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Comparison of nailfold capillaroscopy findings in COVID-19 survivors with and without rheumatic disease: a case-control study

Year 2024, Volume: 49 Issue: 1, 71 - 80, 29.03.2024
https://doi.org/10.17826/cumj.1382804

Abstract

Purpose: The aim of this study was to evaluate the nailfold capillaroscopy (NFC) findings of patients with rheumatic disease and healthy controls (HCs) who survived coronavirus disease 2019 (COVID-19).
Materials and Methods: This study included patients with axial spondyloarthritis (axSpA), psoriatic arthritis (PsA), and rheumatoid arthritis (RA) who recovered from COVID-19 and HCs. NFC was performed for all participants. NFC findings of the three groups [patients with COVID-19 (group 1), HCs with COVID-19 (group 2), and HCs without COVID-19 (group 3)] were compared.
Results: A total of 142 individuals (group 1, n = 42; group 2, n = 50; group 3, n = 50) were included in the study. Hospitalization and oxygen therapy were more common in group 1 than in group 2. The median time from a severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-positive real-time polymerase chain reaction (RT-PCR) test to NFC was 10.3 (6.3–24.4) weeks in group 1 and 17.1 (6.1–44.9) weeks in group 2. All NFC findings did not differ among the groups except for capillary ramifications, which were higher in group 1 than in groups 2 and 3. Underlying rheumatic disease was the only predictor that was significantly associated with capillary ramifications.
Conclusion: The NFC findings of COVID-19 survivors with and without rheumatic disease were substantially similar to those of HCs who did not have COVID-19. Capillary ramifications may result from an underlying rheumatic disease in patients with axSpA, PsA, and RA.

Project Number

None

References

  • Ambrosino P, Calcaterra I, Molino A, Moretta P, Lupoli R, Spedicato GA et al. Persistent endothelial dysfunction in post-acute COVID-19 syndrome: a case-control study. Biomedicines. 2021;9:957.
  • Natalello G, De Luca G, Gigante L, Campochiaro C, De Lorenzis E, Verardi L et al. Nailfold capillaroscopy findings in patients with coronavirus disease 2019: Broadening the spectrum of COVID-19 microvascular involvement. Microvasc Res. 2021;133:104071.
  • Warren AM, Zolfaghari K, Fresnedo M, Bennett M, Pogue J, Waddimba A et al. Anxiety sensitivity, COVID-19 fear, and mental health: results from a United States population sample. Cogn Behav Ther. 2021;50:204-16.
  • Xu S-w, Ilyas I, Weng J-p. Endothelial dysfunction in COVID-19: an overview of evidence, biomarkers, mechanisms and potential therapies. Acta Pharmacol Sin. 2023;44:695-709.
  • Liu N, Long H, Sun J, Li H, He Y, Wang Q et al. New laboratory evidence for the association between endothelial dysfunction and COVID‐19 disease progression. J Med Virol. 2022;94:3112-20.
  • Çakmak F, Demirbuga A, Demirkol D, Gümüş S, Torun SH, Kayaalp GK et al. Nailfold capillaroscopy: a sensitive method for evaluating microvascular involvement in children with SARS-CoV-2 infection. Microvasc Res. 2021;138:104196.
  • Hadeler E, Morrison B, Tosti A. A review of nail findings associated with COVID‐19 infection. J Eur Acad Dermatol Venereol. 2021;35:e699-e709.
  • Mondini L, Confalonieri P, Pozzan R, Ruggero L, Trotta L, Lerda S et al. Microvascular alteration in COVID-19 documented by nailfold capillaroscopy. Diagnostics (Basel). 2023;13:1905.
  • Fragoulis GE, Bournia V-K, Sfikakis PP. Different systemic rheumatic diseases as risk factors for COVID-19-related mortality. Clin Rheumatol. 2022;41:1919-23.
  • Sundaray S, Mishra S, Dash SC, Sundaray NK. Nailfold videocapillaroscopy in connective tissue diseases with Raynaud’s phenomenon in an Indian population. Rambam Maimonides Med J. 2022;13:e0003.
  • Sieper J, Rudwaleit M, Baraliakos X, Brandt J, Braun J, Burgos-Vargas R et al. The Assessment of SpondyloArthritis international Society (ASAS) handbook: a guide to assess spondyloarthritis. Ann Rheum Dis. 2009;68:ii1-44.
  • Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum. 2006;54:2665-73.
  • Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham III CO et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62:2569-81.
  • Yong SJ. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53:737-54.
  • Graceffa D, Amorosi B, Maiani E, Bonifati C, Chimenti MS, Perricone R, Di Carlo A. Capillaroscopy in psoriatic and rheumatoid arthritis: a useful tool for differential diagnosis. Arthritis. 2013;2013:957480.
  • Smith V, Herrick AL, Ingegnoli F, Damjanov N, De Angelis R, Denton CP et al. Standardisation of nailfold capillaroscopy for the assessment of patients with Raynaud's phenomenon and systemic sclerosis. Autoimmun Rev. 2020;19:102458.
  • Sulli A, Secchi ME, Pizzorni C, Cutolo M. Scoring the nailfold microvascular changes during the capillaroscopic analysis in systemic sclerosis patients. Ann Rheum Dis. 2008;67:885-7.
  • Manfredi A, Sebastiani M, Cassone G, Pipitone N, Giuggioli D, Colaci M et al. Nailfold capillaroscopic changes in dermatomyositis and polymyositis. Clin Rheumatol. 2015;34:279-84.
  • Karahan S, Aydin K, Cetinkaya A, Sirakaya HA. Nailfold videocapillaroscopy in patients with COVID-19-associated pneumonia in intensive care units. J Coll Physicians Surg Pak. 2022;32:455-60.
  • Navarro L, Andina D, Noguera‐Morel L, Hernández‐Martín A, Colmenero I, Torrelo A. Dermoscopy features of COVID‐19‐related chilblains in children and adolescents. J Eur Acad Dermatol Venereol. 2020;34:e762-64.
  • Sulli A, Gotelli E, Bica PF, Schiavetti I, Pizzorni C, Aloè T et al. Detailed videocapillaroscopic microvascular changes detectable in adult COVID-19 survivors. Microvasc Res. 2022;142:104361.
  • Rosei CA, Gaggero A, Famà F, Malerba P, Chiarini G, Nardin M et al. Skin capillary alterations in patients with acute SarsCoV2 infection. J Hypertens. 2022;40:2385-93.
  • Ebrahim Nakhli R, Shanker A, Sarosiek I, Boschman J, Espino K, Sigaroodi S et al. Gastrointestinal symptoms and the severity of COVID‐19: Disorders of gut–brain interaction are an outcome. Neurogastroenterol Motil. 2022;34:e14368.
  • Sachdeva S, Manaktala P, Malik FA, Gupta U, Desai R. COVID-19 in patients with rheumatic diseases: Is there a need to worry?. J Clin Rheumatol. 2022;28:e401-6.
  • FAI2R/SFR/SNFMI/SOFREMIP/CRI/IMIDIATE consortium and contributors. Severity of COVID-19 and survival in patients with rheumatic and inflammatory diseases: data from the French RMD COVID-19 cohort of 694 patients. Ann Rheum Dis. 2021;80:527-38.
  • Fredi M, Cavazzana I, Moschetti L, Andreoli L, Franceschini F; Brescia Rheumatology COVID-19 Study Group. COVID-19 in patients with rheumatic diseases in northern Italy: a single-centre observational and case–control study. Lancet Rheumatol. 2020;2:e549-56.
  • Santos CS, Férnandez XC, Morales CM, Álvarez ED, Castro CÁ, Robles AL et al. Biological agents for rheumatic diseases in the outbreak of COVID-19: friend or foe?. RMD Open. 2021;7:e001439.
  • Kraemer-Aguiar L, Maranhao P, Sicuro F, Bouskela E. Microvascular dysfunction: a direct link among BMI, waist circumference and glucose homeostasis in young overweight/obese normoglycemic women?. Int J Obes (Lond). 2010;34:111-7.
  • Maranhão PA, de Souza MdGC, Kraemer-Aguiar LG, Bouskela E. Dynamic nailfold videocapillaroscopy may be used for early detection of microvascular dysfunction in obesity. Microvasc Res. 2016;106:31-5.
  • De Jongh RT, Serné EH, IJzerman RG, De Vries G, Stehouwer CD. Impaired microvascular function in obesity: implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation. 2004;109:2529-35.
  • Cengiz B, Sayılır MÜ, Zengin NY, Küçük ÖN, Soylu AR. Does the COVID-19 vaccination rate change according to the education and income: a study on vaccination rates in cities of Turkey between 2021-September and 2022-February. Vaccines (Basel). 2022;10:1933.
  • Lambova SN, Müller-Ladner U. Capillaroscopic pattern in inflammatory arthritis. Microvasc Res. 2012;83:318-22.

Romatizmal hastalığı olan ve olmayan COVID-19 hastalarında tırnak dibi kapilleroskopi bulgularının karşılaştırılması: vaka-kontrol çalışması

Year 2024, Volume: 49 Issue: 1, 71 - 80, 29.03.2024
https://doi.org/10.17826/cumj.1382804

Abstract

Amaç: Bu çalışmanın amacı koronavirüs hastalığı 2019 (COVİD-19) sonrası hayatta kalan romatizmal hastalığı olan hastaların ve sağlıklı kontrollerin tırnak dibi kapilleroskopisi bulgularını değerlendirmektir.
Gereç ve Yöntem: Bu çalışmaya, COVİD-19’dan sonra iyileşen aksiyal spondiloartrit (akSpA), psoriatik artrit (PsA) ve romatoid artrit (RA) hastaları ve sağlıklı kontroller dâhil edildi. Tüm katılımcılara tırnak dibi kapilleroskopisi uygulandı. Üç grubun [COVID-19 geçiren romatizmal hastalar (grup 1), COVİD-19 geçiren sağlıklı kontroller (grup 2) ve COVİD-19 geçirmeyen sağlıklı kontroller (grup 3)] tırnak dibi kapilleroskopi bulguları karşılaştırıldı.
Bulgular: Çalışmaya grup 1'de 42, grup 2'de 50 ve grup 3'te 50 olmak üzere toplam 142 kişi dâhil edildi. Hastaneye yatış ve oksijen tedavisi oranları grup 1'de grup 2'ye göre daha sıktı. Pozitif bir şiddetli akut solunum sendromu koronavirüs-2 (SARS-CoV-2)-real-time polimeraz zincir reaksiyonu (RT-PCR) testinden tırnak dibi kapilleroskopisine kadar geçen ortalama süre grup 1'de 10,3 (6,3–24,4) hafta ve grup 2'de 17,1 (6,1–44,9) haftaydı. Grup 1'de grup 2 ve 3'e göre daha yüksek oranda olan kapiller dallanmalar dışında, tüm kapilleroskopik bulgular gruplar arasında farklılık göstermedi. Altta yatan romatizmal hastalık kapiller dallanmalarla anlamlı şekilde ilişkili olan tek prediktördü.
Sonuç: Romatizmal hastalığı olan ve olmayan, COVİD-19'dan sağ kurtulanların tırnak dibi kapilleroskopi bulguları, sağlıklı kontrollerle büyük ölçüde benzerdi. AkSpA, PsA ve RA hastalarında kapiller dallanmalar altta yatan romatizmal hastalığın bir sonucu olabilir.

Ethical Statement

This study was approved by the Erciyes University Clinical Research Ethics Committee (Date: 22 September 2021; Approval Number: 2021/615). We also acted in accordance with the Declaration of Helsinki and obtained written informed consent from all patients.

Supporting Institution

None

Project Number

None

Thanks

None

References

  • Ambrosino P, Calcaterra I, Molino A, Moretta P, Lupoli R, Spedicato GA et al. Persistent endothelial dysfunction in post-acute COVID-19 syndrome: a case-control study. Biomedicines. 2021;9:957.
  • Natalello G, De Luca G, Gigante L, Campochiaro C, De Lorenzis E, Verardi L et al. Nailfold capillaroscopy findings in patients with coronavirus disease 2019: Broadening the spectrum of COVID-19 microvascular involvement. Microvasc Res. 2021;133:104071.
  • Warren AM, Zolfaghari K, Fresnedo M, Bennett M, Pogue J, Waddimba A et al. Anxiety sensitivity, COVID-19 fear, and mental health: results from a United States population sample. Cogn Behav Ther. 2021;50:204-16.
  • Xu S-w, Ilyas I, Weng J-p. Endothelial dysfunction in COVID-19: an overview of evidence, biomarkers, mechanisms and potential therapies. Acta Pharmacol Sin. 2023;44:695-709.
  • Liu N, Long H, Sun J, Li H, He Y, Wang Q et al. New laboratory evidence for the association between endothelial dysfunction and COVID‐19 disease progression. J Med Virol. 2022;94:3112-20.
  • Çakmak F, Demirbuga A, Demirkol D, Gümüş S, Torun SH, Kayaalp GK et al. Nailfold capillaroscopy: a sensitive method for evaluating microvascular involvement in children with SARS-CoV-2 infection. Microvasc Res. 2021;138:104196.
  • Hadeler E, Morrison B, Tosti A. A review of nail findings associated with COVID‐19 infection. J Eur Acad Dermatol Venereol. 2021;35:e699-e709.
  • Mondini L, Confalonieri P, Pozzan R, Ruggero L, Trotta L, Lerda S et al. Microvascular alteration in COVID-19 documented by nailfold capillaroscopy. Diagnostics (Basel). 2023;13:1905.
  • Fragoulis GE, Bournia V-K, Sfikakis PP. Different systemic rheumatic diseases as risk factors for COVID-19-related mortality. Clin Rheumatol. 2022;41:1919-23.
  • Sundaray S, Mishra S, Dash SC, Sundaray NK. Nailfold videocapillaroscopy in connective tissue diseases with Raynaud’s phenomenon in an Indian population. Rambam Maimonides Med J. 2022;13:e0003.
  • Sieper J, Rudwaleit M, Baraliakos X, Brandt J, Braun J, Burgos-Vargas R et al. The Assessment of SpondyloArthritis international Society (ASAS) handbook: a guide to assess spondyloarthritis. Ann Rheum Dis. 2009;68:ii1-44.
  • Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum. 2006;54:2665-73.
  • Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham III CO et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62:2569-81.
  • Yong SJ. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53:737-54.
  • Graceffa D, Amorosi B, Maiani E, Bonifati C, Chimenti MS, Perricone R, Di Carlo A. Capillaroscopy in psoriatic and rheumatoid arthritis: a useful tool for differential diagnosis. Arthritis. 2013;2013:957480.
  • Smith V, Herrick AL, Ingegnoli F, Damjanov N, De Angelis R, Denton CP et al. Standardisation of nailfold capillaroscopy for the assessment of patients with Raynaud's phenomenon and systemic sclerosis. Autoimmun Rev. 2020;19:102458.
  • Sulli A, Secchi ME, Pizzorni C, Cutolo M. Scoring the nailfold microvascular changes during the capillaroscopic analysis in systemic sclerosis patients. Ann Rheum Dis. 2008;67:885-7.
  • Manfredi A, Sebastiani M, Cassone G, Pipitone N, Giuggioli D, Colaci M et al. Nailfold capillaroscopic changes in dermatomyositis and polymyositis. Clin Rheumatol. 2015;34:279-84.
  • Karahan S, Aydin K, Cetinkaya A, Sirakaya HA. Nailfold videocapillaroscopy in patients with COVID-19-associated pneumonia in intensive care units. J Coll Physicians Surg Pak. 2022;32:455-60.
  • Navarro L, Andina D, Noguera‐Morel L, Hernández‐Martín A, Colmenero I, Torrelo A. Dermoscopy features of COVID‐19‐related chilblains in children and adolescents. J Eur Acad Dermatol Venereol. 2020;34:e762-64.
  • Sulli A, Gotelli E, Bica PF, Schiavetti I, Pizzorni C, Aloè T et al. Detailed videocapillaroscopic microvascular changes detectable in adult COVID-19 survivors. Microvasc Res. 2022;142:104361.
  • Rosei CA, Gaggero A, Famà F, Malerba P, Chiarini G, Nardin M et al. Skin capillary alterations in patients with acute SarsCoV2 infection. J Hypertens. 2022;40:2385-93.
  • Ebrahim Nakhli R, Shanker A, Sarosiek I, Boschman J, Espino K, Sigaroodi S et al. Gastrointestinal symptoms and the severity of COVID‐19: Disorders of gut–brain interaction are an outcome. Neurogastroenterol Motil. 2022;34:e14368.
  • Sachdeva S, Manaktala P, Malik FA, Gupta U, Desai R. COVID-19 in patients with rheumatic diseases: Is there a need to worry?. J Clin Rheumatol. 2022;28:e401-6.
  • FAI2R/SFR/SNFMI/SOFREMIP/CRI/IMIDIATE consortium and contributors. Severity of COVID-19 and survival in patients with rheumatic and inflammatory diseases: data from the French RMD COVID-19 cohort of 694 patients. Ann Rheum Dis. 2021;80:527-38.
  • Fredi M, Cavazzana I, Moschetti L, Andreoli L, Franceschini F; Brescia Rheumatology COVID-19 Study Group. COVID-19 in patients with rheumatic diseases in northern Italy: a single-centre observational and case–control study. Lancet Rheumatol. 2020;2:e549-56.
  • Santos CS, Férnandez XC, Morales CM, Álvarez ED, Castro CÁ, Robles AL et al. Biological agents for rheumatic diseases in the outbreak of COVID-19: friend or foe?. RMD Open. 2021;7:e001439.
  • Kraemer-Aguiar L, Maranhao P, Sicuro F, Bouskela E. Microvascular dysfunction: a direct link among BMI, waist circumference and glucose homeostasis in young overweight/obese normoglycemic women?. Int J Obes (Lond). 2010;34:111-7.
  • Maranhão PA, de Souza MdGC, Kraemer-Aguiar LG, Bouskela E. Dynamic nailfold videocapillaroscopy may be used for early detection of microvascular dysfunction in obesity. Microvasc Res. 2016;106:31-5.
  • De Jongh RT, Serné EH, IJzerman RG, De Vries G, Stehouwer CD. Impaired microvascular function in obesity: implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation. 2004;109:2529-35.
  • Cengiz B, Sayılır MÜ, Zengin NY, Küçük ÖN, Soylu AR. Does the COVID-19 vaccination rate change according to the education and income: a study on vaccination rates in cities of Turkey between 2021-September and 2022-February. Vaccines (Basel). 2022;10:1933.
  • Lambova SN, Müller-Ladner U. Capillaroscopic pattern in inflammatory arthritis. Microvasc Res. 2012;83:318-22.
There are 32 citations in total.

Details

Primary Language English
Subjects Rheumatology and Arthritis
Journal Section Research
Authors

Hüseyin Kaplan 0000-0002-3292-0907

Gizem Cengiz 0000-0002-0021-7002

Senem Şaş 0000-0002-5616-5723

Hasan Kara 0000-0003-1525-1104

Project Number None
Publication Date March 29, 2024
Submission Date October 30, 2023
Acceptance Date February 3, 2024
Published in Issue Year 2024 Volume: 49 Issue: 1

Cite

MLA Kaplan, Hüseyin et al. “Comparison of Nailfold Capillaroscopy Findings in COVID-19 Survivors With and Without Rheumatic Disease: A Case-Control Study”. Cukurova Medical Journal, vol. 49, no. 1, 2024, pp. 71-80, doi:10.17826/cumj.1382804.