Clinical characteristics and relevant factors of rheumatoid arthritis patients with anemia of chronic disease

Hui WEI; Jingfeng ZHANG; Zhongqiang YAO; Jinxia ZHAO

doi:10.19723/j.issn.1671-167X.2026.02.013

Journal of Peking University(Health Sciences) >

2026 , Vol. 58 >Issue 2: 307 - 312

DOI: https://doi.org/10.19723/j.issn.1671-167X.2026.02.013

Clinical characteristics and relevant factors of rheumatoid arthritis patients with anemia of chronic disease

Hui WEI ,
Jingfeng ZHANG ,
Zhongqiang YAO ,
Jinxia ZHAO ^,*

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Department of Rheumatology and Immunology, Peking University Third Hospital, Beijing 100191, China

ZHAO Jinxia, e-mail, zhao-jinxia@163.com

Received date: 2023-08-29

Online published: 2025-10-28

Supported by

the Peking University Third Hospital Clinical Trial Construction Project(BYSYDL2022017)

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Abstract

Objective: To analyze the related factors of rheumatoid arthritis (RA) patients with anemia of chronic disease (ACD) and to guide the clinical diagnosis and treatment. Methods: A retrospective study was used to analyze the patients admitted to Department of Rheumatology and Immunology in Peking University Third Hospital from January 2013 to December 2018. Clinical data (including general conditions, joint lesions, extra-articular manifestations, and comorbidities), laboratory examinations, and treatment were collected to analyze the differences in clinical characteristics between group RA with ACD (RA-A) and group RA without ACD (RA-nA). Univariate and multivariate Logistic regression analysis was conducted to screen for relevant factors of RA with ACD. Results: A total of 468 RA patients were included, including 194 cases (41.5%) in RA-A group and 274 cases (58.5%) in RA-nA group. There were no significant differences in age, gender, onset age, or course of disease between the two groups (P>0.05). The RA-A group had more joint swelling [13 (2, 14) vs. 10 (2, 11)], more tenderness [10 (2, 12) vs. 7 (2, 10)], and higher 28 joint disease activity scores (DAS28) [DAS28-CRP (C-reactive protein): 5.2±1.4 vs. 4.6±1.5; DAS28-ESR (erythrocyte sedimentation rate): 5.9±1.5 vs. 5.1±1.8] compared with the RA-nA group (P < 0.05). The incidence of pleural effusion (4.6% vs. 1.1%) and venous thrombosis (5.7% vs. 1.5%) were higher in RA-A group (P < 0.05). The platelet count, neutrophil/lymphocyte ratio, platelet/lymphocyte ratio, ESR, CRP, immunoglobulin G (IgG) in RA-A group were significantly higher than those in RA-nA group (P < 0.05). Elevated ESR and CRP levels, DAS28 > 5.1 were relevant factors for anemia in the RA patients. Conclusion: RA patients with ACD had more severe joint involvement, higher inflammatory indicators, and more active conditions, making them more prone to pleural effusion and venous thrombosis. High disease activity, high inflammatory status, and venous thrombosis were risk factors for RA with ACD.

Key words： Rheumatoid arthritis; Anemia; Chronic disease; Risk factors

Cite this article

Hui WEI , Jingfeng ZHANG , Zhongqiang YAO , Jinxia ZHAO . Clinical characteristics and relevant factors of rheumatoid arthritis patients with anemia of chronic disease[J]. Journal of Peking University(Health Sciences), 2026 , 58(2) : 307 -312 . DOI: 10.19723/j.issn.1671-167X.2026.02.013

类风湿关节炎(rheumatoid arthritis，RA)是一种以对称性多关节炎为特征的慢性、进行性、全身多系统受累的自身免疫性疾病。贫血是RA常见的关节外表现，发病率约为30%~70%^[1]，其中慢性病贫血(anemia of chronic disease，ACD)是最常见的类型，但未得到临床医生的足够重视。贫血会加重RA的全身症状及关节破坏程度^[2]，亦可能与RA的疾病活动度相关，可以预测RA早期关节损伤^[3]。关于RA合并ACD的发病机制及相关因素目前并不完全清楚，RA患者血清中的肿瘤坏死因子α (tumor necrosis factor-α，TNF-α)、干扰素γ(interferon- γ，IFN-γ)、白细胞介素1(interleukin-1，IL-1)、IL-6等多种细胞因子增高，不仅参与关节病变，也是引起ACD的重要因素。多种细胞因子参与并影响了红细胞生成，包括促红细胞生成素的产生减少、铁促单核巨噬细胞释放障碍导致的铁利用障碍、抑制红系祖细胞从而促进早期红细胞凋亡等^[4-6]。本研究通过对RA合并ACD患者的临床特点进行回顾，分析RA合并ACD的危险因素，并指导临床合理诊疗。

1 资料与方法

1.1 研究对象

选取2013年1月至2018年12月于北京大学第三医院风湿免疫科住院的RA患者。入选标准：(1)发病年龄>18岁；(2)符合1987年美国风湿病学会(American College of Rheumatology，ACR)^[7]或2010年ACR/欧洲抗风湿病联盟(European League Against Rheumatism，EULAR)RA分类标准^[8]；(3)临床资料完整。排除标准：(1)合并感染；(2)合并其他风湿免疫病者(继发干燥综合征除外)；(3)缺铁性贫血和巨幼细胞性贫血等营养性贫血、消化道出血所致贫血、自身免疫性溶血性贫血等其他病因明确的贫血。本研究获得北京大学第三医院医学科学研究伦理委员会审批通过(IRB00006761-M2023089)。

1.2 研究方法

收集患者的如下信息：(1)一般情况，包括年龄、性别、发病年龄和病程；(2)关节病变情况，包括关节压痛数和肿胀数、28个关节疾病活动度评分(28 joint disease activity scores，DAS28)、疼痛视觉模拟评分(visual analogue scale，VAS)；(3)关节外表现及合并症情况，包括类风湿血管炎、类风湿结节、周围神经病、心包炎、胸腔积液、间质性肺病、继发干燥综合征、静脉血栓形成、贫血、高血压、糖尿病、高脂血症、冠心病、脑血管病、恶性肿瘤病史、消化性溃疡病史；(4)实验室检查结果，包括血常规、类风湿因子(rheumatoid factor，RF)、抗环瓜氨酸多肽(cyclic citrullinated peptide，CCP)抗体、红细胞沉降率(erythrocyte sedimentation rate，ESR)、C反应蛋白(C-reactive protein，CRP)、免疫球蛋白G(immunoglobulin G，IgG)、IgA、IgM，同时收集贫血患者的红细胞压积(hematocrit，HCT)、红细胞体积(mean corpuscular volume，MCV)、平均血红蛋白量(mean corpuscular hemoglobin，MCH)、平均血红蛋白浓度(mean corpuscular hemoglobin concentration，MCHC)、铁蛋白造血原料相关指标。同一患者若多次住院治疗，纳入第一次住院的资料进行分析。

1.3 统计学方法

采用SPSS 20.0统计软件进行数据分析。符合正态分布的计量资料以${\bar x}$±s表示，组间比较采用t检验；非正态分布的计量资料使用M(P₂₅，P₇₅)描述，组间比较采用Wilcoxon秩和检验；计数资料用例数(百分比)表示，两组间率的比较采用χ²检验或Fisher精确概率法。采用多分类及二分类Logistic回归分析合并贫血的相关影响因素。P < 0.05为差异有统计学意义。

2 结果

2.1 患者的一般情况

本研究共纳入468例RA患者，平均年龄(59±14)岁(19~87岁)。合并ACD的RA患者(RA-A组)有194例(41.5%)，包括轻度贫血27例、中度贫血158例、重度贫血9例，不合并ACD的RA患者(RA-nA组)274例(58.5%)，两组患者在年龄、性别、发病年龄、病程方面差异均无统计学意义(P>0.05，表 1)。与正常参考值相比，RA-A组的HCT下降、正常和上升分别有158例(81.4%)、36例(18.6%)和0例(0%)，MCV下降、正常和上升分别有29例(14.9%)、160例(82.5%)和5例(2.6%)，MCH下降、正常和上升分别有67例(34.5%)、116例(59.8%)和11例(5.7%)，MCHC下降、正常和上升分别有118例(60.8%)、64例(33.0%)和12例(6.2%)，具体数值、红细胞参数、造血原料指标与实验室正常参考值比较结果详见表 2。

表1 RA-A组和RA-nA组患者的一般情况比较

Table 1 Comparison of general conditions between group RA-A and RA-nA

Items	RA-A (n=194)	RA-nA (n=274)	χ²/t	P
Age/years, ${\bar x}$±s	58±14	59±15	-0.371	0.714
Male, n(%)	58 (29.9)	64 (23.4)	2.520	0.112
Onset age/years, ${\bar x}$±s	49±15	51±16	-1.093	0.278
Course of disease/years, M (P₂₅, P₇₅)	9 (1, 12)	8 (1, 10)	1.209	0.245

RA-A, rheumatoid arthritis (RA) with anemia of chronic disease; RA-nA, RA without anemia of chronic disease.

表2 RA-A组患者的红细胞参数及造血原料数值(n=194)

Table 2 Erythrocyte parameters and hematopoietic raw materials of group RA-A (n=194)

Items	RA-A, ${\bar x}$±s	Reference (range)
HCT	0.37±0.12	0.35-0.45
MCV/fL	80±11	82-100
MCH/pg	28±5	27-34
MCHC/(g/L)	344±17	316-354
SF/(μmol/L)	45.4±23.6	7.8-32.2
Ferritin/(μg/L)	168±72	13-150
TIBC/%	36.7±2.8	37.5-60.7
UIBC/%	38.2±7.9	35-48
Falate/(nmol/L)	36.1±23.5	7.0-46.4
Vitamin B₁₂/(μmol/L)	403±146	157-602

RA-A, rheumatoid arthritis (RA) with anemia of chronic disease; HCT, hematocrit; MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration; SF, serum ferritin; TIBC, total iron binding capacity; UIBC, unsatura-ted iron binding capacity.

2.2 RA-A组和RA-nA组患者的关节病变情况

RA-A组的关节压痛数及关节肿胀数均大于RA-nA组，DAS28-CRP评分和DAS28-ESR评分亦大于RA-nA组[(5.2±1.4)分vs. (4.6±1.5)分，(5.9±1.5)分vs. (5.1±1.8)分]，差异均有统计学意义(P < 0.001)，但两组VAS评分差异无统计学意义(表 3)。

表3 RA-A组和RA-nA组患者的关节病变比较

Table 3 Comparison of joint conditions between group RA-A and RA-nA

Items	RA-A (n=194)	RA-nA (n=274)	t/Z	P
Swelling, M (P₂₅, P₇₅)	13 (2, 14)	10 (2, 11)	-3.501	< 0.001
Tenderness, M (P₂₅, P₇₅)	10 (2, 12)	7 (2, 10)	-3.129	< 0.001
DAS28-CRP, ${\bar x}$±s	5.2±1.4	4.6±1.5	-4.634	< 0.001
DAS28-ESR, ${\bar x}$±s	5.9±1.5	5.1±1.8	-5.940	< 0.001
VAS, ${\bar x}$±s	4.7±2.1	4.5±2.6	6.793	0.787

RA-A, rheumatoid arthritis (RA) with anemia of chronic disease; RA-nA, RA without anemia of chronic disease; DAS28, 28 joint disease activity scores; CRP, C-reactive protein; ESR, erythrocyte sedimentation rate; VAS, visual analogue scale.

2.3 RA-A组和RA-nA组患者的关节外表现及合并症情况

RA-A组和RA-nA组患者的关节外表现，除胸腔积液比例差异有统计学意义外(4.6% vs. 1.1%，P=0.017)，类风湿血管炎、类风湿结节、周围神经病、心包炎、间质性肺病的比例差异均无统计学意义(P>0.05，表 4)。RA-A组和RA-nA组患者的合并症，除静脉血栓形成比例差异有统计学意义外(5.7% vs. 1.5%， χ²=6.490，P=0.011)，继发干燥综合征、心脑血管疾病、糖尿病、恶性肿瘤、消化性溃疡的比例差异均无统计学意义(P>0.05，表 4)。

表4 RA-A组和RA-nA组患者的关节外表现和合并症情况比较

Table 4 Comparison of extra-articular manifestations and complications between group RA-A and RA-nA

Items	RA-A (n=194)	RA-nA (n=274)	χ²	P
Extra-articular manifestations
Vasculitis	2 (1.0)	1 (0.4)	0.791	0.374
Rheumatoid nodules	11 (5.7)	13 (4.7)	0.200	0.655
Peripheral neuropathy	5 (2.6)	4 (1.5)	0.752	0.386
Pericarditis	4 (2.1)	5 (1.8)	0.034	0.854
Pleural effusion	9 (4.6)	3 (1.1)	5.711	0.017
ILD	43 (22.2)	46 (16.8)	2.132	0.144
Complications
Venous thrombosis	11 (5.7)	4 (1.5)	6.490	0.011
SS	27 (13.9)	25 (9.1)	2.642	0.104
CVD and CBD	26 (13.4)	30 (10.9)	0.649	0.421
Diabetes	32 (16.5)	53 (19.3)	0.620	0.431
Tumor	8 (4.1)	5 (1.8)	2.223	0.136
Peptic ulcer	14 (7.2)	17 (6.2)	0.188	0.664

Data are expressed as n(%). RA-A, rheumatoid arthritis (RA) with anemia of chronic disease; RA-nA, RA without anemia of chronic disease; ILD, interstitial lung disease; SS, Sjögren syndrome; CVD, cardiovascular diseases; CBD, cerebrovascular diseases.

2.4 RA-A组和RA-nA组患者的实验室检查结果

RA-A组患者血红蛋白、淋巴细胞计数明显低于RA-nA组，血小板计数明显高于RA-nA组(P < 0.05)，但白细胞计数、白蛋白水平在两组间差异无统计学意义；此外，RA-A组患者中性粒细胞/淋巴细胞、血小板/淋巴细胞均明显高于RA-nA组，差异有统计学意义(P < 0.05，表 5)。RA-A组患者ESR、CRP、IgG均明显高于RA-nA组(P < 0.05)，但RF、抗CCP抗体的阳性率及IgA和IgM水平在两组间差异无统计学意义(表 5)。

表5 RA-A组和RA-nA组患者的实验室检查结果比较

Table 5 Comparison of laboratory results between group RA-A and RA-nA

Items	RA-A (n=194)	RA-nA (n=274)	t/χ²	P
White cell/(×10⁹/L), ${\bar x}$±s	6.7±2.3	7.1±2.9	1.060	0.050
Hemoglobin/(g/L), ${\bar x}$±s	99.4±13.5	121.6±15.2	23.628	< 0.001
Platelet/(×10⁹/L), ${\bar x}$±s	299.2±111.6	264.1±96.2	-4.758	< 0.001
Neutrophils/(×10⁹/L), ${\bar x}$±s	4.6±2.1	4.7±2.5	0.373	0.435
Lymphocyte/(×10⁹/L)，${\bar x}$±s	1.5±0.6	1.7±0.6	3.658	< 0.001
NLR, ${\bar x}$±s	3.6±2.8	3.1±1.8	-2.437	0.018
PLR, ${\bar x}$±s	232.5±132.1	173.9±88.6	-6.444	< 0.001
Albumin/(g/L), ${\bar x}$±s	27.6±8.9	28.3±9.2	0.492	0.398
RF positive, n(%)	145 (74.7)	201 (73.4)	0.113	0.737
Anti-CCP positive, n(%)	139 (71.6)	216 (78.8)	3.199	0.074
ESR/(mm/h), ${\bar x}$±s	62.1±29.0	37.6±27.9	-11.358	< 0.001
CRP/(mg/dL), ${\bar x}$±s	5.4±4.6	2.9±1.9	-7.498	< 0.001
IgG/(×10⁹/L), ${\bar x}$±s	15.7±5.2	13.9±4.4	-5.860	< 0.001
IgM/(×10⁹/L), ${\bar x}$±s	3.3±1.6	3.3±2.2	-0.595	0.863
IgA/(×10⁹/L), ${\bar x}$±s	1.4±1.3	1.4±0.9	-0.669	0.391

RA-A, rheumatoid arthritis (RA) with anemia of chronic disease; RA-nA, RA without anemia of chronic disease; NLR, the ratio of neutrophils and lymphocyte; PLR, the ratio of platelet and lymphocyte; RF, rheumatoid factor; CCP, cyclic citrullinated peptide; ESR, erythrocyte sedimentation rate; CRP, C-creative protein; IgG, immunoglobulin G; IgM, immunoglobulin M; IgA, immunoglobulin A.

2.5 RA-A和RA-nA组患者的治疗情况

RA-A组患者非甾体抗炎药、改善病情的抗风湿病药物、激素、生物制剂使用率分别为38.1%(74例)、94.8%(184例)、56.7%(110例)、8.2%(16例)，RA-nA组则分别为35.4%(97例)、83.2%(228例)、38.3%(105例)、5.8%(16例)，两组间治疗药物选择差异无统计学意义(P>0.05)。

2.6 RA患者发生ACD的危险因素分析

单因素Logistic回归分析表明，胸腔积液、静脉血栓形成、ESR>20 mm/h、CRP>3 mg/dL、关节肿胀及压痛数大于5个、DAS28评分>5.1与ACD相关(表 6)。将以上因素纳入非条件多因素Logistic回归模型进行进一步分析，发现ESR>20 mm/h、CRP>3 mg/dL、DAS28评分>5.1是RA患者发生ACD的独立危险因素(表 7)。

表6 单因素Logistic回归分析RA患者发生ACD的危险因素

Table 6 Univariate Logistic regression analysis for the risk factors of RA with ACD

Risk factors	B	SE	Wald	P	OR	95%CI
Pleural effusion	1.388	0.673	4.249	0.039	4.005	1.071-14.981
Venous thrombosis	1.307	0.591	4.884	0.027	3.694	1.159-11.770
ESR>20 mm/h	1.474	0.255	33.355	< 0.001	4.366	2.647-7.199
CRP>3 mg/dL	1.177	0.194	36.750	< 0.001	3.245	2.218-4.747
Joint tenderness>5	0.544	0.200	7.428	0.006	1.724	1.165-2.550
Joint swelling>5	0.480	0.185	6.736	0.009	1.617	1.125-2.324
DAS28>5.1	1.411	0.288	24.041	< 0.001	4.100	2.333-7.206
Course of disease>10 years	-0.147	0.185	0.631	0.427	0.863	0.600-1.241

RA, rheumatoid arthritis; ACD, anemia of chronic disease; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein; DAS28, 28 joint disease activity scores.

表7 多因素Logistic回归分析RA患者发生ACD的危险因素

Table 7 Multivariate Logistic regression analysis for the risk factors of RA with ACD

Risk factors	B	SE	Wald	P	OR	95%CI
Pleural effusion	1.323	0.748	3.131	0.077	3.755	0.867-16.260
Venous thrombosis	1.166	0.639	43.329	0.048	3.210	1.317-11.233
ESR>20 mm/h	1.131	0.306	13.620	< 0.001	3.099	1.700-5.649
CRP>3 mg/dL	0.712	0.216	10.830	0.001	2.037	1.334-3.113
Joint tenderness	0.096	0.252	0.145	0.703	1.101	0.672-1.802
Joint swelling	0.162	0.223	0.525	0.469	1.175	0.759-1.819
DAS28＞5.1	1.007	0.445	5.121	0.024	2.738	1.144-6.552

Abbreviations as in Table 6.

3 讨论

贫血是RA常见的关节外表现之一，其中ACD是RA患者贫血最常见的原因，往往与病情活动相关。RA患者发生ACD的可能机制包括：骨髓对贫血的代偿不足、铁释放和利用障碍、氮氧化物通路异常抑制红系祖细胞及造血干细胞的增殖并诱导凋亡、多种细胞因子通过复杂的相互作用网络抑制骨髓红系造血等^{[1, 9-11]}。

既往关于RA患者合并ACD的研究报道中，轻度贫血患病率为33%~60%，未见重度和极重度贫血的报道^[1]。本研究中RA合并ACD的患者也主要表现为轻中度贫血，这可能与RA患者的贫血机制主要是骨髓对促红细胞生成素反应减弱导致骨髓代偿不足，而非骨髓严重受抑制有关。有研究表明，IL-6可使肝细胞合成铁调素增多，进而减少肠道对铁的吸收并增加网状内皮系统对铁的代谢调节^[12]。本研究有9例重度贫血，推测可能与病情活动相关。

RA患者可由炎症细胞因子的释放增加而引发贫血^[13-15]。Singh等^[16]观察到血红蛋白水平的降低与RA的疾病活动度高度相关；Chen等^[3]的回顾性研究也发现，合并ACD的RA患者具有较高的疾病活动度，关节结构损伤和关节功能恶化更严重。本研究中，RA-A组患者的血小板计数、ESR及CRP水平均明显高于RA-nA组，反映了患者疾病活动度更高。NLR与PLR作为新型的炎症标志物，可协助评价RA患者疾病活动度^[17-18]，本研究中RA-A组患者的NLR与PLR均明显高于RA-nA组。总体来说，RA合并ACD的患者血清学炎症指标更高。

血红蛋白水平与DAS28评分、骨侵蚀评分呈负相关，即血红蛋白水平与疾病活动度呈负相关^[19]。本研究发现，与RA-nA组相比，RA-A组患者关节压痛数、关节肿胀数、DAS28评分均明显增高，提示合并ACD的RA患者疾病活动度更高，受累关节数更多，且关节症状更重。虽然两组患者VAS评分差异无统计学意义，但合并ACD者VAS评分更高，关节症状更重。此外，Logistic回归分析也表明，ESR>20 mm/h、CRP>3 mg/dL、DAS28评分＞5.1是RA患者发生ACD的独立危险因素。

本研究中，RA-A组和RA-nA组患者在关节外表现和合并症方面也有差异：RA-A组胸腔积液发生率明显高于RA-nA组，差异有统计学意义；虽然RA-A组类风湿血管炎、类风湿结节、周围神经病、心包炎、间质性肺病发生率高于RA-nA组，但两组间差异并没有统计学意义。结合两组患者间白蛋白水平无明显差异，推测胸腔积液的发生主要与高炎症反应有关，提示对于炎症指标高的RA患者需要加强对胸腔积液的关注。此外，本研究中RA-A组出现静脉血栓的比例明显高于RA-nA组，考虑到合并ACD的RA患者炎症反应更强，推测这可能是导致其更容易出现静脉血栓的原因。同时，尽管本研究发现两组患者合并脑血管病、冠心病、动脉粥样硬化等心脑血管疾病的比例差异无统计学意义，但RA-A组心脑血管疾病的占比更高，提示临床上需要警惕RA合并ACD患者发生血栓事件。

本研究还发现RA-A组与RA-nA组患者的病程和发病年龄差异并无统计学意义，且单因素分析表明，病程超过10年并非RA患者发生ACD的危险因素，与既往研究^[20]结果一致，未来可能还需要更大样本量的前瞻性队列研究进一步验证这一结论，并探讨其可能的发生机制。

综上所述，RA合并ACD患者的关节受累数更多，炎症指标更高，疾病活动度更高，更容易出现胸腔积液和静脉血栓。高疾病活动度、高炎症状态、静脉血栓是RA合并ACD的危险因素，提示在临床诊疗过程中，要特别注意RA合并ACD患者的关节外表现和合并症，特别是血栓性疾病的筛查。

利益冲突 所有作者均声明不存在利益冲突。

作者贡献声明 魏慧：参与设计研究方案，收集、分析、整理数据，撰写论文；张警丰、姚中强：收集、分析、整理数据；赵金霞：提出研究思路，总体把关和审定论文。所有作者均参与论文修改，并对最终文稿进行审读和确认。

References

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