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Journal of Peking University (Health Sciences) ›› 2023, Vol. 55 ›› Issue (6): 966-974. doi: 10.19723/j.issn.1671-167X.2023.06.003

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Clinical characteristics and diagnostic indicators of macrophage activation syndrome in patients with systemic lupus erythematosus and adult-onset Still's disease

Hai-hong YAO1,Fan YANG1,2,Su-mei TANG1,Xia ZHANG1,Jing HE1,Yuan JIA1,*()   

  1. 1. Department of Rheumatology and Immunology, Peking University People's Hospital, Beijing 100044, China
    2. Department of Rheumatology, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China
  • Received:2023-09-01 Online:2023-12-18 Published:2023-12-11
  • Contact: Yuan JIA E-mail:jiayuan1023@sina.com
  • Supported by:
    the National Natural Science Foundation of China(81801618)

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Abstract:

Objective: To analyze and compare the clinical and laboratory characteristics of macrophage activation syndrome (MAS) in patients with systemic lupus erythematosus (SLE) and adult-onset Still's disease (AOSD), and to evaluate the applicability of the 2016 European League Against Rheumatism/American College of Rheumatology/Paediatric Rheumatology International Trials Organization classification criteria for MAS complicating systemic juvenile idiopathic arthritis (sJIA) in different auto-immune diseases contexts and to propose new diagnostic predictive indicators. Methods: A retrospective analysis was conducted on the clinical and laboratory data of 24 SLE patients with MAS (SLE-MAS) and 24 AOSD patients with MAS (AOSD-MAS) who were hospitalized at Peking University People's Hospital between 2000 and 2018. Age- and sex-matched SLE (50 patients) and AOSD (50 patients) diagnosed in the same period without MAS episodes were selected as controls. The cutoff values for laboratory indicators predicting SLE-MAS and AOSD-MAS were determined using receiver operating characteristic (ROC) curves. Furthermore, the laboratory diagnostic predictive values for AOSD-MAS were used to improve the classification criteria for systemic juvenile idiopathic arthritis-associated MAS (sJIA-MAS), and the applicability of the revised criteria for AOSD-MAS was explored. Results: Approximately 60% of SLE-MAS and 40% of AOSD-MAS occurred within three months after the diagnosis of the underlying diseases. The most frequent clinical feature was fever. In addition to the indicators mentioned in the diagnosis criteria for hemophagocytic syndrome revised by the International Society for Stem Cell Research, the MAS patients also exhibited significantly elevated levels of aspartate aminotransferase and lactate dehydrogenase, along with a significant decrease in albumin. Hemophagocytosis was observed in only about half of the MAS patients. ROC curve analysis demonstrated that the optimal discriminative values for diagnosing MAS was achieved when SLE patients had ferritin level≥1 010 μg/L and lactate dehydroge-nase levels≥359 U/L, while AOSD patients had fibrinogen levels≤225.5 mg/dL and triglyceride levels≥2.0 mmol/L. Applying the 2016 sJIA-MAS classification criteria to AOSD-MAS yielded a diagnostic sensitivity of 100% and specificity of 62%. By replacing the less specific markers ferritin and fibrinogen in the 2016 sJIA-MAS classification criteria with new cutoff values, the revised criteria for classifying AOSD-MAS had a notable increased specificity of 86%. Conclusion: Secondary MAS commonly occurs in the early stages following the diagnosis of SLE and AOSD. There are notable variations in laboratory indicators among different underlying diseases, which may lead to misdiagnosis or missed diagnosis when using uniform classification criteria for MAS. The 2016 sJIA-MAS classification criteria exhibit high sensitivity but low specificity in diagnosing AOSD-MAS. Modification of the criteria can enhance its specificity.

Key words: Macrophage activation syndrome, Hemophagocytic lymphohistiocytosis, Systemic lupus erythematosus, Adult-onset Still's disease, Diagnosis

CLC Number: 

  • R593.2

Table 1

Demographic, clinical and laboratory characteristics of HLH patients"

Items AOSD-MAS (n=24) SLE-MAS (n=24) LYM-HLH (n=20)
Epidemiological features
  Female 21/24 (87.5) 20/24 (83.3) 9/20 (45.0)*#
  Age at diagnosis of HLH/years 34.7±15.2 40.0±15.2 49.1±20.0*
  Age at diagnosis of AD or LYM/years 33.0±16.9 38.5±16.5 48.3±20.2*
  Disease duration before HLH/months 22.7±66.9 21.4±43.0 11.3±26.9
Clinical and laboratory characteristics
  Fever (>38.5 ℃) 24/24 (100.0) 23/24 (95.8) 20/20 (100.0)
  Splenomegaly 18/24 (75.0) 13/24 (54.2) 15/20 (75.0)
  Hepatomegaly 1/24 (4.2) 4/24 (16.7) 5/20 (25.0)
  Lymphadenopathy 9/24 (37.5) 10/24 (41.7) 13/20 (65.0)
  Neurological involvement 4/24 (16.7) 3/24 (12.5) 7/20 (35.0)
  Disseminated intravascular coagulation 7/24 (29.2) 1/24 (4.2) 1/20 (5.0)
Cytopenia
  HB < 90 g/L 17/24 (70.8) 20/24 (83.3) 16/20 (80.0)
  PLT < 100×109/L 16/24 (66.7) 22/24 (91.7) 20/20 (100.0)*
  NE < 1×109/L 10/23 (43.5) 15/22 (68.2) 13/19 (68.4)
Hyperferritinemia (SF>500 μg/L) 24/24 (100.0) 23/24 (95.8) 18/19 (94.7)
Hypofibrinogenemia (FIBC < 1.5 g/L) 15/24 (62.5) 12/23 (52.2) 16/20 (80.0)
Hypertriglyceridemia (TG≥3 mmol/L) 14/24 (58.3) 13/23 (56.5) 10/10 (100.0)*#
LDH>250 U/L 23/24 (95.8) 24/24 (100.0) 18/20 (90.0)
Elevated aminotransferases
  ALT>40 U/L 23/24 (95.8) 15/23 (65.2)* 15/20 (75.0)
  AST>40 U/L 23/24 (95.8) 19/23 (82.6) 16/20 (80.0)
Hypoalbuminemia (ALB < 40 g/L) 23/24 (95.8) 24/24 (100.0) 19/20 (95.0)
Elevated ESR (>20 mm/h) 14/23 (60.7) 22/24 (91.7)* 19/20 (95.0)*
Elevated CRP(>8 mg/dL) 23/24 (95.8) 20/24 (83.3) 18/20 (90.0)
Hemophagocytosis in bone marrow 12/23 (52.2) 13/24 (54.2) 8/18 (44.4)
Low NK cell activity 8/21 (38.1) 9/17 (52.9) 6/10 (60.0)
Serum soluble CD25 receptor≥2 400 U/mL 16/17 (94.1) 14/17 (82.4) 9/10 (90.0)

Figure 1

Distribution of disease course in SLE and AOSD when MAS occurs AD, autoimmune disease; AOSD, adult-onset Still's disease; SLE, systemic lupus erythematosus; MAS, macrophage syndrome."

Table 2

Comparison of laboratory data in patients with HLH secondary to different diseases"

Items SLE (n=50) AOSD (n=50) SLE-MAS (n=24) AOSD-MAS (n=24) LYM-HLH (n=20)
WBC/(×109/L) 5.2
(1.0, 12.8)		 15.1
(4.9, 38.0)*#		 2.1
(0.2, 13.4)*		 3.8
(0.3, 27.0)		 1.7
(0.1, 6.4)
NE/(×109/L) 3.4
(0.7, 8.6)		 12.6
(3.3, 35.1)*#		 1.2
(0, 7.4)*		 2.6
(0, 24.2)		 1.1
(0, 5.5)
HB/(g/L) 107.8
(46.0, 180.0)		 107.3
(84.0, 129.0)#		 70.5
(40.0, 104.2)*#		 82.5
(49.0, 122.0)△		 70.4
(47.0, 136.0)
PLT/(×109/L) 155.8
(5.0, 381.0)		 305.0
(84.0, 576.0)*#		 42.8
(2.0, 134.0)*#△		 88.4
(7.0, 296.0)△		 23.6
(2.0, 90.0)
ESR/(mm/h) 31.8
(3.0, 92.0)		 72.3
(1.0, 133.0)*#		 66.6
(7.0, 120.0)*#		 32.0
(2.0, 78.0)		 44.6
(3.0, 129.0)
CRP/(mg/dL) 9.6
(0.3, 50.2)		 89.9
(4.0, 339.0)*		 60.4
(2.3, 364.0)*		 67.8
(7.5, 272.0)		 77.9
(3.0, 211.0)
ALT/(U/L) 33.0
(5.0, 215.0)		 19.8
(5.0, 73.0)*#		 109.4
(5.0, 619.0)*#		 715.8
(28.0, 3 550.0)△		 132.2
(11.0, 286.0)
AST/(U/L) 36.4
(9.0, 477.0)		 58.1
(11.0, 873.0)#		 308.5
(8.0, 1 424.0)*		 682.0
(14.0, 2 174.0)△		 203.5
(13.0, 665.0)
LDH/(U/L) 233.8
(120.0, 867.0)		 421.8
(140.0, 1 269.0)*#		 930.3
(360.0, 2 185.0)*#		 1 814.1
(244.0, 5 099.0)		 1 934.7
(170.0, 8 517.0)
TG/(mmol/L) 1.9
(0.4, 6.9)		 1.4
(0.7, 2.6)*#		 4.0
(1.4, 10.7)*		 3.2
(1.3, 5.8)△		 4.3
(1.0, 9.6)
ALB/(g/L) 34.9
(17.2, 46.8)		 33.1
(20.4, 41.0)*#		 24.6
(16.3, 34.2)*#		 29.3
(20.0, 40.0)△		 26.0
(19.0, 41.0)
FIBC/(mg/dL) 292.2
(123.0, 465.0)		 348.8
(178.0, 737.0)*#		 165.1
(26.0, 436.0)*		 139.0
(55.0, 307.0)		 129.6
(55.0, 349.0)
SF/(μg/L) 308.0
(11.0, 1 665.0)		 5 214.6
(522.0, 21 133.0)*#		 10 968.8
(455.0, 83 039.0)*#		 37 098.8
(2 000.0, 100 000.0)△		 18 364.7
(101.0, 63 917.0)

Table 3

Significant laboratory indicators and their cutoff values for the diagnosis of SLE-MAS"

Items AUC Cutoff value Sensitivity Specificity
SF 0.983 ≥1 010 μg/L 0.95 0.96
LDH 0.973 ≥359 U/L 0.90 1.00
AST 0.898 ≥33.5 U/L 0.82 0.96
PLT 0.887 ≤93.5×109/L 0.86 0.92
WBC 0.869 ≤2.5×109/L 0.86 0.79
NE 0.864 ≤1.6×109/L 0.84 0.83
HB 0.859 ≤85 g/L 0.82 0.83
FIBC 0.857 ≤183.5 mg/dL 0.94 0.71
CRP 0.836 ≥23.5 mg/dL 0.90 0.63
ALB 0.830 ≤29.7 g/L 0.82 0.79
TG 0.823 ≥1.9 mmol/L 0.58 0.96
ALT 0.807 ≥30.5 U/L 0.72 0.83
ESR 0.804 ≥57.0 mm/h 0.86 0.63

Table 4

Significant laboratory indicators and their cutoff values for the diagnosis of AOSD-MAS"

Items AUC Cutoff value Sensitivity Specificity
FIBC 0.988 ≤225.5 mg/dL 0.98 0.92
TG 0.953 ≥2.0 mmol/L 0.84 0.92
WBC 0.948 ≤6.3×109/L 0.96 0.92
NE 0.946 ≤4.3×109/L 0.98 0.92
AST 0.943 ≥110.0 U/L 0.97 0.96
PLT 0.941 ≤164.5×109/L 0.94 0.88
ALT 0.938 ≥74.5 U/L 0.86 0.92
LDH 0.915 ≥667.5 U/L 0.90 0.83
HB 0.900 ≤97.5 g/L 0.76 0.92
ESR 0.862 ≥59.5 mm/h 0.64 0.92
SF 0.833 ≥13 283.5 μg/L 0.88 0.63
ALB 0.758 ≤31.7 g/L 0.70 0.79
CRP 0.636 ≥54.9 mg/dL 0.72 0.58

Table 5

Application of the 2016 sJIA-MAS criteria in AOSD-MAS patients"

Items AOSD-MAS, n(%) AOSD, n(%) Sensitivity/% Specificity/% PPV/% NPV/%
Fulfilling criteria 24 (100.0) 19 (38.0) 100.0 62.0 56.0 100.0
SF>684 μg/L 24 (100.0) 46 (92.0) 100.0 8.0 34.0 100.0
PLT≤181×109/L 21 (87.5) 9 (18.0) 87.5 82.0 70.0 93.0
AST>48 U/L 23 (95.8) 15 (30.0) 95.8 70.0 61.0 97.0
TG>156 mg/dL 22 (91.7) 9 (18.0) 91.7 82.0 71.0 95.0
FIBC≤360 mg/dL 24 (100.0) 32 (64.0) 100.0 36.0 43.0 100.0

Table 6

Application of the revised 2016 sJIA-MAS criteria in AOSD-MAS patients"

Items AOSD-MAS, n(%) AOSD, n(%) Sensitivity/% Specificity/% PPV/% NPV/%
Fulfilling criteria 24 (100.0) 7 (14.0) 100.0 86.0 77.1 100.0
SF>2 000 μg/L 24 (100.0) 32 (64.0) 100.0 36.0 42.9 100.0
PLT≤181×109/L 21 (87.5) 9 (18.0) 87.5 82.0 70.0 93.0
AST>48 U/L 23 (95.8) 15 (30.0) 95.8 70.0 61.0 97.0
TG>156 mg/dL 22 (91.7) 9 (18.0) 91.7 82.0 71.0 95.0
FIBC≤225.5 mg/dL 23 (95.8) 1 (2.0) 95.8 98.0 95.8 98.0
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