Pragmatic language dysfunction in systemic lupus erythematosus patients: Results from a single center Italian study

English version

Autoři: Fulvia Ceccarelli ^aff001; Carmelo Pirone ^aff001; Concetta Mina ^aff002; Alfredo Mascolo ^aff003; Carlo Perricone ^aff001; Laura Massaro ^aff001; Francesca Romana Spinelli ^aff001; Cristiano Alessandri ^aff001; Guido Valesini ^aff001; Fabrizio Conti ^aff001
Působiště autorů: Lupus Clinic, Dipartimento di Medicina Interna e Specialità Mediche, Sapienza University of Rome, Rome, Italy ^aff001; Dipartimento di Neurologia e Psichiatria, Sapienza Università di Roma, Rome, Italy ^aff002; Clinica Neurologica, Dipartimento di Neuroscienze, Università degli studi di Roma Tor Vergata, Rome, Italy ^aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224437

Souhrn

Background

Cognitive impairment (CI) in systemic lupus erythematosus (SLE) is a frequent neuropsychiatric manifestation affecting several domains, even in apparently asymptomatic patients. Current research revealed that the typical CI pattern affects frontal-subcortical circuit and thus executive functions. The impairment of non-literal language or pragmatic language (PL), including metaphors, idioms, inferences or irony has been well described in several conditions such as autism disorders, Parkinson’s disease, brain injury and even in earlier phases of neurodegenerative processes. Even if PL neuro-anatomy remains controversial, correlation between executive dysfunctions and non-literal language involvement has been reported both in traumatic injury and mild cognitive impairment patients. Nonetheless, no specific study has been performed to evaluate PL impairment in SLE patients so far.

Objectives

We aimed at assessing the PL domain in a Italian monocentric SLE cohort in comparison to healthy controls, matched to age and education, through a specific battery, the batteria sul linguaggio dell'emisfero destro (BLED). Secondly, we focused attention on possible correlations between CI and clinical and laboratory SLE-related features.

Methods

Forty adult patients affected by SLE, according to the American College of Rheumatology (ACR) criteria, and thirty healthy subjects were enrolled consecutively in this cross-sectional study. The protocol included complete physical examination, extensive clinical and laboratory data collection (comprehensive of demographics, past medical history, co-morbidities, disease activity, chronic damage evaluation, previous and concomitant treatments) and cognitive assessment for five different domains: memory, attention, pragmatic language, executive and visuospatial functions. Self-reported scale for anxiety and depression were performed to exclude the influence of mood disorders on cognitive dysfunction.

Results

We studied 40 Caucasian SLE patients [male (M)/ female (F) 3/37; mean±standard deviation (SD) age 45.9±10.1 years, mean±SD disease duration 120.8±81.2 months] and 30 healthy subjects (M/F 9/21; mean±SD age 41.3±13 years). According to the low level of disease activity and damage (mean±SD Systemic Lupus Erythematosus Disease Activity Index 2000 (SLEDAI-2K) of 1.3±2.3, mean±SD Systemic Lupus International Collaborative Clinics/American College of Rheumatology (SLICC/ACR) Damage Index (SDI) of 0.2±0.5), only 30% of patients was on glucocorticoid treatment at the study entry. PL was the most compromised domain in terms of Mean Domain Z scores. As for the Domain Cognitive Dysfunction score, a deficit of PL was observed in 45% of patients and was significantly more prevalent than memory, executive and visuospatial functions impairment (P = 0.0002, P = 0.0002 and P<0.000001, respectively). According to Global Cognitive Dysfunction score, 25% of patients experienced a mild impairment and 7.5% a moderate one. Anti-phospholipid antibodies positivity was significantly associated with memory impairment (P<0.0005), whereas the presence of other neuropsychiatric events was associated with executive dysfunctions (P<0.05); no further significant association nor correlation were identified.

Conclusion

In this study we evaluated for the first time PL in SLE patients finding a dysfunction in almost half of patients. The dysfunction of PL was significantly more frequent than the other domains assessed.

Klíčová slova:

Anticoagulant therapy – Attention – Cognitive impairment – Language – Memory – Neuropsychological testing

Zdroje

1. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis and rheumatism. 1999;42(4):599–608 doi: 10.1002/1529-0131(199904)42:4<599::AID-ANR2>3.0.CO;2-F 10211873

2. Buchbinder R, Hall S, Littlejohn GO, Ryan PF. Neuropsychiatric manifestations of systemic lupus erythematosus. Australian and New Zealand journal of medicine. 1988;18(5):679–84. doi: 10.1111/j.1445-5994.1988.tb00150.x 3245822

3. Kozora E, Thompson LL, West SG, Kotzin BL. Analysis of cognitive and psychological deficits in systemic lupus erythematosus patients without overt central nervous system disease. Arthritis Rheum 1996;39:2035–45. doi: 10.1002/art.1780391213 8961909

4. Conti F, Alessandri C, Perricone C, Scrivo R, Rezai S, Ceccarelli F, Spinelli FR, Ortona E, Marianetti M, Mina C, Valesini G. Neurocognitive dysfunction in systemic lupus erythematosus: association with antiphospholipid antibodies, disease activity and chronic damage. PLoS One. 2012;7(3):e33824. doi: 10.1371/journal.pone.0033824 22461897

5. Kozora E, Arciniegas DB, Filley CM, West SG, Brown M, Miller D, Grimm A, Devore MD, Wingrove C, Zhang L. Cognitive and neurologic status in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. Arthritis Rheum. 2008;59:1639–46. doi: 10.1002/art.24189 18975359

6. Sarbu N, Alobeidi F, Toledano P, Espinosa G, Giles I, Rahman A, Yousry T, Capurro S, Jäger R, Cervera R, Bargalló N. Brain abnormalities in newly diagnosed neuropsychiatric lupus: systematic MRI approach and correlation with clinical and laboratory data in a large multicenter cohort. Autoimmun Rev 2015;14:153–9. doi: 10.1016/j.autrev.2014.11.001 25461835

7. Kozora E, Uluğ AM, Erkan D, Vo A, Filley CM, Ramon G, Burleson A, Zimmerman R, Lockshin MD. Functional Magnetic Resonance Imaging of Working Memory and Executive Dysfunction in Systemic Lupus Erythematosus and Antiphospholipid Antibody-Positive Patients. Arthritis Care Res (Hoboken) 2016;68:1655–1663.

8. Cardoso S, Silva D, Maroco J, de Mendonça A, Guerreiro M. Non-literal language deficits in mild cognitive impairment. Psychogeriatrics 2014;14:222–8. doi: 10.1111/psyg.12101 25495083

9. Mazza M, Di Michele V, Pollice R, Casacchia M, Roncone R. Pragmatic language and theory of mind deficits in people with schizophrenia and their relatives. Psychopathology. 2008;41:254–63. doi: 10.1159/000128324 18441527

10. Rapp AM, Mutschler DE, Erb M. Where in the brain is nonliteral language? A coordinate-based meta-analysis of functional magnetic resonance imaging studies. Neuroimage 2012;63:600–10. doi: 10.1016/j.neuroimage.2012.06.022 22759997

11. Gemsbacher MA, Robertson RR. The role of suppression in figurative language comprehension. J Pragmat 1999;31:1619–1630. doi: 10.1016/S0378-2166(99)00007-7 25520540

12. Brown-Schmidt S. The role of executive function in perspective taking during online language comprehension. Psychon Bull Rev 2009;16:893–900. doi: 10.3758/PBR.16.5.893 19815795

13. Douglas JM. Relation of executive functioning to pragmatic outcome following severe traumatic brain injury. J Speech Lang Hear Res 2010;53:365–82. doi: 10.1044/1092-4388(2009/08-0205) 20360462

14. Gaudreau G, Monetta L, Macoir J, Laforce R Jr, Poulin S, Hudon C. Verbal irony comprehension in older adults with amnestic mild cognitive impairment. Neuropsychology 2013;27:702–12. doi: 10.1037/a0034655 24245931

15. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40:1725.

16. Gladman DD, Ibañez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol 2002; 29:288–91. 11838846

17. Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M, Bacon P, Bombardieri S, Hanly J, Hay E, Isenberg D, Jones J, Kalunian K, Maddison P, Nived O, Petri M, Richter M, Sanchez-Guerrero J, Snaith M, Sturfelt G, Symmons D, Zoma A. The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 1996; 39:363–9. doi: 10.1002/art.1780390303 8607884

18. Alarcón GS, Cianfrini L, Bradley LA, Sanchez ML, Brooks K, Friedman AW, Baethge BA, Fessler BJ, Bastian HM, Roseman JM, McGwin G Jr, Reveille JD; Lumina Study Group. Systemic lupus erythematosus in three ethnic groups. X. Measuring cognitive impairment with the cognitive symptoms inventory. Arthritis Rheum 2002;47:310–9. doi: 10.1002/art.10457 12115162

19. Ad Hoc Committee on Lupus Response Criteria: Cognition Sub-committee, Mikdashi JA, Esdaile JM, Alarcón GS, Crofford L, Fessler BJ, Shanberg L, Brunner H, Gall V, Kalden JR, Lockshin MD, Liang MH, Roberts N Jr, Schneider M. Proposed response criteria for neurocognitive impairment in systemic lupus erythematosus clinical trials. Lupus. 2007;16(6):418–25. doi: 10.1177/0961203307079044 17664232

20. Beck AT, Steer RA, Ball R, Ranieri W. Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J Pers Assess. 1996;67:588–97. doi: 10.1207/s15327752jpa6703_13 8991972

21. Zung WW, Gianturco JA. Personality dimension and the Self-Rating Depression Scale. J Clin Psychol. 1971;27:247–8. doi: 10.1002/1097-4679(197104)27:2<247::aid-jclp2270270230>3.0.co;2-6 5100681

22. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189–98. doi: 10.1016/0022-3956(75)90026-6 1202204

23. Spinnler H, Dall'Ora P. On Alzheimer's disease: an overview of diagnostic and research issues for the clinical neurologist. Funct Neurol 1987;2:5–36. 3315875

24. Carlesimo GA, Caltagirone C. Components in the visual processing of known and unknown faces. J Clin Exp Neuropsychol 1995;17:691–705. doi: 10.1080/01688639508405159 8557810

25. Rinaldi M. C., Marangolo P., Lauriola M. (2006). BLED SantaLucia. Batteria sul Linguaggio dell'Emisfero Destro SantaLucia. Firenze. Giunti O.S.

26. Leslie B, Crowe SF. Cognitive functioning in systemic lupus erythematosus: a meta-analysis. Lupus. 2018 Jan 1:961203317751859

27. Ceccarelli F, Perricone C, Pirone C, Massaro L, Alessandri C, Mina C, Marianetti M, Spinelli FR, Valesini G, Conti F. Cognitive dysfunction improves in systemic lupus erythematosus: Results of a 10 years prospective study. PLoS One 2018;13:e0196103. doi: 10.1371/journal.pone.0196103 29723209

28. Leyhe T, Saur R, Eschweiler GW, Milian M. Impairment in proverb interpretation as an executive function deficit in patients with amnestic mild cognitive impairment and early Alzheimer's disease. Dement Geriatr Cogn Dis Extra 2011;1:51–61. doi: 10.1159/000323864 22163233

29. Van Lier S, Batens K, Santens P, Van Roost D, Van Herreweghe M, De Letter M. The influence of subthalamic nucleus stimulation on pragmatic language production in Parkinson's disease. Acta Neurol Belg 2016;116:163–70. doi: 10.1007/s13760-015-0546-5 26442686

30. Carotenuto A. Look beyond the door, not through the keyhole: evidence from a cognitive assessment including social cognition evaluation in multiple sclerosis. Eur J Neurol 2018;25:205–206. doi: 10.1111/ene.13482 29053891

31. Nantes SG, Su J, Dhaliwal A, Colosimo K, Touma Z. Performance of Screening Tests for Cognitive Impairment in Systemic Lupus Erythematosus. J Rheumatol 2017;44:1583–1589. doi: 10.3899/jrheum.161125 28864643

32. Kozora E, Ellison MC, West S. Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis Rheum 2004;51:810–8. doi: 10.1002/art.20692 15478145

33. Kramer S, Bryan K, Frith CD. Mental illness and communication. Int J Lang Commun Disord. 2001;36 Suppl:132–7.

34. Burns MS. Use of the family to facilitate communicative changes in adults with neurological impairments. Semin Speech Lang. 1996;17:115–21. doi: 10.1055/s-2008-1064092 8727275

35. Hanly JG, Fisk JD, McCurdy G, Fougere L, Douglas JA. Neuropsychiatric syndromes in patients with systemic lupus erythematosus and rheumatoid arthritis. J Rheumatol. 2005;32:1459–6. 16078320

Pragmatic language dysfunction in systemic lupus erythematosus patients: Results from a single center Italian study

Souhrn

Background

Objectives

Methods

Results

Conclusion

Klíčová slova:

Zdroje

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