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

doi:10.3877/cma.j.issn.1673-5250.2020.01.011

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(%)]
组别		例数	年龄[岁，M(P₂₅～P₇₅)]	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(%)]
组别		例数	年龄[岁，M(P₂₅～P₇₅)]	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
组别	例数	< 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
组别	例数	< 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

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
临床因素		例数	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 N^a	45	92.9	?	?	86.7	?	?
?	≥ 2 N^a	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
临床因素		例数	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 N^a	45	92.9	?	?	86.7	?	?
?	≥ 2 N^a	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(%)]
疾病情况	例数	发病年龄[岁，M(P₂₅～P₇₅)]	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(%)]
疾病情况	例数	Ⅰ/Ⅱ期	Ⅲ/Ⅳ期	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(%)]
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(%)]
疾病情况	例数	发病年龄[岁，M(P₂₅～P₇₅)]	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(%)]
疾病情况	例数	Ⅰ/Ⅱ期	Ⅲ/Ⅳ期	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(%)]
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 N^a
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 N^a
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 N^a	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

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 N^a	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

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