Timing of onset affects arthritis presentation pattern in antisynthetase syndrome - IRIS Uniroma1
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Timing of onset affects arthritis presentation pattern
in antisynthetase syndrome
M.A. González-Gay1, C. Montecucco2, A. Selva-O’Callaghan3, E. Trallero-Araguas3,
O. Molberg4, H. Andersson4, J. Rojas-Serrano5, D.I. Perez-Roman5, J. Bauhammer6, C. Fiehn6,
R. Neri7, S. Barsotti7, H.M. Lorenz8, A. Doria9, A. Ghirardello9, F. Iannone10, M. Giannini10,
F. Franceschini11, I. Cavazzana11, K. Triantafyllias12, M. Benucci13, M. Infantino14, M. Manfredi14,
F. Conti15, A. Schwarting16, G. Sebastiani17, A. Iuliano17, G. Emmi18, E. Silvestri18, M. Govoni19,
C.A. Scirè19, F. Furini19, F.J. Lopez-Longo20, J. Martínez-Barrio20, M. Sebastiani21, A. Manfredi21,
J. Bachiller-Corral22, W.A. Sifuentes Giraldo22, M. Cimmino23, C. Cosso23, A. Belotti Masserini24,
G. Cagnotto25, V. Codullo2, M. Romano2, G. Paolazzi26, R. Pellerito27, L.A. Saketkoo28,
N. Ortego-Centeno29, L. Quartuccio30, A. Batticciotto31, E. Bartoloni32, R. Gerli32, C. Specker33,
E. Bravi34, C. Selmi35, S. Parisi36, F. Salaffi37, F. Meloni38, E. Marchioni39, A. Pesci40, G. Dei40,
M. Confalonieri41, P. Tomietto42, L. Nuno43, F. Bonella44, N. Pipitone45, A. Mera-Valera46,
N. Perez-Gomez46, S. Gerzeli47, R. Lopez-Mejias1, C.J. Matos-Costa48, J.A. Pereira da Silva48,
J. Cifrian49, C. Alpini50, I. Olivieri51, M.Á. Blázquez Cañamero52, A.B. Rodriguez Cambrón52,
S. Castañeda53, L. Cavagna2, on behalf of AENEAS (American and European NEtwork of
Antisynthetase Syndrome) collaborative group.
Abstract
Objective
To evaluate if the timing of appearance with respect to disease onset may influence the arthritis presentation pattern in
antisynthetase syndrome (ASSD).
Methods
The patients were selected from a retrospective large international cohort of ASSD patients regularly followed-up in
centres referring to AENEAS collaborative group. Patients were eligible if they had an antisynthetase antibody testing
positive in at least two determinations along with arthritis occurring either at ASSD onset (Group 1) or during the
course of the disease (Group 2).
Results
445 (70%; 334 females, 110 males, 1 transsexual) out of the 636 ASSD we collected had arthritis, in the majority of cases
(367, 83%) from disease onset (Group 1). Patients belonging to Group 1 with respect to Group 2 had an arthritis more
commonly polyarticular and symmetrical (p=0.015), IgM-Rheumatoid factor positive (p=0.035), erosions at hands and
feet plain x-rays (p=0.036) and more commonly satisfying the 1987 revised classification criteria for rheumatoid arthritis
(RA) (p=0.004). Features such as Raynaud’s phenomenon, mechanic’s hands and fever (e.g. accompanying findings)
were more frequently reported in Group 2 (p=0.005).
Conclusion
In ASSD, the timing of appearance with respect to disease onset influences arthritis characteristics. In particular,
RA features are more common when arthritis occurs from ASSD onset, suggesting an overlap between RA and ASSD in
these patients. When arthritis appears during the follow-up, it is very close to a connective tissue disease-related arthritis.
Also, the different prevalence of accompanying features between these two groups is in line with this possibility.
Key words
antisynthetase syndrome, arthritis pattern, timing of onset
Clinical and Experimental Rheumatology 2018; 36: 44-49.Arthritis subsets in antisynthetase syndrome / M.A. González-Gay et al.
Miguel A. González-Gay, Carlomaurizio Introduction defined instrumentally by a restrictive
Montecucco, Albert Selva-O’Callaghan, Arthritis is a well-established feature pulmonary function test (PFT) pattern
Ernesto Trallero-Araguas, Ovynd Molberg, of antisynthetase syndrome (ASSD), (FVC ≤80%, FEV1/FVC ≥70%, de-
Helena Andersson, Jorge Rojas-Serrano,
reported in up to 80% of cases and creased or normal FEV1, and/orArthritis subsets in antisynthetase syndrome / M.A. González-Gay et al.
Table I. Main demographics and clinical characteristics of patients according to cluster and Anti-Jo-1 antibodies were positive
timing of arthritis appearance with respect to other classic triad findings. If not otherwise in 366 (82%) patients, non-anti Jo-1
stated, percentage are calculated according to the number of patients with available infor- antibodies in 79 (18%). Within non-
mation within the group.
anti-Jo-1 positive patients, 33 (42%)
Group 1: Group 2: p-value were anti-PL-7 positive, 29 (37%) anti-
arthritis at arthritis after PL-12, 9 (11%) anti-EJ and 4 (5%) anti-
disease onset disease onset OJ. Also, 4 patients (5%) had a double
(ex novo arthritis)
positivity (1 OJ/EJ and 3 PL-7/PL-12).
Number of patients (% of total) 367 (83) 78 (17) – ̭ Anti-Jo-1 and non-anti-Jo-1 positive pa-
Median age in years at disease onset (IQR) 51 (41-60) 53 (39-61) 0.940 tients were equally distributed between
Median diagnostic delay in months (IQR) 6 (2-27) 9 (3-18) 0.107** the two clinical groups (p=0.489). In
Median follow-up in months (IQR) 74 (32-143) 95 (48-178) 0.038** particular, Group 1 included 303 (83%)
Females (%) 272 (74) 62 (79) 0.337 anti-Jo-1 and 63 (17%) non-anti-Jo-1
Males (%) 94 (26)* 16 (21) positive patients, Group 2, 62 (79%)
Anti Jo-1 positive (%) 304 (83) 62 (79) 0.483
anti-Jo-1 and 16 (21%) non-anti-Jo-1
Non-anti JO-1 positive (%) 63 (17) 16 (21)
Anti-Ro antibodies positive (%) 200 (56) 41 (53) 0.544
positive patients.
Anti-RO antibodies negative (%) 155 (44) 37 (47) Clinical, laboratory and radiologic find-
Symmetrical polyarthritis (%) 258 (71) 43 (57) 0.015 ings of all patients are shown in table 1.
Oligoarticular/asymmetrical arthritis (%) 106 (29) 33 (43) Whereas the 1987 revised ACR classi-
IgM-RF positive (%) 94 (27) 11 (15 0.035 fication criteria for RA (10) were tested
IgM-RF) negative (%) 257 (73) 62 (85) in the majority of patients, we could
ACPA positive (%) 33 (11) 5 (8) 0.575
test only 78 (18%) for the new 2010
ACPA negative (%) 274 (89) 55 (92)
Patients with x-rays joint erosions (%) 51 (16) 4 (6) 0.036
ACR/EULAR classification criteria for
Patients without x-rays joint erosions (%) 273 (84) 63 (94) RA (11), reason that lead us to not in-
Patients satisfying the 1987 revised ACR 241 (69) 37 (51) 0.004 clude the obtained result in the study.
classification criteria for RA (%) Even if this study was not aimed at
Patients NOT satisfying the 1987 revised 109 (31) 35 (49) comparing the inter-centre variability,
ACR classification criteria for RA (%) arthritis characteristics were equally
Fever (%)§ 91 (26) 25 (33) 0.211 distributed between the different cen-
No fever (%)§ 261 (74) 51 (67)
tres involved and between different re-
Raynaud’s phenomenon (%)§ 95 (27) 33 (43) 0.007
No Raynaud’s phenomenon (%)§ 254 (73) 44 (57)
ferral areas (data not shown). Regard-
Mechanic’s hands (%)§ 91 (26) 27 (36) 0.082 ing treatments, the majority of group 2
No Mechanic’s hands (%)§ 258 (74) 48 (64) patients were on immunosuppressants
Accompanying features (%)§ 183 (56) 56 (74) 0.005 when arthritis appeared. All 78 patients
No accompanying findings (%)§ 144 (44) 20 (26) (100%) were on low dose prednisone
(< 5mg/day), 35 (45%) on azathioprine,
RF: Rheumatoid factor; ACPA: anticyclic citrulinated peptide antibodies; ILD: interstitial lung disease.
*plus one transexual. §number of accompanying findings ever presented, concomitantly or before arthri- 12 (15%) on mycophenolate mofetil, 8
tis occurrence. Median time from disease to arthritis onset in group 2 (interquartile range): 20 months (10%) on cyclosporine, 4 (5%) on cyclo-
(10-46 months). ̭ phosphamide and 1 (1%) on hydroxy-
Statistical analysis: Independent sample t-test, **Welch-test. Other: Chi square test.
chloroquine.
Figure 1 shows the cluster of triad find-
tive after two testing confirmations tribution. Comparison between groups ings presented at disease onset in the 2
along with at least one positivity ob- was firstly tested by chi-square test, t- Groups.
tained in the leading reference/tertiary test or Mann-Whitney test, based on the
centre. In leading centres, besides variable type and distribution. Analyses Discussion
antisynthetase antibodies, other addi- were performed using STATA software To date, this is the largest study ever to
tional anti-extractable nuclear antigen package (2009, release 11; StataCorp, address arthritis assessment in ASSD,
specificities and IgM-RF and ACPA TX, USA). and the first to include a large number
were tested by well-validated methods of non-anti-Jo-1 positive patients. Our
(Appendix). Results findings indicate that arthritis in ASSD
In our cohort of 636 ASSD, 445 patients occurs mainly at disease onset and to a
Statistical analysis (70%; 334 females, 110 males, 1 trans- lesser extent during the follow-up. Fur-
Descriptive data were reported or con- sexual) had arthritis. In these patients, thermore, we found that arthritis char-
sidered as absolute and relative fre- the median (IQR) age at disease onset acteristics are heterogeneous within the
quencies, mean and standard deviation, was 51 (41–60) years, the diagnostic de- syndrome and influenced by its timing
median and interquartile range (IQR) lay was 7 (2–23) months and the dura- of onset. In particular, RA-like clinical,
based on the type of the variable dis- tion of follow-up 79 (36–149) months. laboratory and radiologic features are
46 Clinical and Experimental Rheumatology 2018Arthritis subsets in antisynthetase syndrome / M.A. González-Gay et al.
ported in the first studies, to that of sym-
metrical polyarthritis described in the
last ones. Furthermore, we showed that
the overlapping aspects between ASSD
and RA are common in anti-Jo-1 posi-
tive patients presenting with arthritis
from disease onset in general and with
an isolated arthritis in particular (4, 5).
At that time, due to the limited number of
patients developing an ex-novo arthritis
during the follow-up, we left a relevant
question unanswered: is arthritis pheno-
type different in patients in whom joint
involvement appears ex-novo during the
Fig. 1. Cluster of triad findings in different groups. Inner circles: Group 1, triad findings occurring follow-up? With the increased number
concomitantly to arthritis at disease onset. Group 2, triad findings presented before the appearance of of centres participating in the AENEAS
arthritis. MYO: myositis; ILD: interstitial lung disease. collaborative group, in the present study
we have reached a number of patients
Appendix that may be large enough to answer this
question. Furthermore, we enlarged the
List of kits/methodologies used
spectrum of analysis by including also a
Anti synthetase antibodies relevant number of patients with other
• INNO-LIA, Immunogenetics Ghent, Belgium antisyntethase antibodies specificities.
• EliA Jo-1, Phadia, Freiburg, Germany First of all, in this study we confirmed
• ELiA CTD screen, Phadia, Freiburg, Germany
• Zenit RA Jo-1, Menarini Diagnostic, Firenze, Italy
that it is often difficult to perform a dif-
• QUANTA Flash Jo-1, Inova Diagnostics, Werfen Groupe San Diego, USA ferential diagnosis between ASSD and
• ENA-abs, Euroimmun, Lübeck, Germany RA at disease onset because of several
• Counterimmunoelectrophoresis, Bunn CC, Gharavi AE, Hughes GRV. J Clin Lab Immunol clinical, laboratory and radiology simi-
1982; 8: 13-17.
• Dot Blot Miositis/Esclero Palex Medical, Barcelona, Spain larities. However, the most interesting
• ELISA ORG 514, ORGENTEC, Mainz, Germany results we disclosed was that ex-novo
• Myositis Profile Euroline Blot test kit, Euroimmun, Lübeck, Germany arthritis is more frequently oligoarticu-
• DotDiver ANAcyto 10, GA Generic Assays GmbH, Berlin, Germany lar and asymmetrical with respect to that
• MYOSITIS PROFILE - 12 Ag, AL AD-MYOS12D ALIFAX Srl, Padua, Italy BD
appearing at disease onset. Conversely,
Anticyclic citrullinated peptide antibodies IgM RF positivity and the radiographic
• Aeskulisa 3166 CCP, Aesku.system GmbH & Co, Wendelsheim, Germany evidence of joint erosions were more
• Anti-CCP EDIA, Eurodiagnostica, Malmoe, Sweden
commonly observed in Group 1 with
• Quanta Flash (CIA) CCP3, INOVA Diagnostics a Werfen Company, San Diego
• Home-made ELISA, Anzilotti C et al. Antibodies to viral citrullinated peptide in respect to Group 2. Furthermore, the
rheumatoid arthritis. J Rheumatol 2006; 33: 647-51. 1987 ACR revised classification criteria
• Zenit RA CCP, Menarini Diagnostic, Firenze, Italy for RA were less frequently satisfied in
• EliA CCP, Phadia, Freiburg, Germany (Torino)
• Anti-CCP Ab’s, Roche Diagnostics, Mannheim, Germany
patients from Group 2 when compared
• anti-CCP2 ELISA, Immunoscan RA, Euro-Diagnostica, Malmoe, Sweden to Group 1. Unfortunately, we were able
to test only a limited number of patients
Rheumatoid factor IgM antibodies with the 2010 new classification criteria
• Nephelometry
• Reuma Latex test, Sclavo diagnostics International, Sovicille, Italy
for RA, without the possibility of draw-
• Elia RF IgM, Phadia, Freiburg, Germany ing conclusions. From the serological
• RF Ab’s: Roche Diagnostics, Mannheim, Germany point of view, anti-Ro antibodies were
• RF IgM, (K6078) Vista 1500, Siemens Healthcare Diagnostics equally distributed among groups, thus
without other implications to that of po-
more likely observed in patients pre- tis at disease onset) when compared to tential ASSD markers, at least for arthri-
senting arthritis from disease onset and Group 2 (arthritis after disease onset tis aspects.
to a lesser extent in those presenting -ex-novo arthritis). If we consider the treatments ongoing
with an ex-novo arthritis during the fol- We have recently published a study fo- when arthritis appeared, in the majority
low-up. Conversely, we first observed cused on the evolution of the concept of of cases, the drugs used are not consid-
that ASSD accompanying findings (e.g. articular involvement in ASSD (5). In ered effective from the articular point
fever, Raynaud’s phenomenon and me- this paper, we have shown how this con- of view along the entire spectrum of
chanic’s hands) are significantly less cept steadily changed over time, from rheumatic conditions. We may suppose
frequent in the clinical Group 1 (arthri- the simple term of polyarthralgia re- that the influence of these treatments
Clinical and Experimental Rheumatology 2018 47Arthritis subsets in antisynthetase syndrome / M.A. González-Gay et al.
11
on arthritis presentation pattern (and on checked only few patients for the newly Rheumatology Unit, University
joint erosions) was minimal. available RA classification criteria (11) and AO Spedali Civili, Brescia, Italy;
12
Our results indicate that arthritis in and not for the new 2010 ACR/EULAR ACURA Rheumatology Center,
Bad Kreuznach, Germany;
ASSD is a heterogeneous condition, classification criteria for RA. This bias 13
Rheumatology Unit, Azienda Sanitaria
with different characteristics that are could be overcome in the incoming pro- di Firenze, S. Giovanni di Dio Hospital,
linked to the timing of the appearance of spective part of the AENEAS project. Florence, Italy;
arthritis. In particular, patients present- Finally, we cannot exclude that some of 14
Immunology and Allergy Laboratory,
ing ex-novo arthritis during the follow- the patients included in Group 1, who S. Giovanni di Dio Hospital, Florence,
up less frequently have laboratory, clini- had an isolated arthritis at disease onset, Italy;
15
Dept. of Internal Medicine and
cal and radiology features typical of RA, could have presented an asymptomatic
Medical Specialties-Rheumatology,
suggesting that different mechanisms ILD or myositis. We think that this limi- Sapienza University of Rome, Italy;
may drive arthritis occurrence in the dif- tation could be resolved only in the case 16
Dept. of Internal Medicine,
ferent phases of ASSD. Another factor of a very early identification of antisyn- Rheumatology and Clinical Immunology,
supporting this hypothesis is that the tethetase antibodies and of a very early University Hospital Johannes-Gutenberg,
typical accompanying findings of ASSD diagnosis of ASSD. However, we think Mainz, Germany;
17
U.O.C. Reumatologia, Ospedale
were rare in Group 1 and more common that thanks to the results obtained by
San Camillo-Forlanini, Roma, Italy;
in Group 2. As recently suggested by the the AENEAS collaborative group (4, 5) 18
Dept. of Experimental and Clinical
members of the French “Club Rhuma- and by the French “Club Rhumatisme Medicine, University of Florence, Italy;
tisme and inflammation” (8), we think et inflammation” (2, 8, 21) the sensibil- 19
UOC Reumatologia, Azienda
that an overlap between RA and ASSD ity of clinicians in the early diagnosis of Ospedaliero Universitaria S. Anna,
may occur in the first phases of the dis- ASSD in arthritis patients could stead- University of Ferrara, Italy;
20
ease, whilst a “true” ASSD-related ar- ily increase in the next years. Servicio de Reumatología,
Hospital General Universitario
thritis during the follow-up. In conclusion, we have shown that Gregorio Marañón, Madrid, Spain;
Another interesting observation de- heterogeneity is a typical hallmark 21
Rheumatology Unit, University of
rived from the evaluation of Group 1 of arthritis in ASSD, that differences Modena and Reggio Emilia, Azienda
was that the association between ar- found in our series may indicate differ- Ospedaliero-Universitaria Policlinico
thritis and ILD was observed in 157 ent phenotypes of the disease and that di Modena, Italy;
22
patients (44% of the group), 56 of them arthritis pathogenesis in ASSD is com- Dept. of Rheumatology, University
Hospital Ramón y Cajal, Madrid, Spain;
(15% of the group) without concomi- plex and potentially different in vari- 23
Research Laboratory and Academic
tant myositis. Since ILD frequently ous disease phases. Division of Clinical Rheumatology,
occurs at RA onset (12), arthritis in Dept. of Internal Medicine, University
ASSD is frequently “RA-like” (4, 5, Authors’ affiliations of Genoa, Italy;
1
8), and ILD is a common manifestation Division of Rheumatology, Hospital 24
ASST Bergamo Ovest, UOC Medicina,
of ASSD (2, 3, 13-18), we think that Universitario Marqués de Valdecilla, Ospedale di Treviglio, Italy;
IDIVAL, University of Cantabria, 25
Lund University, Skane University
some patients diagnosed with RA with Santander, Spain; Hospital, Dept. of Clinical Sciences
lung involvement could be in fact not 2
Division of Rheumatology, University Lund, Rheumatology, Lund, Sweden;
diagnosed ASSD. and IRCCS Policlinico S. Matteo 26
Rheumatology Unit, Santa Chiara
The study has some limits. In particu- Foundation, Pavia, Italy; Hospital, Trento, Italy;
3
lar, the main criticism is related to its Dept. of Internal Medicine, Vall d’Hebron 27
Division of Rheumatology,
retrospective design. It is well known General Hospital, Barcelona, Spain; Mauriziano Hospital, Turin, Italy;
4
Dept. of Rheumatology, Oslo University 28
Tulane University Lung Center Tulane/
that these studies are intrinsically as-
Hospital (OUH), Norway; UMC Scleroderma and Sarcoidosis
sociated with an increased risk of in- 5
Interstitial Lung Disease and Patient Care and Research Center
completeness (19, 20). In fact, arthri- Rheumatology Units, Instituto Nacional New Orleans, LA, USA;
tis serological, radiology and clinical de Enfermedades Respiratorias, Ismael 29
Systemic Autoimmune Diseases Unit,
data were available in the majority of Cosío Villegas, México City, México; Hospital Clínico San Cecilio, Granada,
6
cases but not in all cases. Another po- ACURA Centre for Rheumatic Diseases, Spain;
30
tential limitation is that anti-synthetase Baden-Baden, Germany; Clinic of Rheumatology, Dept. of
7
Division of Rheumatology, Medical and Biological Sciences
antibodies were assessed using dif- Dept. of Clinical and Experimental (DSMB), Santa Maria della
ferent commercially available kits in Medicine, University of Pisa, Italy; Misericordia Hospital, Udine, Italy;
different centres. Nevertheless, when 8
Dept. of Internal Medicine V, 31
Rheumatology Unit, Luigi Sacco
considering these limitations, we have Division of Rheumatology, University University Hospital, Milan, Italy;
32
to take into account that so far no pro- of Heidelberg, Germany; Rheumatology Unit, Dept. of Medicine,
9
spective studies that address ASSD are Division of Rheumatology, University of Perugia, Italy;
33
Dept. of Medicine (DIMED), Dept. of Rheumatology and Clinical
available, and that other multicentre
University of Padova, Italy; Immunology, St. Josef Krankenhaus,
studies previously performed had the 10
Interdisciplinary Dept. of Medicine University Clinic, Essen, Germany;
same problems that we have discussed (DIM), Rheumatology Unit, 34
Rheumatology Unit, Ospedale Guglielmo
(2, 9, 21, 22). Another bias is that we University of Bari, Italy; da Saliceto, Piacenza, Italy;
48 Clinical and Experimental Rheumatology 2018Arthritis subsets in antisynthetase syndrome / M.A. González-Gay et al.
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