Transcultural adaptation of the "EULAR Sjögren's Syndrome Disease Activity Index (ESSDAI)" into Brazilian Portuguese

Abstracts

INTRODUÇÃO: O EULAR Sjögren's Syndrome Disease Activity Index (ESSDAI) é um índice de atividade sistêmica da síndrome de Sjögren primária (SSP). OBJETIVO: Realizar a adaptação transcultural do ESSDAI para a língua portuguesa. MÉTODO: Estudo transversal com 62 pacientes com SSP de acordo com consenso europeu-americano de 2002. Foram realizadas seis etapas: equivalência conceitual, de item, semântica, operacional, funcional e de mensuração (reprodutibilidade interobservador e a validade de constructo). Para a validade, o ESSDAI foi comparado com a avaliação global do médico (PhGA), o Sjögren's Syndrome Disease Activity Index (SSDAI) e o Sjögren's Systemic Clinical Activity Index (SCAI). Os pacientes foram classificados por um médico especialista conforme a atividade da doença em dois grupos, "ativo" e "inativo", e conforme a intenção de tratar nos grupos "aumento de terapia" e "sem aumento de terapia". O ESSDAI foi testado nesses grupos. Utilizou-se os testes estatísticos: coeficiente de correlação intraclasse (CCI) e método de Bland Altman para a reprodutibilidade; e coeficiente de Spearman (r s) e teste de Mann-Whitney para a validade (P < 0,05 e IC 95%). RESULTADOS: A média do ESSDAI foi de 4,95 ± 6,73. A reprodutibilidade obteve um forte CCI de 0,89 e boa concordância. Na comparação com outros índices, apresentou forte coeficiente de Spearman com o PhGA (r s = 0,83; P < 0,000), moderado com o SSDAI (r s = 0,658 ; P < 0,000) e fraco com o SCAI (r s = 0,411; P = 0,001). O grupo "ativo" e o grupo "com aumento de terapia" obtiveram maiores valores de ESSDAI (P = 0,000). CONCLUSÃO: a versão em português do ESSDAI mostrou ser adaptável, reprodutível e válida para a língua portuguesa.

Síndrome de Sjögren; Escalas; Estudos de validação; ESSDAI

ORIGINAL ARTICLE

Transcultural adaptation of the "EULAR Sjögren's Syndrome Disease Activity Index (ESSDAI)" into Brazilian Portuguese

Érica Vieira Serrano^I,II,III; Valéria Valim^IV,V,VI,*; Samira Tatiyama Miyamoto^IV,VII; Raquel Altoé Giovelli^II,VIII; Maurício Aquino Paganotti^IX; Nágela Valadão Cadê^X,XI,XII

^IPost-graduation Program in Collective Health, Universidade Federal do Espírito Santo, Vitória, ES, Brazil

^IIDepartment of Internal Medicine, Escola Superior de Ciências, Santa Casa de Misericórdia de Vitória, Vitória, ES, Brazil

^IIIHospital Universitário Cassiano Antônio de Moraes, Vitória, ES, Brazil

^IVEscola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, SP, Brazil

^VDepartment of Internal Medicine, Universidade Federal do Espírito Santo, Vitória, ES, Brazil

^VIRheumatology Outpatient Clinic, Hospital Universitário Cassiano Antônio de Moraes, Vitória, ES, Brazil

^VIIDiscipline of Physical Therapy, Universidade Federal do Espírito Santo, Vitória, ES, Brazil

^VIIIMaster's Degree Program in Medicine, Universidade Federal do Espírito Santo, Vitória, ES, Brazil

^IXPost-graduation Program in Pharmaceutical Sciences, Universidade de Vila Velha, Vila Velha, ES, Brazil

^XPost-graduation Program in Nursing, Universidade de São Paulo, São Paulo, SP, Brazil

^VIDiscipline of Nursing, Universidade Federal do Espírito Santo, Vitória, ES, Brazil

^VIIPost-graduation Program in Collective Health, Universidade Federal do Espírito Santo, Vitória, ES, Brazil

ABSTRACT

INTRODUCTION: The EULAR Sjögren's Syndrome Disease Activity Index (ESSDAI) is an index of primary Sjögren's syndrome (PSS) systemic activity.

OBJECTIVE: To perform the ESSDAI transcultural adaptation into Brazilian Portuguese.

METHOD: This was a cross-sectional study with 62 patients with PSS according to the criteria of the 2002 American-European Consensus. Six stages were conducted: conceptual, item, semantic, operational, functional, and measurement equivalences (interobserver reproducibility and construct validity). For the validity assessment, the ESSDAI was compared with the Physician's Global Assessment (PhGA), the Sjögren's Syndrome Disease Activity Index (SSDAI), and the Sjögren's Systemic Clinical Activity Index (SCAI). Patients were classified by a specialist physician into two groups according to disease activity (active and inactive), and according to the intention-to-treat (increase in therapy and no increase in therapy). The ESSDAI was tested in these groups. The following statistical tests were used: intraclass correlation coefficient (ICC), Bland-Altman plot for reproducibility, and Spearman's correlation coefficient (r_s) and Mann-Whitney's test for validity (P < 0.05 and 95% CI).

RESULTS: The mean ESSDAI score was 4.95 ± 6.73. The reproducibility obtained a strong ICC of 0.89 and good agreement. When compared with other indices, it showed a strong r_s with PhGA (0.83; P < 0.000), a moderate r_s with SSDAI (0.658; P < 0.000) and a weak r_s with the SCAI (0.411; P = 0.001). The group "active" and the group " increase in therapy" had higher ESSDAI values (P = 0.000).

CONCLUSION: The Brazilian Portuguese version of ESSDAI was shown to be adaptable, reproducible, and valid for this language.

Keywords: Sjögren's syndrome; Scales; Validation studies; ESSDAI

Introduction

Primary Sjögren's syndrome (PSS) is the second most common autoimmune rheumatic disease,¹ after rheumatoid arthritis, with an estimated prevalence in the Brazilian population of 0.17%.² However, due to the scarcity of studies focused on the treatment of its systemic manifestations, PSS still has treatment directed to its dryness manifestations. This limitation arises from the lack of appropriate tools to assess the systemic activity of PSS. ^3,4 Moreover, the few studies published on PSS used different methods to measure the same parameter, creating a heterogeneous field of results within the same subject, which prevents the progress of research in the construction of knowledge.⁵ Therefore, validated tools assessing PSS activity are necessary^6,7 to evaluate the effectiveness of new therapies that focus both on severe systemic ^8-12 and glandular ^8,13,14 manifestations.

The European League Against Rheumatism (EULAR) Sjögren's Syndrome Disease Activity Index (ESSDAI) was constructed from a study consensus of the EULAR group and North-American for the study of PSS, and aims to quantify systemic disease activity. It comprises 12 areas: constitutional, lymphadenopathy, glandular, articular, cutaneous, pulmonary, renal, muscular, peripheral nervous system, central nervous system, hematological, and biological. These areas are scored based on clinical parameters evaluated by the physician.¹⁵

The transcultural adaptation of tools developed in another culture or language is not restricted to a simple translation of the original item. The process should contain a sequence of the following equivalence steps:¹⁶ conceptual and item equivalence (whether domains, concepts, and items assess the same parameters in both languages ); semantic equivalence (whether words or phrases have the same meaning; comprising the following steps: translation, back-translation, discussion with experts, and pre-test); operational equivalence (whether the format, instructions, administration and measurement methods are equivalent in both cultures); measurement (testing the psychometric properties); and functional equivalence (whether the original tool and summarized version are equivalent).

In measurement equivalence, the psychometric properties assessed are reproducibility (whether measures of individuals at different times and in different circumstances produce the same or similar results) and validity (whether the test is actually measuring what it intends to measure).^5,17

In preliminary studies of tool construction, ESSDAI was proven to be a tool with high content validity, good construct validity and reproducibility, with a clear and objective scoring system, good association of their domains with disease activity, and better responsiveness and accuracy to detect changes in the activity of the patients compared to previous tools.^11,15,18-22

In addition to the need for validation of this tool, it is essential that its properties are tested in several languages and in different populations of patients with PSS. This allows for the performance of transcultural studies and comparisons between national and international studies, thus providing scientific communication between countries of different languages.²³ Currently, the ESSDAI has been published only in the English language; this study aimed to perform its transcultural adaptation into Brazilian Portuguese.

Method

This was a cross-sectional observational study approved by the Research Ethics Committee of the Centro de Ciências da Saúde of the Universidade Federal do Espírito Santo (UFES), in 2010, and developed at the Sjögren's syndrome outpatient clinic of the Rheumatology Service of the Hospital Universitário Cassiano Antonio de Moraes, in Vitória, state of Espírito Santo, Brazil.

The procedures to perform the transcultural adaptation of ESSDAI followed the methodology proposed by Herdman et al.,¹⁶ which covers six steps: conceptual, item, semantic, operational, measurement, and functional equivalences.

Twenty patients were selected for the semantic equivalence, and 62 patients for the evaluation of measurement equivalence. Inclusion criteria were: diagnosis of PSS based on the European-American classification criteria for Sjögren's syndrome,²⁴ age equal to or greater than 18 years, and signing of the informed consent. Patients with other concomitant autoimmune diseases were excluded.

The sample was calculated based on the use of at least five patients per domain of the tool,²⁵ in a total of 62 patients, with 57 patients from the Sjögren's syndrome outpatient clinic of the Rheumatology Service of HUCAM, two from other teaching hospitals, and three from private practices. Among the 115 patients enrolled in the service, 30 did not meet the inclusion criteria and 28 were not found to participate in the interview.

The conceptual, item, semantic, and operational equivalences of ESSDAI were verified at the time of the translation and back-translation by a committee comprising a rheumatologist, a physical therapist specialized in Rheumatology, both of whom had experience managing patients with PSS and were fluent in English, and an English teacher. The translation of the ESSDAI was performed independently by two English teachers whose native language is Brazilian Portuguese, and who were aware of the purpose of the study. At the back-translation, this version was submitted to translation into English by two other English teachers, whose native language is English, blinded to the original version and to the study objective.

In the pretest, the consensus version in Portuguese was applied to 20 consecutive patients diagnosed with PSS by a rheumatologist experienced in the management of these patients.

In the measurement equivalence, the psychometric properties were compared to the original tool, according to Streiner and Norman⁵ and Kirshner and Guyatt¹⁷. The evaluated properties were reliability (interobserver reproducibility) and construct validity. The 62 patients underwent medical consultation, and the Physician Global Assessment (PhGA), ESSDAI, Sjögren's Systemic Clinical Activity Index (SCAI),¹⁸ and Sjögren's Syndrome Disease Activity Index (SSDAI)¹⁹ tools were completed on the same day by two independent rheumatologists (examiner A and B) experienced in the management of patients with PSS who were blinded and in separate rooms. The tools were scored from 0 to 10 for PhGA, 0 to 123 for ESSDAI, 0 to 72 for SCAI, and 0 to 21 for SSDAI.^15,18,19

For construct validity, the ESSDAI was compared with the following tools: numerical PhGA, and SSDAI and SCAI translated into Brazilian Portuguese.^26,27 Subsequently, the sample was divided into two groups (active and inactive) according to the onset or worsening of potentially reversible signs and symptoms of the disease in the past four weeks, as defined by a medical specialist.

The ESSDAI was also compared with the "intention to treat" on the day of medical assessment compared to the previous evaluation. Intention to treat was defined as a change in therapy, whether change in drug dosage, drug withdrawal, or inclusion of a new drug. The medications of interest were immunosuppressants, hydroxychloroquine, oral or intravenous corticosteroids, immunoglobulins, and biological agents. The sample was classified into two groups: increase and non-increase of therapy.

The collected data were analyzed and processed with the Statistical Package for Social Sciences (SPSS), release 19.0.The intraclass correlation coefficient (ICC), Bland-Altman plots, and weighted kappa were used for interobserver reproducibility. Spearman's coefficient was used for construct validity, when comparing ESSDAI with numerical PhGA, SCAI, and SSDAI.²⁸ Mann-Whitney's test was used to test ESSDAI in the comparison between the "active" and "inactive" groups and between the "increase in therapy" and "non-increase in therapy" groups.²⁸ A P-value < 0.05 was considered to be statistically significant in all analyses.

Results

There were no differences between the versions in the two languages regarding the phases of item, conceptual, semantic, and operational equivalences; and thus the final consensual Brazilian version was obtained.

Demographic characteristics and disease manifestations of the 62 patients are shown in Table 1.

Regarding the study's interobserver reproducibility, a strong and significant intraclass correlation coefficient (0.898) was obtained between the two examiners when assessing the total ESSDAI score, showing high reproducibility. The analysis by the Bland-Altman plot (Fig. 1) presented a good interobserver agreement of ESSDAI, with only three patients outside the standard deviation interval of ± 1.96 (outliers).

Weighted kappa was used for the interobserver correlation regarding the different domains of ESSDAI. There was no agreement in the lymphadenopathy domain; in the constitutional domain, the agreement was low (kappa: 0.1-0.4); in the glandular and articular domains, it was moderate (kappa: 0.41-0.60); and in the cutaneous, respiratory, renal, peripheral nervous system, hematological, and biological domains there was good agreement (kappa: 0.61 to 0.8) (Table 2). The renal and cutaneous domains showed the highest agreement, 0.791 and 0.792, respectively.

For construct validity, in comparison with numerical PhGA, a strong Spearman's coefficient of 0.832 (P < 0.000) was obtained; a moderate result was obtained with SSDAI (0.658, P < 0.000), and a weak result with SCAI (0.411, P = 0.001) - Table 3.

Table 4 presents the mean and median of ESSDAI; in the active group, it was greater than in the inactive group by nominal PhGA, and there was a statistically significant difference between the groups (P = 0.000).The active group had the highest mean rank in the ESSDAI when compared to the inactive group.

When comparing the ESSDAI according to the intention to treat between the groups, a statistically significant difference was observed between the groups (P = 0.000) (Table 4). The group with increase in therapy had higher ESSDAI values when compared to the group with no increase in therapy.

Discussion

There were no differences in the interpretation and , since it is a tool with mostly clinical domains, which are technical and objective in nature, with clear language and good understanding by the physician.

The demographic and clinical characteristics of the 62 patients were similar to those found in other studies of PSS tools (SCAI, SSDAI) and cohorts of patients with a prevalence of women > 93%; mean age 47 to 59 years; long disease duration, with a mean of 7.2 years;^{15,18,19,22,29-33} and mean interval between symptom onset and diagnosis of five years, which demonstrates a long delay in the diagnosis of this disease, previously reported by other authors.³⁴

There was a high prevalence of dryness, confirmed by objective testing and high positivity of minor salivary gland biopsy (90.3%), similar to other studies.^15,18

One of the difficulties of validation studies of PSS activity tools, such as the SCAI and SSDAI, is that most of the study patients had inactive or slightly active disease.^15,18,19,29 The total ESSDAI score ranges from 0 to 123. In the Argentinean study of ESSDAI validation into Spanish, a mean ESSDAI score of 5 was observed (ranging from 3 to 9), as well as a mean PhGA of 1.0 (0.4 to 2.2), that is, a prevalence of patients with low disease activity and inactivity.²⁹ Cohorts from different countries where ESSDAI was applied showed a mean of: 4 (0 to 43) in the English, 5.7 (0 to 29) in the French, 3.18 (0 to 29) in the Dutch, and 11.1 (0 to 37) in the Finnish cohort; ^30,31,33,35 all these samples showed patients with low disease activity.

In the ESSDAI construction study, the mean total score was 15.5 (2 to 47), with only 25% of patients with a score > 13.¹⁵ In the present study, 46.8% of the patients included had systemic manifestations at the moment of inclusion, and 61.3% had already had a disease flare. At the time of evaluation, active disease was detected in 53.2% according to the nominal PhGA; however, there was a predominance of low activity, which was observed in 38.7% of patients. This low activity was confirmed by the mean numerical PhGA score of 1.92 and the mean total ESSDAI score of 4.95 (0 to 39), with 11.3% of patients with a score > 12, similar results to those of the Argentinean validation study.²⁹

Disease activity in PSS is more difficult to detect than in other systemic rheumatic diseases, such as systemic lupus and rheumatoid arthritis, and the clinical course of PSS is usually more insidious.³⁶ Furthermore, it can be observed that systemic manifestations are observed in only one-third of patients with PSS, which can hinder the inclusion of a large number of patients in the studies. One way to solve this problem would be to perform multicenter national or international studies, to attain a better composition of the research sample.

The study interobserver reproducibility was substantial between the two examiners (ICC = 0.898). In the Argentinean validation study, reproducibility was good, but lower, with an ICC = 0.67 (P = 0.06) for ESSDAI.²⁹ Regarding other PSS activity tools, the SSDAI validation study did not assess reproducibility, and the SCAI study obtained a good correlation of 0.71.^18,19 Although these results did not present a strong correlation (ICC > 0.8), they are still better than the reproducibility results of PhGA in PSS in the literature, which showed an ICC = 0.41.¹⁵ The disease assessment by the physician through PhGA is subject to considerable variability, as it is greatly influenced by the patient's symptoms such as fatigue and pain, which are subjective parameters that are difficult to measure and highly variable in such a polymorphic disease. This also justifies the need for the validation of a more objective tool that includes systemic manifestations, such as ESSDAI, to be used in different situations, by different physicians, whether experienced or not.

When analyzing the results of ESSDAI interobserver agreement by the Bland-Altman method, a good agreement was obtained; however, the mean difference between examiners was 1.1. This indicates that there may have been a score overestimation by one examiner in relation to the other. Some hypotheses to explain this result are the difference in time of experience in the clinical management of PSS between the examiners and the absence of tool calibration between the two examiners.

There are no similar studies in the literature to compare whether an error variation of 1.1 between examiners for ESS-DAI is clinically relevant or not. Furthermore, this tool does not have stratification values of its total score or an established cutoff to define disease activity. After the cutoff value and the clinically important minimal difference are established by an international multicenter ESSDAI validation study that will soon be completed, the difference between examiners can be better interpreted regarding clinical relevance.

The interobserver reproducibility per ESSDAI domain demonstrates that the agreement was satisfactory in the six domains, i.e., they had a large number of cases whose result was the same among examiners (weighted kappa between 0.61 and 0.8). No other studies were found in the literature that performed this domain-by-domain comparison for PSS tools.

The two domains with regular agreement, the glandular and articular domains, contain subjective parameters that may have influenced the outcome. In the glandular domain, the distinction between mild or significant increase in glandular, submandibular, and lacrimal volume is at the examiner's discretion, which can generate an over- or underestimation from one examiner in relation to the other. In the articular domain, the item "arthralgia in hands, wrists, ankles, and feet accompanied by morning stiffness > 30 minutes" is a parameter answered by the patient, which can be a source of bias between examiners, as the patient may have other causes of associated joint pain, causing an examiner to score differently from the other.

The sample showed a frequency of associated fibromyalgia of 43.5% (n = 27) and patients with comorbidities were not excluded. Nevertheless, it is worth remembering that the tool itself asks not to take into account other causes of joint pain, such as osteoarthritis and fibromyalgia,¹⁵ frequently found in individuals with PSS.

Another factor that may have contributed to little or no agreement in some domains was the lack of training of the two examiners on individual items prior to the application or calibration. In some similar studies, the physicians were trained to score the tools to improve their reproducibility;^18,37,38 however, in order to simulate and adhere to daily clinical practice, the authors chose not to perform the calibration in this study.

The ESSDAI tool is a formative model, in which the items themselves have no value, but rather are assembled together to constitute a final construct.³⁹ This construct, measured by the total score, should have adequate reliability and reproducibility. When these items are evaluated individually, there may not be complete agreement, as examiners may disagree on an item and agree on others. What should be ultimately considered, thus, is the agreement of the tool's total score.⁵

The construct validity of ESSDAI with PhGA was good (coefficient 0.83, P < 0.000), and slightly better than that found in the ESSDAI construction study (0.61, P < 0.001)¹⁵ and in the Argentinean validation study (0.79, P < 0.01).²⁹ The validity of SSDAI with PhGA showed similar results (0.87, P < 0.0001).¹⁹ The construct validity of ESSDAI with SSDAI was moderate, whereas it was weak with SCAI. This result can be explained in part by the limitations of the method, as the SCAI and SS-DAI are not the gold standard for comparing validity data. They are transition tools that did not achieve good results in their psychometric properties, as they showed low content validity and reproducibility. Moreover, the SCAI has patientreported subjective items such as fatigue, morning stiffness, dyspnea, and Raynaud's phenomenon, which may have contributed to its poor correlation with ESSDAI.

Any measure of validity that is performed will show some associated error, and as a consequence, it should be expected that the correlation between tools of the same attribute should achieve a mean between 0.4 and 0.8. Any correlation lower than that suggests that the reliability of one or the other tool is unacceptably low, or that they are measuring different phenomena.^5,24 Thus, the coefficient of 0.411 found for SCAI is within the minimally acceptable limit suggested by the literature.

When evaluating validity between groups, ESSDAI was able to discriminate between active and inactive groups classified by PhGA, and by intention to treat and therapeutic change by the expert physician, despite the low variability of patients and the sample size. A mean of 1.2 was obtained in the inactive group and of 8.2 in the active group, with significant difference (P < 0.05), i.e., higher values of ESSDAI accompany higher values of disease activity assessed by the physician, as well as greater use of immunosuppressive therapy. There are no other studies in the literature that used this type of evaluation per groups for ESSDAI to compare these results.

Currently, ESSDAI has been applied to several European cohorts,^30,31,40,41 and the tendency of recommendations is to use it in practice and medical research, not alone, but together with other activity parameters such as the EULAR Sjogren's Syndrome Patient Reported Index (ESSPRI) symptom questionnaire,⁴² objective tests of saliva (sialometry sialochemistry) and tears (ocular dryness score), and laboratory parameters of autoimmune inflammation (measurement of cytokines, gammaglobulins, IgG, and β2 microglobulins).^11,43 Its multicenter validation, which is in progress, as well as its translation into different languages, are crucial to achieve a uniform scientific language in different countries and to compare studies, in order to facilitate clinical research on PSS.

Conclusion

This study demonstrated that the use of ESSDAI in the evaluated sample, which had demographic and clinical characteristics similar to other populations from PSS activity index studies, showed a strong correlation with the overall assessment of activity scored by the physician and was able to discriminate active from inactive patients in the Brazilian setting.

The authors conclude that the Brazilian Portuguese version of ESSDAI was shown to be adaptable, reproducible, and valid for this language.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgements

The authors would like to thank the EULAR Sjögren's Task Force group for granting the consent to publish ESSDAI in its entirety in the Brazilian Journal of Rheumatology.

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Received 5 December 2012

Accepted 23 April 2013

Appendix - Click to enlarge

Appendix - Click to enlarge

Appendix - Click to enlarge

Publication Dates

• Publication in this collection
  27 Jan 2014
• Date of issue
  Dec 2013

History

• Received
  05 Dec 2012
• Accepted
  23 Apr 2013