Case Report Open Access
Copyright ©The Author(s) 2023. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Clin Cases. Feb 16, 2023; 11(5): 1086-1093
Published online Feb 16, 2023. doi: 10.12998/wjcc.v11.i5.1086
Angioimmunoblastic T-cell lymphoma induced hemophagocytic lymphohistiocytosis and disseminated intravascular coagulopathy: A case report
Mei Jiang, Jing-Hua Wan, Clinical Laboratory, The First Affiliated Hospital of Nanchang University, Nanchang 330006, Jiangxi Province, China
Yi Tu, Department of Pathology, The First Affiliated Hospital of Nanchang University, Nanchang 330006, Jiangxi Province, China
Yan Shen, Department of Anesthesia, Medical College of Nanchang University, Nanchang 330006, Jiangxi Province, China
Fan-Cong Kong, Department of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang 330006, Jiangxi Province, China
Zhang-Lin Zhang, Department of Transfusion, The First Affiliated Hospital of Nanchang University, Nanchang 330006, Jiangxi Province, China
ORCID number: Mei Jiang (0000-0003-4128-4903); Zhang-Lin Zhang (0000-0001-8712-0264).
Author contributions: Jiang M and Wan JH contributed equally to this work; Zhang ZL and Kong FC contributed equally and should share the corresponding authorship; Jiang M, Wan JH, Kong FC, and Zhang ZL wrote the manuscript; Jiang M, Tu Y, Shen Y, and Zhang ZL collected the data and revised the manuscript; all authors have read and approved the final manuscript.
Supported by the National Natural Science Foundation of China, No. 82160692 and No. 82160037.
Informed consent statement: Informed written consent was obtained from the patient for the publication of this report and any accompanying images.
Conflict-of-interest statement: The authors declare that they have no conflict of interest to disclose.
CARE Checklist (2016) statement: The authors have read the CARE Checklist (2016), and the manuscript was prepared and revised according to the CARE Checklist (2016).
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Zhang-Lin Zhang, Doctor, Associate Chief Technician, Transfusion, The First Affiliated Hospital of Nanchang University, No. 17 Yongwai Street, Nanchang 330006, Jiangxi Province, China. ndyfy02270@ncu.edu.cn
Received: September 18, 2022
Peer-review started: September 18, 2022
First decision: November 11, 2022
Revised: November 15, 2022
Accepted: January 28, 2023
Article in press: January 28, 2023
Published online: February 16, 2023
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Abstract
BACKGROUND

Angioimmunoblastic T-cell lymphoma (AITL) is a subtype of peripheral T-cell lymphoma, with heterogenous clinical manifestations and poor prognosis. Here, we report a case of AITL induced hemophagocytic lymphohistiocytosis (HLH) and disseminated intravascular coagulopathy (DIC).

CASE SUMMARY

An 83-year-old man presented with fever and purpura of both lower limbs for one month. Groin lymph node puncture and flow cytometry indicated a diagnosis of AITL. Bone marrow examination and other laboratory related indexes indicated DIC and HLH. The patient rapidly succumbed to gastrointestinal bleeding and septic shock.

CONCLUSION

This is the first reported case of AITL induced HLH and DIC. AITL is more aggressive in older adults. In addition to male gender, mediastinal lymphadenopathy, anaemia, and sustained high level of neutrophil-to-lymphocyte ratio may indicate a greater risk of death. Early diagnosis, early detection of severe complications, and prompt and effective treatment are vital.

Key Words: Angioimmunoblastic T-cell lymphoma; Hemophagocytic lymphohistiocytosis; Disseminated intravascular coagulopathy; Prognostic factors; Case report

Core Tip: Angioimmunoblastic T-cell lymphoma (AITL) is a subtype of peripheral T-cell lymphoma, with heterogenous clinical manifestations and poor prognosis. Early diagnosis is particularly important. Herein, we report a patient with AITL induced hemophagocytic lymphohistiocytosis (HLH) and disseminated intravascular coagulopathy (DIC). The patient rapidly succumbed to gastrointestinal bleeding and septic shock. The time between onset and death was about one month. To the best of our knowledge, this is the first case of AITL induced HLH and DIC. AITL is more aggressive in older adults. In addition to male gender, mediastinal lymphadenopathy, anaemia, and sustained high level of neutrophil-to-lymphocyte ratio may indicate a greater risk of death. Early diagnosis, early detection of severe complications, and prompt and effective treatment are vital.



INTRODUCTION

Angioimmunoblastic T-cell lymphoma (AITL) is a subtype of peripheral T-cell lymphoma (PTCL), which accounts for 1%-2% of non-Hodgkin’s lymphomas and 15%-20% of PTCLs[1], and presents with heterogenous clinical manifestations and poor prognosis[2]. Early diagnosis is particularly important. Herein, we report a patient with AITL induced hemophagocytic lymphohistiocytosis (HLH) and disseminated intravascular coagulopathy (DIC).

CASE PRESENTATION
Chief complaints

An 83-year-old man presented with fever and purpura of both lower limbs for one month (Figure 1A).

Figure 1
Figure 1 Examinations. A: Purpura was observed on both lower limbs of the patient; B: Groin lymph node puncture specimen showed that the normal structure of lymph nodes disappeared and heterogeneous infiltration of small to medium-sized lymphoma cells, with proliferation of eosinophils (hematoxylin and eosin staining, × 40); C-E: Flow cytometry. Neoplastic T cells are shown in red and benign T cells in blue (analysis was gating on lymphocytes). The neoplastic T cells were positive for CD3, CD4, CD10, and PD1, but negative for CD7 and CD8; F: Bone marrow examination showed hemophagocytosis; G: Capillary electrophoresis revealed monoclonal IgG kappa.
History of present illness

The patient presented with fever and purpura of both lower limbs for one month. He had chills and fever, with the highest body temperature of 40 °C, accompanied by cough and phlegm, no nausea and vomiting, and no abdominal distention, abdominal pain, dizziness, headache, or other discomfort.

History of past illness

The patient was diagnosed with diabetes mellitus for more than one month, had a history of hypertension for more than 30 years, coronary heart disease for 10 years, and renal insufficiency for many years. He denied any history of tuberculosis.

Physical examination

Physical examination showed an appearance of mild anemia, neck, armpit, and groin lymph node enlargement, splenomegaly, and edema and visible purpura of both lower limbs, without other special manifestations.

Laboratory examinations

Groin lymph node puncture showed disappearance of the normal structure of lymph nodes and heterogeneous infiltration of small to medium-sized lymphoma cells, with proliferation of eosinophils (Figure 1B). The lymphoma cells were positive for CD3, CD4, CD10, and PD1, but negative for CD7 and CD8 by flow cytometry (Figure 1C-E). Bone marrow examination showed hemophagocytosis (Figure 1F) without evidence of lymphoma involvement. The hemoglobin concentration and platelet count declined rapidly, with the minimum value of 65 g/L and 53 × 109/L, respectively. A serological examination showed hypertriglyceridemia (triglycerides 3.14 mmol/L), normal value of serum ferritin (299.50 μg/L), elevated levels of soluble interleukin (IL)-2 receptor (16080 U/mL), and hypergammaglobulinaemia. The capillary electrophoresis revealed monoclonal IgG kappa (Figure 1G), without evidence of monoclonal plasma cells in bone marrow and lymph nodes. The coagulation function examination rapidly showed the maximum level of D-dimer (3.85 mg/L), prolonged prothrombin time (52.6 s), prolonged activated partial thromboplastin time (54.1 s), maximum value of International Normalized Ratio (4.57), and hypofibrinogenemia (fibrinogen 1.2 g/L). The dynamic changes of white blood cell (WBC) count, lymphocyte cell count, neutrophil count, and neutrophil-to-lymphocyte ratio (NLR) from nearly onset to death are listed in Table 1.

Table 1 Dynamic changes of white blood cell count, lymphocyte cell count, neutrophil count, and neutrophil-to-lymphocyte ratio of the present patient.
Index date
WBC count (× 109/L)
Lymphocyte cell count (× 109/L)
Neutrophil count (× 109/L)
NLR
4-97.590.107.2672.6
4-144.780.483.988.29
4-225.220.214.8523.01
4-255.140.343.9011.47
4-273.830.332.898.76
4-295.770.324.7414.81
5-15.190.404.6111.53
Imaging examinations

Positron emission tomography showed splenomegaly, generalized lymphadenopathy, and enhanced activity in the posterior pharyngeal wall, bilateral neck, hilum of the lung and mediastinum, pelvic wall, mesenteric lymph nodes, and groin, suggestive of lymphoma (Figure 2).

Figure 2
Figure 2 Positron emission tomography. A-F: Positron emission tomography showed generalized lymphadenopathy, enhanced activity in the posterior pharyngeal wall (A), bilateral neck (B), hilum of the lung and mediastinum (C), pelvic wall (D), mesenteric lymph nodes (E), and groin (F).
FINAL DIAGNOSIS

The patient was finally diagnosed as having AITL induced HLH and DIC.

TREATMENT

The patient’s son chose to refuse treatment.

OUTCOME AND FOLLOW-UP

The patient rapidly succumbed to gastrointestinal bleeding and septic shock. The time between onset and death was about one month.

DISCUSSION

AITL is aggressive and mainly affects older individuals (median age of 65 years), with a median survival of < 3 years[2,3]. The survival time of our patient was only about one month from onset to death. This was rare and indicated that the disease course was very aggressive.

A few studies reported that AITL was associated with plasma cell proliferation[4-6]. Monoclonal immunoglobulins were detected in this case, without evidence of monoclonal plasma cells. We speculated that AITL related to immunoregulatory disorder stimulated clonal plasma cell proliferation, but it may be undetectable. However, the mechanism involved in the development of the concomitant monoclonal immunoglobulins remains to be clarified. High levels of cytokines, such as IL-6, IL-10, and TNF-α, may serve as possible contributing factors[4,5,7-10]. Whether the concomitant plasma cell proliferation indicated a poor prognosis in AITL deserves further investigation.

There have been few reported cases of AITL associated HLH. One study reported that HLH occurred in a 57-year-old man with AITL during chemotherapy. He subsequently developed multi-organ failure and died after a few days[11]. Another case report described an AITL patient who relapsed with HLH two months after receiving chemotherapy supported by autologous peripheral blood stem cell transplantation (PBSCT). The patient was successfully treated with allogeneic PBSCT with reduced intensity conditioning regimen[12]. Including our case, three cases of AITL induced HLH were confirmed at the time of AITL diagnosis, not during chemotherapy or relapse[13,14]. The clinical features of the three cases are listed in Table 2 (patients 1, 2, and 4. Patient 4 was the present case). HLH is a life-threatening severe complication of AITL. AITL lymphoma cells may produce cytokines and chemokines that cause systemic complications[15]. Epstein-Barr virus (EBV) infected lymphocytes have been reported in up to 97% of AITL cases[16,17]. EBV infection may suggest a possible role for the virus in the etiology. EBV DNA was detectable in these three cases (Table 2). AITL associated HLH had a poor prognosis due to aggressive disease course, especially in the presence of EBV infection, in conjunction with genetic abnormalities and immune dysfunction[16]. Patients 1 and 2 were successfully treated with etoposide together with CHOP regimen and allogeneic HSCT with RIC, respectively. However, our patient (patient 4) had AITL associated HLH with concomitant DIC, and rapidly succumbed to gastrointestinal bleeding and septic shock. There was only one AITL induced DIC case reported previously[18]. The clinical features of the case are listed in Table 2 (patient 3). DIC was mostly caused by sepsis, shock, solid cancer, and hematological malignancies[19,20]. When associated with hematological malignancy, DIC was most frequently accompanied by newly diagnosed acute promyelocytic leukemia (APL) (approximately 70%)[21], followed by non-APL acute myeloid leukemia (17%) and non-Hodgkin’s lymphoma (11%)[22,23]. Coagulopathy with hypofibrinogenemia could also occur with HLH. We could not exclude that DIC was part of the HLH process in our patient. The disease course was very aggressive when accompanied by DIC. Patient 3 succumbed to DIC and fatal gastrointestinal bleeding. Both of patient 3 and patient 4 had a very poor prognosis.

Table 2 Clinical features of angioimmunoblastic T-cell lymphoma patients with hemophagocytic lymphohistiocytosis or disseminated intravascular coagulopathy.

Patient 1
Patient 2
Patient 3
Patient 4 (the present case)
Sex/age (yr) at the time of diagnosis53/male62/female72/female83/male
Laboratory findings in peripheral blood
% atypical lymphocytes in the blood of all lymphocytes9%NANANA
Hypereosinophilia (%)NANAYes (17%)Yes (9%)
AutoantibodiesAntinuclear antibodies and anti-double-stranded DNA antibodies were negativeNANAAnti-TIF-1γ antibodies and anti-Jo-1 antibodies were positive
HypergammaglobulinaemiaYes (polyclonal)NAYes (polyclonal)Yes (monoclonal)
EBV DNA copies (IU/mL)8.42 × 104NA, but positive in lymph node biopsyNA131
Immunophenotype/immunohistochemical stainingCD2+, CD3+, CD5+, CD7+, CD10+; CD20dim, PAX5dim, and telomerase Bdim (biopsies of the left cervical lymph node)CD3+, CD4+, CD8,CD30, CD56 andCD20were negative (cervical lymph node biopsy)CD4+, CD5+, CD10+ (lymph node)CD3+, CD4+, CD10+, PD1+, CD7 and CD8 were negative- (lymph node)
Clinical manifestation
Generalized lymphadenopathyYesYesYesYes
Bone marrow involvementHemophagocytosis and abnormal lymphocytesHemophagocytosis, but withoutevidence of lymphoma involvementNo lymphoma infiltration and no evidence of hemophagocytosis, bone marrow infiltration two weeks laterHemophagocytosis, but without evidence of lymphoma involvement
HepatomegalyYesYes Yes No
SplenomegalyYesYes Yes Yes
Skin rash/purpuraYes NANAYes
Pleural effusionNANANAYes
Severe complication
HLHYes Yes No Yes
DICNo No Yes Yes
TherapyEtoposide together with CHOP regimenCHOP, mesna, ifosfamide, mitoxantrone, etoposide; allogeneic HSCT with RICSteroidsAnti-infection and other symptomatic treatment
OutcomeSuccessfully treatedSuccessfully treated Succumbed to DIC and fatal gastrointestinal bleedingSuccumbed to gastrointestinal bleeding and septic shock

The risk of death increased and treatment effectiveness decreased with age. Patient 4 was the oldest, followed by patient 3. To the best of our knowledge, our patient was the first case with AITL induced HLH and DIC. Survival was significantly related to age, male gender, mediastinal lymphadenopathy, and anaemia[2,24] which were adverse prognostic factors in our patient. Notably, NLR in AITL was a significant, independent prognostic factor for overall survival (OS), and NLR ≥ 2.2 indicated shorter OS[25]. Table 1 shows that the level of WBC count in our patient was almost within the normal range, whereas lymphocyte count was consistently at a low level and NLR was significantly high from nearly onset to death. We speculated that the patient suffered from severe immunosuppression, and the risk of death was greater when NLR was irreversibly sustained high. Consequently, HLH and DIC were induced, which resulted in rapid and fatal septic shock and gastrointestinal bleeding.

CONCLUSION

AITL is more aggressive in older adults. In addition to male gender, mediastinal lymphadenopathy, anaemia, and sustained high level of NLR may indicate a greater risk of death. Early diagnosis, early detection of severe complications, and prompt and effective treatment are vital.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Hematology

Country/Territory of origin: China

Peer-review report’s scientific quality classification

Grade A (Excellent): 0

Grade B (Very good): B

Grade C (Good): C

Grade D (Fair): 0

Grade E (Poor): E, E

P-Reviewer: Chaturvedi HTC, India; Goldman M, Belgium; Yikilmaz AS, Turkey S-Editor: Chen YL L-Editor: Wang TQ P-Editor: Chen YL

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