Capillaroscopy

doi:10.1016/j.berh.2008.09.001

Best Practice & Research Clinical Rheumatology

Volume 22, Issue 6, December 2008, Pages 1093-1108

https://doi.org/10.1016/j.berh.2008.09.001 Get rights and content

Capillaroscopy is the most reliable way to distinguish between primary and secondary Raynaud's phenomenon (RP) through identification of an early pattern of systemic sclerosis (SSc). The presence of giant capillaries and microhaemorrhages on nailfold videocapillaroscopy (NVC) is sufficient to identify the scleroderma pattern (early), and an increase in these features and the addition of loss of capillaries (active pattern) is followed by neo-angiogenesis, fibrosis and ‘desertification’ (late pattern). The sensitivity of the American College of Rheumatology's classification criteria for SSc increases from 67% to 99% with the addition of these specific NVC abnormalities. Based on the appearance of the scleroderma pattern on NVC, almost 15% of patients shift from primary to secondary RP over a mean follow-up period of 29.4 ± 10 months. Follow-up by NVC (every 6 months) is suggested for RP patients. A scoring system for NVC changes is available, and scores change significantly during follow-up of SSc patients. Several other NVC patterns have also been identified, such as in dermatomyosistis, systemic lupus eythaematosus, mixed connective tissue disease and antiphospholipid syndrome.

Section snippets

Capillaroscopy and classification criteria for systemic sclerosis

In 1980, the American College of Rheumatology (ACR, formerly American Rheumatism Association) proposed classification criteria for systemic sclerosis (SSc) with the aim of establishing ‘a standard for definite disease in order to permit comparison of groups of patients from different centers’ and not for diagnostic purposes.¹ However, these criteria have been used by clinicians for more than two decades as diagnostic criteria.2, 3

In 1988, SSc was classified into subsets by LeRoy et al.⁴ Limited

Brief history of capillaroscopy

Italian physician Giovanni Rasori (1766–1837) first noted the close relationship between conjunctival inflammation and the presence of an ‘inextricable knot of capillary loops’ using a magnifying glass.¹⁰ Following these descriptions (obtained in the mid-19th Century), at the beginning of the 20th Century, Hutchinson was able to differentiate RP into a primary phenomenon and a phenomenon secondary to different diseases by detecting microvascular changes.¹¹ Following these observations,

How to perform videocapillaroscopy in the nail bed

Morphological evaluation of skin capillaries is generally performed at the nail fold because this area is easily accessible for examination, and the major axis of the capillaries is parallel to the skin surface (in other areas, it has a perpendicular status) (Figure 1).¹⁴

Each subject must remain in the test room for a minimum of 15 min before the nailfold analysis, and the room temperature should be maintained at 20–22 °C. The nail folds usually at least 8 fingers should be examined (out first

Most important capillaroscopic changes in secondary RP

In normal conditions or in primary RP (excluding during the cold-exposure test), the normal nailfold capillaroscopic pattern shows regular disposition of the capillary loops along the nailbed (Figure 2).

However, in patients suffering from secondary RP, one or more abnormal capillaroscopic findings should alert the physician to the possibility of a previously undetected connective auto-immune disease.

Scleroderma pattern

The peripheral microvascular damage in SSc is characterized by progressive alterations of the capillaries with a decrease in their density. Blood flow is also reduced.18, 19

Studies have partially graded the capillaroscopic aspects of vascular damage in SSc into two major patterns: active and slow.²⁰

More recently, new classifications in relation to selected characteristics of disease progression have been proposed in order to improve the diagnostic and prognostic power of capillaroscopic

Scoring the SSc capillaroscopic patterns

In order to quantify the microvascular changes, a semiquantitative rating scale was recently adopted to score each capillary abnormality observed during NVC (0, no changes; 1, <33% of capillary alterations/reduction; 2, 33–66% of capillary alterations/reduction; 3, >66% of capillary alterations/reduction per linear millimetre) according to previous studies.²² The mean score for each capillaroscopic parameter was calculated from the analysis of four consecutive fields (each of 1 linear

Transition from primary to secondary RP: the role of NVC

Specific microvascular alterations are found by capillaroscopic analysis in several different connective tissue diseases [i.e. dermatomyositis, mixed connective tissue disease (MCTD) and systemic lupus erythaematosus (SLE)].¹⁴ In addition, distinct morphological patterns on NVC and a significant and gradual increase in these microvascular abnormalities are observed during the progression of SSc, and seem to reflect the evolution of the pathophysiological process.²¹

In a recent investigation, 20%

Clinical applications of NVC

NVC has a predictive value. In a recent large study, NVC was performed in 1024 consecutive patients for RP.²⁸ Follow-up was undertaken with observation of the pathological features of nailfold capillaroscopy in all patients who had neither clinical nor serological signs of a connective tissue disease (CTD) at the time of NVC.

Of 308 patients with neither serological nor clinical signs of CTD but with RP and pathological features on NVC suspicious for CTD, follow-up data were available for 133

Patterns in other CTDS

A well-defined pattern has been reported in patients affected by dermatomyositis.³¹ This pattern, often associated with aspects of the scleroderma pattern, includes the presence of two or more of the following findings in at least two fingers: twisted enlarged capillaries and capillary haemorrhages, enlargement of capillary loops, loss of capillaries, disorganization of the normal distribution of capillaries, and budding (bushy) capillaries.

The typical SLE pattern includes morphological

Conclusions

The increasing interest in capillary microscopy and its clear diagnostic usefulness in SSc and other CTDs is now a reality.42, 43 Few diagnostic techniques can combine all the positive features typical of capillaroscopy with such low cost, uninvasiveness, repeatability, high sensitivity, good specificity and easy interpretation of results.⁴⁴ The third EULAR course on capillaroscopy in rheumatic diseases (held in 2008) supported the augmented request for its application as the standard

References (44)

M. Cutolo et al.
Capillaroscopy
Best Practice & Research. Clinical Rheumatology
(2005)
A. Herrick
Diagnosis and management of scleroderma peripheral vascular disease
Rheumatic Diseases Clinics of North America
(2008)
Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee
Preliminary criteria for the classification of systemic sclerosis (scleroderma)
Arthritis and Rheumatism
(1980)
F.M. Wigley
Systemic sclerosis: clinical features
F. Atzeni et al.
Localized and systemic forms of scleroderma in adults and children
Clinical and Experimental Rheumatology
(2006)
E.C. LeRoy et al.
Scleroderma (systemic sclerosis): classification, subsets and pathogenesis
The Journal of Rheumatology
(1988)
E.C. LeRoy et al.
Criteria for the classification of early systemic sclerosis
The Journal of Rheumatology
(2001)
M. Hudson et al.
Improving the sensitivity of the American College of Rheumatology classification criteria for systemic sclerosis
Clinical and Experimental Rheumatology
(2007)
L.S. Lonzetti et al.
Updating the American College of Rheumatology preliminary classification criteria for systemic sclerosis: addition of severe nailfold capillaroscopy abnormalities markedly increases the sensitivity for limited scleroderma
Arthritis and Rheumatism
(2001)
E. Genth et al.
Systemic sclerosis – diagnosis and classification
Zeitschrift für Rheumatologie
(2006)

M. Cutolo et al.

Nailfold capillaroscopy and classification criteria for systemic sclerosis

Clinical and Experimental Rheumatology

(2007)

M. Cutolo et al.

Raynaud's phenomenon and the role of capillaroscopy

Arthritis and Rheumatism

(2003)

H. Hutchinson

Raynaud's phenomenon

La Presse médicale

(1901)

H.R. Maricq et al.

Patterns of finger capillary abnormalities in connective tissue disease by ‘wide-field’ microscopy

Arthritis and Rheumatism

(1973)

M. Cutolo et al.

Nailfold videocapillaroscopy assessment of microvascular damage in systemic sclerosis

The Journal of Rheumatology

(2000)

M. Cutolo et al.

The contribution of capillaroscopy to the differential diagnosis of connective autoimmune diseases

Best Practice & Research. Clinical Rheumatology

(2007)

M. Cutolo et al.

Nailfold capillaroscopy is useful for the diagnosis and follow-up of autoimmune rheumatic diseases. A future tool for the analysis of microvascular heart involvement?

Rheumatology (Oxford, England)

(2006)

J.A. Colwell et al.

Vascular disease in diabetes. Pathophysiological mechanisms and therapy

Archiv für innere Medizin

(1979)

P.M. Houtman et al.

Diagnostic significance of nailfold capillary patterns in patients with RP: an analysis of patterns discriminating patients with and without connective tissue disease

The Journal of Rheumatology

(1986)

M.I.V. Jayson

The microcirculation in systemic sclerosis

Clinical and Experimental Rheumatology

(1984)

M. Cutolo et al.

Capillaroscopy and rheumatic diseases: state of the art

Zeitschrift für Rheumatologie

(2006)

H.R. Maricq et al.

Diagnostic potential of in vivo capillary microscopy in scleroderma and related disorders

Arthritis and Rheumatism

(1980)

Cited by (135)

Nailfold capillaroscopy as diagnostic test in patients with psoriasis and psoriatic arthritis: A systematic review
2023, Microvascular Research
Up to 30 % of patients with psoriasis (PsO) develop psoriatic arthritis (PsA), and diagnosis can be difficult. Nailfold capillaroscopy (NC) is an easily applicable, non-invasive procedure to assess skin microcirculation. This systematic review investigates NC as diagnostic tool for PsO and PsA, including correlations between NC outcome measures to clinical and laboratory outcome measures. This systematic review was built on the PICO and PRISMA guidelines. In total 22 relevant studies were found Searching in the Web of Science, PubMed and Embase, latest update June 13th, 2022. The following NC outcome measures are found to be significantly more prevalent in PsO patients than healthy controls: reduced density, reduced length and more abnormal morphology. Likewise, in PsA patients, reduced density, more abnormal morphology, more microhaemorrhages and fewer hairpin shapes are found to be significantly more prevalent. Results were non-conclusive in terms of disease activity and duration with NC findings. Random-effects meta-analysis showed a significant reduction of density in PsO patients compared to healthy controls (studies: 6, n = 249; SMD = -0.91; 95 % CI [−1.41, −0.40], p = 0.0058, heterogeneity I²=74 %, AUC = 0.740) and in PsA patients compared to healthy controls (studies: 5, n = 130; SMD = -1.22; 95 % CI [−2.38, −0.06], p = 0.0432, heterogeneity I²=89 %, AUC = 0.806). No NC outcome measures were overall conclusive in differentiating PsO from PsA. Considering the conflicting results and small sample sizes further large-scale research on the identification of capillaroscopic changes in PsO and PsA and correlations with standardised clinical and laboratory outcome measures are necessary.
Deep learning and computer vision techniques for microcirculation analysis: A review
2023, Patterns
Citation Excerpt :
Capillaroscopy is a method that noninvasively checks the dermal papillary capillaries using a microscopy system.43 The image(s) obtained can then be evaluated for capillary density, dimension, and morphology.43 Figure 1 was obtained from Ruaro et al.44 and best illustrates this.
The analysis of microcirculation images has the potential to reveal early signs of life-threatening diseases such as sepsis. Quantifying the capillary density and the capillary distribution in microcirculation images can be used as a biological marker to assist critically ill patients. The quantification of these biological markers is labor intensive, time consuming, and subject to interobserver variability. Several computer vision techniques with varying performance can be used to automate the analysis of these microcirculation images in light of the stated challenges. In this paper, we present a survey of over 50 research papers and present the most relevant and promising computer vision algorithms to automate the analysis of microcirculation images. Furthermore, we present a survey of the methods currently used by other researchers to automate the analysis of microcirculation images. This survey is of high clinical relevance because it acts as a guidebook of techniques for other researchers to develop their microcirculation analysis systems and algorithms.
Capillaroscopic abnormalities in systemic lupus erythematosus and its association with clinical manifestation
2023, Revista Colombiana de Reumatologia
Capillaroscopy is a non-invasive tool used to evaluate microcirculation and determine whether a Raynaud's phenomenon is primary or secondary. Capillaroscopic changes are well-described in systemic sclerosis; however, these alterations have been less studied in other autoimmune diseases.
The aim of this study is to determine videocapillaroscopic alterations in lupus, and its association with clinical manifestations.
A cross-sectional study with analytical intention was performed. Videocapillaroscopy and medical evaluations were performed on 76 patients with lupus, according to SLICC 2012 classificatory criteria, from January to June 2019. Chi², Fisher, and Mann–Whitney U tests were used to evaluate association, and the prevalence ratios (PR) were determined. A multivariate analysis was performed.
Seventy-one (93.4%) of the patients were female with a median age of 33.5 years (interquartile range [IQR]: 27–44.8); the median lupus duration was 84 months (IQR: 30–168). The main clinical manifestations were articular, cutaneous, hematological, and Raynaud's phenomenon. A non-specific pattern was found in 43 patients (56.6%), and a systemic sclerosis-like pattern was found in 7 patients (9.2%). In bivariate and multivariate analyses, Raynaud episodes occurring more than once a week (PR 1.24; 95% CI: 1.13–1.33) were more frequent in patients with a sclerosis-like or a non-specific pattern.
Lupus patients frequently have videocapillaroscopic alterations with non-specific and systemic sclerosis like patterns, which are more common in patients with Raynaud's phenomenon that occurs more than once a week. Due to the study's design, it is impossible to determine causality.
La capilaroscopia es una herramienta no invasiva utilizada para evaluar la microcirculación y determinar si el fenómeno de Raynaud es primario o secundario. Los cambios capilaroscópicos están bien descritos en la esclerosis sistémica, sin embargo, estas alteraciones se han estudiado menos en otras enfermedades autoinmunes.
El objetivo de este estudio es determinar las alteraciones videocapilaroscópicas en el lupus y su asociación con manifestaciones clínicas.
Estudio transversal con intención analítica. Se realizó videocapilaroscopia y evaluación médica a 76 pacientes con lupus de enero a junio del 2019. Se utilizaron las pruebas U de Mann-Whitney, Chi cuadrado y Fisher para evaluar la asociación, y se determinaron las razones de prevalencia (PR). Se realizó un análisis multivariado.
Setenta y un (93,4%) pacientes eran mujeres, con edad media de 33,5 años (rango intercuartil [RIQ]: 27-44,8); la mediana de duración del lupus fue de 84 meses (RIQ: 30-168). Las principales manifestaciones clínicas fueron articulares, cutáneas, hematológicas y el fenómeno de Raynaud. Se encontró un patrón no específico en 43 pacientes (56,6%) y un patrón similar a la esclerosis sistémica en siete pacientes (9,2%). En los análisis bivariados y multivariados, los episodios de Raynaud que ocurren más de una vez por semana (PR 1,24; IC 95%: 1,13-1,33) fueron más frecuentes en pacientes con un patrón de esclerosis no específico.
Los pacientes con lupus con frecuencia tienen alteraciones videocapilaroscópicas con patrones no específicos, que son más comunes en pacientes con fenómeno de Raynaud que ocurre más de una vez por semana.
Rheumatological manifestations of chronic graft versus host disease - Case series
2023, Blood Cells, Molecules, and Diseases
To present the rheumatological manifestations of chronic graft versus host disease (cGVHD) and describe how they differ from primary systemic connective tissue diseases.
Description of 7 patients with cGVHD with symptoms resembling Sjögren's syndrome and scleroderma, with a critical review of the literature.
7 patients treated at the hematology department, who developed cGVHD with present antinuclear antibodies, were referred to the rheumatology department for further evaluation. All patients presented symptoms of dry eye syndrome confirmed with ophthalmic tests. If the diagnosis of GVHD was not an exclusion criterion, Sjögren's syndrome criteria would be met by 4 of our patients – they presented not only with dryness but also with typical antibodies, inflammatory changes in salivary glands on ultrasound examination, and mononuclear cell infiltration in histopathological examination of labial salivary glands. Additionally, three patients presented with scleroderma-like syndromes, but with symptoms easy to differentiate from systemic sclerosis.
cGVHD may be difficult to distinguish from Sjögren's syndrome, but such distinction is important due to the different standards of treatment in cGVHD and primary connective tissue diseases.
Detailed videocapillaroscopic microvascular changes detectable in adult COVID-19 survivors
2022, Microvascular Research
COVID-19 is a multisystem disease that causes endothelial dysfunction and organ damage. Aim of the study was to evaluate the microvascular status in COVID-19 survivors with past different disease severity, in comparison with age and sex-matched primary Raynaud's phenomenon (PRP) patients and control subjects (CNT), including possible effects of concomitant therapies.
Sixty-one COVID-19 survivors (mean age 58 ± 13 years, mean days from disease onset 126 ± 53 and mean days from recovery 104 ± 53), thirty-one PRP patients (mean age 59 ± 15 years, mean disease duration 11 ± 10 years) and thirty CNT (mean age 58 ± 13 years) underwent nailfold videocapillaroscopy (NVC) examination. The following capillaroscopic parameters were searched and scored (0–3): dilated capillaries, giant capillaries, isolated microhemorrhages, capillary ramifications (angiogenesis) and capillary number, including absolute capillary number per linear millimeter at the nailfold bed.
The mean nailfold capillary number per linear millimeter was significantly lower in COVID-19 survivors when compared with PRP patients and CNT (univariate and multivariate analysis p < 0.001). On the contrary, COVID-19 survivors showed significantly less isolated microhemorrhages than PRP patients and CNT (univariate and multivariate analysis, p = 0.005 and p = 0.012, respectively). No statistically significant difference was observed between COVID-19 survivors and control groups concerning the frequency of dilated capillaries and capillary ramifications. COVID-19 selective therapies showed a promising trend on preserving capillary loss and deserving further investigations.
SARS-CoV-2 seems to mainly induce a significant loss of capillaries in COVID-19 survivors at detailed NVC analysis in comparison to controls. The presence of a significant reduced score for isolated microhaemorrhages in COVID-19 survivors deserves further analysis.
Retinal vascular network: Changes with aging and systemic vascular disease (cardiac and cerebral)
2022, Journal Francais d'Ophtalmologie
La description du réseau microvasculaire rétinien bénéficie, depuis plus de 10 ans, du développement de nouvelles techniques d’imagerie. Les logiciels automatiques d’analyse d’images, ainsi que l’OCT-angiographie (OCT-A) permettent de mettre en évidence des modifications subtiles et précoces de l’arbre vasculaire rétinien grâce à de nombreuses données quantitatives microvasculaires. L’enjeu des recherches actuelles est de démontrer l’association entre ces modifications microvasculaires, le vieillissement vasculaire systémique et les pathologies cérébro et cardiovasculaires. En effet, un continuum physiopathologique existe entre altérations microvasculaires rétiniennes et pathologies vasculaires systémiques. Dans l’étude de population Montrachet, nous avons montré qu’un réseau vasculaire suboptimal, évalué sur fond d’œil avec le logiciel Singapore I Vessel Assessment (SIVA), était significativement associé à l’existence d’un diabète traité et d’un sur risque de mortalité cardiovasculaire. Par ailleurs, nous avons complété nos recherches sur le réseau vasculaire rétinien avec l’utilisation de l’OCT-A. Dans l’étude EYE-MI, nous avons démontré le potentiel intérêt de caractériser, de manière quantitative, le réseau microvasculaire rétinien en OCT-A afin d’évaluer le profil de risque cardiovasculaire des patients atteints de cardiopathies ischémiques. Un score de risque AHA (American Heart Association) élevé était associé à une faible densité vasculaire rétinienne indépendamment des modifications hémodynamiques systémiques. Ainsi, une meilleure compréhension du lien entre microvascularisation rétinienne et pathologie macrovasculaire permettrait d’envisager son utilisation pour une identification précoce des patients à risque et de leur proposer un programme de prévention primaire personnalisé. Le réseau vasculaire rétinien pourrait donc être un témoin de l’histoire vasculaire systémique mais aussi un biomarqueur prédictif intéressant d’événements vasculaires systémiques.
For over 10 years, the description of the retinal microvascular network has benefited from the development of new imaging techniques. Automated retinal image analysis software, as well as OCT angiography (OCT-A), are able to highlight subtle, early changes in the retinal vascular network thanks to a large amount of microvascular quantitative data. The challenge of current research is to demonstrate the association between these microvascular changes, the systemic vascular aging process, and cerebrovascular and cardiovascular disease. Indeed, a pathophysiological continuum exists between retinal microvascular changes and systemic vascular diseases. In the Montrachet study, we found that a suboptimal retinal vascular network, as identified by the Singapore I Vessel Assessment (SIVA) software, was significantly associated with treated diabetes and an increased risk of cardiovascular mortality. In addition, we supplemented our research on the retinal vascular network with the use of OCT-A. In the EYE-MI study, we showed the potential role of quantitative characterization of the retinal microvascular network by OCT-A in order to assess the cardiovascular risk profile of patients with a history of myocardial infarction. A high AHA (American Heart Association) risk score was associated with low retinal vascular density independently of hemodynamic changes. Thus, a better understanding of the association between the retinal microvasculature and macrovascular disease might make its use conceivable for early identification of at-risk patients and to suggest a personalized program of preventative care. The retinal vascular network could therefore represent an indicator of systemic vascular disease as well as an interesting predictive biomarker for vascular events.

View all citing articles on Scopus

View full text

9Capillaroscopy

Section snippets

Capillaroscopy and classification criteria for systemic sclerosis

Brief history of capillaroscopy

How to perform videocapillaroscopy in the nail bed

Most important capillaroscopic changes in secondary RP

Scleroderma pattern

Scoring the SSc capillaroscopic patterns

Transition from primary to secondary RP: the role of NVC

Clinical applications of NVC

Patterns in other CTDS

Conclusions

Best Practice & Research. Clinical Rheumatology

Rheumatic Diseases Clinics of North America

Preliminary criteria for the classification of systemic sclerosis (scleroderma)

Arthritis and Rheumatism

Systemic sclerosis: clinical features

Localized and systemic forms of scleroderma in adults and children

Clinical and Experimental Rheumatology

Scleroderma (systemic sclerosis): classification, subsets and pathogenesis

The Journal of Rheumatology

Criteria for the classification of early systemic sclerosis

The Journal of Rheumatology

Improving the sensitivity of the American College of Rheumatology classification criteria for systemic sclerosis

Clinical and Experimental Rheumatology

Updating the American College of Rheumatology preliminary classification criteria for systemic sclerosis: addition of severe nailfold capillaroscopy abnormalities markedly increases the sensitivity for limited scleroderma

Arthritis and Rheumatism

Systemic sclerosis – diagnosis and classification

Zeitschrift für Rheumatologie

Nailfold capillaroscopy and classification criteria for systemic sclerosis

Clinical and Experimental Rheumatology

Raynaud's phenomenon and the role of capillaroscopy

Arthritis and Rheumatism

Raynaud's phenomenon

La Presse médicale

Patterns of finger capillary abnormalities in connective tissue disease by ‘wide-field’ microscopy

Arthritis and Rheumatism

Nailfold videocapillaroscopy assessment of microvascular damage in systemic sclerosis

The Journal of Rheumatology

The contribution of capillaroscopy to the differential diagnosis of connective autoimmune diseases

Best Practice & Research. Clinical Rheumatology

Nailfold capillaroscopy is useful for the diagnosis and follow-up of autoimmune rheumatic diseases. A future tool for the analysis of microvascular heart involvement?

Rheumatology (Oxford, England)

Vascular disease in diabetes. Pathophysiological mechanisms and therapy

Archiv für innere Medizin

Diagnostic significance of nailfold capillary patterns in patients with RP: an analysis of patterns discriminating patients with and without connective tissue disease

The Journal of Rheumatology

The microcirculation in systemic sclerosis

Clinical and Experimental Rheumatology

Capillaroscopy and rheumatic diseases: state of the art

Zeitschrift für Rheumatologie

Diagnostic potential of in vivo capillary microscopy in scleroderma and related disorders

Arthritis and Rheumatism

9
Capillaroscopy