Skip to main content

Advertisement

SpringerLink
Log in

Patients with psoriatic arthritis have higher levels of FeNO than those with only psoriasis, which may reflect a higher prevalence of a subclinical respiratory involvement

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Background

Psoriatic arthritis (PsA) patients are often affected by numerous comorbidities. However, contrasting results have been reported with regard to the respiratory involvement in PsA patients. The aim of this study was to evaluate the presence of subclinical airway inflammation in non-smoking PsA patients compared to patients with only psoriasis using the fraction of exhaled nitric oxide (FeNO) as an indirect marker of airway inflammation.

Methods

The study included 164 non-smoking psoriatic patients (Psoriasis Area of Severity Index or PASI score > 10): 82 with and 82 without PsA, who underwent FeNO tests at different flow rates (30, 50, 100, 200 mL/s). PsA patients were evaluated with Disease Activity in PSoriatic Arthritis Score (DAPSA). Both study groups were compared in terms of FeNO values and its association with the PASI score. The correlations between the variables were evaluated by means of Pearson’s coefficient.

Results

Patient with PsA had higher levels of FeNO than those with psoriasis but without arthritis (at 30 mL/s, 71.09 ± 18.40 ppb vs 66.88 ± 19.12 ppb (NS); at 50 mL/s, 36.61 ± 9.30 ppb vs 30.88 ± 9.73 ppb (p < 0.001); at 100 mL/s, 19.09 ± 4.66 ppb vs 16.63 ± 4.90 ppb (p < 0.001); and at 200 mL/s, 10.88 ± 2.53 ppb vs 9.43 ± 2.55 ppb (p < 0.001), respectively). PASI score correlated to FeNO only in psoriatic patients without arthritis. However, CASPAR index correlated with FeNO (FeNO30: r = 0.81, p < 0.001; FeNO50: r = 0.84, p < 0.001; FeNO100: r = 0.71, p < 0.001; FeNO200: r = 0.58, p < 0.001). DAPSA was also correlated with FeNO to all flows (FeNO30: r = 0.43, p < 0.001; FeNO50: r = 0.33, p < 0.001; FeNO100: r = 0.34, p < 0.001; FeNO200: r = 0.25, p < 0.001).

Conclusions

PsA patients seem to have more commonly subclinical airway inflammation than those with only psoriasis. Further studies are needed to replicate these findings.

Key Points

• Fraction of exhaled nitric oxide (FeNO) is a useful device to detect and monitor airway inflammation not only in asthma but also in systemic inflammatory diseases such as psoriatic arthritis and psoriasis.

• Clinicians should be aware to check respiratory diseases in patients with psoriatic arthritis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Lowes MA, Suárez-Fariñas M, Krueger JG (2014) Immunology of psoriasis. Annu Rev Immunol 32:227–255

    Article  CAS  Google Scholar 

  2. Ogdie A, Gelfand JM (2015) Clinical risk factors for the development of psoriatic arthritis among patients with psoriasis: a review of available evidence. Curr Rheumatol Rep 17(10):64

    Article  CAS  Google Scholar 

  3. Kharitnov SA, Barnes PJ (2006) Exhaled biomarkers. Chest 130:1541–1546

    Article  Google Scholar 

  4. Abeyakrthi S, Mowbray M, Bredenkamp N et al (2010) Arginase is overactive in psoriatic skin. Br J Dermatol 163:193–196

    Google Scholar 

  5. Bilgiç Ö, Altınyazar HC, Baran H et al (2015) Serum homocysteine, asymmetric dimethyl arginine (ADMA) and other arginine-NO pathway metabolite levels in patients with psoriasis. Arch Dermatol Res 307:439–444

    Article  CAS  Google Scholar 

  6. Damiani G, Radaelli A, Olivini A, Calzavara-Pinton P, Malerba M (2016) Increased airway inflammation in patients with psoriasis. Br J Dermatol 175:797–799

    Article  CAS  Google Scholar 

  7. Malerba M, Damiani G, Radaeli A et al (2015) Narrowband ultraviolet B phototherapy in psoriasis reduces proinflammatory cytokine levels and improve vitiligo and neutrophilic asthma. Br J Dermatol 173:1544–1545

    Article  CAS  Google Scholar 

  8. Donohue JF, Jain N (2013) Exhaled nitric oxide to predict corticosteroid responsiveness and reduce asthma exacerbation rates. Respir Med 107:943–952

    Article  Google Scholar 

  9. Santus P, Rizzi M, Radovanovic D et al (2018) Psoriasis and respiratory comorbidities: the added value of fraction of exhaled nitric oxide as a new method to detect, evaluate, and monitor psoriatic systemic involvement and therapeutic efficacy. Biomed Res Int 2018:3140682

    Article  CAS  Google Scholar 

  10. Dreiher J, Weitzman D, Shapiro J, Davidovici B, Cohen AD (2008) Psoriasis and chronic obstructive pulmonary disease: a case-control study. Br J Dermatol 159:956–960

    Article  CAS  Google Scholar 

  11. Chiang YY, Lin HW (2012) Association between psoriasis and chronic obstructive pulmonary disease: a population-based study in Taiwan. J Eur Acad Dermatol Venereol 26:59–65

    Article  Google Scholar 

  12. Yeung H, Takeshita J, Mehta NN, Kimmel SE, Ogdie A, Margolis DJ, Shin DB, Attor R, Troxel AB, Gelfand JM (2013) Psoriasis severity and the prevalence of major medical comorbidity: a population-based study. JAMA Dermatol 149:1173–1179

    Article  Google Scholar 

  13. Yang YW, Kang JH, Lin HC (2012) Increased risk of psoriasis following obstructive sleep apnea: a longitudinal population-based study. Sleep Med 13:285–289

    Article  Google Scholar 

  14. Hajdarbegovic E, Nijsten T, Westgeest A, Habraken F, Hollestein L, Thio B (2013) Decreased prevalence of atopic features in patients with psoriatic arthritis, but not in psoriasis vulgaris. J Am Acad Dermatol 68:270–277

    Article  Google Scholar 

  15. Raychaudhuri SP, Wiken R, Sukhov AC et al (2017) Management of psoriatic arthritis: early diagnosis, monitoring of disease severity and cutting edge therapies. J Autoimmun 76:21–37

    Article  Google Scholar 

  16. Dweik RA, Boggs PB, Erzurum SC et al (2011) An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FeNO) for clinical applications. Am J Resp Crit Care Med 184:602–615

    Article  CAS  Google Scholar 

  17. Al-Mutairi N, Al-Farag S, Al-Mutairi A, Al-Shiltawy M (2010) Comorbidities associated with psoriasis: an experience from the Middle East. J Dermatol 37:146–155

    Article  Google Scholar 

  18. Khraishi M, MacDonald D, Rampakakis E, Vaillancourt J, Sampalis JS (2011) Prevalence of patient-reported comorbidities in early and established psoriatic arthritis cohorts. Clin Rheumatol 30:877–885

    Article  Google Scholar 

  19. Højgaard P, Glintborg B, Hetland ML, Hansen TH, Lage-Hansen PR, Petersen MH, Holland-Fischer M, Nilsson C, Loft AG, Andersen BN, Adelsten T, Jensen J, Omerovic E, Christensen R, Tarp U, Østgård R, Dreyer L (2015) Association between tobacco smoking and response to tumour necrosis factor α inhibitor treatment in psoriatic arthritis: results from the DANBIO registry. Ann Rheum Dis 74:2130–2136

    Article  CAS  Google Scholar 

  20. Armstrong AW, Harskamp CT, Dhillon JS, Armstrong EJ (2014) Psoriasis and smoking: a systematic review and meta-analysis. Br J Dermatol 170:304–314

    Article  CAS  Google Scholar 

  21. Amatngalim GD, Broekman W, Daniel NM et al (2016) Cigarette smoke modulates repair and innate immunity following injury to airway epithelial cells. PLoS One 11:e0166255

    Article  CAS  Google Scholar 

  22. Costa L, Caso F, Del Puente A et al (2016) Incidence of malignancies in a cohort of psoriatic arthritis patients taking traditional disease modifying antirheumatic drug and tumor necrosis factor inhibitor therapy: an observational study. J Rheumatol 43:2149–2152

    Article  Google Scholar 

  23. Makredes M, Don Robinson D, Bala M, Kimball AB (2009) The burden of autoimmune disease: a comparison of prevalence ratios in patients with psoriatic arthritis and psoriasis. J Am Acad Dermatol 61:405–410

    Article  Google Scholar 

  24. Gossec L, Smolen JS, Gaujoux-Viala C et al (2012) European League Against Rheumatism recommendations for the management of psoriatic arthritis with pharmacological therapies. Ann Rheum Dis 71:4–12

    Article  CAS  Google Scholar 

  25. Pathirana D, Nast A, Ormerod AD, Reytan N, Saiag P, Smith CH, Spuls P, Rzany B (2010) On the development of the European S3 guidelines on the systemic treatment ofpsoriasis vulgaris: structure and challenges. J Eur Acad Dermatol Venereol 24:1458–1467

    Article  CAS  Google Scholar 

  26. Dalamaga M, Papadavid E, Vlami K (2013) Unmasking the Janus face of the association between psoriasis, metabolic syndrome and obstructive sleep apnea. Sleep Breath 17:449–450

    Article  Google Scholar 

  27. Sigurdardottir SL, Thorleifsdottir RH, Valdimarsson H, Johnston A (2013) The association of sore throat and psoriasis might be explained by histologically distinctive tonsils and increased expression of skin-homing molecules by tonsil T cells. Clin Exp Immunol 174:139–151

    Article  CAS  Google Scholar 

  28. Keller JJ, Wu CS, Lin HC (2013) Increased risk of psoriasis following chronic rhinosinusitis without nasal polyps: a population-based matched-cohort study. Br J Dermatol 168:289–294

    Article  CAS  Google Scholar 

  29. Maniscalco M, Vitale C, Vatrella A et al (2016) Fractional exhaled nitric oxide-measuring devices: technology update. Med Devices (Auckl) 9:151–160

    CAS  Google Scholar 

  30. Fyhrquist N, Ruokolainen L, Suomalainen A et al (2014) Acinetobacter species in the skin microbiota protect against sensitization and inflammation. J Allergy Clin Immunol 134:1301–1309

    Article  CAS  Google Scholar 

  31. McGonagle D (2009) Enthesitis: an autoinflammatory lesion linking nail and joint involvement in psoriatic disease. J Eur Acad Dermatol Venereol 23(Suppl 1):9–13

    Article  CAS  Google Scholar 

  32. Hedrich CM (2016) Shaping the spectrum-from autoinflammation to autoimmunity. Clin Immunol 165:21–28

    Article  CAS  Google Scholar 

  33. Abdel-Hamid MF, Aly DG, Saad NE, Emam HM, Ayoub DF (2011) Serum levels of interleukin-8, tumor necrosis factor-α and γ-interferon in Egyptian psoriatic patients and correlation with disease severity. J Dermatol 38:442–446

    Article  CAS  Google Scholar 

  34. Chhabra S, Narang T, Joshi N, Goel S, Sawatkar G, Saikia B, Dogra S, Bansal F, Minz R (2016) Circulating T-helper 17 cells and associated cytokines in psoriasis. Clin Exp Dermatol 41:806–810

    Article  CAS  Google Scholar 

  35. Osei ET, Noordhoek JA, Hackett TL et al (2016) Interleukin-1α drives the dysfunctional cross-talk of the airway epithelium and lung fibroblasts in COPD. Eur Respir J 48:359–369

    Article  CAS  Google Scholar 

  36. Wong CK, Cao J, Yin YB, Lam CW (2010) Interleukin-17A activation on bronchial epithelium and basophils: a novel inflammatory mechanism. Eur Respir J 35:883–893

    Article  CAS  Google Scholar 

  37. Atzeni F, Turiel M, Boccassini L, Sitia S, Tomasoni L, Battellino M, Marchesoni A, de Gennaro Colonna V, Sarzi-Puttini P (2011) Cardiovascular involvement in psoriatic arthritis. Reumatismo. 63:148–154

    Article  CAS  Google Scholar 

  38. Staab EB, Weigel J, Xiao F et al (2015) Asymmetric dimethyl-arginine metabolism in a murine model of cigarette smoke-mediated lung inflammation. J Immunotoxicol 12:273–282

    Article  CAS  Google Scholar 

  39. Stolz D, Leeming DJ, Edfort Kristensen JH et al (2017) Systemic biomarkers of collagen and elastin turnover are associated with clinically relevant outcomes in COPD. Chest. 151:47–59

    Article  Google Scholar 

  40. Huang T, Hazen M, Shang Y et al (2016) Depletion of major pathogenic cells in asthma by targeting CRTh2. JCI Insight 1:e86689

    Article  Google Scholar 

Download references

Funding

GD is supported by the P50 AR 070590 01A1 National Institute of Arthritis and Musculoskeletal and Skin Diseases.

Author information

Authors and Affiliations

  1. Clinical Dermatology, IRCCS Galeazzi Orthopedic Institute, Milan, Italy

    Giovanni Damiani

  2. Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy

    Giovanni Damiani

  3. Phototherapy Unit, San Gallicano Dermatological Hospital, Rome, Italy

    Alessia Pacifico

  4. Respiratory Unit, Center for Sleep and Respiratory Disorders, “Luigi Sacco” University Hospital, Milan, Italy

    Maurizio Rizzi & Pierachille Santus

  5. Department of Biomedical Sciences L. Sacco, University of Milan, Milan, Italy

    Pierachille Santus

  6. Section of Musculoskeletal Disease, Leeds Institute of Molecular Medicine, University of Leeds, NIHR Leeds Musculoskeletal Biomedical Research Unit, Chapel Allerton Hospital, Leeds, UK

    Charlie Bridgewood

  7. Laboratory for Industrial and Applied Mathematics (LIAM), Department of Mathematics and Statistics, York University, Toronto, Canada

    Nicola Luigi Bragazzi

  8. Padeh and Ziv Hospitals, Azrieli Faculty of Medicine, Bar-Ilan University, Ramat Gan, Israel

    Mohammed Adawi

  9. Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

    Abdulla Watad

  10. Department of Medicine B, Sheba Medical Center, Tel Hashomer, Israel

    Abdulla Watad

Authors
  1. Giovanni Damiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alessia Pacifico
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurizio Rizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierachille Santus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Charlie Bridgewood
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicola Luigi Bragazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mohammed Adawi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Abdulla Watad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giovanni Damiani.

Ethics declarations

All the procedures performed in the present study involving human beings were carried out in accordance with the ethical standards of the institutional and national research committee, and the principles laid down in the 1964 Declaration of Helsinki and its later amendments, or comparable ethical standards. Patients enrolled had signed an informed consent form.

Disclosures

None.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Damiani, G., Pacifico, A., Rizzi, M. et al. Patients with psoriatic arthritis have higher levels of FeNO than those with only psoriasis, which may reflect a higher prevalence of a subclinical respiratory involvement. Clin Rheumatol 39, 2981–2988 (2020). https://doi.org/10.1007/s10067-020-05050-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-020-05050-2

Keywords

Search

Navigation