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Research ArticleSjögren Syndrome

Tongue Atrophy in Sjögren Syndrome Patients with Mucosa-associated Lymphoid Tissue Lymphoma: Autoimmune Epithelitis beyond the Epithelial Cells of Salivary Glands?

Evangelia Zampeli, Eleni-Marina Kalogirou, Evangelia Piperi, Clio P. Mavragani and Haralampos M. Moutsopoulos
The Journal of Rheumatology November 2018, 45 (11) 1565-1571; DOI: https://doi.org/10.3899/jrheum.180101
Evangelia Zampeli
From the Institute for Systemic Autoimmune and Neurological Diseases; Department of Oral Medicine and Oral Pathology, Faculty of Dentistry, School of Health Sciences, National and Kapodistrian University of Athens; Department of Pathophysiology, and Department of Physiology, Medical School, National and Kapodistrian University of Athens; Academy of Athens, Athens, Greece.
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  • ORCID record for Evangelia Zampeli
  • For correspondence: zampelieva@gmail.com
Eleni-Marina Kalogirou
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Evangelia Piperi
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Clio P. Mavragani
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Haralampos M. Moutsopoulos
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Article Figures & Data

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  • Figure 1.
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    Figure 1.

    Tongue atrophy scoring. The lingual dorsum is divided into posterior, middle, and anterior parts, and the grade of atrophy of the filiform and fungiform papillae is scored from 0 to 2 for each tertile. This scoring system results in a maximum (max.) final tongue atrophy score (filiform and fungiform papillae for the entire tongue) of 12.

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    Figure 2.

    Representative tongue images of pSS patients with (A) normal, nonatrophic lingual papillae and nonfissured tongue (maximum final tongue atrophy score = 0/12); (B) fissured (scrotal) tongue with flattened or rounded filiform papillae and flattened fungiform papillae in all 3 tongue tertiles (maximum final tongue atrophy score = 7/12); (C) dry, lobulated, and shiny atrophic tongue appearance because of loss of filiform and fungiform papillae, especially in the anterior and middle tongue tertiles (maximum final tongue atrophy score = 11/12). pSS: primary Sjögren syndrome.

Tables

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    Table 1.

    Clinical manifestations and histopathological/laboratory/serological features in the 2 groups of patients. Values are n (%).

    VariablespSS non-MALT, n = 57pSS-MALTδ, n = 19p
    Clinical manifestations
      Oral dryness (subjective)46/57 (81)18/19 (95)0.274
      Ocular dryness (subjective)43/57 (75)17/19 (89)0.330
      SGE13/57 (23)11/19 (58)0.009
      Raynaud phenomenon13/57 (23)7/19 (37)0.243
      Palpable purpura5/57 (9)2/19 (10)1.000
      Arthralgias/myalgias35/55 (64)14/19 (73)0.576
      Arthritis10/57 (17)4/19 (21)0.740
      Lymphadenopathy3/57 (5)5/19 (26)0.020
    Histopathological/laboratory/serological features
      MSG biopsy focus score ≥ 129/57 (51)17/19 (89)0.003
      MSG biopsy Tarpley score > 217/57 (30)17/19 (89)< 0.001
      Leukopenia*6/56 (11)2/19 (10)1.000
      ANA-positive†36/57 (63)16/19 (84)0.153
      C4 hypocomplementemia◊27/51 (53)9/17 (53)1.000
      Anti-Ro/SSA- and/or anti-La/SSB-positive36/57 (63)14/19 (74)0.235
      RF-positive26/57 (46)16/19 (84)0.001
      Monoclonal gammopathy0/44 (0)5/17 (29)0.001
    • ↵δ pSS-MALT: pSS patients with MALT lymphoma, matched 1:3 for age, sex, and disease duration with pSS non-MALT patients.

    • ↵* Defined as white blood cells < 3000/mm3 on 3 separate occasions.

    • ↵† Titers > 1:160.

    • ↵◊ Defined as serum C4 levels < 20 mg/dl on 3 separate occasions. Values in bold face are statistically significant. pSS: primary Sjögren syndrome; MALT: mucosa-associated lymphoid tissue; SGE: salivary gland enlargement; MSG: minor salivary gland; ANA: antinuclear antibodies; RF: rheumatoid factor.

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    Table 2.

    Oral examination findings in the 2 groups of patients. Values are n (%).

    Oral Examination FindingspSS non-MALT, n = 57pSS-MALTδ, n = 19p
    UWSF ≤ 1.5 ml/15 min14/57 (25)16/19 (84)< 0.001
    Presence of tongue atrophy17/57 (30)13/19 (68)0.006
    Fissured tongue19/57 (33)17/19 (89)< 0.001
    • ↵δ pSS-MALT: pSS patients with MALT lymphoma, matched 1:3 for age, sex, and disease duration with pSS non-MALT patients. Values in bold face are statistically significant. pSS: primary Sjögren syndrome; MALT: mucosa-associated lymphoid tissue; UWSF: unstimulated whole salivary flow.

    • View popup
    Table 3.

    Multivariate analysis. Independent oral and clinical findings associated with MALT lymphoma in patients with pSS.

    Independent VariablesOR (95% CI)p
    Oral findings
      UWSF ≤ 1.5 ml/15 min0.09 (0.015–0.560)0.010
      Fissured tongue0.11 (0.017–0.711)0.020
      Presence of tongue atrophy2.364 (0.401–14.500)0. 352
    Oral and clinical findings
      UWSF ≤ 1.5 ml/15 min0.169 (0.033–0.867)0.033
      Fissured tongue0.070 (0.007–0.669)0.021
      Lymphadenopathy0.071 (0.005–1.031)0.050
      SGE0.249 (0.058–1.079)0.063
    • Values in bold face are statistically significant. MALT: mucosa-associated lymphoid tissue; pSS: primary Sjögren syndrome; UWSF: unstimulated whole salivary flow; SGE: salivary gland enlargement.

    • View popup
    Table 4.

    Clinical manifestations and histopathological/laboratory/serological features in the pSS-MALT patients with and without tongue atrophy. Values are n (%).

    VariablespSS-MALT without Tongue Atrophy, n = 6pSS-MALT with Tongue Atrophy, n = 13p
    Clinical manifestations
      Oral dryness (subjective)6/6 (100)12/13 (92)1.000
      Ocular dryness (subjective)6/6 (100)11/13 (85)1.000
      SGE4/6 (67)7/13 (54)1.000
      Raynaud phenomenon1/6 (17)6/13 (46)0.333
      Palpable purpura1/6 (17)1/13 (7)1.000
      Arthralgias/myalgias4/6 (67)10/13 (77)1.000
      Arthritis2/6 (33)2/13 (15)0.557
      Lymphadenopathy0/6 (0)5/13 (38)0.128
    Histopathological/laboratory/serological features
      MSG biopsy focus score ≥ 15/6 (83)11/13 (85)1.000
      MSG biopsy Tarpley score > 26/6 (100)11/13 (85)1.000
      Leukopenia*0/6 (0)2/13 (15)1.000
      ANA-positive†5/6 (83)11/13 (85)1.000
      C4 hypocomplementemia◊1/5 (20)8/12 (67)0.131
      Anti-Ro/SSA and/or anti-La/SSB positive2/5 (40)12/13 (92)0.015
      RF-positive4/4 (100)12/12 (100)1.000
      Monoclonal gammopathy2/5 (40)3/12 (25)0.600
    • ↵* Defined as white blood cells < 3000/mm3 on 3 separate occasions.

    • ↵† Titers > 1:160.

    • ↵◊ Defined as serum C4 levels < 20 mg/dl on 3 separate occasions. Values in bold face are statistically significant. pSS: primary Sjögren syndrome; MALT: mucosa-associated lymphoid tissue; SGE: salivary gland enlargement; MSG: minor salivary gland; ANA: antinuclear antibody; RF: rheumatoid factor.

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The Journal of Rheumatology
Vol. 45, Issue 11
1 Nov 2018
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Tongue Atrophy in Sjögren Syndrome Patients with Mucosa-associated Lymphoid Tissue Lymphoma: Autoimmune Epithelitis beyond the Epithelial Cells of Salivary Glands?
Evangelia Zampeli, Eleni-Marina Kalogirou, Evangelia Piperi, Clio P. Mavragani, Haralampos M. Moutsopoulos
The Journal of Rheumatology Nov 2018, 45 (11) 1565-1571; DOI: 10.3899/jrheum.180101

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Tongue Atrophy in Sjögren Syndrome Patients with Mucosa-associated Lymphoid Tissue Lymphoma: Autoimmune Epithelitis beyond the Epithelial Cells of Salivary Glands?
Evangelia Zampeli, Eleni-Marina Kalogirou, Evangelia Piperi, Clio P. Mavragani, Haralampos M. Moutsopoulos
The Journal of Rheumatology Nov 2018, 45 (11) 1565-1571; DOI: 10.3899/jrheum.180101
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Keywords

SJÖGREN SYNDROME
TONGUE ATROPHY
RISK FACTORS
MALT LYMPHOMA

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