Clinical Rheumatology

, Volume 37, Issue 4, pp 987–997 | Cite as

Malnutrition and sarcopenia in a large cohort of patients with systemic sclerosis

  • C. CaimmiEmail author
  • P. Caramaschi
  • A. Venturini
  • E. Bertoldo
  • E. Vantaggiato
  • O. Viapiana
  • M. Ferrari
  • G. Lippi
  • L. Frulloni
  • M. Rossini
Original Article


Systemic sclerosis (SSc) is an autoimmune disease which may lead to malnutrition. Previous studies have defined it with different criteria. No thorough evaluations of sarcopenia in SSc are available. The aim of the present study was to assess the prevalence and the potential association of malnutrition and sarcopenia in a large cohort of SSc cases. A total of 141 SSc consecutive outpatients were enrolled. Body composition was analyzed by densitometry. Malnutrition was defined according to recently published ESPEN criteria, whereas sarcopenia was diagnosed in patients with reduced skeletal muscle index. Malnutrition was diagnosed in 9.2% of patients (95% CI, 4.4–14.0%). Malnourished patients had worse gastrointestinal symptoms according to UCLA SCTC GIT 2.0 questionnaire (p = 0.007), lower physical activity (p = 0.028), longer disease duration (p = 0.019), worse predicted DLCO/VA and FVC (p = 0.009, respectively), worse disease severity according to Medsger severity score (p < 0.001), lower hemoglobin (p = 0.023), and fat-free mass (p < 0.001) and were more often sarcopenic (p < 0.001). In multivariate analysis, only FVC (p = 0.006) and disease severity (p = 0.003), in particular for the lungs (p = 0.013), were confirmed to be worse in malnourished patients. Sarcopenia was diagnosed in 29\140 patients (20.7%; 95% CI, 14.0–27.4%); 11\29 were also malnourished. In multivariate analysis, sarcopenic patients had longer disease duration (p = 0.049), worse DLCO/VA (p = 0.002), and lung (p = 0.006) and skin (p = 0.014) involvement. In SSc, malnutrition defined with ESPEN criteria was found to be lower than previously reported. Sarcopenia was found to be somewhat common. Lung involvement was significantly associated with nutritional status and may not be explained only by muscle weakness.


Lung involvement Malnutrition Sarcopenia Systemic sclerosis 



This work had no funds.

Compliance with ethical standards

The study was performed according to the Helsinki declaration and approved by Verona Medical School Institutional review board, with protocol number 18493. All patients provided written informed consent for participating the study.




  1. 1.
    Butt S, Emmanuel A (2013) Systemic sclerosis and gut. Expert Rev Gastroenterol Hepatol 7(4):331–339. CrossRefPubMedGoogle Scholar
  2. 2.
    Akesson A, Gustafson T, Wollheim F, Brismar J (1987) Esophageal dysfunction and radionuclide transit in progressive systemic sclerosis. Scand J Rheumatol 16(4):291–299. CrossRefPubMedGoogle Scholar
  3. 3.
    Sallam H, McNearney TA, Chen JD (2006) Systematic review: phatophysiology and management of gastrointestinal dysmotility in systemic sclerosis (scleroderma). Aliment Pharmacol Ther 23(6):691–712. CrossRefPubMedGoogle Scholar
  4. 4.
    Sobotka L (2012) Basics in clinical nutrition, 4th edn. Galen, PragueGoogle Scholar
  5. 5.
    Baron M, Hudson M, Steele R, Canadian scleroderma research group (2009) Malnutrition is common in systemic sclerosis: results from the Canadian scleroderma research group database. J Rheumatol 36(12):2737–2743. CrossRefPubMedGoogle Scholar
  6. 6.
    Krause L, Becker MO, Brueckner CS, Bellinghausen CJ, Becker C, Schneider U, Haeupl T, Hanke K, Hensel-Wiegel K, Ebert H, Ziemer S, Ladner UM, Pirlich M, Burmester GR, Riemekasten G (2010) Nutritional status as marker for disease activity and severity predicting mortality in patients with systemic sclerosis. Ann Rheum Dis 69(11):1951–1957. CrossRefPubMedGoogle Scholar
  7. 7.
    Murtaugh M, Frech T (2013) Nutritional status and gastrointestinal symptoms in systemic sclerosis patients. Clin Nutr 32(1):130–135. CrossRefPubMedGoogle Scholar
  8. 8.
    Caporali R, Caccialanza R, Bonino C, Klersy C, Cereda E, Xoxi B, Crippa A, Rava ML, Orlandi M, Bonardi C, Cameletti B, Codullo V, Montecucco C (2012) Disease-related malnutrition in outpatients with systemic sclerosis. Clin Nutr 31(5):666–671. CrossRefPubMedGoogle Scholar
  9. 9.
    Rosato E, Gigante A, Gasperini ML, Molinaro I, Di Lazzaro Giraldi G, Afeltra A, Amoroso D, Salsano F, Rossi Fanelli F, Laviano A (2014) Nutritional status measured by BMI is impaired and correlates with left ventricular mass in patients with systemic sclerosis. Nutrition 30(2):204–209. CrossRefPubMedGoogle Scholar
  10. 10.
    Cereda E, Codullo V, Klersy C, Breda S, Crippa A, Rava ML, Orlandi M, Bonardi C, Fiorentini ML, Caporali R, Caccialanza R (2014) Disease-related nutritional risk and mortality in systemic sclerosis. Clin Nutr 33(3):558–561. CrossRefPubMedGoogle Scholar
  11. 11.
    Spanjer MJ, Bultink IEM, de van der Schueren MAE, Voskuyl AE (2017) Prevalence of malnutrition and validation of bioelectrical impedance analysis for the assessment of body composition in patients with systemic sclerosis. Rheumatology 56(6):1008–1012. CrossRefPubMedGoogle Scholar
  12. 12.
    Gyger G, Baron M (2012) Gastrointestinal manifestations of scleroderma: recent progress in evaluation, pathogenesis, and management. Curr Rheumatol Rep 14(1):22–29. CrossRefPubMedGoogle Scholar
  13. 13.
    Isola G, Williams RC, Lo Gullo A, Ramaglia L, Matarese M, Iorio-Siciliano V, Cosio C, Matarese G (2017) Risk association between scleroderma disease characteristics, periodontitis, and tooth loss. Clin Rheumatol 36(12):2733–2741. CrossRefPubMedGoogle Scholar
  14. 14.
    Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, de Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12(4):249–256. CrossRefPubMedGoogle Scholar
  15. 15.
    Ali S, Garcia JM (2014) Sarcopenia, cachexia and aging: diagnosis, mechanisms and therapeutic options—a mini-review. Gerontology 60(4):294–305. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Marighela TF, Genaro Pde S, Pinheiro MM, Szejnfeld VL, Kayser C (2013) Risk factors for body composition abnormalities in systemic sclerosis. Clin Rheumatol 32(7):1037–1044. CrossRefPubMedGoogle Scholar
  17. 17.
    Cederholm T, Bosaeus I, Barazzoni R, Bauer J, Van Gossum A, Klek S, Muscaritoli M, Nyulasi I, Ockenga J, Schneider SM, de van der Schueren MAE, Singer P (2015) Diagnostic criteria for malnutrition: an ESPEN consensus statement. Clin Nutr 34(3):335–340. CrossRefPubMedGoogle Scholar
  18. 18.
    Medsger TA, Bombardieri S, Czirjak L, Scorza R, Della Rossa A, Bencivelli W (2003) Assessment of disease severity and prognosis. Clin Exp Rheumatol 21(3 suppl 29):S42–S46PubMedGoogle Scholar
  19. 19.
    Khanna D, Hays RD, Maranian P, Seibold JR, Impens A, Mayes MD, Clements PJ, Getzug T, Fathi N, Bechtel A, de Furst (2009) Reliability and validity of UCLA Scleroderma Clinical Trial Consortium Gastrointestinal Tract (UCLA SCTC GIT 2.0) instrument. Arthritis Rheum 61(9):1257–1263. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G, Clements PJ, Denton CP, Distler O, Allanore Y, de Furst, Gabrielli A, Mayes MD, van Laar JM, Seibold JR, Czirjak L, Steen VD, Inanc M, Kowal-Bielecka O, Müller-Ladner U, Valentini G, Veale DJ, Vonk MC, Walker UA, Chung L, Collier DH, Ellen Csuka M, Fessler BJ, Guiducci S, Herrick A, Hsu VM, Jimenez S, Kahaleh B, Merkel PA, Sierakowski S, Silver RM, Simms RW, Varga J, Pope JE (2013) 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747–1755. CrossRefPubMedGoogle Scholar
  21. 21.
    LeRoy EC, Black CM, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr et al (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15(2):202–205PubMedGoogle Scholar
  22. 22.
    Akesson A, Fiori G, Krieg T, van den Hoogen FHJ, Seibold JR (2002) Assessment of skin, joint, tendon and muscle involvement. Clin Exp Rheumatol 21(3 suppl 29):S5–S8Google Scholar
  23. 23.
    Valentini G, Della Rossa A, Bombardieri S, Bencivelli W, Silman AJ, D'Angelo S, Cerinic MM, Belch JF, Black CM, Bruhlmann P, Czirják L, de Luca A, Drosos AA, Ferri C, Gabrielli A, Giacomelli R, Hayem G, Inanc M, McHugh NJ, Nielsen H, Rosada M, Scorza R, Stork J, Sysa A, van den Hoogen FH, Vlachoyiannopoulos PJ (2001) European multicentre study to define disease activity criteria for systemic sclerosis. II. Identification of disease activity variables and development of preliminary activity indexes. Ann Rheum Dis 60(6):592–598. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Elia M (2003) Screening for malnutrition: a multidisciplinary responsibility. Development and use of the ‘malnutrition universal screening tool’ (‘MUST’) for adults. Malnutrition Advisory Group (MAG), a standing committee of BAPEN Redditch, WorcsGoogle Scholar
  25. 25.
    Stratton RJ, Hackston A, Longmore D, Dixon R, Price S, Stroud M, King C, Elia M (2004) Malnutrition in hospital outpatients and inpatients: prevalence, concurrent validity and ease of use of the ‘malnutrition universal screening tool’ (‘MUST’) for adults. Br J Nutr 92(05):799–808. CrossRefPubMedGoogle Scholar
  26. 26.
    Neelemaat F, Meijers J, Kruizenga H, van Ballegooijen H, van Bokhorst-de van der Schueren M (2011) Comparison of five malnutrition screening tools in one hospital inpatient sample. J Clin Nurs 20(15-16):2144–2152. CrossRefPubMedGoogle Scholar
  27. 27.
    Leistra E, Langius JA, Evers AM, van Bokhorst-de van der Schueren MA, Visser M, de Vet HC et al (2013) Validity of nutritional screening with MUST and SNAQ in hospital outpatients. Eur J Clin Nutr 67(7):738–742. CrossRefPubMedGoogle Scholar
  28. 28.
    Baumgartner R, Koehler K, Gallagher D, Romero L, Heymsfield SB, Ross RR et al (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147(8):755–763. CrossRefPubMedGoogle Scholar
  29. 29.
    Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE et al (2003) International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35(8):1381–1395. CrossRefPubMedGoogle Scholar
  30. 30.
    March C, Siegert E, Preis E, Makowka A, Buttgereit F, Riemekasten G et al (2017) Prevalence of sarcopenia in patients with systemic sclerosis according to the revised criteria of the european working group on sarcopenia in older people. Ann Rheum Dis 15:897–898Google Scholar
  31. 31.
    Schweitzer L, Geisler C, Johannsen M, Glüer CC, Müller MJ (2017) Associations between body composition, physical capabilities and pulmonary function in healthy older adults. Eur J Clin Nutr 71(3):389–394. CrossRefPubMedGoogle Scholar
  32. 32.
    Massaro D, Massaro GD (2004) Hunger disease and pulmonary alveoli. Am J Respir Crit Care Med 170(7):723–724. CrossRefPubMedGoogle Scholar
  33. 33.
    Tyndall AJ, Bannert B, Vonk M, Airò P, Cozzi F, Carreira PE et al (2010) Causes and risk factors for death in systemic sclerosis: a study from the EULAR Scleroderma Trials and Research (EUSTAR) database. Ann Rheum Dis 69(10):1809–1815. CrossRefPubMedGoogle Scholar
  34. 34.
    Caimmi C, Caramaschi P, Barausse G, Orsolini G, Idolazzi L, Gatti D, Viapiana O, Adami S, Biasi D, Rossini M (2016) Bone metabolism in a large cohort of patients with systemic sclerosis. Calcif Tissue Int 99(1):23–29. CrossRefPubMedGoogle Scholar
  35. 35.
    Caramaschi P, Dalla Gassa A, Ruzzenente O, Volpe A, Ravagnani V, Tinazzi I, Barausse G, Bambara LM, Biasi D (2010) Very low levels of vitamin D in systemic sclerosis patients. Clin Rheumatol 29(12):1419–1425. CrossRefPubMedGoogle Scholar
  36. 36.
    Giuggioli D, Colaci M, Cassone G, Fallahi P, Lumetti F, Spinella A, Campomori F, Manfredi A, Manzini CU, Antonelli A, Ferri C (2017) Serum 25-OH vitamin D levels in systemic sclerosis: analysis of 140 patients and review of the literature. Clin Rheumatol 36(3):583–590. CrossRefPubMedGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2017

Authors and Affiliations

  • C. Caimmi
    • 1
    Email author
  • P. Caramaschi
    • 1
  • A. Venturini
    • 1
  • E. Bertoldo
    • 1
  • E. Vantaggiato
    • 1
  • O. Viapiana
    • 1
  • M. Ferrari
    • 2
  • G. Lippi
    • 3
  • L. Frulloni
    • 4
  • M. Rossini
    • 1
  1. 1.Rheumatology UnitUniversity of VeronaVeronaItaly
  2. 2.Respiratory Physiopathology UnitUniversity of VeronaVeronaItaly
  3. 3.Section of Clinical BiochemistryUniversity of VeronaVeronaItaly
  4. 4.Gastroenterology UnitUniversity of VeronaVeronaItaly

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