Publications by authors named "Cosimo Bruni"

74 Publications

THE ROLE OF CHEST CT IN DECIPHERING INTERSTITIAL LUNG INVOLVEMENT: SYSTEMIC SCLEROSIS VERSUS COVID-19.

Rheumatology (Oxford) 2021 Jul 28. Epub 2021 Jul 28.

Department of Experimental and Clinical Medicine, University of Florence, and Infectious and TropicalDiseases Unit, AOUC, Florence, Italy.

Objective: To identify the main computed tomography (CT) features that may help distinguishing a progression of interstitial lung disease (ILD) secondary to Systemic sclerosis (SSc) from COVID-19 pneumonia.

Methods: This multicentric study included 22 international readers divided in the radiologist group (RAD) and non-radiologist group (nRAD). A total of 99 patients, 52 with COVID-19 and 47 with SSc-ILD, were included in the study.

Results: Fibrosis inside focal ground glass opacities (GGO) in the upper lobes; fibrosis in the lower lobe GGO; reticulations in lower lobes (especially if bilateral and symmetrical or associated with signs of fibrosis) were the CT features most frequently associated with SSc-ILD. The CT features most frequently associated with COVID- 19 pneumonia were: consolidation (CONS) in the lower lobes, CONS with peripheral (both central/peripheral or patchy distributions), anterior and posterior CONS and rounded-shaped GGOs in the lower lobes. After multivariate analysis, the presence of CONS in the lower lobes (p < 0.0001) and signs of fibrosis in GGO in the lower lobes (p < 0.0001) remained independently associated with COVID-19 pneumonia or SSc-ILD, respectively. A predictive score was created which resulted positively associated with the COVID-19 diagnosis (96.1% sensitivity and 83.3% specificity).

Conclusion: The CT differential diagnosis between COVID-19 pneumonia and SSc-ILD is possible through the combination the proposed score and the radiologic expertise. The presence of consolidation in the lower lobes may suggest a COVID-19 pneumonia while the presence of fibrosis inside GGO may indicate a SSc-ILD.
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http://dx.doi.org/10.1093/rheumatology/keab615DOI Listing
July 2021

Oral Species in Systemic Sclerosis.

Microorganisms 2021 Jun 15;9(6). Epub 2021 Jun 15.

Department of Experimental and Clinical Medicine, Department of Geriatric Medicine, Division of Rheumatology, University of Firenze, 50124 Firenze, Italy.

In systemic sclerosis (SSc), the gastrointestinal tract (GIT) plays a central role in the patient's quality of life. The microbiome populates the GIT, where a relationship between the and gastrointestinal motility has been suggested. In this study, the analysis of oral species in SSc patients and healthy subjects using culture-independent molecular techniques, together with a review of the literature on microbiota and lactobacilli in SSc, has been carried out. Twenty-nine SSc female patients (mean age 62) and twenty-three female healthy subjects (HS, mean age 57.6) were enrolled and underwent tongue and gum swab sampling. Quantitative PCR was conducted in triplicate using specific primers 1, 1o and 2 for the RNA-polymerase β subunit gene. Our data show significantly ( = 0.0211) lower spp sequences on the tongue of patients with SSc compared to HS. The mean value of the amount of gene on the gumsofSSc patients was minor compared to HS. A significant difference between tongue and gums ( = 0.0421) was found in HS but not in SSc patients. In conclusion, our results show a lower presence of in the oral cavity of SSc patients. This strengthens the hypothesis that may have both a protective and therapeutic role in SSc patients.
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http://dx.doi.org/10.3390/microorganisms9061298DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8232208PMC
June 2021

Correlation between Potential Risk Factors and Pulmonary Embolism in Sarcoidosis Patients Timely Treated.

J Clin Med 2021 Jun 2;10(11). Epub 2021 Jun 2.

Department of Pulmonology, University Hospital of Cattinara, 34127 Trieste, Italy.

Background: Some studies with inconclusive results have reported a link between sarcoidosis and an increased risk of pulmonary embolism (PE). This study aimed at assessing a possible correlation between potential risk factors and PE in sarcoidosis patients.

Methods: A total of 256 sarcoidosis patients (84 males and 172 females; mean age at diagnosis 49 ± 13) were enrolled after giving written informed consent. Clinical evaluations, laboratory and radiology tests were performed to evaluate the presence of pulmonary embolism.

Results: Fifteen sarcoidosis patients with PE (4 males and 11 females; mean age at diagnosis 50 ± 11), diagnosed by lung scintigraphy and 241 sarcoidosis patients without PE (80 males and 161 females; mean age at diagnosis 47 ± 13), were observed. There was a statistically significant increase of the presence of antiphospholipid antibodies in the sarcoidosis group with pulmonary embolism. There was no statistically significant difference between the two groups as to smoking habit, obesity or hereditary thrombophilia frequency ( > 0.05, respectively).

Conclusions: This study demonstrates a significant correlation between the presence of antiphospholipid antibody positivity and the pulmonary embolism events in our sarcoidosis patients. Furthermore, we propose screening for these antibodies and monitoring, aimed at timely treatment.
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http://dx.doi.org/10.3390/jcm10112462DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8199598PMC
June 2021

Baricitinib in the treatment of rheumatoid arthritis: clinical and ultrasound evaluation of a real-life single-centre experience.

Ther Adv Musculoskelet Dis 2021 10;13:1759720X211014019. Epub 2021 May 10.

Department Experimental and Clinical Medicine & Division of Rheumatology, Azienda Ospedaliero Universitaria Careggi, Firenze, Italy.

Background: Ultrasound (US) is useful in monitoring RA patients, with the US7 score allowing grey-scale and power-Doppler (PD) semi-quantitative evaluation of synovitis and teno-synovitis. We evaluated real-life efficacy and safety of Baricitinib, an oral selective JAK1-2 inhibitor, in RA patients using clinical, clinimetric, and US assessments.

Methods: Disease activity score in 28 joints calculated with C-reactive protein (DAS28-CRP), disease activity score in 28 joints calculated with erythrocyte sedimentation rate (DAS28-ESR), clinical disease activity index (CDAI), simplified disease activity index (SDAI), visual analogue scale (VAS)-pain, health assessment questionnaire (HAQ), COCHIN scale, adverse events (AE), concomitant medications, laboratory parameters, and US7 were performed/recorded at baseline, 1, 3, and 6 months in RA patients starting Baricitinib. Responder/non-responder status was determined according to the EULAR Response Criteria at 3 months. SDAI clinical remission or low disease activity (LDA) were calculated at 3 and 6 months.

Results: In 43 enrolled patients, a significant improvement in disease activity and US7 components (except tendon PD) and a reduction of steroid dosage were observed. Responders at 3 months showed a significantly higher reduction of CDAI, SDAI, COCHIN scale, VAS-pain, and US7 synovialPD, compared with non-responders. At 3 and 6 months, remission/LDA was achieved by 12.8/53.8% and 21.6/51.3% patients, respectively. The csDMARD co-treatment was independently associated with remission/LDA at 3 months. Safety-related drop-outs were in line with literature data. The steroid dosage was associated with AE development at 6 months.

Conclusion: The real-life data, also obtained with US evaluation, confirmed the Baricitinib efficacy in RA disease control, as well as the utility of assessment during the follow up of disease activity.
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http://dx.doi.org/10.1177/1759720X211014019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8120535PMC
May 2021

Systemic sclerosis and COVID-19: what's new in the literature.

Clin Exp Rheumatol 2021 Jul-Aug;39 Suppl 131(4):157-158. Epub 2021 May 3.

Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Firenze, Italy.

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August 2021

The Relationship between Pulmonary Damage and Peripheral Vascular Manifestations in Systemic Sclerosis Patients.

Pharmaceuticals (Basel) 2021 Apr 23;14(5). Epub 2021 Apr 23.

Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Firenze, 50121 Florence, Italy.

Systemic sclerosis (SSc) is an autoimmune disease, characterized by the presence of generalized vasculopathy and tissue fibrosis. Collagen vascular disorder in SSc is due to fibroblast and endothelial cell dysfunctions. This leads to collagen overproduction, vascular impairment and immune system abnormalities and, in the last stage, multi-organ damage. Thus, to avoid organ damage, which has a poor prognosis, all patients should be carefully evaluated and followed. This is particularly important in the initial disease phase, so as to facilitate early identification of any organ involvement and to allow for appropriate therapy. Pulmonary disease in SSc mainly involves interstitial lung disease (ILD) and pulmonary arterial hypertension (PAH). High-resolution computed tomography (HRCT) and pulmonary function tests (PFT) have been proposed to monitor parenchymal damage. Although transthoracic echocardiography is the most commonly used screening tool for PAH in SSc patients, definitive diagnosis necessitates confirmation by right heart catheterization (RHC). Moreover, some studies have demonstrated that nailfold videocapillaroscopy (NVC) provides an accurate evaluation of the microvascular damage in SSc and is able to predict internal organ involvement, such as lung impairment. This review provides an overview of the correlation between lung damage and microvascular involvement in SSc patients.
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http://dx.doi.org/10.3390/ph14050403DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8145021PMC
April 2021

Interleukin-1 and Systemic Sclerosis: Getting to the Heart of Cardiac Involvement.

Front Immunol 2021 23;12:653950. Epub 2021 Mar 23.

Department of Experimental and Clinical Medicine, University of Florence, and Division of Rheumatology AOUC, Florence, Italy.

Systemic sclerosis (SSc) is rare, severe connective tissue disease characterized by endothelial and vascular damage, immune activation, and resulting in inflammation and fibrosis of skin and internal organs, including the heart. SSc is associated with high morbidity and mortality. Cardiac involvement is frequent in SSc patients, even though often asymptomatic at early stages, and represents one of the major causes of SSc-related mortality. Heart involvement has a variable clinical presentation, and its pathogenesis is not completely understood. Myocardial fibrosis is traditionally considered the immunopathologic hallmark of heart involvement in SSc. This unique histological feature is paralleled by distinctive clinical and prognostic features. The so-called "vascular hypothesis" represents the most credited hypothesis to explain myocardial fibrosis. More recently, the prominent role of an inflammatory myocardial process has been identified as a cardinal event in the evolution to fibrosis, thus also delineating an "inflammation-driven pathway to fibrosis". The pro-inflammatory cytokine interleukin (IL)-1 has an apical and cardinal role in the myocardial inflammatory cascade and in cardiac dysfunction. The primary aim of this perspective article is: to present the emerging evidence on the role of IL-1 and inflammasome in both SSc and heart inflammation, to review the complex interplay between cellular metabolism and inflammasome activation, and to discuss the rationale for targeted inhibition of IL-1 for the treatment of SSc-heart involvement, providing preliminary experimental and clinical data to support this hypothesis.
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http://dx.doi.org/10.3389/fimmu.2021.653950DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8021854PMC
March 2021

Cardiac involvement in systemic sclerosis: Getting to the heart of the matter.

Best Pract Res Clin Rheumatol 2021 Mar 15:101668. Epub 2021 Mar 15.

Department of Medicine, The University of Melbourne at St Vincent's Hospital, 41 Victoria Pde Fitzroy VIC, 3065, Australia; Department of Rheumatology, St Vincent's Hospital, Melbourne 41 Victoria Pde Fitzroy VIC, 3065, Australia. Electronic address:

Primary systemic sclerosis heart involvement (pSHI) is an important disease manifestation that accounts for a significant proportion of systemic sclerosis (SSc)-associated mortality. A broad clinical spectrum of pSHI exists, which ranges from asymptomatic perfusion abnormalities to diastolic dysfunction or acute myocarditis and congestive heart failure. With improving sensitivity of cardiac investigations, it is increasingly recognized that there is a large burden of subclinical cardiac disease in patients with SSc. Early signs of pSHI can be subtle and determining the etiology of cardiac abnormalities from other causes of cardiomyopathy such as hypertension, ischemic heart disease (IHD), and pulmonary vascular disease remain challenging. Early identification of pSHI potentially provides clinicians with a window of opportunity for intervention to avert progression to heart failure. However, optimal screening and treatment guidelines are lacking, and it is an area of much needed further clinical research.
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http://dx.doi.org/10.1016/j.berh.2021.101668DOI Listing
March 2021

Ultrasonographic imaging of systemic sclerosis digital ulcers: A systematic literature review and validation steps.

Semin Arthritis Rheum 2021 04 19;51(2):425-429. Epub 2021 Feb 19.

Department of Medicine, Rheumatology Division, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, United States; Department of Experimental and Clinical Medicine, University of Florence, and Division of Rheumatology AOUC, Florence, Italy; Department of Rheumatology, University of Washington, Seattle, WA, United States. Electronic address:

Introduction/background: Skin ulcers are a complex array of clinical manifestations of systemic sclerosis (SSc) and are often difficult to treat. However, the definition of SSc-skin ulcers has to date not been promising, demonstrating poor reliability and accuracy. There are emerging data that ultrasound has significant potential to evaluate SSc-skin ulcers.

Objective: To perform a systematic literature review (SLR) to understand the degree to which ultrasound of SSc skin ulcers has been validated according to OMERACT criteria.

Methods: In a SLR, we investigated the Cochrane Library, Web of Science and Pubmed databases for manuscripts from inception to 1st April 2020. Inclusion and exclusion criteria included manuscripts on SSc patients aged over 16 years, performing SSc-related skin ulcer evaluation with ultrasound machines. Papers on animal model, diseases other than SSc, venous ulcers were excluded. Data extraction used a uniform case report form which collected data on patient demographics, disease activity, description of the ultrasound machine and procedures and the degree to which domains of validity were fulfilled. Manuscript evaluation and extraction was performed by two independent assessors, with a third author being consulted in case of disagreement.

Results: amongst 308 manuscripts that were identified, 6 published manuscripts/ posters fulfilled the inclusion/exclusion criteria and were extracted. Face validity was found. Three studies developed an US definition of SSc-ulcers across patients (content validity); one study evaluated the concordance between US image and clinical assessment. Criterion validity was shown by one study and ultrasound detected improvement (sensitivity to change) of SSc-skin ulcer in response to therapy. Feasibility was demonstrated by US use for skin ulcers in multiple settings (the 6 manuuscripts/posters).

Conclusion: This systematic literature review shows that ultrasound for skin ulcers in SSc has been partially validated. It has face, content, criterion validity, responsiveness and reasonable feasibility. Further validation for construct validity, reliability and discrimination is required.
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http://dx.doi.org/10.1016/j.semarthrit.2021.02.008DOI Listing
April 2021

The Treatment of Lung Involvement in Systemic Sclerosis.

Pharmaceuticals (Basel) 2021 Feb 13;14(2). Epub 2021 Feb 13.

Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Firenze, 50121 Firenze FI, Italy.

Systemic sclerosis (SSc) patients are often affected by interstitial lung disease (ILD) and, although there have been recent treatment advances, it remains the leading cause of death among SSc, with a 10-year mortality up to 40%. African Americans and subjects with diffuse cutaneous SSc or anti-topoisomerase 1 antibodies are most commonly affected. Currently, early ILD diagnosis can be made, and it is pivotal to improve the prognosis. The diagnostic mainstay test for SSc-ILD is high-resolution computed tomography for the morphology and pulmonary function tests for the functional aspects. Treatment planning and intensity are guided by the disease severity and risk of progression. Traditionally, therapy has depended on combinations of immunosuppressants, particularly cyclophosphamide and mycophenolate mofetil, which can be supplemented by targeted biological and antifibrotic therapies. Benefits have been observed in trials on hematopoietic autologous stem cell transplantation for patients with progressive SSc, whilst lung transplantation is reserved for refractory SSc-ILD cases. Herein, recent advances in SSc-ILD treatment will be explored.
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http://dx.doi.org/10.3390/ph14020154DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7918752PMC
February 2021

Prediction and primary prevention of major vascular complications in systemic sclerosis.

Eur J Intern Med 2021 May 5;87:51-58. Epub 2021 Feb 5.

Div. Rheumatology, Department of Experimental and Clinical Medicine, AOU Careggi, University of Florence, Florence, Italy.

Objective: In Systemic Sclerosis (SSc), vasculopathy is the background of major vascular complications (MVCs), like digital ulcers (DUs), pulmonary arterial hypertension (PAH) and scleroderma renal crisis (SRC). We aimed to identify the predictors and to test the primary preventive effect of vasoactive/vasodilating drugs (VVD) for the development of MVCs in SSc MVCs-naïve patients.

Methods: patients fulfilling the ACR/EULAR 2013 classification criteria for SSc without history of MVCs were eligible. Data about clinical manifestations, laboratory and instrumental assessments and treatments were retrospectively collected at baseline and latest available follow-up.

Results: 134 SSc patients were enrolled (mean age 56.5 years ± 14.2, females 88.1%, limited subset 61.9%, ACA positivity 60.4%). In a mean of 43 ± 19 months of follow-up 12 (9.0%) patients developed at least 1 MVC (10 DU, 2 PAH and 1 SRC). Dyspnoea and arthritis at baseline were independent predictors for MVCs development (p = 0.012, and p = 0.002 respectively). No primary preventive effect of VVD on MVCs development was found. However, sildenafil reduced the renal resistive index increase (p = 0.042) and alprostadil slowed the DLco decline (p = 0.029). Both iloprost and angiotensin-receptor blockers (ARBs) delayed MVCs development, while angiotensin converting enzyme inhibitors (ACEi) determined an earlier onset of such MCVs.

Conclusions: in SSc patients, our data confirm the role of arthritis and dyspnea as independent predictors of major vascular complications, in particular in MVCs-naïve patients. Prostanoids, sildenafil and ARBs, even in absence of a primary preventive action, might help in slowing disease progression and postponing the onset of MVCs.
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http://dx.doi.org/10.1016/j.ejim.2021.01.022DOI Listing
May 2021

Digital Ulcers in Systemic Sclerosis.

Presse Med 2021 Feb 3;50(1):104064. Epub 2021 Feb 3.

Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Firenze, & Department of Geriatric Medicine, Division of Rheumatology AOUC, Firenze, Italy. Electronic address:

Digital ulcers (DU) are one of the most common complication of Systemic Sclerosis (SSc)-related vasculopathy and represent an important burden for the patients as well as for the society. Still today there is no agreement on the definition, classification and cathegorization of DU even if they are of pivotal importance in clinical practice, for treatment choice and prognostic outcomes, as well as for clinical trials. DU management requires a dedicated multidisciplinary team, that must remain ever vigilant for the development of infective complications and gangrene throughout their disease course, as well as patient education that is crucial to obtain the best compliance to assure the success of the treatment. Currently several drugs are available for DU treatment but in the future, more investigations will be needed to ameliorate the approach and the systemic and local therapies.
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http://dx.doi.org/10.1016/j.lpm.2021.104064DOI Listing
February 2021

Glycolysis-derived acidic microenvironment as a driver of endothelial dysfunction in systemic sclerosis.

Rheumatology (Oxford) 2021 Jan 20. Epub 2021 Jan 20.

Department of Experimental and Clinical Biomedical Sciences "Mario Serio", Section of Experimental Pathology and Oncology, University of Florence, Florence, Italy.

Objectives: Systemic sclerosis (SSc) is an autoimmune disease characterized by peripheral vasculopathy and skin and internal organ fibrosis. Accumulating evidence underlines a close association between a metabolic reprogramming of activated fibroblasts and fibrosis. This prompted us to determine the metabolism of SSc dermal fibroblasts and the effect on the vasculopathy characterizing the disease.

Methods: Seahorse XF96 Extracellular Flux Analyzer was exploited to evaluate SSc fibroblast metabolism. In vitro invasion and capillary morphogenesis assays were used to determine the angiogenic ability of endothelial cells (EC). Immunofluorescence, flow cytometer and real time PCR techniques provided evidence of the molecular mechanism behind the impaired vascularization that characterizes SSc patients.

Results: SSc fibroblasts, compared with control, showed a boosted glycolytic metabolism with increased lactic acid release and subsequent extracellular acidification, that in turn was found to impair EC invasion and organization in capillary-like networks without altering cell viability. A molecular link between extracellular acidosis and endothelial dysfunction was identified as acidic EC up-regulated MMP-12 which cleaves and inactivates uPAR, impairing angiogenesis in SSc. Moreover, the acidic environment was found to induce the loss of endothelial markers and the acquisition of mesenchymal-like features in EC, thus promoting the endothelial-to-mesenchymal transition (EndoMT) process that contributes to both capillary rarefaction and tissue fibrosis in SSc.

Conclusion: This study disclosed a liaison among the metabolic reprogramming of SSc dermal fibroblasts, extracellular acidosis and endothelial dysfunction that may contribute to the impairment and loss of peripheral capillary networks in SSc disease.
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http://dx.doi.org/10.1093/rheumatology/keab022DOI Listing
January 2021

What Role Does Trabecular Bone Score Play in Chronic Inflammatory Rheumatic Diseases?

Front Med (Lausanne) 2020 30;7:600697. Epub 2020 Nov 30.

Division of Rheumatology, Department of Experimental and Clinical Medicine, University of Firenze, Florence, Italy.

Patients suffering from rheumatic inflammatory diseases, e.g., systemic sclerosis, rheumatoid arthritis, and ankylosing spondylitis, are at risk of low bone mass. Dual-energy X-ray Absorptiometry (DXA) is the traditional radiological measurement technique for bone mineral density (BMD). The recently developed trabecular bone score (TBS) enhances the skeletal information provided by standard BMD. It re-analyzes the spatial dynamics of pixel intensity changes in lumbar spine DXA images, defining a quantitative index, characterizing trabecular bone microarchitecture. It has been demonstrated that low TBS values are associated with an increased incidence of fractures in patients with rheumatic diseases. These methods used together for bone damage evaluation can be of value to identify individuals who will potentially fracture. The main scientific literature on the clinical aspects of osteoporosis, including the use of TBS in evaluating this pathology, are herein reported aimed at shedding light on the role trabecular bone score plays in chronic inflammatory rheumatic diseases.
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http://dx.doi.org/10.3389/fmed.2020.600697DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7793927PMC
November 2020

Response to: 'Correspondence on 'Systemic sclerosis and the COVID-19 pandemic: World Scleroderma Foundation preliminary advice for patient management'' by Snarskaya and Vasileva.

Ann Rheum Dis 2021 Jan 6. Epub 2021 Jan 6.

Department of Experimental and Clinical Medicine, Division of Rheumatology, Università degli Studi di Firenze, Firenze, Italy

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http://dx.doi.org/10.1136/annrheumdis-2020-219533DOI Listing
January 2021

Pleuroparenchymal fibroelastosis in rheumatic autoimmune diseases: a systematic literature review.

Rheumatology (Oxford) 2020 Dec;59(12):3645-3656

Division of Rheumatology, Department of Experimental and Clinical Medicine, University of Florence, Florence.

Objectives: Pleuroparenchymal fibroelastosis (PPFE) is characterized by predominantly upper lobe pleural and subjacent parenchymal fibrosis; PPFE features were described in patients with rheumatic autoimmune diseases (RAID). A systematic literature review was performed to investigate the prevalence, prognosis and potential association of PPFE with previous immunosuppression in RAID.

Methods: EMBASE, Web of Science and PubMed databases were questioned from inception to 1 September 2019. Articles published in English and addressing PPFE in patients with RAID were selected.

Results: Twenty out of 794 papers were selected with a total of 76 cases of RAID-PPFE patients (20 SSc, 9 RA, 6 IIM6 primary SS, 5 overlap syndromes, 3 ANCA-associated vasculitides, 2 granulomatosis with polyangiitis, 1 microscopic polyangiitis, 1 UCTD, 1 SLE, 1 GCA and 21 patients with non-specified RAID). Dyspnoea was the most frequently reported symptom (37/48 patients, 77%). Patients frequently presented with a restrictive pattern and decline in diffusing lung capacity for carbon monoxide. During the follow-up, 7/12 patients had progression at imaging, 22/39 presented a generic clinical worsening, 19/38 had a functional deterioration and 15/43 remained stable.

Conclusion: The present systematic literature review confirms that PPFE features are present in RAID. Rheumatologists should be aware of this new radiological pattern that holds a bad prognosis.
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http://dx.doi.org/10.1093/rheumatology/keaa451DOI Listing
December 2020

Infection or Autoimmunity? The Clinical Challenge of Interstitial Lung Disease in Systemic Sclerosis During the COVID-19 Pandemic.

J Rheumatol 2021 05 1;48(5):790-792. Epub 2020 Dec 1.

Department of Allergy and Rheumatology, Nippon Medical School Graduate School of Medicine, Tokyo, Japan.

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http://dx.doi.org/10.3899/jrheum.200832DOI Listing
May 2021

The burning question: To use or not to use cyclophosphamide in systemic sclerosis.

Eur J Rheumatol 2020 Oct 1;7(Suppl 3):S237-S241. Epub 2020 Oct 1.

Division of Rheumatology, Department of Experimental and Clinical Medicine, University of Firenze, Firenze, Italy.

Fibrosis, inflammation, and vasculopathy are the main determinants of systemic sclerosis (SSc) pathogenesis. Cyclophosphamide (CYC), an alkylating agent, has been used to treat skin fibrosis and interstitial lung diseases in SSc for many years and still represents a mainstay in hematopoietic stem cell transplantation. Despite significant effect in reducing lung functional impairment and skin tightness, CYC has a significant safety burden, including infection risk and bone marrow and bladder toxicity. Moreover, it can affect fertility and also cause a predisposition for cancer development in the future, particularly in the bladder. This review summarizes the current evidences regarding the use of CYC to treat SSc, its efficacy and safety profile, and currently available or tested alternative drugs for lung and skin involvement in SSc.
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http://dx.doi.org/10.5152/eurjrheum.2020.19104DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7647679PMC
October 2020

Lung magnetic resonance imaging in systemic sclerosis: a new promising approach to evaluate pulmonary involvement and progression.

Clin Rheumatol 2021 May 7;40(5):1903-1912. Epub 2020 Nov 7.

Department of Experimental and Clinical Medicine, Department of Geriatric Medicine, Division of Rheumatology AOUC, University of Florence, Florence, Italy.

Introduction/objectives: Interstitial lung disease (ILD) is frequent and highly disabling in systemic sclerosis (SSc). Magnetic resonance imaging (MRI) is not routinely used to evaluate the lung, due to poorer spatial resolution compared to high-resolution computed tomography (HRCT). We aimed to compare lung MRI signal with HRCT and evaluate the role of MRI in predicting ILD progression.

Methods: Thirty SSc patients underwent lung MRI and HRCT. STIR and T1 mapping sequences were acquired before and after gadolinium injection. Patients were classified as normal (group 1 with normal HRCT and MRI), discordant (group 2 without ILD signs on HRCT but areas of hyperintensity on MRI), and abnormal (group 3 with ILD signs on HRCT and areas of hyperintensity on MRI). Patients were followed up for ILD progression.

Results: Mean STIR and T1 values were different between the three groups (p < 0.0001). STIR values correlated with HRCT score (R = 0.79, p < 0.0001), lung ultrasound B-lines (R = 0.73, p < 0.0001), and %DLco (R = - 0.63, p = 0.0001). Nine events were recorded during a follow-up of 25 ± 20 months. Continuous STIR values were independently associated with events (HR 1.018; CI 1.005-1.031, p = 0.005). A STIR value >90 ms discriminated patients at a higher risk of worsening pulmonary involvement (HR 8.80; CI 1.81-42.74; p < 0.007).

Conclusions: Lung MRI can detect SSc-related ILD, with good correlations with other ILD markers. STIR values, independently of HRCT appearance, may predict worsening lung involvement. Lung MRI, although very preliminary, is a promising tool that in a near future could help selecting patients for an early treatment of SSc-related ILD and a more appropriate use of HRCT. Key points • Lung MRI has the potential to differentiate inflammation-predominant versus fibrosis-predominant lesions, but it is not currently used in routine clinical practice to assess SSc-related ILD. • Lung MRI STIR and T1 values are significantly different between patients with and without SSc-related ILD. STIR values, independently of HRCT appearance, are also able to predict worsening lung involvement over time. • These preliminary data suggest that, in a near future, MRI could support the choice for an early treatment of SSc-related ILD, as well as a more appropriate use of HRCT.
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http://dx.doi.org/10.1007/s10067-020-05491-9DOI Listing
May 2021

The switch from etanercept originator to SB4: data from a real-life experience on tolerability and persistence on treatment in joint inflammatory diseases.

Ther Adv Musculoskelet Dis 2020 13;12:1759720X20964031. Epub 2020 Oct 13.

Department Experimental and Clinical Medicine, Division of Rheumatology, University of Florence, Florence, Italy.

Aims: Switching from originator to biosimilar is part of current practice in inflammatory rheumatic musculoskeletal diseases (iRMDs) such as rheumatoid arthritis (RA), psoriatic arthritis (PsA) and axial spondylarthritis (axSpA), with evidences derived from both etanercept (ETN) to SB4-switching randomized controlled trials and real-life registries. We investigated the safety and treatment persistence of ETN/SB4 in a multi-iRMD cohort derived from two rheumatology departments in our region.

Methods: Adult patients with iRMDs, treated with ETN for at least 6 months and switched to SB4 in stable clinical condition, were eligible for this retrospective evaluation. Retrospective data on adverse events, loss of efficacy and persistence on treatment were collected until latest available follow-up.

Results: A total of 220 patients (85 RA, 81 PsA, 33 axSpA, 14 juvenile idiopathic arthritis and seven other conditions; 142 females, mean age 58 ± 7 years, disease duration 12 ± 4 years, ETN duration 7 ± 4 years) were enrolled, with median follow-up of 12.1 (9.7-15.8) months. A total of 50 patients (22.7%) presented with at least one adverse event, with 36 (16.4%) disease flares and 30 (13.6%: 11 for safety and 19 loss of efficacy) SB4 withdrawals. Cumulative SB4 treatment persistence was 99.1%, 88.6% and 64.6% at 6, 12 and 18 months respectively. Back-switch to ETN was performed in 17/30 cases, the remaining cases were managed with change of biologic disease modifying or conventional synthetic anti-rheumatic drug. Age was the only significant predictor of SB4 interruption at 6 months.

Conclusion: Our real-life data confirm the safety profile of switching from ETN to SB4, with slightly higher treatment persistence rates compared with other real-life registries.
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http://dx.doi.org/10.1177/1759720X20964031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7576915PMC
October 2020

Intravenous versus oral cyclophosphamide for lung and/or skin fibrosis in systemic sclerosis: an indirect comparison from EUSTAR and randomised controlled trials.

Clin Exp Rheumatol 2020 May-Jun;38 Suppl 125(3):161-168. Epub 2020 Aug 27.

Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Firenze, Italy, and Department of Medicine, Division of Rheumatology, University of California Los Angeles, CA, USA.

Objectives: Both intravenous (IV) and oral (PO) cyclophosphamide (CYC) showed beneficial effects on skin and lung involvement in systemic sclerosis (SSc) in placebo-controlled randomised clinical trials and observational studies. Our goal was to compare the relative efficacy and safety of PO- versus IV-CYC for treating interstitial lung disease and/or skin involvement in SSc.

Methods: Patients were derived from the EUSTAR centres and the Scleroderma Lung Studies I and II. A minimum of 6 months of CYC treatment and 12 months follow-up were required. Serious (SAEs) and non-serious adverse events and efficacy data (change in FVC%, DLCO%, mRSS) were analysed at the end of CYC treatment (EoT) and at follow-up (FU). Analysis included descriptive statistics and linear regressions.

Results: Differences in ethnicity, previous DMARD exposure, previous and concomitant steroid exposure/dosage were observed in the PO (n=149) and IV (n=153) CYC groups. Adjusted and unadjusted changes in FVC%, DLCO% and mRSS were similar irrespective of mode of administration. PO patients had more leukopenia (p<0.001), haemorrhagic cystitis (p=0.011) and alopecia (p<0.001) at the EoT visit, while the IV group had more SAEs (p=0.025) and need for oxygen supplementation at FU (p=0.049).

Conclusions: In a comparison of PO- to IV-CYC for SSc, we found no differences in lung function or cutaneous sclerosis after one year. Some differences in side effects were seen. The results need to be considered as preliminary; however, because we needed to use a combination of RCT and registry data, with some differences in demographics and concomitant medications, well-controlled studies are warranted.
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September 2020

The need for a holistic approach for SSc-ILD - achievements and ambiguity in a devastating disease.

Respir Res 2020 Jul 23;21(1):197. Epub 2020 Jul 23.

Center for Interstitial and Rare Lung Diseases, Pneumology, Thoraxklinik, Heidelberg University Hospital and German Center for Lung Research, Heidelberg, Germany.

Systemic sclerosis (SSc) is a multi-organ autoimmune disease with complex interactions between immune-mediated inflammatory processes and vascular pathology leading to small vessel obliteration, promoting uncontrolled fibrosis of skin and internal organs. Interstitial lung disease (ILD) is a common but highly variable manifestation of SSc and is associated with high morbidity and mortality. Treatment approaches have focused on immunosuppressive therapies, which have shown some efficacy on lung function. Recently, a large phase 3 trial showed that treatment with nintedanib was associated with a reduction in lung function decline. None of the conducted randomized clinical trials have so far shown convincing efficacy on other outcome measures including quality of life determined by patient reported outcomes. Little evidence is available for non-pharmacological treatment and supportive care specifically for SSc-ILD patients, including pulmonary rehabilitation, supplemental oxygen, symptom relief and adequate information. Improved management of SSc-ILD patients based on a holistic approach is necessary to support patients in maintaining as much quality of life as possible throughout the disease course and to improve long-term outcomes.
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http://dx.doi.org/10.1186/s12931-020-01459-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7379834PMC
July 2020

Quantitative analysis of pulmonary vasculature in systemic sclerosis at spirometry-gated chest CT.

Ann Rheum Dis 2020 09 30;79(9):1210-1217. Epub 2020 Jun 30.

Dept Experimental and Clinical Medicine, University of Florence, Florence, Italy.

Objective: To prospectively investigate whether differences in pulmonary vasculature exist in systemic sclerosis (SSc) and how they are distributed in patients with different pulmonary function.

Methods: Seventy-four patients with SSc undergoing chest CT scan for interstitial lung disease (ILD) screening or follow-up were prospectively enrolled. A thorough clinical, laboratory and functional evaluation was performed the same day. Chest CT was spirometry gated at total lung capacity and images were analysed by two automated software programs to quantify emphysema, ILD patterns (ground-glass, reticular, honeycombing), and pulmonary vascular volume (PVV). Patients were divided in restricted (FVC% <80, DLco%<80), isolated DLco% reduction (iDLco- FVC%≥80, DLco%<80) and normals (FVC%≥80, DLco%≥80). Spearman ρ, Mann-Whitney tests and logistic regressions were used to assess for correlations, differences among groups and relationships between continuous variables.

Results: Absolute and lung volume normalised PVV (PVV/LV) correlated inversely with functional parameters and positively with all ILD patterns (ρ=0.75 with ground glass, ρ=0.68 with reticular). PVV/LV was the only predictor of DLco at multivariate analysis (p=0.007). Meanwhile, the reticular pattern prevailed in peripheral regions and lower lung thirds, PVV/LV prevailed in central regions and middle lung thirds. iDLco group had a significantly higher PVV/LV (2.2%) than normal (1.6%), but lower than restricted ones (3.8%).

Conclusions: Chest CT in SSc detects a progressive increase in PVV/LV as DLco decreases. Redistribution of perfusion to less affected lung regions rather than angiogenesis nearby fibrotic lung may explain the results. Further studies to ascertain whether the increase in PVV/LV reflects a real increase in blood volume are needed.
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http://dx.doi.org/10.1136/annrheumdis-2020-217359DOI Listing
September 2020

Monitoring the microcirculation in the diagnosis and follow-up of systemic sclerosis patients: Focus on pulmonary and peripheral vascular manifestations.

Microcirculation 2020 11 26;27(8):e12647. Epub 2020 Jul 26.

Division of Rheumatology, Department of Experimental and Clinical Medicine, University of Firenze, Firenze, Italy.

Systemic sclerosis (SSc) is a connective tissue disease, characterized by vascular damage and progressive fibrosis, affecting the skin and internal organs. The vascular changes include functional and structural abnormalities in the microcirculation, which play a central role not only in diagnosis but also in the prognosis and follow-up of systemic sclerosis patients. Nailfold videocapillaroscopy (NVC) is a safe, validated, noninvasive, inexpensive, reliable, and reproducible method that allows for the evaluation of structural changes in scleroderma microangiopathy. However, capillary blood flow/perfusion cannot be measured by NVC under standard conditions and, consequently, must rely on various laser techniques and thermography for the assessment and quantification of cutaneous blood perfusion. Other emerging technologies, such as optical Doppler tomography and spectroscopy, may be used to evaluate the skin flow. This review updates current knowledge on the use of microvascular evaluation techniques in SSc, including complications such as digital ulcers and pulmonary arterial hypertension.
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http://dx.doi.org/10.1111/micc.12647DOI Listing
November 2020

Screening for pulmonary arterial hypertension in systemic sclerosis: A systematic literature review.

Eur J Intern Med 2020 08 12;78:17-25. Epub 2020 Jun 12.

Dept. Experimental and Clinical Medicine, Division of Rheumatology, University of Florence, Viale Pieraccini 18, Florence, 50139, Italy.

Pulmonary arterial hypertension (PAH) carries a high morbidity and mortality burden in Systemic Sclerosis (SSc). Therefore, PAH screening and early detection are pivotal. A systematic literature review (SLR) to search for all screening tools and modalities for SSc-PAH was performed in reference to right heart catheterization as diagnostic gold standard. Papers from 2 previously published SLRs and derived from a systematic search on Pubmed, EMBASE, Web of Science for papers published from 03/10/2017 to 31/12/2018 were manually included. A total of 199 papers were reviewed and 32 were extracted, with a low bias risk according to QUADAS2. Echocardiography, pulmonary function tests, clinical features and serum biomarkers were the most frequently tools used for screening, with different parameters combined in a variable fashion, as single item or as part of composite algorithms. Among the composite algorithms, the DETECT score, ESC/ERS 2009 or 2015 guidelines, ASIG and ITINER-air algorithms were the most commonly used in a wide range of patients. In different cohorts, DETECT and ASIG showed higher sensitivity and negative predictive value than ESC/ERS 2009. In conclusion, the literature shows echocardiography as the leading screening tool for SSc-PAH. In particular, systolic pulmonary arterial pressure (sPAP) and tricuspid regurgitation velocity (TRV), both as single items or part of composite algorithms, including also serum biomarkers, clinical and functional items, are the most frequent parameters evaluated.
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http://dx.doi.org/10.1016/j.ejim.2020.05.042DOI Listing
August 2020

Efficacy and safety of switching from reference adalimumab to SB5 in a real-life cohort of inflammatory rheumatic joint diseases.

Clin Rheumatol 2021 Jan 8;40(1):85-91. Epub 2020 Jun 8.

Department of Experimental and Clinical Medicine, Division of Rheumatology, University of Firenze, Via delle Oblate 4, 50141, Florence, Italy.

Objective: SB5 showed comparable efficacy and safety profile in respect to adalimumab originator (ADA) in randomized clinical trials of rheumatoid arthritis (RA) and psoriasis. We aimed to describe the efficacy and safety of SB5 after switching from ADA in RA, axial spondyloarthritis (axSpA), psoriatic arthritis (PsA) and juvenile idiopathic arthritis (JIA) patients.

Method: Adult RA, PsA, axSpA, JIA patients treated with ADA for at least 6 months, switched to SB5 in stable clinical conditions, were eligible. Data on safety, activity indexes and patient-reported outcomes were collected at baseline, 3 and 6 months after switching.

Results: Eighty-two patients (19 RA, 28 PsA, 32 axSpA and 3 JIA; 45 females, mean age 54 ± 14 years, disease duration 13 ± 7 years, ADA duration 6 ± 3 years) were enrolled. RA patients showed stable conditions, while PsA patients showed an increase in both HAQ, DAS28(CRP) and DAPSA and axSpA patients an increase in VAS pain, VAS patient disease activity and ASDAS, both at 3 months. There were changes in the concomitant medications profile, with regression of activity indexes increases at 6 months. Adverse events were reported by 33.7% patients at 3 months and 16.6% patients at 6 months, mostly disease flares and infectious events. Two patients stopped SB5.

Conclusions: Despite temporary changes in the concomitant medication profile for mild disease flares, our real-life data replicate the safety profile of switching from ADA to SB5 in RA, with additional data for its applicability in PsA and axSpA patients, further supporting switching to biosimilars in treating inflammatory rheumatic conditions. Key Points • Switching from adalimumab originator to SB5 is feasible in real life rheumatic inflammatory joint diseases. • Mild disease flares can present after switching from originator adalimumab to SB5, in particular in axial spondyloarthritis and psoriatic arthritis. • Changes in concomitant medications profile allows the control of minor disease flares presenting after switching from adalimumab originator to SB5.
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http://dx.doi.org/10.1007/s10067-020-05199-wDOI Listing
January 2021

The systemic sclerosis patient in the COVID-19 era: the challenging crossroad between immunosuppression, differential diagnosis and long-term psychological distress.

Clin Rheumatol 2020 Jul 8;39(7):2043-2047. Epub 2020 Jun 8.

Department of Experimental and Clinical Medicine, Department of Geriatric Medicine, Division of Rheumatology AOUC & Scleroderma Unit, University of Florence, Florence, Italy.

COVID-19 is a world health emergency which may inevitably affect the management of a complex autoimmune disease such as systemic sclerosis (SSc). Several SSc patients are frail and, in this pandemic, need a careful protection. The COVID-19 infection might complicate the clinical scenario of interstitial lung disease (ILD) in SSc because it determines a severe pneumonia characterized by radiological features similar to SSc-ILD. The striking CT similarities between the 2 diseases make it difficult to distinguish a worsening of SSc-ILD from COVID-19-ILD superinfection. Moreover, other aspects, like isolation during lock down, may cause a significant psychological stress which will pile up on the already difficult contact with the patients for a routine check-up. Moreover, the drug shortage is a real problem in these times. For these reasons, the rheumatologist in daily clinical practice should carefully differentiate the possible COVID-19 infection in order to optimize the patient management. Therefore, the challenge in everyday life will be to achieve in due time the differential diagnosis as well as the long-term psychological impact.Key Points• SSc patients should be encouraged to continue their chronic therapy; in case of immunosuppressive therapy it must be discontinued for safety in case of COVID-19 infection.• Psychological support must be guaranteed to every SSc patients.• COVID-19 pneuminia is hard to distinguish from an interstitial lung disease due to SSc lung involvment.• Data sharing is fundamental for an optimal managment of SSc patients during COVID-19 pandemia.
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http://dx.doi.org/10.1007/s10067-020-05193-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7276334PMC
July 2020

Safety and efficacy of rituximab biosimilar (CT-P10) in systemic sclerosis: an Italian multicentre study.

Rheumatology (Oxford) 2020 Dec;59(12):3731-3736

Unit of Immunology, Rheumatology, Allergy and Rare Diseases, IRCCS San Raffaele Hospital, Vita-Salute San Raffaele University, Milan.

Objectives: Recent data have shown a significant efficacy of rituximab (RTX) in SSc. An RTX biosimilar (RTX-B) is a more affordable option. We assessed the safety and efficacy of an RTX-B (CT-P10) in SSc.

Methods: SSc patients treated with RTX-B with at least 6 months of follow-up were retrospectively identified from six Italian referral centres. SSc patients naïve to RTX-B (RTX-Bn) or already treated with RTX originator and switched to an RTX-B (RTX-Bs) were evaluated. A comprehensive assessment of disease characteristics and organ involvement at baseline and after 6 months was obtained.

Results: Thirty-three SSc patients were selected: 29 (87.9%) females, mean age 51.6 years (s.d. 14.2), mean disease duration 9.8 years (s.d. 8.1); 21 (64.5%) with dcSSc, 20 (60.1%) anti-topoisomerase I, 7 (21.2%) anti-RNA polymerase III and 6 (18.2%) anti-centromere positive. Seventeen (51.5%) were RTX-Bn and 16 were on RTX-Bs (48.5%). RTX was introduced because of skin progression in 18 patients (54.5%), interstitial lung disease (ILD) worsening in 11 (33.3%) and arthritis in 12 (36.4%). All patients were previously treated with immunosuppressants. At RTX-B introduction, 21 (63.6%) patients were on concomitant immunosuppressants: 15 (71.4%) on MMF and 6 (28.6%) on MTX. Twenty-three (69.7%) were on low-dose steroids. After 6 months, a significant reduction of the modified Rodnan skin score (mRSS), 28-joint DAS and CRP was observed (P = 0.002, 0.005 and 0.008, respectively); the mRSS significantly improved both in RTX-Bn (P < 0.024) and RTX-Bs patients (P < 0.031). No significant changes were observed for lung function tests, either in the entire cohort or in the subgroup of ILD patients. Only one RTX-Bs patient experienced transient neutropenia.

Conclusion: Our data suggest that RTX-B can represent a cheaper option in SSc patients, as it is effective in improving skin and joint involvement and in stabilizing lung function.
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http://dx.doi.org/10.1093/rheumatology/keaa136DOI Listing
December 2020

The emerging role of lung ultrasound in COVID-19 pneumonia.

Eur J Rheumatol 2020 Aug 7;7(Suppl 2):S129-S133. Epub 2020 May 7.

Division of Rheumatology, Department of Experimental and Clinical Medicine, Università degli Studi di Firenze, Firenze, Toscana, Italy.

In the last decades lung ultrasound (LUS) has become of crucial importance in the evaluation and monitoring of a widely range of pulmonary diseases. One of the major benefits which favours this examination, is that this is a non-invasive, low-cost and radiation-free imaging modality which allows repeated imaging. LUS plays an important role in a wide range of pathologies, including cardiogenic oedema, acute respiratory distress syndrome and fibrosis. Specific LUS findings have proved useful and predictive of acute respiratory distress syndrome which is of particular relevance in the suspicion and monitoring of patients with lung disease. Furthermore, several studies have confirmed the role of LUS in the screening of interstitial lung diseases in connective tissue diseases. Given these data, LUS will likely play an important role in the management of COVID-19 patients from identification of specific abnormalities corresponding to definite pneumonia phases and CT scans findings. In addition, LUS could allow reduction in the exposure of health-care workers to potential infection. Herein, we provide a summary on emerging role of lung ultrasound in COVID-19 pneumonia.
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http://dx.doi.org/10.5152/eurjrheum.2020.2063DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7431334PMC
August 2020

Effect of Dysmetabolisms and Comorbidities on the Efficacy and Safety of Biological Therapy in Chronic Inflammatory Joint Diseases.

J Clin Med 2020 May 2;9(5). Epub 2020 May 2.

Division of Rheumatology, Department of Experimental and Clinical Medicine, University of Florence, Via delle Oblate 4, 50141 Florence, Italy.

In the present study we evaluated how systemic arterial hypertension (SAH), dyslipidemia and diabetes mellitus influence the efficacy, safety and retention rate of biological disease-modifying anti-rheumatic drug (bDMARD) treatment in rheumatic musculoskeletal disorders (RMDs). The charts of RMD patients treated with the first-line bDMARD were reviewed, collecting data on safety, efficacy and comorbidities at prescription (baseline, BL), after 6 months (6M) and at last observation on bDMARD (last observation time, LoT). In 383 RMD patients, a higher rate of adverse events at 6M ( = 0.0402) and at LoT ( = 0.0462) was present in dyslipidemic patients. Patients who developed dyslipidemia or SAH during bDMARD treatment had similar results (dyslipidemia = 0.0007; SAH = 0.0319) with a longer bDMARD retention as well (dyslipidemia < 0.0001; SAH < 0.0001). SAH patients on angiotensin converting enzyme inhibitors (ACEis) or angiotensin-II receptor blockers (ARBs) continued bDMARDs for longer than non-exposed patients ( = 0.001), with higher frequency of drug interruption for long-standing remission rather than inefficacy or adverse reactions ( = 0.0258). Similarly, dyslipidemic patients on statins had a better bDMARD retention than not-exposed patients ( = 0.0420). In conclusion, SAH and dyslipidemia may be associated with higher frequency of adverse events but a better drug retention of first-line bDMARD in RMDs, suggesting an additional effect of ACEis/ARBs or statins on the inflammatory process and supporting their use in RMD bDMARD patients with SAH/dyslipidemia.
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http://dx.doi.org/10.3390/jcm9051310DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7290363PMC
May 2020
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