Home Medicine Acute myeloid leukemia with leukemic pleural effusion and high levels of pleural adenosine deaminase: A case report and review of literature
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Acute myeloid leukemia with leukemic pleural effusion and high levels of pleural adenosine deaminase: A case report and review of literature

  • Sing-Ting Wang , Chieh-Lung Chen , Shih-Hsin Liang , Shih-Peng Yeh and Wen-Chien Cheng EMAIL logo
Published/Copyright: March 12, 2021
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From the journal Open Medicine Volume 16 Issue 1

Abstract

Pleural effusions are rarely observed in association with acute myeloid leukemia (AML), and their true incidence remains unknown. Given the low diagnostic yield from cytopathologic analysis of malignant pleural effusions and the fact that patients with leukemia are often thrombocytopenic and unable to tolerate invasive procedures, the incidence of leukemic effusions may be underestimated. Here, we report a rare case of pleural effusion in a patient with newly diagnosed AML. Initial analysis revealed an exudative, lymphocyte-predominant effusion. High levels of adenosine deaminase (ADA) were detected in pleural fluid, consistent with a diagnosis of tuberculosis. However, the analysis of pleural cytology revealed leukemic cells, permitting the diagnosis of leukemic effusion to be made. The patient underwent induction chemotherapy and pleural effusion resolved without recurrence. This case emphasizes the diagnostic dilemma presented by high levels of ADA in a leukemic pleural effusion, as this association has not been previously considered in the literature.

Keywords: acute myeloid leukemia; leukemic pleural effusion; adenosine deaminase; extramedullary

1 Introduction

Nearly, all hematologic malignancies can present with pleural effusions. Among the most common diseases associated with this complication are Hodgkin lymphoma and non-Hodgkin lymphoma because the mediastinum is a typical site of primary disease [1]. Leukemic pleural effusions are observed rarely only in patients with leukemia and even more infrequently among those diagnosed with acute myeloid leukemia (AML). The true incidence of leukemic effusion is not known, but it is believed to be underestimated; this complication may become more common with improved supportive care and prolonged survival for patients with AML [2].

In patients with leukemia, other causes of the pleural effusion such as infections, other disseminated solid tumors, and/or treatment-associated toxicities should be excluded [3]. The results from immunocytologic examination, as well as flow cytometry and polymerase chain reaction methodologies applied to cytology specimens, can contribute to the differential diagnosis [4].

Leukemic pleural effusion has been considered to be a reflection of the severity of the underlying hematologic malignancy; most cases have been associated with a poor prognosis [3,5,6]. The treatment of the primary disease usually results in resolution of the pleural effusion [1]; survival relies on an appropriate response to the treatment [2,3].

Adenosine deaminase (ADA) is an enzyme involved in the proliferation and differentiation of lymphocytes, especially T lymphocytes. The two principal isoenzymes are ADA1 and ADA2 [7]. While ADA1 can be detected in all cells, ADA2 is found only in macrophages and monocytes [8]. The presence of live intracellular microorganisms stimulates the release of ADA [9]. Currently, well-established evidence suggests that ADA levels >40 U/L in lymphocytic pleural effusions can be used as virtually diagnostic for tuberculous pleural effusion (TPE); this is especially true in the regions of high disease prevalence [10]. ADA levels in nontuberculous lymphocytic effusions seldom exceed the diagnostic cutoff for TPE [11]. Conversely, similar or higher ADA levels have occasionally been reported in parapneumonic effusion [12]; furthermore, empyema or lymphoma should be considered in cases with extremely high ADA activity [13]. In one retrospective study that evaluated 156 patients with malignant pleural effusion, ADA levels >40 U/L were detected in only 16 patients (1%) and none were related to acute leukemia [14].

2 Case report

A 55-year-old man with no medical history presented with a chief complaint of dyspnea on exertion for a period of 1 month. His body temperature was 37.4°C, pulse rate was 105 beats per minute, blood pressure was 111/63 mm Hg, respiratory rate was 18 breaths per minute, and oxygen saturation was 98% with ambient air. Physical examination was normal except for pallor. Chest radiograph (Figure 1a) and electrocardiogram were normal at presentation. A complete blood count revealed leukocytosis (white blood cell [WBC] count, 97,600/µL) with 26% blasts and an elevated fraction of circulating monocytic cells (45%), anemia (hemoglobin 6.6 g/dL), and thrombocytopenia (platelet count, 23,000/µL). Other laboratory test results are presented in Table 1. Bone marrow examination was notable for hypercellularity with increased myeloblasts (Figure 2a). Immunophenotyping of bone marrow cells by flow cytometry revealed that cells were positive for CD13, CD123, CD7, CD34, CD117, and HLA-DR, but not for CD56 or terminal deoxynucleotidyl transferase (Tdt). A cytogenetic study revealed an abnormal karyotype of 47, XY, +21. e8e2(e11e3); a histone-lysine N-methyltransferase 2A (KMT2A)-partial tandem duplication (PTD) fusion was detected by a real-time reverse transcriptase-polymerase chain reaction (RT-PCR). A diagnosis of AML with e11e3(e8e2) MLL-PTD was made. However, the patient developed direct type hyperbilirubinemia (Table 1) and progressive shortness of breath during hospitalization; chest radiograph revealed rapid growth of left side pleural effusion (Figure 1b). Abdominal sonography showed no evidence of mechanical obstruction. Subsequently, 650 mL of a bloody effusion was withdrawn through ultrasound-guided thoracentesis. Laboratory analysis of the pleural fluid indicated an exudative, lymphocyte-predominant effusion (red blood cells, 21,692/L; WBCs, 2,025/L with a leukocyte differential including 46% lymphocytes, 38% monocytes, and 16% neutrophils; protein <3 mg/dL, glucose 84 mg/dL, and lactate dehydrogenase [LDH] 922 U/L). A high level of ADA (42 U/L) was also detected in pleural fluid. Given these findings, a diagnosis of tuberculous pleural effusion was considered. Nevertheless, rapid growth of tuberculous pleural effusion is relatively uncommon. Antituberculosis agents were not prescribed because of the diagnostic uncertainty and hyperbilirubinemia. MTB quantitative PCR (Cepheid Xpert MTB/RIF TEST with real-time PCR) of the pleural fluid yielded negative results. Chest computed tomography showed no evidence of pulmonary tuberculosis, mass lesion, or pulmonary embolism. However, cytologic examination of the pleural fluid revealed some abnormally large cells with fine chromatin and scant cytoplasm; the morphological features of these cells resembled those of the myeloblasts in the bone marrow (Figure 2b). Therefore, the diagnosis of AML with leukemic pleural effusion and suspected liver involvement was considered. The patient was treated with induction chemotherapy that included Idarubicin (12 mg/m2 from days 1 to 3) and Cytarabine (100 mg/m2 from days 1 to 7). Follow-up chest radiograph on day 7 of induction chemotherapy revealed significant resolution of the pleural effusion, and laboratory test results showed alleviation of hyperbilirubinemia (Table 1). The patient developed neutropenic fever after chemotherapy and underwent several courses of broad-spectrum antibiotic treatment. Bacterial cultures were negative in all sterile sites. Bone marrow examination on day 14 revealed significant cytoreduction with a low percentage of residual blasts. There was no recurrence of the pleural effusion (Figure 1c); culture of the pleural fluid was negative for Mycobacterium tuberculosis. Subsequently, the patient experienced a relapse and developed refractory disease in the clinical course and eventually died of septic shock ∼4 months after the diagnosis. Nevertheless, there was no recurrence of left side pleural effusion throughout the clinical course.

Figure 1 (a) Initial chest radiograph revealed no abnormal findings. (b) Chest radiograph taken revealed rapid accumulation of a left side pleural effusion within 1 week of admission. (c) Pleural effusion largely resolved after induction chemotherapy.
Figure 1

(a) Initial chest radiograph revealed no abnormal findings. (b) Chest radiograph taken revealed rapid accumulation of a left side pleural effusion within 1 week of admission. (c) Pleural effusion largely resolved after induction chemotherapy.

Table 1

Laboratory parameters

Variable Reference range On admission Day 7 of hospitalization Day 7 of induction chemotherapy
White blood cell count (per μL) 3,600–11,200 97,600 41,500 5,900
Differential count (%)
Neutrophils 43.4–76.6 9 22.9 53.6
Lymphocytes 16–43.5 7 1.8 20.5
Monocytes 4.5–12.5 45 63.5 25.9
Eosinophils 0.6–7.9 0 0 0
Atypical lymphocytes — 5 — —
Hemoglobin (g/dL) 13.7–17 6.6 9.1 7.9
Platelet count (per μL) 1,30,000–4,00,000 23,000 15,000 <10,000
Prothrombin time (s) 9.5–11.7 13.8 — 15.7
Prothrombin time international normalized ratio 0.9–1.2 1.37 — 1.57
Activated partial thromboplastin time (s) 24.3–32.7 30.7 — 33.3
Sodium (mmol/L) 135–147 137 139 131
Potassium (mmol/L) 3.5–4.5 3.0 3.1 4.6
Urea nitrogen (mg/dL) 7–25 18 16 31
Creatinine (mg/dL) 0.7–1.3 1.6 1.11 0.61
Uric acid (mg/dL) 4.4–7.6 11.4 2.8 3.5
Lactate dehydrogenase (U/L) 140–271 419 646 157
Alanine aminotransferase (U/L) 5–40 11 15 45
Aspartate aminotransferase (U/L) 13–39 13 18 8
Total bilirubin (mg/dL) 0.2–1.3 1.14 5.21 2.24
Direct bilirubin (mg/dL) 0–0.4 — 3.34 —
Alkaline phosphatase (U/L) 38–126 — 70 64
C-Reactive protein (mg/dL) <1.0 — 24.35 0.34
Procalcitonin (ng/mL) <0.5 — 2.5 —
Figure 2 (a) Bone marrow aspiration revealed a hypercellular marrow with diffuse infiltration of myeloblasts with vesicular nuclei and scanty cytoplasm. (b) Pleural fluid cytology (cell block) was notable for the presence of atypical cells with enlarged and hyperchromatic nuclei and scant cytoplasm (arrow).
Figure 2

(a) Bone marrow aspiration revealed a hypercellular marrow with diffuse infiltration of myeloblasts with vesicular nuclei and scanty cytoplasm. (b) Pleural fluid cytology (cell block) was notable for the presence of atypical cells with enlarged and hyperchromatic nuclei and scant cytoplasm (arrow).

  1. Informed consent: Written informed consent was obtained from the patient for publication of this case report and any accompanying images.

3 Discussion

Leukemic effusion, similar to other extramedullary manifestations, can develop simultaneously with or precede bone marrow involvement. Pleural effusions have been reported to be associated with different phases of AML, including at the time of initial diagnosis, during advanced refractory disease, upon relapse, or after stem cell transplantation; it may even be an isolated finding after bone marrow remission [15,16] (Table 2). Some studies report that the development of pleural effusion may serve as an indicator of the development of AML in patients with myelodysplastic syndrome [17,18].

Table 2

Summary of case reports of AML pleural effusiona

Year Author (Ref.) Age (years)/sex How the diagnosis was achieved Pleural ADA Leukemia status at leukemic effusion diagnosis Treatment Outcome
1955 Raynolds et al. [34] 26/M Cytologic examination, necropsy Not reported AML, newly diagnosed Supportive care Death 5 months after diagnosis
1974 Wu and Burns [15] 67/F Cytologic examination Not reported AML, in BM remission COAP therapy, intrapleural araC, radiation therapy Effusion resolved
1989 Green et al. [35] 59/M Cytologic examination Not reported AML, M1, newly diagnosed Chemotherapy with mitozantrone and araC CR with the resolution of effusion after the first course of chemotherapy
1994 Ohe et al. [36] 51/M Not reported Not reported CD7 + AML, newly diagnosed Induction araC + Daunorubicin, then autologous HSCT CR for minimum 8 months
1996 Schmetzer et al. [37] 49/F Cytologic examination Not reported AML, M5b, relapse Induction chemotherapy, then daunomycin and araC containing consolidation Second CR; died 6 years after diagnosis during fourth relapse of AML
2002 Park et al. [38] 41/M Cytologic examination with cytogenetic confirmation Not reported AML, M2, s/p HSCT, with isolated pleural relapse 31 months after HSCT, in BM remission Chemotherapy Died of septicemia while undergoing chemotherapy
2003 Azoulay et al. [39] 19/F By clinical history Not reported AML, M5, newly diagnosed Chemotherapy Died, respiratory status deteriorated and cardiac arrest developed after chemotherapy
2003 Azoulay et al. [39] 45/F By clinical history Not reported AML, M5, newly diagnosed Chemotherapy Died, respiratory status deteriorated after chemotherapy
2003 Azoulay et al. [39] 50/M By clinical history Not reported AML, M5, newly diagnosed Chemotherapy Alive, respiratory failure developed after chemotherapy
2003 Disel et al. [40] 39/M Pleural biopsy Not reported APL, with pleural relapse Chemotherapy with FLAG-IDA regimen CR with resolution of pulmonary signs and symptoms
2004 Khan et al. [17] 71/F Cytologic examination Not reported MDS with transformation to AML M5 Induction araC + Daunorubicin Died of overwhelming sepsis 22 days after the initiation of induction chemotherapy
2005 Farray et al. [41] 45/F Cytologic examination, flow cytometry Not reported Acute megakaryoblastic leukemia, M7, newly diagnosed Not reported Not reported
2005 Leong et al. [42] 25/M Cytologic examination Not reported AML, M4Eo, newly diagnosed Induction araC + Daunorubicin, re-induction with high dose araC due to refractory disease Refractory disease, death 8 weeks after diagnosis
2007 Fatih et al. [43] 50/M Cytologic examination, flow cytometry Not reported AML, M1, newly diagnosed 3 + 7 induction with Idarubicin + araC, then FLAG-IDA regimen due to refractory and old age Effusion resolved without recurrence, but leukemia was refractory; death 3 months after discharge
2008 Huang et al. [18] 56/F Cytologic examination Not reported CMMoL with transformation to AML 3 + 7 induction with Idarubicin + araC Respiratory failure; died on day 64 during hospitalization
2008 Raina et al. [44] 22/M Cytologic examination Not reported AML, M4, newly diagnosed Chemotherapy Died on day 3 of initiating treatment
2009 Rigamonti et al. [45] 52/M Cytologic examination, cytogenetic study Not reported AML, newly diagnosed Induction chemotherapy with EMA protocol Died of septic emboli with ICH 4 weeks after initiation of induction chemotherapy
2011 Stoll et al. [46] 54/M Cytologic examination, flow cytometry Not reported AML–MDS with erythroid differentiation, refractory to chemotherapy None, ineligible due to renal function Home hospice; death 6 months after diagnosis
2011 Ou et al. [16] 53/M Cytologic examination, flow cytometry Not reported AML, newly diagnosed 3 + 7 induction with Idarubicin + araC, re-induction with high-dose araC due to refractory pleural effusion CR with first induction, but effusions did not resolve. After re-induction with high-dose Cytarabine, effusions resolved. Later underwent HSCT, remained disease free for minimum 1 year
2012 Nieves-Nieves et al. [47] 66/M Cytologic examination Not reported AML, newly diagnosed 3 + 7 induction with Idarubicin + araC, re-induction with EMA protocol due to refractory disease Effusion resolved without recurrence, but leukemia was refractory; death through complications of leukemia
2013 Chang [2] 74/F Cytologic examination Not reported AML, M4, newly diagnosed Induction araC and four cycles of postremission chemotherapy with araC and etoposide Effusions resolved; CR for minimum 11 months
2013 Chang [2] 75/M Cytologic examination Not reported CMMoL with transformation to AML M4 None, ineligible due to poor performance status Death 1 month after diagnosis
2013 Chang [2] 74/M Cytologic examination Not reported AML, M4, refractory Induction araC and subsequently four different regimens due to refractory disease Death 1 month after diagnosis
2013 Agrawa [48] 45/M Cytologic examination Not reported AML, M2, newly diagnosed Chemotherapy Death 1 week after diagnosis
2013 Oka et al. [49] 63/F Cytologic examination, flow cytometry Not reported AML without maturation, with CD56 expression, newly diagnosed Not reported Death 11 month after diagnosis
2014 Duhan et al. [50] 26/F Cytologic examination Not reported AML, M4, newly diagnosed Induction chemotherapy with Daunorubicin, araC, and cladribine Died of refractory disease
2014 Morell-García et al. [51] 76/M Cytologic examination, flow cytometry Not reported AML, during the treatment 5-Azacitidine Death 15 days after diagnosis
2014 Pemmaraju et al. [33] 55/M Cytogenetic studyb Not reported Progression of PV to AML Decitabine for 5 days then BIDFA for 4 days Relapsed prior to stem cell transplant; died 11 months after transformation to AML
2014 Hanenberg and Marionneaux [52] 64/F Cytologic examination Not reported Progression of PV to AML Induction araC + Daunorubicin, replaced with decitabine and ruxolitinib Not reported
2014 Agarwal et al. [53] 22/M Cytologic examination 20 U/L AML, M2, diagnosed 2 months after leukemic effusion Induction araC + Daunorubicin, second induction with HAM, consolidation with HiDAC Bone marrow remission on day 47 of HAM; died during the neutropenic phase
2015 Lokireddy et al. [54] 74/M Cytologic examination, flow cytometry Not reported AML, newly diagnosed Induction araC + Daunorubicin Clearance of blast cells in pleural fluid
2015 Suharti et al. [55] 46/F Cytologic examination Not reported AML, M0, newly diagnosed Induction araC + Daunorubicin Refused further chemotherapy and home hospice
2020 Present study 55/M Cytologic examination 42 U/L AML, M4, newly diagnosed 3 + 7 induction with Idarubicin + araC Effusion resolved without recurrence, patient died of septic shock about 4 months after diagnosis

Abbreviations: BM = Bone marrow; COAP = Cyclophosphamide, Vincristine, Cytarabine, and Prednisone; araC = Cytarabine; CR = Complete remission; HSCT = Hematopoietic stem cell transplant; APL = Acute promyelocytic leukemia; ATRA = All trans retinoic acid; FLAG-IDA regimen = Fludarabine, Cytarabine, Idarubicin and G-CSF; MDS = Myelodysplastic syndrome; CMMoL = Chronic myelomonocytic leukemia; EMA protocol = Etoposide, Mitoxantrone, and Cytarabine; ICH = Intracerebral hemorrhage; PV = Polycythemia vera; BIDFA = twice-daily Fudarabine and Cytarabine; HAM = High-dose Cytarabine and Mitoxantrone.

  1. a

    Only studies with full-text or abstract in English available from PubMed were included.

  2. b

    Negative finding from cytologic examination and flow cytometry.

Predisposing risk factors associated with extramedullary involvement include monocytic or myelomonocytic differentiation (French-American-British [FAB] subtypes M4/M5), chromosomal abnormalities such as t(8:21) and inv(16), and expression of T cell markers including CD2, CD4, and CD7 [6,19,20]. Adhesion molecules, including CD15 and CD56, are believed to play a crucial role in the adhesion of leukemic cells to interstitial tissues [21]. In this case, high pleural ADA levels might be attributed to excessive extramedullary proliferation of monocytic leukemic cells.

The incidence of tuberculosis is twofold higher in patients with hematological malignancies when compared to that in the general population [22]. Both Gupta et al. [23] and Chen et al. [22] reported significantly higher incidences of tuberculosis disease among patients with AML than among those with other subtypes of hematological malignancies, at 6.3% (n = 95) and 2.87% (n = 1,011), respectively. The main risk factors associated with the development of tuberculosis included reduced immunity due to the primary hematological disease, age ≥50 years, and treatment with cytotoxic chemotherapy or steroids. Definitive diagnosis of M. tuberculosis infection is based on the clinical signs and symptoms as well as positive sputum and/or tissue culture(s); these methods can be very time consuming. As such, ADA in the pleural fluid has been used since 1983 [24] to facilitate early diagnosis of tuberculous pleural effusion; currently, this test is in wide use and has notably high sensitivity and specificity [25]. The ADA cut-off level typically considered in regions with high disease prevalence is 40 IU/L. Reportedly, high-ADA level in the pleural fluid is associated with a higher probability of TPE; furthermore, the diagnostic accuracy of ADA in TPE was influenced by age [26]. ADA level in the pleural fluid of 40 IU/L in a 55-year-old patient indicated the possibility of TPE with 60% certainty [26]. The ADA level in our 55-year-old patient was 42 IU/L. Therefore, it is possible that the evidence is not strong enough to consider TPE as a differential diagnosis in our patient. However, immunosuppressed patients may reportedly have significantly lower ADA activity [27]. Indeed, this case suggests that ADA levels detected in pleural effusions in patients with AML may introduce diagnostic complexities and lead to inappropriate therapy. Of note, this patient was unable to undergo more invasive procedures, including pleuroscopy or thoracoscopy with surgical biopsy, due to severe thrombocytopenia. Interferon-gamma release assays (IGRA) are in vitro blood tests to assess cell-mediated immune response by measuring the release of interferon-γ by T cells following the stimulation by antigens specific to the M. tuberculosis complex; these assays are now widely used to identify latent tuberculosis infections [28]. Because of the simplicity and noninvasive nature of IGRAs, these offer an attractive alternative to promptly diagnose TPE. However, two meta-analyses have suggested that commercial IGRAs that use either whole blood or pleural fluid have poor diagnostic accuracy in patients with suspected TPE [29,30].

Although the diagnosis of leukemic pleural effusion resulted from direct cytologic examination in our patient and in most of the previous case reports (Table 2), cytopathology typically plays a limited role in most cases of hematologic malignancy due to its low diagnostic potential, reported at 2.7% by Cakir et al. [31] and at 1.58% by Johnston [32]. To prevent misdiagnosis, clinicians need to be aware of this atypical and rare presentation of AML. To improve the diagnostic yield, cytogenetic studies might be considered as a routine component of the pleural fluid analysis in patients diagnosed with AML and presenting with a pleural effusion [33].

Reportedly, leukemic effusion typically resolved after chemotherapy (Table 2). A case report described a patient with newly diagnosed AML in whom complete remission was achieved with first induction chemotherapy; however, the effusions did not resolve. The effusions resolved after re-induction with high-dose Cytarabine [16]. In addition, Huang et al. reported a good relationship between peripheral blast counts and the magnitude of pleural effusion [18].

This is possibly the first case report of a patient diagnosed with AML with leukemic pleural effusion associated with a high pleural ADA level. Additional studies are needed to determine more precise relationships between AML-associated pleural effusions and pleural ADA levels.

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Appendix

Table A1

Vital signs before, during and after the induction chemotherapy

Body temperature (°C) Heart rate (per minute) Respiratory rate (per minute) Blood pressure (mm Hg) SpO2 (%) Oxygen use
One day before chemotherapy 36.9 110 18 95/68 97 Ambient air
Day 1 of chemotherapy 36.5 113 20 113/80 94 Ambient air
Day 2 of chemotherapy 35.9 108 20 120/80 96 Ambient air
Day 3 of chemotherapy 36.1 102 20 92/53 95 Ambient air
Day 4 of chemotherapy 36 88 18 92/61 97 Ambient air
Day 5 of chemotherapy 36.1 93 18 97/64 96 Ambient air
Day 6 of chemotherapy 35.8 98 18 93/58 96 Ambient air
Day 7 of chemotherapy 36 88 18 90/62 99 Ambient air
One Day after chemotherapy 36.2 97 18 93/56 98 Ambient air

  1. Authors contribution: Sing-Ting Wang, Chieh-Lung Chen, Shih-Hsin Liang, Shih-Peng Yeh, and Wen-Chien Cheng designed the report; Chieh-Lung Chen and Shih-Hsin Liang collected the patients’ clinical date; Sing-Ting Wang and Wen-Chien Cheng wrote the paper.

  2. Conflict of interest: There are no conflicts of interest.

  3. Data availability statement: Data sharing is not applicable to this article as no datasets were generated or analysed during the current study.

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Received: 2020-09-11
Revised: 2021-01-07
Accepted: 2021-01-29
Published Online: 2021-03-12

© 2021 Sing-Ting Wang et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/med-2021-0243
Keywords for this article
acute myeloid leukemia; leukemic pleural effusion; adenosine deaminase; extramedullary
Creative Commons
BY 4.0

Articles in the same Issue

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  44. Intestinal fatty acid-binding protein as a biomarker for the diagnosis of strangulated intestinal obstruction: A meta-analysis
  45. miR-128-3p inhibits apoptosis and inflammation in LPS-induced sepsis by targeting TGFBR2
  46. Dynamic perfusion CT – A promising tool to diagnose pancreatic ductal adenocarcinoma
  47. Biomechanical evaluation of self-cinching stitch techniques in rotator cuff repair: The single-loop and double-loop knot stitches
  48. Review Articles
  49. The ambiguous role of mannose-binding lectin (MBL) in human immunity
  50. Case Report
  51. Membranous nephropathy with pulmonary cryptococcosis with improved 1-year follow-up results: A case report
  52. Fertility problems in males carrying an inversion of chromosome 10
  53. Acute myeloid leukemia with leukemic pleural effusion and high levels of pleural adenosine deaminase: A case report and review of literature
  54. Metastatic renal Ewing’s sarcoma in adult woman: Case report and review of the literature
  55. Burkitt-like lymphoma with 11q aberration in a patient with AIDS and a patient without AIDS: Two cases reports and literature review
  56. Skull hemophilia pseudotumor: A case report
  57. Judicious use of low-dosage corticosteroids for non-severe COVID-19: A case report
  58. Adult-onset citrullinaemia type II with liver cirrhosis: A rare cause of hyperammonaemia
  59. Clinicopathologic features of Good’s syndrome: Two cases and literature review
  60. Fatal immune-related hepatitis with intrahepatic cholestasis and pneumonia associated with camrelizumab: A case report and literature review
  61. Research Articles
  62. Effects of hydroxyethyl starch and gelatin on the risk of acute kidney injury following orthotopic liver transplantation: A multicenter retrospective comparative clinical study
  63. Significance of nucleic acid positive anal swab in COVID-19 patients
  64. circAPLP2 promotes colorectal cancer progression by upregulating HELLS by targeting miR-335-5p
  65. Ratios between circulating myeloid cells and lymphocytes are associated with mortality in severe COVID-19 patients
  66. Risk factors of left atrial appendage thrombus in patients with non-valvular atrial fibrillation
  67. Clinical features of hypertensive patients with COVID-19 compared with a normotensive group: Single-center experience in China
  68. Surgical myocardial revascularization outcomes in Kawasaki disease: systematic review and meta-analysis
  69. Decreased chromobox homologue 7 expression is associated with epithelial–mesenchymal transition and poor prognosis in cervical cancer
  70. FGF16 regulated by miR-520b enhances the cell proliferation of lung cancer
  71. Platelet-rich fibrin: Basics of biological actions and protocol modifications
  72. Accurate diagnosis of prostate cancer using logistic regression
  73. miR-377 inhibition enhances the survival of trophoblast cells via upregulation of FNDC5 in gestational diabetes mellitus
  74. Prognostic significance of TRIM28 expression in patients with breast carcinoma
  75. Integrative bioinformatics analysis of KPNA2 in six major human cancers
  76. Exosomal-mediated transfer of OIP5-AS1 enhanced cell chemoresistance to trastuzumab in breast cancer via up-regulating HMGB3 by sponging miR-381-3p
  77. A four-lncRNA signature for predicting prognosis of recurrence patients with gastric cancer
  78. Knockdown of circ_0003204 alleviates oxidative low-density lipoprotein-induced human umbilical vein endothelial cells injury: Circulating RNAs could explain atherosclerosis disease progression
  79. Propofol postpones colorectal cancer development through circ_0026344/miR-645/Akt/mTOR signal pathway
  80. Knockdown of lncRNA TapSAKI alleviates LPS-induced injury in HK-2 cells through the miR-205/IRF3 pathway
  81. COVID-19 severity in relation to sociodemographics and vitamin D use
  82. Clinical analysis of 11 cases of nocardiosis
  83. Cis-regulatory elements in conserved non-coding sequences of nuclear receptor genes indicate for crosstalk between endocrine systems
  84. Four long noncoding RNAs act as biomarkers in lung adenocarcinoma
  85. Real-world evidence of cytomegalovirus reactivation in non-Hodgkin lymphomas treated with bendamustine-containing regimens
  86. Relation between IL-8 level and obstructive sleep apnea syndrome
  87. circAGFG1 sponges miR-28-5p to promote non-small-cell lung cancer progression through modulating HIF-1α level
  88. Nomogram prediction model for renal anaemia in IgA nephropathy patients
  89. Effect of antibiotic use on the efficacy of nivolumab in the treatment of advanced/metastatic non-small cell lung cancer: A meta-analysis
  90. NDRG2 inhibition facilitates angiogenesis of hepatocellular carcinoma
  91. A nomogram for predicting metabolic steatohepatitis: The combination of NAMPT, RALGDS, GADD45B, FOSL2, RTP3, and RASD1
  92. Clinical and prognostic features of MMP-2 and VEGF in AEG patients
  93. The value of miR-510 in the prognosis and development of colon cancer
  94. Functional implications of PABPC1 in the development of ovarian cancer
  95. Prognostic value of preoperative inflammation-based predictors in patients with bladder carcinoma after radical cystectomy
  96. Sublingual immunotherapy increases Treg/Th17 ratio in allergic rhinitis
  97. Prediction of improvement after anterior cruciate ligament reconstruction
  98. Effluent Osteopontin levels reflect the peritoneal solute transport rate
  99. circ_0038467 promotes PM2.5-induced bronchial epithelial cell dysfunction
  100. Significance of miR-141 and miR-340 in cervical squamous cell carcinoma
  101. Association between hair cortisol concentration and metabolic syndrome
  102. Microvessel density as a prognostic indicator of prostate cancer: A systematic review and meta-analysis
  103. Characteristics of BCR–ABL gene variants in patients of chronic myeloid leukemia
  104. Knee alterations in rheumatoid arthritis: Comparison of US and MRI
  105. Long non-coding RNA TUG1 aggravates cerebral ischemia and reperfusion injury by sponging miR-493-3p/miR-410-3p
  106. lncRNA MALAT1 regulated ATAD2 to facilitate retinoblastoma progression via miR-655-3p
  107. Development and validation of a nomogram for predicting severity in patients with hemorrhagic fever with renal syndrome: A retrospective study
  108. Analysis of COVID-19 outbreak origin in China in 2019 using differentiation method for unusual epidemiological events
  109. Laparoscopic versus open major liver resection for hepatocellular carcinoma: A case-matched analysis of short- and long-term outcomes
  110. Travelers’ vaccines and their adverse events in Nara, Japan
  111. Association between Tfh and PGA in children with Henoch–Schönlein purpura
  112. Can exchange transfusion be replaced by double-LED phototherapy?
  113. circ_0005962 functions as an oncogene to aggravate NSCLC progression
  114. Circular RNA VANGL1 knockdown suppressed viability, promoted apoptosis, and increased doxorubicin sensitivity through targeting miR-145-5p to regulate SOX4 in bladder cancer cells
  115. Serum intact fibroblast growth factor 23 in healthy paediatric population
  116. Algorithm of rational approach to reconstruction in Fournier’s disease
  117. A meta-analysis of exosome in the treatment of spinal cord injury
  118. Src-1 and SP2 promote the proliferation and epithelial–mesenchymal transition of nasopharyngeal carcinoma
  119. Dexmedetomidine may decrease the bupivacaine toxicity to heart
  120. Hypoxia stimulates the migration and invasion of osteosarcoma via up-regulating the NUSAP1 expression
  121. Long noncoding RNA XIST knockdown relieves the injury of microglia cells after spinal cord injury by sponging miR-219-5p
  122. External fixation via the anterior inferior iliac spine for proximal femoral fractures in young patients
  123. miR-128-3p reduced acute lung injury induced by sepsis via targeting PEL12
  124. HAGLR promotes neuron differentiation through the miR-130a-3p-MeCP2 axis
  125. Phosphoglycerate mutase 2 is elevated in serum of patients with heart failure and correlates with the disease severity and patient’s prognosis
  126. Cell population data in identifying active tuberculosis and community-acquired pneumonia
  127. Prognostic value of microRNA-4521 in non-small cell lung cancer and its regulatory effect on tumor progression
  128. Mean platelet volume and red blood cell distribution width is associated with prognosis in premature neonates with sepsis
  129. 3D-printed porous scaffold promotes osteogenic differentiation of hADMSCs
  130. Association of gene polymorphisms with women urinary incontinence
  131. Influence of COVID-19 pandemic on stress levels of urologic patients
  132. miR-496 inhibits proliferation via LYN and AKT pathway in gastric cancer
  133. miR-519d downregulates LEP expression to inhibit preeclampsia development
  134. Comparison of single- and triple-port VATS for lung cancer: A meta-analysis
  135. Fluorescent light energy modulates healing in skin grafted mouse model
  136. Silencing CDK6-AS1 inhibits LPS-induced inflammatory damage in HK-2 cells
  137. Predictive effect of DCE-MRI and DWI in brain metastases from NSCLC
  138. Severe postoperative hyperbilirubinemia in congenital heart disease
  139. Baicalin improves podocyte injury in rats with diabetic nephropathy by inhibiting PI3K/Akt/mTOR signaling pathway
  140. Clinical factors predicting ureteral stent failure in patients with external ureteral compression
  141. Novel H2S donor proglumide-ADT-OH protects HUVECs from ox-LDL-induced injury through NF-κB and JAK/SATA pathway
  142. Triple-Endobutton and clavicular hook: A propensity score matching analysis
  143. Long noncoding RNA MIAT inhibits the progression of diabetic nephropathy and the activation of NF-κB pathway in high glucose-treated renal tubular epithelial cells by the miR-182-5p/GPRC5A axis
  144. Serum exosomal miR-122-5p, GAS, and PGR in the non-invasive diagnosis of CAG
  145. miR-513b-5p inhibits the proliferation and promotes apoptosis of retinoblastoma cells by targeting TRIB1
  146. Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p
  147. The diagnostic and prognostic value of miR-92a in gastric cancer: A systematic review and meta-analysis
  148. Prognostic value of α2δ1 in hypopharyngeal carcinoma: A retrospective study
  149. No significant benefit of moderate-dose vitamin C on severe COVID-19 cases
  150. circ_0000467 promotes the proliferation, metastasis, and angiogenesis in colorectal cancer cells through regulating KLF12 expression by sponging miR-4766-5p
  151. Downregulation of RAB7 and Caveolin-1 increases MMP-2 activity in renal tubular epithelial cells under hypoxic conditions
  152. Educational program for orthopedic surgeons’ influences for osteoporosis
  153. Expression and function analysis of CRABP2 and FABP5, and their ratio in esophageal squamous cell carcinoma
  154. GJA1 promotes hepatocellular carcinoma progression by mediating TGF-β-induced activation and the epithelial–mesenchymal transition of hepatic stellate cells
  155. lncRNA-ZFAS1 promotes the progression of endometrial carcinoma by targeting miR-34b to regulate VEGFA expression
  156. Anticoagulation is the answer in treating noncritical COVID-19 patients
  157. Effect of late-onset hemorrhagic cystitis on PFS after haplo-PBSCT
  158. Comparison of Dako HercepTest and Ventana PATHWAY anti-HER2 (4B5) tests and their correlation with silver in situ hybridization in lung adenocarcinoma
  159. VSTM1 regulates monocyte/macrophage function via the NF-κB signaling pathway
  160. Comparison of vaginal birth outcomes in midwifery-led versus physician-led setting: A propensity score-matched analysis
  161. Treatment of osteoporosis with teriparatide: The Slovenian experience
  162. New targets of morphine postconditioning protection of the myocardium in ischemia/reperfusion injury: Involvement of HSP90/Akt and C5a/NF-κB
  163. Superenhancer–transcription factor regulatory network in malignant tumors
  164. β-Cell function is associated with osteosarcopenia in middle-aged and older nonobese patients with type 2 diabetes: A cross-sectional study
  165. Clinical features of atypical tuberculosis mimicking bacterial pneumonia
  166. Proteoglycan-depleted regions of annular injury promote nerve ingrowth in a rabbit disc degeneration model
  167. Effect of electromagnetic field on abortion: A systematic review and meta-analysis
  168. miR-150-5p affects AS plaque with ASMC proliferation and migration by STAT1
  169. MALAT1 promotes malignant pleural mesothelioma by sponging miR-141-3p
  170. Effects of remifentanil and propofol on distant organ lung injury in an ischemia–reperfusion model
  171. miR-654-5p promotes gastric cancer progression via the GPRIN1/NF-κB pathway
  172. Identification of LIG1 and LIG3 as prognostic biomarkers in breast cancer
  173. MitoQ inhibits hepatic stellate cell activation and liver fibrosis by enhancing PINK1/parkin-mediated mitophagy
  174. Dissecting role of founder mutation p.V727M in GNE in Indian HIBM cohort
  175. circATP2A2 promotes osteosarcoma progression by upregulating MYH9
  176. Prognostic role of oxytocin receptor in colon adenocarcinoma
  177. Review Articles
  178. The function of non-coding RNAs in idiopathic pulmonary fibrosis
  179. Efficacy and safety of therapeutic plasma exchange in stiff person syndrome
  180. Role of cesarean section in the development of neonatal gut microbiota: A systematic review
  181. Small cell lung cancer transformation during antitumor therapies: A systematic review
  182. Research progress of gut microbiota and frailty syndrome
  183. Recommendations for outpatient activity in COVID-19 pandemic
  184. Rapid Communication
  185. Disparity in clinical characteristics between 2019 novel coronavirus pneumonia and leptospirosis
  186. Use of microspheres in embolization for unruptured renal angiomyolipomas
  187. COVID-19 cases with delayed absorption of lung lesion
  188. A triple combination of treatments on moderate COVID-19
  189. Social networks and eating disorders during the Covid-19 pandemic
  190. Letter
  191. COVID-19, WHO guidelines, pedagogy, and respite
  192. Inflammatory factors in alveolar lavage fluid from severe COVID-19 pneumonia: PCT and IL-6 in epithelial lining fluid
  193. COVID-19: Lessons from Norway tragedy must be considered in vaccine rollout planning in least developed/developing countries
  194. What is the role of plasma cell in the lamina propria of terminal ileum in Good’s syndrome patient?
  195. Case Report
  196. Rivaroxaban triggered multifocal intratumoral hemorrhage of the cabozantinib-treated diffuse brain metastases: A case report and review of literature
  197. CTU findings of duplex kidney in kidney: A rare duplicated renal malformation
  198. Synchronous primary malignancy of colon cancer and mantle cell lymphoma: A case report
  199. Sonazoid-enhanced ultrasonography and pathologic characters of CD68 positive cell in primary hepatic perivascular epithelioid cell tumors: A case report and literature review
  200. Persistent SARS-CoV-2-positive over 4 months in a COVID-19 patient with CHB
  201. Pulmonary parenchymal involvement caused by Tropheryma whipplei
  202. Mediastinal mixed germ cell tumor: A case report and literature review
  203. Ovarian female adnexal tumor of probable Wolffian origin – Case report
  204. Rare paratesticular aggressive angiomyxoma mimicking an epididymal tumor in an 82-year-old man: Case report
  205. Perimenopausal giant hydatidiform mole complicated with preeclampsia and hyperthyroidism: A case report and literature review
  206. Primary orbital ganglioneuroblastoma: A case report
  207. Primary aortic intimal sarcoma masquerading as intramural hematoma
  208. Sustained false-positive results for hepatitis A virus immunoglobulin M: A case report and literature review
  209. Peritoneal loose body presenting as a hepatic mass: A case report and review of the literature
  210. Chondroblastoma of mandibular condyle: Case report and literature review
  211. Trauma-induced complete pacemaker lead fracture 8 months prior to hospitalization: A case report
  212. Primary intradural extramedullary extraosseous Ewing’s sarcoma/peripheral primitive neuroectodermal tumor (PIEES/PNET) of the thoracolumbar spine: A case report and literature review
  213. Computer-assisted preoperative planning of reduction of and osteosynthesis of scapular fracture: A case report
  214. High quality of 58-month life in lung cancer patient with brain metastases sequentially treated with gefitinib and osimertinib
  215. Rapid response of locally advanced oral squamous cell carcinoma to apatinib: A case report
  216. Retrieval of intrarenal coiled and ruptured guidewire by retrograde intrarenal surgery: A case report and literature review
  217. Usage of intermingled skin allografts and autografts in a senior patient with major burn injury
  218. Retraction
  219. Retraction on “Dihydromyricetin attenuates inflammation through TLR4/NF-kappa B pathway”
  220. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part I
  221. An artificial immune system with bootstrap sampling for the diagnosis of recurrent endometrial cancers
  222. Breast cancer recurrence prediction with ensemble methods and cost-sensitive learning
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