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ORIGINAL ARTICLE
Year : 2022  |  Volume : 18  |  Issue : 7  |  Page : 1961-1966

Comprehensive analysis of clinicalf eatures, treatment options, overall survival, and prognostic factors in lymphoma cell leukemia patients: A retrospective study


1 Department of Hematology, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China
2 Department of Sales, Kindstar Global, Wuhan, China

Date of Submission07-Jan-2022
Date of Decision01-Jul-2022
Date of Acceptance30-Aug-2022
Date of Web Publication11-Jan-2023

Correspondence Address:
Mengchang Wang
Department of Hematology, The First Affiliated Hospital of Xifan Jiaotong University, 277 West Yanta Road, Xifan 710061, Shanxi Province
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.jcrt_42_22

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 > Abstract 


Objective: Lymphoma cell leukemia (LCL) is regarded as patients presenting a high extensive lymphoma cell ratio in bone marrow (BM), which is recognized as lymphoma of stage IV by invading into BM. This study aimed to investigate the clinical characteristics, treatment options, survival profiles, and prognostic factors in patients with LCL.
Methods: Clinical data of 42 patients with LCL were retrospectively reviewed, and baseline characteristics and treatment records were extracted. In addition, overall survival (OS) was calculated, and the causes of death were analyzed.
Results: Out of the 42 patients with LCL, 9 (21.4%) had primary BMLCL, 20 (47.6%) had Non-Hodgkin lymphoma (NHL) complicated with LCL, and 13 (31.0%) had NHL evolving into LCL. Common clinical characteristics included B syndromes (n = 21, 50.0%), abnormal white blood count (n = 28, 66.5%), decreased hemoglobin (n = 28, 66.7%), and platelet (n = 30, 71.4%). Additionally, elevated Eastern Cooperative Oncology Group (ECOG) with a score greater than one occurred in 26 patients (61.9%), and elevated lactate dehydrogenase (LDH) occurred in 25 patients (59.5%). For treatments, chemotherapy was the most common therapy (n = 35, 83.2%), followed by symptomatic treatment and radiotherapy plus chemotherapy. Additionally, the mean OS of the patients was 16.9 (95% CI: 12.8–20.9) months, among which primary patients with BMLCL showed shorter OS than those with NHL complicated with LCL and NHL evolving into patients with LCL. A total of 9 (21.4%) patients with LCL died during follow-up, among which the central nervous system (CNS) invasion was the most common cause of death. Furthermore, primary BMLCL, higher ECOG, and higher LDH were potential predictive factors for worse OS in patients with LCL.
Conclusion: This study gives an overview of the treatment and prognosis of LCL, which provides additional information for the management of LCL.

Keywords: Clinical characteristics, lymphoma cell leukemia, prognostic factors, survival, treatment


How to cite this article:
Kang Y, Fang K, Wang M. Comprehensive analysis of clinicalf eatures, treatment options, overall survival, and prognostic factors in lymphoma cell leukemia patients: A retrospective study. J Can Res Ther 2022;18:1961-6

How to cite this URL:
Kang Y, Fang K, Wang M. Comprehensive analysis of clinicalf eatures, treatment options, overall survival, and prognostic factors in lymphoma cell leukemia patients: A retrospective study. J Can Res Ther [serial online] 2022 [cited 2023 Jan 27];18:1961-6. Available from: https://www.cancerjournal.net/text.asp?2022/18/7/1961/367471




 > Introduction Top


A lymphoma is a heterogeneous group of lymphoid malignancies, which can be broadly divided into two major types, Hodgkin lymphoma (HL) and Non-Hodgkin lymphoma (NHL).[1],[2],[3],[4],[5],[6] Global cancer statistics indicate that in 2018, HL occurred in 79,990 individuals resulting in 26,167 deaths, and NHL occurred in 509,590 individuals and caused 248,724 deaths.[7] Progression of lymphoma is accompanied by a high potential to spread to other tissues throughout the body such as the nasopharynx, gastrointestinal tract, skin, and bone marrow (BM).[1],[2],[7],[8],[9] The involvement of BM, which is classified as stage IV of lymphoma according to the Ann Arbor staging system, is regarded as a sign of the advanced stage of the disease progression, especially BM involvement arising from NHL, which accounts for 16%~75% of the lymphoma with BM involvement cases.[8],[10]

Lymphoma cell leukemia (LCL) is defined as the cases with extensive lymphoma cell ratio in BM, which is recognized as lymphoma of stage IV that invades BM nowadays.[11] Although great advances have been made in understanding lymphoma pathophysiology, the incidence and histopathological patterns of LCL vary from country to country, and only a few Chinese studies focusing on LCL have been published so far. Apart from that, it is of great concern to differentiate LCL from acute lymphoblastic leukemia. Therefore, it is urgent to expand knowledge of the clinical characteristics and prognosis of LCL, which might help to establish timely and appropriate treatment. In this study, we retrospectively investigated the clinical characteristics, treatments, and survival profiles of 42 patients with LCL, and we assessed the factors affecting overall survival (OS), to provide more documented information that can be used for the management of LCL.


 > Methods Top


Patients

A total of 42 patients with invasive LCL were screened from the Digital Medical Record Application System of The First Affiliated Hospital of Xi'an Jiaotong University by searching the key words “lymphoma” and “leukemia” through the Medical Record Browser. All reviewed cases had a diagnosis of LCL, and complete clinical and follow-up data. Among the 42 invasive LCL cases, 20 cases were diagnosed as lymphoma by lymph node biopsy and complicated with LCL in the BM; 13 cases were diagnosed as primary NHL evolving into LCL after 1 to 38 months of treatment, and 9 cases were diagnosed as primary BMLCL by BM biopsy. The diagnosis of all cases was performed according to the 2008 World Health Organization (WHO) classification of Tumors of Hematopoietic and Lymphoid Tissue.[12] This study was approved by the Ethics Committee of the First Affiliated Hospital of Xi'an Jiaotong University, and verbal agreements with tape recording or written informed consent were obtained from all cases or their guardians. The procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation and with the Helsinki Declaration of 1975, as revised in 2000 (available at http://www.wma.net/e/policy/17-c_e.html).

Data collection

Clinical data of reviewed cases were extracted from the Digital Medical Record Application System. The clinical data included demographic characteristics (age and gender), diagnosis, B symptoms (weight loss, night sweat, and fever), Eastern Cooperative Oncology Group (ECOG) scores, laboratory detections (lymphoma cell ratio) in BM, lactate dehydrogenase (LDH), white blood cell (WBC) counts, hemoglobin (Hb) level, and platelet (PLT) counts, treatment strategies, follow-up information, and causes of deaths.

Assessment

According to the follow-up records, the total follow-up duration of patients ranged from 1 month to 24 months. Based on the follow-up data, OS was calculated from the date of the confirmed diagnosis of LCL to the date of death or censoring.

Statistical analysis

Data were described as mean and standard deviation (SD), median and interquartile range (IQR), or count (percentage). Kaplan–Meier curve was used to assess OS, and the comparison of OS was determined by the log-rank test. Univariable and multivariable Cox proportional hazard regression model analysis was performed to evaluate the prognostic factors. Tests were considered statistically significant if P < 0.05. SPSS version 24.0 statistical software (IBM, Chicago, IL, USA) and GraphPad Prism 7.02 software (GraphPad Software Inc., San Diego, CA, USA) were used for statistical data analysis and plotting graphs.


 > Results Top


Baseline characteristics

Clinical data of 42 patients with LCL were reviewed in this study, including 29 (69.0%) males and 13 (31.0%) females. The mean and median ages of the patients were 43.8 ± 20.1 years, and 43.0 (range 6.0–78.0) years, respectively [Table 1]. Regarding diagnosis, 9 (21.4%) patients were diagnosed as primary BMLCL, 20 (47.6%) patients were diagnosed as NHL complicated with LCL, and 13 (31.0%) patients were diagnosed as NHL evolving into LCL. For B symptoms, the numbers of patients diagnosed with fever, night sweats, fever and night sweats, and weight loss were 14 (33.3%), 2 (4.8%), 3 (7.1%), and 2 (4.8%), respectively. Moreover, there were 9 (21.4%), 7 (16.7%), 11 (26.1%), 7 (16.7%), 7 (16.7%), and 1 (2.4%) patients classified as ECOG scores 0, 1, 2, 3, 4, and unknown, respectively. The median lymphoma cell ratio in BM was 50.0 (IQR 32.4–73.3)%, and the numbers of patients with lymphoma cell ratios in BM of ≤40% and >40% were 17 (40.5%) and 25 (59.5%), respectively. Furthermore, median values of WBC, Hb, and PLT were 6.4 (IQR 2.8–16.0) *109/L, 98.0 (IQR 81.0–114.5) g/L, and 54.0 (IQR 35.0–105.5) *109/L, respectively. The numbers of patients with abnormal levels of blood cells, including WBC <4 * 109/L, WBC >10 * 109/L, Hb ≤110 g/L, and PLT ≤100 * 109/L were 14 (33.3%), 14 (33.3%), 28 (66.7%), and 30 (71.4%), respectively. Additionally, the median value of LDH was 341.0 (IQR 233.0–881.0) U/L, and the number of patients with abnormal LDH level (>245 U/L) was 25 (59.5%). These data indicated that the presence of pancytopenia, B syndromes, elevated ECOG score, and increased LDH were commonly observed in patients with LCL [Table 2]. Detailed clinical data of each patient are presented in [Supplementary Table 1] to [Supplementary Table 2], [Supplementary Table 3].
Table 1: Baseline characteristics of patients with LCL

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Table 2: Blood routine examination and biochemical indexes of patients with LCL

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Treatment of patients with LCL

The major treatment for patients with LCL was chemotherapy, which accounted for 83.2% (n = 35) of treatments among the patients with LCL [Table 3]. The other treatment methods used on the patients with LCL included symptomatic treatment, radiotherapy plus chemotherapy, PDT plus chemotherapy, splenectomy plus chemotherapy, and intrathecal injection plus chemotherapy, with the following respective frequencies: 2 (4.8%), 2 (4.8%), 1 (2.4%), 1 (2.4%), and 1 (2.4%), respectively. Chemotherapy and symptomatic treatments were applied in primary patients with BMLCL; chemotherapy, symptomatic treatment, radiotherapy plus chemotherapy, splenectomy plus chemotherapy, and intrathecal injection plus chemotherapy were applied in NHL complicated with patients with LCL; chemotherapy and PDT plus chemotherapy were applied in NHL evolving into patients with LCL [Table 3]. Conclusively, 40 (95.2%) patients received the VDLP regimen (vincristine, daunorubicin, L-asp, and prednisolone), while 2 (4.8%) patients only received the symptomatic treatment.
Table 3: Treatment for patients with LCL

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Survival profile of patients with LCL

The mean OS was 16.9 (95% CI: 12.8–20.9) months in patients with LCL [Figure 1]a. OS differed among the different subgroups. NHL complicated patients with LCL had the longest OS (mean OS: 21.7, 95% CI: 18.7–24.7) months, followed by NHL evolving into patients with LCL (mean OS: 15.2, 95% CI: 9.7–20.6) months, and finally the primary patients with BMLCL (mean OS: 7.5, 95% CI: 3.2–11.9) months [Figure 1]b. There were 33 (78.6%) survivors and 9 (21.4%) deaths during the follow-up [Table 4]. The causes of death among the patients with LCL included CNS invasion (3, 33.3%), heart failure (2, 22.2%), intracranial hemorrhage (2, 22.2%), renal failure (1, 11.1%), and infectious shock (1, 11.1%).
Figure 1: OS in patients with LCL. (a) OS in 42 patients with LCL. (b) Comparison of OS among primary patients with BMLCL, NHL complicated with patients with LCL, and NHL evolving into patients with LCL. K–M curves were used to display OS. Comparison among groups was determined by a log-rank test. P < 0.05 was considered significant. OS, overall survival; LCL, lymphoma cell leukemia; BM, bone marrow; BMLCL, bone marrow lymphoma cell leukemia; NHL, Non-Hodgkin lymphoma; K–M, Kaplan–Meier

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Table 4: Overall survival and subgroup analysis on the cause of death

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Analysis of factors affecting OS

Univariate Cox's regression analysis showed that primary BMLCL (vs. others) was numerically associated with lower OS, but without a statistical difference (P = 0.058) [Table 5]. Higher ECOG scores (P = 0.028) and higher LDH (P = 0.021) were associated with shorter OS in patients with LCL. And further forward stepwise multivariate Cox's regression showed that a high ECOG score (P = 0.028) was an independent predictive factor for short OS in patients with LCL.
Table 5: Univariate and multivariate Cox's proportional hazard model regression analyses of factors predicting OS

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 > Discussion Top


The common presentation of NHL is localized lymphadenopathy, whereas in some cases, lymphoma may be primary in extranodal such as the head, neck, oropharyngeal region, gastrointestinal tract, and skin. Moreover, in patients with unexplained pancytopenia, the BM may even be the only initial site of the disease detection, which is known as primary BM lymphoma.[10] Because BM involvement indicates stage IV (advanced stage) of lymphoma and affects both the treatment and prognosis, identification of BM involvement is an important step in the work-up of patients with lymphoma, and BM biopsy is the major method to detect BM involvement.[11],[13] Apart from BM biopsy detection, some clinical characteristics are also commonly observed in lymphoma with BM involvement patients, which may be applied as alert indications for BM involvement. For instance, incidences of B syndromes, reduced Hb levels, and increased LDH levels have been recorded in both T cell-LCL and patients with B cell-LCL.[11] Moreover, clinical characteristics such as B symptoms, elevated LDH level, and increased ECOG score have been associated with peripheral T cell lymphomas in BM involvement patients.[14]

LCL is regarded as the case presenting a high extensive lymphoma cell ratio in BM; besides, recently, it has been also called lymphoma of stage IV by invading into BM. Considering that BM involvement indicates an advanced stage of lymphoma and that the incidence and disease condition varies from country to country, only a few studies on Chinese patients with LCL were reported. Therefore, we opined that expanding the knowledge of the clinical characteristics in Chinese patients with LCL could facilitate the management of LCL. In our study, we reviewed the clinical data of 42 Chinese patients with LCL consisting of 20 (47.6%) with NHL complicated patients with LCL, 13 (31%) with NHL evolving into patients with LCL, and 9 (21.4%) with primary patients with BMLCL. In line with previous studies, we found that pancytopenia, B syndromes, elevated ECOG score, and increased LDH were clinical characteristics most commonly observed in patients with LCL and that elevated ECOG score indicated poor performance at diagnosis.

Although treatment for lymphoma varies according to the stage or type of disease at diagnosis, chemotherapy is a frequently-used treatment for lymphoma patients with BM involvement since most lymphomas are chemo-sensitive.[15],[16] In our study, about 83% of the patients with LCL received chemotherapy, indicating that chemotherapy was the most common therapy in patients with LCL, confirming the findings of previous studies. Subgroup analysis indicated that chemotherapy was also the most common treatment received in NHL with complicated LCL (75.0%), NHL evolving into LCL (92.3%), and primary patients with BMLCL (88.9%). Apart from chemotherapy, photodynamic, radioactive, and surgical treatments were used in NHL complicated with patients with LCL, and in NHL evolving into patients with LCL but not in primary patients with BMLCL. Thus, only chemotherapy and symptomatic treatment were suitable for primary patients with BMLCL.

Considering BM involvement signifying stage IV of lymphoma is associated with a dismal prognosis, enrichment of the clinical experiences and exploration of predictive factors for prognosis are critical to improving treatment outcomes in time.[1] A previous study reported a 10-month median OS in 107 primary BM-DLBCL patients,[17] and another one reported a mean PFS and OS in 21 DLBCL patients with BM involvement of 67.5 months and 54.4 months, respectively.[18] In our study, we recorded a mean OS of 16.9 months (95% CI: 12.8–20.9) for the patients with LCL, which was different from those reported in the previous studies. These discrepancies might be attributed to the following reasons: (1) all patients enrolled in one of the previous studies were primary BM-DLBCL patients[17] and patients with primary BM lymphoma usually present with deteriorative disease condition at diagnosis, thus those patients might have fewer chances to achieve treatment response consequently leading to shorter OS, resulting in the shorter OS; and (2) in another study,[18] the median ECOG score of patients was lower than that of patients in our study, indicating that the baseline disease condition of patients was much better than that of our patients. The follow-up duration was longer than that in our study, and these reasons might have led to the longer OS in the previous study compared to ours. Additionally, severe infection is reported as the most common cause of death in some lymphoma cases but only a few studies report on the cause of death in lymphoma with BM involvement cases.[19],[20] In our study, we found that CNS invasion was the most common cause of death in patients with LCL, followed by heart failure, and intracranial hemorrhage. Patients should, therefore, pay close attention to these complications.

We performed Cox's regression analysis and found that a higher ECOG score was an independent predictive factor for worse OS in patients with LCL. The predictive value of a higher ECOG score for unfavorable survival profiles has also been observed in some previous studies.[21],[22] The reason might be that patients with higher ECOG scores have poorer performance status, which causes a deteriorative disease condition and poor tolerance to chemotherapy, thereby lowering the treatment response of the patients resulting in unfavorable OS.

Our study had some limitations: (1) although the sample size in our study (n = 42) was larger than that of other similar studies, our results still needed validation with larger sample size; (2) this was a single-center study, which might have selective bias; (3) follow-up duration (range 1–24 months) was relatively short, and long-term observational study in patients with LCL was needed; (4) as a retrospective study, its inherent limitation should be noticed, such as the patients' selection bias; and (5) the genetic pattern of these LCL patients should be determined in further study, which might uncover the essence of this disease and potential prognostic factors.

In conclusion, patients with LCL commonly present B symptoms, higher LDH, pancytopenia, and elevated ECOG score, which are often associated with poor prognosis. Thus, a BM biopsy is needed to evaluate BM involvement in lymphoma, which may contribute to the effective management of LCL. Moreover, primary BMLCL, higher ECOG, and higher LDH that correlate with poor prognosis may provide support for predicting prognosis and contribute to establishing personal treatment in patients with LCL.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

This study was supported by Key Research and Development Program of Shanxi Province (2021SF-079).

Conflicts of interest

There are no conflicts of interest.



 
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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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