Advanced microvascular damage associated with occurrence of sarcopenia in systemic sclerosis patients: results from a retrospective cohort study
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Advanced microvascular damage associated with
occurrence of sarcopenia in systemic sclerosis patients:
results from a retrospective cohort study
S. Paolino1, F. Goegan1, M.A. Cimmino1, A. Casabella1, C. Pizzorni1, M. Patanè1,
C. Schenone1, V. Tomatis1, A. Sulli1, E. Gotelli1, V. Smith2, M. Cutolo1
1
Research Laboratory and Academic ABSTRACT penic SSc patients (pMicrovascular damage and sarcopenia in SSc / S. Paolino et al.
data have been reported about body All patients and the HS were aged over NVC (see below). Skin involvement
composition abnormalities, in particular 18 years. The main exclusion criteria was assessed by modified Rodnan skin
sarcopenia and micro/macroarchitectur- included a history of malignancies, the score (mRSS; range 0–51) to evalu-
al changes in bone status (8-13). overlap with other autoimmune diseases ate skin thickness. Peripheral vascular
Sarcopenia is defined as degenerative (such as rheumatoid arthritis, Sjögren’s involvement assessment included the
loss of skeletal muscle mass, quality, and syndrome, systemic lupus erythemato- history of pitting scars, ulceration or
strength generally associated with aging, sus and inflammatory myopathies) or gangrene, presence of Raynaud’s phe-
but it has been associated in SSc with a with other possible causes of sarcopenia nomenon (RP).
more aggressive disease characterised and osteoporosis (such as severe neuro- Diagnosis of limited cutaneous (lcSSC)
by the diffuse subset, longer disease logical, pulmonary, cardiac and endo- and diffuse cutaneous (dcSSC) system-
activity, higher modified Rodnan skin crine diseases). ic sclerosis was made according to the
score (mRSS), higher C-reative protein Patients treated with bisphosphonate LeRoy classification (22).
(CRP) levels and erythrocyte sedimenta- or with supplementation on calcium Pulmonary involvement was defined by
tion rate (ESR) levels, as well as positiv- and vitamin D were not excluded be- the evidence of high-resolution com-
ity of Scl70 antibodies (8-11, 14). ing the present a real-life investigation, puted tomography interstitial lung and
Among the causes that can explain sar- however concomitant treatment were reporting the pulmonary function tests
copenia in SSc are included malnutri- recorded. This study was conducted (PFT) with determination of forced
tion, chronic inflammation, older age, in accordance with the principles of vital capacity (FVC) and diffusion for
comorbidities, endocrine factors and Good Clinical Practices and the dec- carbon monoxide (DLCO/VA% and
physical inactivity due to skin fibrosis laration of Helsinski. All patients pro- DLCOAdj%) and six minute walking
and the progression of the disease (15). vided at the right time, the mandatory test (6MWT) (23).
Microvascular structure and function are signed informed consent form to enter Cardiac involvement was evaluated by
key aspects of tissue and organ health and the Scleroderma Clinic assistance. All Doppler echocardiography study (with
it has been suggested that capillary rare- the standard clinical investigations per- estimated PAPs) and ejection fraction
faction may precede sarcopenia (16, 17). formed at the Scleroderma Clinic were (FE%), and with evaluation of conduc-
In addition, considering that muscle approved by the local Ethical Board tion defect or presence of arrhythmia on
and bone are not independent of each Committee (ECB). the electrocardiogram (ECG).
other, but exert their functions together Pulmonary arterial hypertension (PAH)
as a single unit, due the anatomic posi- Assessment of SSc patients was screened as proposed by the 2015
tion and endocrine common regulation, All SSc patients underwent clinical European Society of cardiology/Euro-
it is supposed that the same risk factors evaluation, laboratory and instrumental pean Respiratory Society guidelines
responsible for body composition ab- exams within a maximum 3-month peri- and a non-invasive echographic assess-
normalities could influence both mus- od, as a part of the regular follow-up ap- ment of increased systolic pulmonary
cle and bone (12, 13). proved by SSc international guidelines, arterial pressure (sPAP) was made with
The aim of this study was to evaluate, and local clinical practice (ECB) (20). a cut-off of 38 mmHg (24-27).
body composition in a cohort of SSc Gastrointestinal (GI) involvement was
patients, focusing on sarcopenia and Clinical and instrumental evaluation defined as distal oesophageal hypomo-
microcirculation status in relation to Demographic and lifestyle data in- tility or aperistalsis documented by
different patterns of nailfold microvas- cluded: sex, age, disease duration manometric study and/or presence of
cular damage evaluated and scored by (defined since the first non-Raynaud’s upper and lower GI tract symptoms (re-
NVC and the microangiopathy evolu- phenomenon symptom that satisfy the flux, vomiting, early satiety, bloating,
tion score (MES) (18). 2013 American College of Rheumatol- diarrhoea, constipation, diagnosis of
ogy (ACR)/European League against malabsorptive syndrome or episodes of
Methods Rheumatology (EULAR) criteria), age pseudo-obstruction).
Study population at diagnosis, smoking condition, alco- Renal involvement was defined by el-
In this retrospective study a cohort of hol consumption, prior fragility frac- evated serum creatinine levels and/
43 consecutive SSc patients and 43 tures, familiarity for femoral fractures, or elevated renal artery resistive index
age- and sex-matched healthy subjects menopausal status, body weight and (RI) (28).
(HS) were recruited during routine height (with relative body mass index – Muscoloskeletal involvement was de-
clinical assessment at the Scleroderma BMI), weight loss. No one was cachet- fined as the history of myopathy, ar-
Clinic of Rheumatology Division, Uni- ic. The patients were classified as un- thralgia, arthritis and joint conctractures
versity of Genova (Italy). derweight, normal weight, overweight (29). Medsger severity score was calcu-
The diagnosis of SSc was based on the and obese according to World Health lated for each organ (30).
2013 American College of Rheumatol- Organization (WHO) criteria (21).
ogy (ACR)/European League against Laboratory tests
Rheumatology (EULAR) classification Clinical parameters Routine follow-up laboratory tests were
criteria (19). Microvascular damage was assessed by performed, such as haemoglobin (Hb),
S-66 Clinical and Experimental Rheumatology 2020Microvascular damage and sarcopenia in SSc / S. Paolino et al. creatinine (crea), erythrocyte sedimen- to assess the progression of the vascu- All scans were carried out on the same tation rate (ESR), C reactive protein lar damage (18). machine by the same operator (AC) and (CRP), creatine kinase (CK), bone alka- Considering that capillary density is the were analysed by the same dedicated line phosphatase (BAP), calcium (Ca), most reliable NVC parameter and cor- physician (SP). phosphorus (Ph), 25-hydroxyvitamin relates with disease severity, we also D (25OH)D. Antinuclear antibodies manually counted the capillary number Statistical analysis (ANAs) were assessed using indirect per linear mm, by using the NVC im- Means were compared by the Student’s immunofluorescence on Hep-2/liver ages for each SSc patient (5, 33). t-test or by one way analysis of vari- cells (EUROPLUS ANA Mosaic FA Peripheral blood flow was analysed in ance; medians were compared by the 1510-1), with a 1:80 serum dilution as a sample of sarcopenic SSc patients by Kruskall Wallis test; and frequencies by cut-off value. Extractable Nuclear An- Laser speckle contrast analysis (LAS- the chi square test. Correlations were tigen antibodies (ENA) were assessed CA) at the level of both volar and dor- calculated by the Pearson’s method. using ELISA (EUROASSAY Anti-ENA sal fingertips (expressed as perfusion A p-value
Microvascular damage and sarcopenia in SSc / S. Paolino et al. Table I. Demographic, past medical history and clinical characteristics of patients with SSc, according to the NVC patterns (“Early”, “Active” and “Late”). SSc (n=43) SSc with “Early” SSc with “Active” SSc with “Late” p-value NVC pattern NVC pattern NVC pattern (n=11) (n=16) (n=16) Age, media ± SD, years 64.1 ± 11.2 68.6 ± 8.3 64.4 ± 11.2 60.8 ± 12.2 NS Male, n (%) 7 (16.3) 1 (9) 4 (25) 2 (12.5) NS Female, n (%) 36 ( 83.7) 10 (91) 8 (16) 14 (87.5) Disease duration, media ± SD, years 10.23 ± 6.0 9.6 ± 4.9 9 ± 5.4 11.8 ± 7.6 NS Weight, median (IQR), kg 62 (45-105) 71.1 ± 15.8 64.7 ± 12.5 58.6 ± 10.4
Microvascular damage and sarcopenia in SSc / S. Paolino et al.
Table II. Comparison of body composition parameters between SSc patients and healthy subjects according to the microvascular involve-
ment (NVC patterns) and body area.
SSc patients Pt with “Early” Pt with “Active” Pt with “Late” Healthy p-value
(n=43) NVC pattern NVC pattern NVC pattern subjects
(n=11) (n=16) (n=16) (n=43)
Age, media ± SD years 64.1 ± 11.2 68.6 ± 8.3 64.4 ± 11.2 60.8 ± 12.2 62.2 ± 11.7 0.29
Prevalence of sarcopenia, n (%) 10 (23.26) 1 (9.1) 2 (12.5) 7 (43.75) 2 (4.65) 0.002
RSMI,** median (IQR), kg/m2 5.9 (5.4 -8.5) 6.7(5.5-8.5) 5.8(4.5-7.6) 5.3 (3.8-8.8) 6.2 (3.8-6.6) 0.003
Upper limbs
TM, media ± SD, gr 7055 ± 1924 8164 ± 1832 7401 ± 1942 5947 ± 1422 7020 ± 1397 0.004
LM, median (IQR), gr 3802 (1525-7019) 4250 (3267-6518) 4150 (2232-7019) 3133 (1525-5150) 3902 (1971-7200) 0.002
FM, media ± SD, gr 2736 ± 1120 3444 ± 1138 2581 ± 1167 2405 ± 882.2 2990 ± 871.4 0.03
BMC, median (IQR), gr 259 (167-493) 306 (198-442) 284 (198-493) 228 (169-394) 257 (167-391) NS
Lower limbs
TM, media ± SD, gr 21602 ± 4463 23515 ± 4230 21555 ± 4016 20335 ± 4830 21413 ± 3084 NS
LM, median (IQR), gr 12770 (7341-19747) 13381 (10605-19747) 13092 (9315- 18988) 11297 (7341-18895) 12610 (9392-19050) NS
FM, media ± SD, gr 7784 ± 2312 8674 ± 2414 7108 ± 2008 7835 ± 2445) 8739 ± 1927 NS
BMC, median (IQR), gr 701 (495-1257) 786 (522-972) 721 (495-1257) 635 (507-1015) 697 (505-1114) NS
Trunk
TM, media ± SD, gr 30800 (21613-55127) 31400 (2700-55127) 31150 (22381-52600) 27350 (21613-45037) 31509 (20641-48981) NS
LM, median (IQR), gr 18127 (14358-28439) 20350 (16205-24760) 18302 (14358- 28439) 17119 (14462-25568) 18300 (12682- 26185) NS
FM, media ± SD, gr 12297 ± 5345 16283 ± 6645 11725 ± 5156 10814 ± 4438 14343 ± 4802 NS
BMC, median (IQR), gr 557 (357-987) 621 (468-922) 581 (377-987) 536 (357-788) 565 (290-953) NS
RSMI: relative skeletal muscle index; TM: total mass; LM: lean mass; FT: fat mass; BMC: bone mineral content.
**The values included male and female SSc patients with relative altered values of RSMI accorning to their gender.
ratory tests, neither differences between compared to controls. (data not shown). tive” NVC patterns (p=0.003) (Table II).
the three subgroups according to the dif- In the trunk of SSc patients, FM was The values included male and female
ferent NVC patterns (Suppl. Table S2). found significantly lower than in con- SSc patients with relative altered values
No significant difference was detected trol group (p=0.036), but no statistical of RSMI according to their gender.
among treatment in the present co- differences was noted regarding LM In addition, SSc patients who showed
hort of patients. It was only observed p=0.99 and BMC p=0.83. Interesting- the most advanced NVC patterns, had a
that patients in “Late” NVC pattern ly, even if the prevalence of sarcope- lower LM (p=0.04) and FM (p=0.017)
subgroup versus earliest NVC pat- nia was higher in SSc patients than in for the whole body; of note, by analysing
terns, received mycophenolate mofetil healthy subjects, no differences were the body composition of each individual
(MMF) and endothelin receptor antag- reported in RSMI median values in two anatomical region it was found that pa-
onist (ERA) in a significant higher % groups (p=0.97) (data not shown). tients with “Late” NVC pattern showed
(p=0.038 and p=0.002, respectively), Concerning the analysis of bone sta- lower LM (p=0.002), FM (p=0.029)
possibly due to their higher disease se- tus, the prevalence of femoral OP and FM (p=0.004) at the upper limbs,
verity. (Suppl. Table S1). was found higher only in SSc patients but only reduction of FM on the trunk
with BMD values and T-score index at (p=0.016) and lower limbs (p=0.052).
Occurrence of sarcopenia femoral neck lower than in the healthy Concerning the bone status, there was
and altered body composition in control group (p= 0.038 and p=0.047) a more significant incidence of femo-
SSc patients vs. healthy subjects (data not shown). ral OP (p = 0.016) in SSc patients with
Significantly higher prevalence of sar- The analysis of bone mass in different “Late” NVC pattern by a decrease of
copenia was found in SSc patients ver- body areas showed no significant dif- T-score (p=0.007) and BMD of femoral
sus age-matched subjects: 23.26% ver- ferences in the median BMD values at neck (p=0.027) versus the other NVC
sus 4.65%, p=0.03, respectively. the level of head (p=0.06), upper limbs patterns.
Regarding the analysis of body compo- (p=0.22), trunk (p=0.79), ribs (p=0.69), In addition, the incidence of vertebral OP
sition no significant differences were and lower limbs (p=0.44). in patients with “Late” NVC pattern ap-
observed in the distribution of fat mass pear to be greater than in the “Early” and
(FM p=0.40), lean mass (LM p=0.97) Comparison of body composition “Active” (p=0.018), whereas no signifi-
and bone mineral content (BMC in SSc patients according to the cant differences were observed on L1-L4
p=0.33) both in the evaluation of the NVC pattern vs. healthy subjects T-score and L1-L4 BMD (Table III).
whole-body and in the analysis of upper Interestingly, SSc patients presenting
limbs (FM p=0.08, LM p=0.47, BMC with the “Late” NVC pattern showed Features of sarcopenic
p=0.51), lower limbs (FM p=0.04, LM higher prevalence of sarcopenia, com- vs. non-sarcopenic SSc patients
p=0.69, BMC p=0.82) in SSc patients pared to patients with “Early” or “Ac- As reported in details in Table III, sar-
Clinical and Experimental Rheumatology 2020 S-69Microvascular damage and sarcopenia in SSc / S. Paolino et al. copenic SSc patients showed a signifi- Table III: Comparison of capillary number, MES and body composition between SSc cant loss of capillaries (p
Microvascular damage and sarcopenia in SSc / S. Paolino et al.
penic SSc patients, was the significant- a previous report from Corrado et al. damage, identified by the “Late” NVC
ly higher incidence of digital ulcers in (46). On the contrary, Marighela et al. pattern and the MES/LASCA values,
upper limbs, in concomitance with the showed a lower lean and fat mass in recommend that microvascular param-
“Late” NVC pattern (81%, p=0.0002). SSc patients versus the control group, eters should be considered as biomark-
On the other hand, fibrosis is a prevalent and results were confirmed also by ers of the disease progression and se-
histopathologic feature in muscle biop- Souza et al. (10, 47). verity in SSc, as well as in connective
sies of SSc patients with muscle disease The sarcopenic SSc patients showed in tissue diseases (50-52).
together with microangiopathy (16, 42). the present study a lower BMD more Finally, all parameters related to body
As detected, fibrosing myopathy, or fi- evident in presence of advanced mis- composition were found within sarco-
brosis predominance on muscle histo- crovascular damage. Few studies have penic SSc patients significantly more
pathology, is associated with a unique evaluated BMD in SSc patients and a altered in upper limbs versus lower
clinical phenotype in SSc patients and previous study reported that low weight limbs and trunk, further suggesting a
participate in sarcopenia (16). and reduced lean mass were associated strong link between severity of local
Interestingly, and for the first time, with a decrease in lumbar and femoral microvascular failure and associated
the present study revealed differences BMD in SSc women probably due to muscle sufference at least in SSc.
in body composition at different body the chronic tissue inflammation and fi-
areas according to the different NVC brosis, but also to the progressive and Acknowledgements
patterns. generalised microvascular damage (46). S. Paolino, A. Sulli, C. Pizzorni, V.
Particularly, patients with “Late” NVC Recently, the literature data suggest a Smith and M. Cutolo are members of
pattern showed a significant reduction new interpretation of the role of at least the EULAR Study Group on Micro-
of fat mass in upper and lower limbs some SSc-specific antibodies (ENAs) circulation in Rheumatic Diseases.
and trunk, but a significant reduction of to explain different organ involvement
lean mass only in the upper limbs. and complication of the disease, having References
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