication date: 01-09-2019
Publisher: Springer London
Keyword: Systemic Sclerosis
Published in: Clinical Rheumatology / Issue 9/2019
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI: https://doi.org/10.1007/s10067-019-04644-9

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2019

Arterial stiffness in Familial Mediterranean Fever: correlations with disease-related parameters and colchicine treatment

Association of cumulative anti-cyclic citrullinated protein antibodies with radiographic progression in patients with rheumatoid arthritis

Comorbidity burden and clinical characteristics of patients with difficult-to-control rheumatoid arthritis

Nailfold capillaroscopy in rheumatology: ready for the daily use but with care in terminology

Corticosteroids combined with doublet or single-agent immunosuppressive therapy for active proliferative lupus nephritis

Differing X-ray patterns in seronegative and seropositive rheumatoid arthritis

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage