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中华妇幼临床医学杂志(电子版)

中华妇幼临床医学杂志(电子版) ›› 2020, Vol. 16 ›› Issue (01) : 81 -92. doi: 10.3877/cma.j.issn.1673-5250.2020.01.011

所属专题： 文献；

论著

儿童成熟B细胞非霍奇金淋巴瘤临床特点和预后分析
饶艳琼1, 郭霞1, 万智1, 沈成奇1, 代依灵1, 朱易萍1, 高举1,†()   
  1. 1. 四川大学华西第二医院儿科、出生缺陷与相关妇儿疾病教育部重点实验室，成都　610041
  • 收稿日期:2019-10-05 修回日期:2020-01-14 出版日期:2020-02-01
  • 通信作者: 高举

Clinical characteristics and prognosis of mature B-cell non-Hodgkin lymphoma in children

Yanqiong Rao1, Xia Guo1, Zhi Wan1, Chengqi Shen1, Yiling Dai1, Yiping Zhu1, Ju Gao1,†()   

  1. 1. Department of Pediatrics, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
  • Received:2019-10-05 Revised:2020-01-14 Published:2020-02-01
  • Corresponding author: Ju Gao
  • About author:
    Corresponding author: Gao Ju, Email:
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引用本文：

饶艳琼, 郭霞, 万智, 沈成奇, 代依灵, 朱易萍, 高举. 儿童成熟B细胞非霍奇金淋巴瘤临床特点和预后分析[J]. 中华妇幼临床医学杂志(电子版), 2020, 16(01): 81-92.

Yanqiong Rao, Xia Guo, Zhi Wan, Chengqi Shen, Yiling Dai, Yiping Zhu, Ju Gao. Clinical characteristics and prognosis of mature B-cell non-Hodgkin lymphoma in children[J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2020, 16(01): 81-92.

目的

探讨儿童成熟B细胞非霍奇金淋巴瘤(B-NHL)患儿的临床特征、疗效、生存情况，以及预后相关危险因素。

方法

选择2010年1月至2018年12月，四川大学华西第二医院收治的67例儿童B-NHL患儿为研究对象。其中，伯基特淋巴瘤/L3急性淋巴细胞白血病(BL/L3-ALL)、弥漫大B细胞淋巴瘤(DLBCL)及其他B-NHL(病理检查结果为骨髓B淋巴细胞高增殖活性，除外上述2种B-NHL)分别为51、11及5例，将其分别纳入BL组、DLBCL组及其他B-NHL组。采用回顾性分析方法，收集3组患儿的临床病例资料，包括确诊年龄、性别、临床特征、实验室检查结果、B-NHL临床分期、治疗与随访结果及预后等。对本组67例B-NHL患儿进行生存分析，如2年和5年总体生存(OS)率、无事件生存(EFS)率。3组患儿的生存曲线比较，采用Cox比例风险回归模型进行分析。根据既往研究结果，并结合临床经验及B-NHL患儿预后影响因素的单因素分析结果，对B-NHL患儿预后影响因素，进行多因素非条件logistic回归分析。本研究遵循的程序符合2013年修订的《世界医学协会赫尔辛基宣言》要求。3组患儿病程比较，差异无统计学意义(P>0.05)。

结果

①患儿年龄、性别：67例B-NHL患儿确诊时，中位年龄为7.0岁(1.8～14.6岁)；其中男性患儿为48例(71.6%)，女性为19例(28.4%)，男、女患儿比为2.5∶1。3组患儿的年龄、性别构成比比较，差异均有统计学意义(χ2＝8.054、8.677，P＝0.018、0.013)，并且DLBCL组患儿年龄和男性患儿所占比例，分别大于或高于BL组，差异亦均有统计学意义(Z＝2.866、P＝0.004，χ2＝3.892、P＝0.049)。②B-NHL原发部位及骨髓和CNS受累情况：化疗前，67例B-NHL患儿均完成影像学、骨髓穿刺涂片及脑脊液检查。BL组中，BL/L3-ALL原发部位位于腹腔者最多，占39.2%(20/51)，DLBCL组患儿中，DLBCL原发部位位于外周淋巴结为主，占45.5%(5/11)，其他B-NHL组患儿中，原发部位位于腹腔者最多，占60.0%(3/5)。此外，11例患儿存在骨髓和CNS受累(均为BL组患儿)。③实验室检查结果：39例(58.2%)患儿血清LDH水平升高，中位血清LDH水平为498 U/L(153～6 640 U/L)。BL组患儿Bcl-6阳性表达率(86.4%，38/44)和C-MYC基因重排阳性率(96.3%，26/27)，均显著高于DLBCL组的54.5%(6/11)和0，并且差异均有统计学意义(χ2＝6.960、26.527，P＝0.031、<0.001)。④临床分期：3组患儿的临床分期构成比比较，差异有统计学意义(χ2＝13.949、P＝0.012)。BL组患儿临床分期为Ⅲ/Ⅳ期所占比例(80.4%，41/51)，均显著高于DLBCL组的36.4%(4/11)，并且差异有统计学意义(χ2＝6.740、P＝0.009)。⑤随访结果：对67例患儿随访截至时间为2019年3月1日，中位随访时间为49个月(2～104个月)，完全缓解(CR)为49例，部分缓解(PR)为7例，进展/复发为9例(5例死亡、3例失访、1例经治疗后无病存活)，其他原因所致患儿死亡为2例(1例因严重感染放弃治疗而死亡，1例化疗疗程结束后死亡)。⑥生存情况：67例B-NHL患儿的2年OS率、EFS率分别为88.8%、85.7%，5年OS率、EFS率分别为88.8%、83.2%。3组患儿5年OS率和5年EFS率组间分别比较，差异均无统计学意义(P>0.05)。67例患儿的中位复发时间为9个月(2～37个月)，2年、5年累积复发率(CIR)分别为11.3%、13.9%。存在骨髓/CNS受累患儿的5年OS率(71.6%)和5年EFS率(59.7%)，均显著低于无骨髓/CNS受累者的92.2%和87.6%，并且差异均有统计学意义(χ2＝5.001、6.319，P＝0.025、0.012)。⑦单因素分析：复发/进展和非复发/进展患儿的单因素分析结果显示，复发/进展患儿骨髓/CNS受累者所占比例和肿瘤裂解综合征发生率分别为50.0%(4/8)和25.0%(2/8)，显著高于非复发/进展患儿的11.9%(7/59)和1.7%(1/59)，二者比较，差异有统计学意义(χ2＝4.946、P＝0.026；P＝0.036)；复发/进展患儿2个疗程内达CR率(12.5%，1/8)显著低于非复发/进展患儿(69.5%，41/59)，二者比较，差异亦有统计学意义(χ2＝9.782、P＝0.002)。⑧多因素分析：结合已有研究结果及临床经验，以及单因素分析结果，对B-NHL患儿预后影响因素的多因素非条件logistic回归分析结果显示，骨髓/CNS受累(OR＝6.536，95%CI：1.085～39.380，P＝0.040)和2个疗程内未达CR(OR＝14.682，95%CI：1.582～136.240，P＝0.018)是B-NHL患儿疾病复发/进展的独立危险因素。

结论

儿童B-NHL以病理类型为BL最为常见，原发部位位于回盲部最为常见；其次为DLBCL，其原发部位位于外周淋巴结最为常见。骨髓/CNS受累和2个疗程未达CR是B-NHL患者发生复发/进展的危险因素。尽管B-NHL患儿2年EFS及5年EFS均>80%，但是，临床分期为Ⅳ期及进展/复发的B-NHL患儿的预后仍然尚待提高。

关键词: 淋巴瘤，非霍奇金, B淋巴细胞, 复发, 失随访, Logistic模型, 无病生存, 预后, 儿童
Objective

To study clinical features and prognosis of childhood mature B-cell non-Hodgkin lymphoma (B-NHL).

Methods

Sixty-seven cases of pathologically-confirmed B-NHL from January 2010 to December 2018 in West China Second University Hospital, Sichuan University were enrolled in this retrospective study. According to different pathological types, they were divided into Burkitt lymphoma (BL) group (n=51), diffuse large B-cell lymphoma (DLBCL) group (n=11) and other B-NHL group (n=5, pathological examination results were high proliferative activity B cell lymphoma). The retrospective analysis method was used to collect the clinical data of these subjects, including age, gender, clinical characteristics, laboratory examination results, clinical stages, treatment results and follow-up. Kaplan-Meier method was used to analyze the survival of children with B-NHL in this group, such as 2-year and 5-year overall survival (OS) rate and event-free survival (EFS) rate, and Cox propertional hazards model was used to compare OS and EFS curves among three groups. According to previous research results, combined with clinical experience and single factor analysis results of clinical factors affecting the prognosis of children with B-NHL, multivariate non-conditional logistic analysis was carried out on the influencing factors of prognosis of children with B-NHL. This study was in line with the requirements of World Medical Association Declaration of Helsinki revised in 2013. There was no significant difference among 3 groups in the course of the diseases (P>0.05).

Results

① The median age of 67 children with B-NHL was 7 years old (1.8-14.6 years old). Among them, 48 cases (71.6%) were boys, and 19 cases (28.4%) were girls, and the ratio of boys to girls was 2.5∶1. There was statistically significant differences in age and gender ratio among three groups (χ2=8.054, 8.677; P=0.018, 0.013). The age and the proportion of boys in DLBCL group were older and higher than those in BL group, respectively, and the differences were statistically significant (Z=2.866, P=0.004; χ2=3.892, P=0.049). ②All of the 67 cases completed imaging examination, bone marrow smear and cerebrospinal fluid examination before chemotherapy. The primary tumor sites in BL group tended to be more common in the abdomen, while peripheral lymph nodes were more commonly involved at disease onset in DLBCL group. In addition, 11 children had bone marrow and CNS involvement (all children in the BL group). ③ Laboratory findings showed that 39 cases (58.2%) had elevated serum LDH levels, with a median serum LDH level of 498 U/L (153-6 640 U/L). The positive expression rate of Bcl-6 (86.4%, 38/44) and the positive rate of C-MYC gene rearrangement (96.3%, 26/27) in BL group were significantly higher than those of 54.5% (6/11) and 0 in DLBCL group, and the differences were statistically significant (χ2=6.960, 26.527; P=0.031, <0.001). ④There was a significant difference in the constituent ratio of different clinical stages among 3 groups (χ2=13.949, P=0.012). The proportion of children with clinical stage Ⅲ/Ⅳ in BL group (80.4%, 41/51) was significantly higher than those of 36.4% (4/11) in DLBCL group, and the difference was statistically significant (χ2=6.740, P=0.009). ⑤All the 67 cases were followed up until March 1, 2019. The median follow-up time was 49 months (2-104 months). Complete remission (CR) was achieved in 49 cases, partial remission (PR) in 7 cases, progression/recurrence in 9 cases (5 cases died, 3 cases were lost visit to follow-up, 1 case survived without disease). Other causes of death were 2 cases (1 case died of severe infection after giving up treatment, 1 case died after the end of chemotherapy course). ⑥ The 2-year OS and EFS rates of the 67 cases were 88.8% and 85.7%, respectively, and the 5-year OS and EFS rates were 88.8% and 83.2%, respectively. There were no significant differences in 5-year OS rate and 5-year EFS rate among three groups (P>0.05). The median time to recurrence was 9 months (2-37 months), and the 2-year and 5-year cumulative incidence of relapse (CIR) were 11.3% and 13.9%, respectively. In addition, the 5-year OS rate (71.6%) and 5-year EFS rate (59.7%) in patients with bone marrow/CNS involvement were significantly lower than those of 92.2% and 87.6% in patients without bone marrow/CNS involvement, and the differences were statistically significant (χ2=5.001, 6.319, P=0.025, 0.012). ⑦ The results of univariate analysis for children with recurrence/progression and non-recurrence/progression showed that the proportion of bone marrow/CNS involvement and the incidence rate of tumor lysis syndrome in children with recurrence/progression were 50.0% (4/8) and 25.0% (2/8), respectively, which were significantly higher than those of 11.9% (7/59) and 1.7% (1/59) in children without recurrence/progression, and the differences were statistically significant (χ2=4.946, P=0.026; P=0.036); the CR rate (12.5%, 1/8) within 2 courses in children with recurrence/progression was significantly lower than that of 69.5%(41/59) in children without recurrence/progression, and the difference was also statistically significant (χ2=9.782, P=0.002). ⑧ Combined with the results of existing studies and clinical experience, as well as the results of above univariate analysis, the results of multivariate non-conditional logistic analysis of prognostic factors in children with B-NHL showed that bone marrow/CNS involvement (OR=6.536, 95%CI: 1.085-39.380, P=0.040) and failure to achieve CR within 2 courses of treatment (OR=14.682, 95%CI: 1.582-136.240, P=0.018) were independent risk factors for disease relapse/progression in children with B-NHL.

Conclusions

BL is the most common type of B-NHL in children, with the ileocecum as the prevalent site of tumor primaries. While DLBCL is the second most common type of B-NHL, which commonly occurs in the peripheral lymph node. Involvements of bone marrow/CNS, and incomplete response within 2 courses of chemotherapy may predict poor prognosis of patients. The clinical outcomes of B-NHL children with stage Ⅳ and relapsed/progressive B-NHL remain to be improved.

Key words: Lymphoma, non-Hodgkin, B-lymphocytes, Recurrence, Lost to follow-up, Logistic models, Disease-free survival, Prognosis, Child
表1 3组成熟B细胞非霍奇金淋巴瘤患儿一般临床资料比较
组别 例数 年龄[岁，M(P25～P75)] 性别[例数(%)]
男 女
BL组 51 6.1(2.4～14.6) 33(64.7) 18(35.3)
DLBCL组 11 9.0(5.6～13.4) 11(100.0) 0(0)
其他B-NHL组 5 9.1(3.1～12.8) 4(80.0) 1(20.0)
总体比较 ? ? ? ?
? χ2值 ? χ2＝8.054 χ2＝8.677 a
? P值 ? 0.018 0.013
BL组 vs DLBCL组 ? ? ? ?
? 检验值 ? Z＝2.866 χ2＝3.892 a
? P值 ? 0.004 0.490
BL组 vs其他B-NHL组 ? ? ? ?
? 检验值 ? Z＝0.690 χ2＝0.038 a
? P值 ? 0.049 0.846
DLBCL组 vs其他B-NHL组 ? ? ? ?
? 检验值 ? Z＝—0.624 —
? P值 ? 0.533 0.515
表2 3组成熟B细胞非霍奇金淋巴瘤患儿血清乳酸脱氨酶水平比较[例数(%)]
组别 例数 血清LDH水平
< 2 N (2～4) N >4 N
BL组 51 30(58.8) 10(19.6) 11(21.6)
DLBCL组 11 10(90.9) 0(0) 1(9.1)
其他B-NHL组 5 5(100.0) 0(0) 0(0)
χ2值 ? 10.269
P值 ? 0.036
表3 3组成熟B细胞非霍奇金淋巴瘤患儿临床分期比较[例数(%)]
组别 例数 Ⅰ期 Ⅱ期 Ⅲ期 Ⅳ期
BL组 51 3(5.9) 7(13.7) 30(58.8) 11(21.6)
DLBCL组 11 0(0) 7(63.6) 4(36.4) 0(0)
其他B-NHL组 5 0(0) 3(60.0) 2(40.0) 0(0)
χ2值 ? 13.949
P值 ? 0.012
表4 3组成熟B细胞非霍奇金淋巴瘤患儿5年生存分析(%)
组别 例数 5年OS率 5年EFS率
BL组 51 87.5 85.3
DLBCL组 11 88.9 53.3
其他B-NHL组 5 100.0 100.0
χ2值 ? 0.684 2.836
P值 ? 0.718 0.242
图1 67例成熟B细胞非霍奇金淋巴瘤患儿总体生存曲线及无事生存曲线(图1A：总体生存曲线，图1B：无事件生存曲线)
图2 3组成熟B细胞非霍奇金淋巴瘤患儿总体生存曲线及无事件生存曲线(图2A：总体生存曲线，图2B：无事件生存曲线)
表5 67例成熟B细胞非霍奇金淋巴瘤患儿不同临床因素的5年总体生存率及无事件生存率比较
临床因素 例数 5年OS 5年EFS
OS率(%) χ2值 P值 EFS率(%) χ2值 P值
年龄(岁) ? ? 1.191 0.275 ? 0.294 0.588
? ≥7 33 85.1 ? ? 80.8 ? ?
? <7 34 92.6 ? ? 86.2 ? ?
性别 ? ? 2.933 0.087 ? 2.021 0.155
? 男 48 84.4 ? ? 78.6 ? ?
? 女 19 100.0 ? ? 94.1 ? ?
临床分期(期) ? ? 3.286 0.070 ? 2.133 0.144
? Ⅰ/Ⅱ 20 100.0 ? ? 90.0 ? ?
? Ⅲ/Ⅳ 47 83.9 ? ? 79.6 ? ?
血清LDH水平 ? ? 2.269 0.132 ? 1.743 0.187
? < 2 Na 45 92.9 ? ? 86.7 ? ?
? ≥ 2 Na 22 80.5 ? ? 76.5 ? ?
骨髓/CNS受累 ? ? 5.001 0.025 ? 6.319 0.012
? 是 11 71.6 ? ? 59.7 ? ?
? 否 56 92.2 ? ? 87.6 ? ?
联合利妥昔单抗治疗(Ⅲ/Ⅳ期)b ? ? 0.297 0.585 ? 0.552 0.458
? 是 31 85.2 ? ? 82.5 ? ?
? 否 16 80.8 ? ? 74.0 ? ?
联合AHSCT(Ⅲ/Ⅳ期)b ? ? 1.483 0.223 ? 0.036 0.849
? 是 7 100.0 ? ? 85.7 ? ?
? 否 40 80.8 ? ? 83.7 ? ?
表6 影响成熟B细胞非霍奇金淋巴瘤患儿预后临床因素的单因素分析结果
疾病情况 例数 发病年龄[岁，M(P25～P75)] 性别[例数(%)] 病理类型[例数(%)]
男 女 BL DLBCL 其他B-NHL组
复发/进展 8 8.9(1.8～12.9) 7(87.5) 1(12.5) 6(75.0) 2(25.0) 0(0)
非复发/进展 59 6.9(2.4～14.6) 41(69.5) 18(30.5) 45(76.3) 9(15.2) 5(8.5)
检验值 ? Z＝0.638 χ2＝1.125 χ2＝1.087
P值 ? 0.402 0.289 0.581
疾病情况 例数 临床分期[例数(%)] 血清LDH水平≥2 N a[例数(%)] 存在骨髓/CNS受累[例数(%)] 是否发生肿瘤裂解综合征[例数(%)] 2个疗程内达到CR[例数(%)]
Ⅰ/Ⅱ期 Ⅲ/Ⅳ期
复发/进展 8 1(12.5) 7(87.5) 5(62.5) 4(50.0) 2(25.0) 1(12.5)
非复发/进展 59 19(32.2) 40(67.8) 17(28.8) 7(11.9) 1(1.7) 41(69.5)
χ2值 ? 0.535 3.625 4.946 — 9.782
P值 ? 0.465 0.057 0.026 0.036 0.002
表7 影响成熟B细胞非霍奇金淋巴瘤患儿预后的8项临床因素的多因素非条件logistic回归分析变量含义及其赋值情况
自变量/因变量 变量名 赋值
疾病是否复发/进展 y y＝0表示疾病无复发/进展，y＝1表示疾病有复发/进展
年龄 x1 x1＝0表示年龄<9岁；x1＝1表示年龄≥9岁
性别 x2 x2＝0表示女性；x2＝1表示男性
病理类型是否为BL x3 x3＝0表示病理类型为非BL；x3＝1表示病理类型为BL
临床分期 x4 x4＝0表示临床分期为Ⅰ/Ⅱ期；x4＝1表示临床分期为Ⅲ/Ⅳ期
血清LDH水平 x5 x5＝0表示血清LDH水平<4 N；x5＝1表示血清LDH水平≥4 Na
骨髓/CNS是否受累 x6 x6＝0表示骨髓/CNS未受累；x6＝1表示骨髓/CNS受累
是否发生肿瘤裂解综合征 x7 x7＝0表示未发生肿瘤裂解综合征；x7＝1表示发生肿瘤裂解综合征
2个疗程内是否达到CR x8 x8＝0表示2个疗程内未达到CR；x8＝1表示2个疗程内达到CR
表8 影响成熟B细胞非霍奇金淋巴瘤患儿预后的8项临床因素的多因素非条件logistic回归分析
影响因素 B SE Wald值 P值 OR值 OR值95%CI
年龄≥9岁 0.732 1.205 0.369 0.543 2.079 0.196～22.057
男性 0.240 1.373 0.030 0.861 1.271 0.086～18.722
病理类型为BL —2.471 1.681 2.161 0.142 0.085 0.003～2.279
临床分期为Ⅲ/Ⅳ期 1.275 1.776 0.515 0.473 3.579 0.110～116.346
血清LDH水平≥4 Na 1.172 1.197 0.958 0.328 3.227 0.309～33.699
骨髓/CNS受累 1.877 0.916 4.197 0.040 6.536 1.085～39.380
发生肿瘤裂解综合征 1.009 2.102 0.230 0.631 2.744 0.045～169.026
2个疗程内未达到CR 2.687 1.137 5.587 0.018 14.682 1.582～136.240
[1]
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