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中华肾病研究电子杂志

中华肾病研究电子杂志 ›› 2022, Vol. 11 ›› Issue (04) : 181 -190. doi: 10.3877/cma.j.issn.2095-3216.2022.04.001

论著

青少年特发性膜性肾病的临床和病理特点及其转归影响因素
王琳娜1, 郭存霞2, 苗艳3, 田素革3, 乔东鸽4, 阎磊3, 刘冰3, 朱清3, 邵凤民3, 陈香美5,†()   
  1. 1. 450003　河南省人民医院　郑州大学人民医院肾内科；450002　河南省中医院（河南中医药大学第二附属医院）肾病科
    2. 450002　河南省中医院（河南中医药大学第二附属医院）肾病科
    3. 450003　河南省人民医院　郑州大学人民医院肾内科
    4. 450099　河南中医药大学第一附属医院
    5. 100853　北京，解放军总医院第一医学中心肾脏病医学部、解放军肾脏病研究所、肾脏疾病国家重点实验室、国家慢性肾病临床医学研究中心、肾脏疾病研究北京市重点实验室
  • 收稿日期:2021-09-27 出版日期:2022-08-28
  • 通信作者: 陈香美
  • 基金资助:
    中国博士后科学基金面上项目(2015M582858); 河南省基础与前沿研究计划(162300410243); 河南省中医药科学研究专项课题(20-21ZY2050)

Clinical and pathological features of adolescent idiopathic membranous nephropathy and its outcome-affecting factors

Linna Wang1, Cunxia Guo2, Yan Miao3, Suge Tian3, Dongge Qiao4, Lei Yan3, Bing Liu3, Qing Zhu3, Fengmin Shao3, Xiangmei Chen5,†()   

  1. 1. Department of Nephrology, Henan Provincial People′s Hospital, People′s Hospital of Zhengzhou University, Zhengzhou 450003; Department of Nephrology, Henan Provincial Hospital of Traditional Chinese Medicine, Second Affiliated Hospital of Henan University of Traditional Chinese Medicine, Zhengzhou 450002
    2. Department of Nephrology, Henan Provincial Hospital of Traditional Chinese Medicine, Second Affiliated Hospital of Henan University of Traditional Chinese Medicine, Zhengzhou 450002
    3. Department of Nephrology, Henan Provincial People′s Hospital, People′s Hospital of Zhengzhou University, Zhengzhou 450003
    4. First Affiliated Hospital of Henan University of Traditional Chinese Medicine, Zhengzhou 450099; Henan Province
    5. Department of Nephrology, First Medical Center of Chinese PLA General Hospital, Chinese PLA Institute of Nephrology, State Key Laboratory of Kidney Diseases, National Clinical Research Center for Kidney Diseases, Beijing Key Laboratory of Kidney Diseases, Beijing 100853; China
  • Received:2021-09-27 Published:2022-08-28
  • Corresponding author: Xiangmei Chen
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引用本文：

王琳娜, 郭存霞, 苗艳, 田素革, 乔东鸽, 阎磊, 刘冰, 朱清, 邵凤民, 陈香美. 青少年特发性膜性肾病的临床和病理特点及其转归影响因素[J]. 中华肾病研究电子杂志, 2022, 11(04): 181-190.

Linna Wang, Cunxia Guo, Yan Miao, Suge Tian, Dongge Qiao, Lei Yan, Bing Liu, Qing Zhu, Fengmin Shao, Xiangmei Chen. Clinical and pathological features of adolescent idiopathic membranous nephropathy and its outcome-affecting factors[J]. Chinese Journal of Kidney Disease Investigation(Electronic Edition), 2022, 11(04): 181-190.

目的

分析青少年特发性膜性肾病(IMN)的临床和病理特征、治疗及预后。

方法

回顾性分析2011年1月1日至2018年4月30日在解放军总医院肾脏病科经肾活检确诊的164例13~24岁青少年IMN患者的基本资料、实验室检查、肾活检病理、治疗方案等资料。患者分为少年组(13~18岁)60例，青年组(19~24岁)104例，以肾活检时间为起点随访6~24个月，分析不同药物治疗的有效性及预后。

结果

患者的男女比例约为1.6∶1；少年组的血尿发生率(P＝0.002)和eGFR(P＝0.002)高于青年组，而IgA(P＝0.017)和IgG(P＝0.050)水平则低于青年组。两组的临床表现均以肾病综合征为主，肾脏病理以膜性肾病Ⅱ期最多见。少年组和青年组的血清磷脂酶A2受体(PLA2R)抗体阳性率分别为44.4%和40%。平均随访时间8.5(6，24)月，两组使用他克莫司和(或)糖皮质激素治疗IMN的总缓解率均为75%。少年组和青年组的24个月总缓解率分别为85.7%和96%(χ2＝1.303，P＝0.254)，而24个月完全缓解率则分别为61.5%和79.2%(χ2＝1.329，P＝0.254)。少年组及青年组均无患者进展至终末期肾病(ESRD)。单因素Cox回归分析显示，血尿和低IgG血症(<4.0 g/L)预示IMN患者较低的24个月总缓解率。多因素Cox回归分析发现，血尿(HR＝0.345，95%CI: 0.035~0.188，P＝0.005)和IgG<4.0 g/L(HR＝0.278，95%CI: 0.034~0.434，P＝0.023)均为24个月总缓解率的独立危险因素，而且IgG<4.0 g/L(HR＝3.538，95%CI: 1.193~10.499，P＝0.028)还是24个月完全缓解率的独立危险因素。接受者操作特征(ROC)曲线下面积(AUC)也证实，IgG<3.48 g/L(AUC＝0.765，特异性69.4%，灵敏度88.7%，P＝0.001)是预测24个月不缓解的最佳临界点。

结论

少年组IMN患者的临床表现较青年组严重；随访24个月时青少年IMN患者的转归良好；血尿和低IgG血症是青少年IMN缓解率的独立危险因素。

关键词: 膜性肾病, 青少年, 临床病理, 治疗, 预后
Objective

To analyze the clinical and pathological features, treatment, and prognosis of adolescent idiopathic membranous nephropathy (IMN).

Methods

A retrospective analysis was performed on the basic data, laboratory tests, renal biopsy pathology, and treatment protocols, etc, of 164 adolescent IMN patients aged 13-24 years who were diagnosed by renal biopsy in the Department of Nephrology of Chinese PLA General Hospital from January 1, 2011 to April 30, 2018. The patients were divided into a juvenile group (13-18 years old) of 60 cases and a youth group (19-24 years old) of 104 cases, and followed up for 6-24 months from the time of renal biopsy, and the effectiveness of drug treatments and the prognosis were analyzed.

Results

The patients′ male to female ratio was approximately 1.6∶1. The incidence of hematuria (P=0.002) and eGFR (P=0.002) in the juvenile group were higher than those in the youth group, while the levels of IgA (P=0.017) and IgG (P=0.050) were lower in the juvenile group than in the youth group. The clinical manifestations of both groups were mainly those of nephrotic syndrome, and the most common renal pathological feature was membranous nephropathy stage Ⅱ. The positive rate of serum anti-phospholipase A2 receptor antibody in the juvenile group and the youth group was 44.4% and 40%, respectively. The mean follow-up time of the two groups was 8.5 (6, 24) months, and the overall remission rate of IMN treated with tacrolimus and/or glucocorticoids was 75% in both groups. The 24-month overall remission rates in the juvenile group and the youth group were 85.7% and 96%, respectively (χ2=1.303, P=0.254), while the 24-month complete remission rates were 61.5% and 79.2%, respectively (χ2=1.329, P=0.254). None of the patients in the juvenile and youth groups progressed to end-stage renal disease (ESRD). Univariate Cox regression analysis showed that hematuria and hypoimmunoglobulinemia of IgG (<4.0 g/L) suggested a lower 24-month overall remission rate in the IMN patients. Multivariate Cox regression analysis found that hematuria (HR=0.345, 95%CI: 0.035-0.188, P=0.005) and IgG<4.0 g/L (HR=0.278, 95%CI: 0.034-0.434, P=0.023) were both the independent risk factors of 24-month overall remission rate. Besides, IgG<4.0 g/L (HR=3.538, 95%CI: 1.193-10.499, P=0.028) was also an independent risk factor for the 24-month complete remission rate. The area under the receiver operating characteristic (ROC) curve (AUC) also confirmed that IgG<3.48 g/L (AUC=0.765, specificity 69.4%, sensitivity 88.7%, P=0.001) was the best cut-off point for predicting the 24-month non-remission.

Conclusion

The clinical manifestations in the juvenile group were more severe than those in the youth group. The outcome of the adolescent IMN patients was good at 24 months of follow-up. Hematuria and hypoimmunoglobulinemia of IgG were independent risk factors of the remission rate of the adolescent IMN patients.

Key words: Membranous nephropathy, Adolescent, Clinicopathology, Treatment, Prognosis
表1 两组IMN基线临床特征比较
项目 所有患者 少年组(n＝60) 青少年组(n＝104) t/Z/χ2值 P值
男性[例(%)] 101(61.5) 35(58.3) 66(63.5) 0.410 0.522
年龄 19.62±3.05 16.13±1.35 21.63±1.6    
发病至肾穿时病程(月) 4.0(1.0~5.0) 2.0(0.7~4.0) 2.0(1.0~5.0) 2.656 0.103
抗PLA2R抗体阳性率 42.9% 44.4% 40% 0.046 0.831
抗PLA2R抗体滴度 28.69(6.11~73.21) 27.02(16.77~31.08) 31.5(5.72~73.21) －0.268 0.793
高血压[例(%)] 65(40.1) 23(38.3) 42(41.1) 0.067 0.796
收缩压(mmHg) 124.02±16.45 123.37±14.32 124.40±17.57 －0.380 0.704
舒张压(mmHg) 77.30±9.76 76.41±9.59 77.82±9.82 －0.884 0.378
肾病综合征[例(%)] 119(72.6) 45(75.0) 74(71.2) 0.283 0.595
血尿[例(%)] 99(60.4) 46(76.6) 59(56.7) 9.327 0.002
血红蛋白(g/L) 131.92±18.16 130.87±17.36 132.53±18.58 －0.562 0.575
血白蛋白(g/L) 25.12±6.96 24.93±6.67 25.22±7.20 －0.258 0.797
24 h尿蛋白(g) 4.76±2.94 4.86±3.24 4.69±2.77 0.336 0.738
血尿素氮(mmol/L) 4.76±5.82 5.37±9.46 4.42±1.62 0.998 0.320
血肌酐(μmol/L) 65.40±25.99 64.13±38.58 66.13±14.87 －0.473 0.637
血尿酸(μmol/L) 345.62±101.31 333.76±98.96 352.08±102.12 －1.079 0.282
胱抑素C 0.91±0.34 0.85±0.26 0.95±0.38 －1.383 0.17
NAG 51.38±43.15 48.44±40.69 53.21±45.19 －0.53 0.597
胆固醇(mmol/L) 7.23±2.42 7.14±2.24 7.27±5.54 －0.311 0.756
三酰甘油(mmol/L) 2.20±1.56 2.08±1.86 2.28±1.37 －0.753 0.452
空腹血糖(mmol/L) 4.76±0.93 4.56±0.81 4.59±0.81 －1.002 0.308
高密度脂蛋白(mmol/L) 1.49±0.81 1.60±0.77 1.43±0.84 1.123 0.264
eGFR[ml/(min·1.73 m2)] 121.29±28.75 134.08±20.85 125.77±12.38 3.195 0.002
免疫学指标(g/L)          
  IgA 1.65±0.72 1.47±0.68 1.75±0.73 －2.413 0.017
  IgG 4.53±0.25 4.00±2.13 4.83±0.27 －1.976 0.050
  IgM 1.27±0.69 1.31±0.57 1.24±0.75 0.552 0.582
  C3 1.10±0.37 1.04±0.25 1.12±0.42 －1.429 0.155
  C4 0.24±0.11 0.21±0.07 0.26±0.11 －2.737 0.007
表2 青少年IMN治疗方案比较
肾穿后治疗方案(以缓解方案为准，例) 少年组(n＝25) 青年组(n＝48) χ2值 P值
非免疫抑制治疗 1 7 0.958a 0.328
糖皮质激素 5 7 2.698b 0.100
他克莫司 6 10 0.278b 0.598
糖皮质激素+他克莫司 6 10 0.278b 0.598
糖皮质激素+霉酚酸酯 2 3   1.000c
糖皮质激素+来氟米特 3 3 － 0.399c
糖皮质激素+环孢素 0 2 － 0.304c
糖皮质激素+环磷酰胺 0 2 － 0.304c
雷公藤 0 1 － 1.000c
3种d 2 3 － 1.000c
表3 不同治疗方案治疗青少年IMN的疗效分析
项目 少年组 青年组 CR PR 无缓解(失访) 肾穿前使用免疫抑制剂 复发 CR时间(月) PR时间(月)
少年组 青年组 少年组 青年组 少年组 青年组 少年组 青年组 少年组 青年组
例数 25 48 7 17 10 23 8 8 2 9 1 2    
治疗方案(例)                            
  NIAT 1 7 0 4 1 2 0 1 0 0 0 0 7(4~12.5) 7(4.3~11)
  G 5 7 1 0 2 5 2 2 0 1a 0 1 3 3(2, 4)
  T 6 10 0 2 3 7 3 1 0 0 1 1 9(8~10) 7(4~10)
  G+T 6 10 2 4 2 6 2 2 1b 2bc 0 0 15(5.5~21) 4(3，10)
  G+L 2 4 1 1 1 2 0 1 0 2ab 0 0 5.5(4.5~6.5) 3.5(3~5.3)
  G+M 2 3 1 2 0 1 1 0 1b 2b 0 0 7(6.5~9.0) 3.5(2.8~4.3)
  G+CsA 0 2 0 0 0 0 0 1 0 1a 0 0    
  G+CTX 0 1 0 1 0 0 0 0 0 1a 0 0    
  雷公藤 0 1 0 0 0 0 0 1 0 0 0 0    
  3种 2 3 1 3 1 0 0 0 0 0 0 2    
  4种 1 0 1 0 0 0 0 0 0 0 0 0    
图1 两组24月总缓解率生存曲线
图2 两组24月完全缓解率生存曲线
表4 青少年IMN的肾脏病理特点[例(%)]
项目 所有患者 少年组(n＝60) 青年组(n＝104) χ2值 P值
球囊粘连 29(17.7) 11(18.3) 18(17.3) 0.027a 0.868
肾小球硬化 25(15.4) 2(3.3) 10(19.2) 1.385b 0.239
节段硬化 16(9.8) 6(10) 10(9.6) 0.006 0.936
新月体 3(1.8) 1(1.7) 2(1.9)   1.000c
Ehrenreich-Churg分期          
  Ⅰ期 56 (34.1) 23(38.3) 39(33.9) 0.011a 0.916
  Ⅱ期 104(63.4) 34(56.7) 70(60.9) 1.857a 0.173
  Ⅲ期 8(4.9) 3(6.1) 5(4.3) － 1.000 c
免疫荧光          
  IgAa 8(4.9) 2(3.3) 5(4.8) － 1.000c
  IgG 164(10%) 60(100) 104(100)    
  IgM 3(1.8) 2(3.3) 1(0.9)   0.555c
  C3 130(79.3) 51(85.0) 79(76.0) 1.891a 0.169
  C4 14(8.5) 4(6.7) 10(9.6) 0.130a 0.718b
  C1q 14(8.5) 4(6.7) 10(9.6) 0.130a 0.718b
  肾间质病变 111(67.7) 40(66.7) 71(68.3) 0.045a 0.833
  动脉病变 28(17.1) 6(10.0) 22(21.2) 3.343a 0.067
表4 两组不良反应发生率对比[例(%)]
项目 少年组 青年组 t值或χ2值 P值
每人至少发生一次 5(20.0) 14(29.2) 0.717a 0.397
类型        
  感染(次) 4(16.0) 8(32.0) 0.034b 0.854
  非感染 1(4.0) 6(12.5)   1.351c
  糖尿病 1(4.0) 4(8.3)   0.477c
  肌酐升高 0 1(2.1)   0.521c
  3个以上 0 1(2.1)   0.521c
表5 两组患者青少年24月缓解率危险因素分析(Cox回归分析)
项目 总缓解率 完全缓解率
影响因素HR(95%CI) P值 影响因素HR(95%CI) P值 影响因素HR(95%CI) P值 影响因素HR(95%CI) P值
男性 0.933(0.072~12.122) 0.958     1.899(0.407~8.863) 0.414    
年龄>18岁 0.497(0.048~5.098) 0.556     0.697(0.191~2.542) 0.584    
高血压(≥130/80mmHg) 0.458(0.037~5.619) 0.541     1.477(0.349~6.249) 0.597    
低白蛋白血症(<25 g/L) 4.090(0.076~218.853) 0.998     0.559(0.089~3.514) 0.535    
大量蛋白尿(>3.5 g/d) 0.073(0.002~3.449) 0.998     1.055(0.227~4.905) 0.946    
eGFR[ml/(min·1.73 m2)] 1.018(0.094~1.103) 0.663     0.993(0.945~1.004) 0.784    
血尿 21.237(1.009~447.173) 0.049 11.493(1.324~99.768) 0.027 1.691(0.416~6.871) 0.463    
高胆固醇血症(>5.6 mmol/L) 4.404(0.175~111.057) 0.368     1.842(0.391~8.680) 0.440    
IgA(<0.7 g/L) 2.385(0.082~69.168) 0.613     1.297(0.156~10.765) 0.810    
IgG(<4 g/L) 6.213(0.821~47.038) 0.077 6.124(1.138~32.953) 0.035 4.425(0.859~22.799) 0.075 3.538(1.193~10.499) 0.023
C4(<0.19 g/L) 0.674(0.024~19.191) 0.818     0.457(0.066~3.171) 0.428    
C3阳性 0.732(0.065~8.231) 0.801     1.303(0.282~6.028) 0.735    
肾间质病变 1.395(0.142~13.739) 0.775     0.481(0.105~2.201) 0.345    
动脉病变 0.150(0.006~4.030) 0.259     1.352(0.238~7.685) 0.733    
表6 各指标在评价24月总缓解率时的诊断价值分析
指标 AUC 最佳临界点 敏感度(%) 特异性(%) P值
血清白蛋白(g/L) 0.742 22.40 71.4 80.0 0.012
IgG(g/L) 0.765 3.48 69.4 86.7 0.001
血尿程度评分 0.752 0.50 87.5 51.1 0.011
IgA(g/L) 0.548 1.96 36.7 80.0 0.691
C4(g/L) 0.503 0.20 77.6 40.0 0.960
年龄(岁) 0.580 21.50 40.8 73.3 0.154
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