Home Antiphospholipid antibodies and the risk of thrombosis in myeloproliferative neoplasms
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Antiphospholipid antibodies and the risk of thrombosis in myeloproliferative neoplasms

  • Rūta Dambrauskienė EMAIL logo , Rolandas Gerbutavičius , Milda Rudžianskienė , Renata Paukštaitienė , Astra Vitkauskienė , Erika Skrodenienė , Diana Remeikienė , Inga Zaborienė and Elona Juozaitytė
Published/Copyright: February 7, 2023

Abstract

The morbidity and mortality of BCR-ABL-negative myeloproliferative neoplasia (MPN) patients is highly dependent on thrombosis that may be affected by antiphospholipid antibodies (aPLA) and lupus anticoagulant. Our aim was to evaluate the association of the aPLA together with platelet receptor glycoprotein (GP) Ia/IIa c.807C>T CT/TT genotypes and thrombotic complications in patients with MPNs. The study included 108 patients with BCR-ABL-negative MPN with data of previous thrombosis. Two different screening and one confirmatory test for the lupus anticoagulant were performed. Thrombotic complications were present in 59 (54.6%) subjects. aPLA were more frequently found in MPN patients with thrombosis vs no thrombosis (25.4 and 6.1%; p = 0.007). MPN patients with arterial thrombosis were more frequently positive for aPLA vs no arterial thrombosis (38.8 and 11.9%; p = 0.001). aPLA were more frequently found in patients with cerebrovascular events vs other arterial thrombotic complications or no thrombosis, respectively (39.3, 6.1, and 12.9%; p < 0.001). MPN patients with thrombosis were more frequently positive with aPLA and had platelet receptor GP Ia/IIa c.807C>T CT/TT genotypes compared to MPN patients without thrombosis (18.6 and 2.0%; p = 0.006). aPLA alone or with coexistence with platelet receptor GP Ia/IIa c.807C>T CT/TT polymorphism could be associated with thrombotic complications in patients with MPN.

1 Introduction

BCR-ABL-negative myeloproliferative neoplasms (MPNs) – polycythemia vera (PV), essential thrombocythemia (ET), and primary myelofibrosis (PMF) – are grouped together within the WHO MPN category [1]. The most important BCR-ABL-negative MPN complications that interfere patient’s morbidity and mortality are thrombosis. They occur in all MPN entities range from 13 to 40% of patients [2,3,4].

The pathogenesis of thrombosis in MPN is multifactorial. Hematopoietic cell’s clonal proliferation, blood cells, and endothelial activation as well as close interactions of circulating plasma markers are known to take role in thrombosis pathogenesis in MPNs [5,6]. aPLA – anti-β2 glycoprotein 1 antibodies (anti-β2GP1) – bind to the β2GP1 receptors on the platelet surface, activating them that is important for thrombus formation [7]. In MPN patients, circulating platelets are already activated and they secret higher levels of surface P-selectin and tissue factor (TF) [8]. These processes allow thrombin formation on the platelet surface and initiation of thrombosis via thromboxane A2 synthesis [7]. Other cells are are activated as well: monocytes and endothelial cell. Recent data also suggest that neutrophils with TF expression and the release of neutrophil extracellular traps (NETosis) may contribute to aPLA-related vasculopathy in antiphospholipid syndrome (APS). Antiphospholipid syndrome is characterized by the presence of persistent aPL antibodies including anticardiolipin antibodies (aCL), lupus anticoagulant (LA) and anti-β2GP1 [8]. We included the analysis of anti-β2GP1 as in MPN patients, circulating platelets are already activated, and they secret higher levels of surface P-selectin and TF [9]. These processes allow thrombin formation on the platelet surface and initiation of thrombosis via thromboxane A2 synthesis [7]. Endothelial cells are additionally activated in MPN after aPLA interaction, and this process plays an important role in the pathogenesis of thrombosis [10].

There are limited data that analyzed aPLA in MPN patients. In 50 patients of Jensen et al.’s cohort, immunoglobulin M (IgM)–aCL were detected in 22% of MPN patients and only 3% of the control group [11]. Bidot et al. found at least one positive aPLA in 66% of tested subjects with ET. The incidence of aPLA in patients with thrombotic complications was 92.8% for those with thrombosis and 47.6% for those without thrombosis [12].

In the prospective study of 1,179 patients, conducted by Schwarz et al., aPLA were significantly associated with thrombotic complications [13].

In a study of 192 patients with MPNs, Tevet et al. identified aPLA (LA) in nine patients (14.51%), which were significantly related to thromboses [14].

The main purpose of our study was to evaluate the antiphospholipid antibodies (aPLA) and possibly their association with thrombosis as well as in their possible relationship with other risk factors in patients with MPNs. We also investigated combined aPLA effect on thrombotic complications together with the platelet receptor glycoprotein (GP) Ia/IIa c.807C>T CT/TT polymorphisms at the Department of Oncology and Hematology of the Institute of Oncology, the Lithuanian University of Health Sciences.

2 Methods

2.1 Samples and baseline

The study was conducted at the Department of Hematology of the Institute of Oncology, the Lithuanian University of Health Sciences. It included 108 patients with BCR-ABL-negative MPN. The diagnosis of ET, PV, and PMF was according to the WHO 2016 diagnostic criteria. Data of previous thrombosis and risk factors as well as clinical and laboratory findings were collected. Arterial or venous thrombosis, such as stroke, myocardial infarction, transient ischemic attack, unstable angina, legs’ deep vein thrombosis, legs’ superficial vein thrombosis, thrombosis of abdominal veins, and thrombosis of the pulmonary artery (PE) were defined as vascular events. Those complications were assessed with reference to medical documentation.

There were two different selective and one confirmatory tests for the aPL determination. Tests were performed at the Laboratory Clinic of Kaunas Clinics of the Lithuanian University of Health Sciences Hospital.

The genomic DNA was isolated from peripheral blood leukocytes using the DNA-purification kit according to the manufacturer’s standard protocol at the Oncology Research Laboratory, Institute of Oncology. For all patients included in the study, genotyping of platelet receptor GP Ia/IIa (c.807C>T) polymorphism was performed. Results of other platelet receptor GP polymorphism were published before [15].

All comparisons were performed between two groups of MPN patients – who experienced thrombosis and who did not experience thrombosis. Informed consent has been obtained from patients who participated in clinical investigations.

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies, and in accordance with the tenets of the Helsinki Declaration and has been approved by the authors’ institutional review board or equivalent committee.

2.2 Statistical analysis

Statistical analyses were performed with IBM SPSS Statistics 22 (SPSS Inc., Chicago, IL, USA). Categorical (qualitative) variables were compared using the Pearson chi-square feature independence (homogeneity) criterion. The results are described by the frequencies and relative frequencies (percent) of the significance values of the traits. Quantitative characteristics that satisfied the conditions of the normal partition were compared in independent groups using the Student’s t criterion and those that did not meet the Mann–Whitney U criterion. The data are described in the first case with mean (standard deviation [SD]) and in the second case with median (minimum - maximum values; means). All statistical tests were two-sided, and the level of statistical significance was established at α = 0.05 (p-value <0.05).

3 Results

In the study population of 108 patients, 60 (55.6%) patients were diagnosed with ET, 41 (38%) patients were diagnosed with PV, and 7 (6.5%) were PMF patients. Demographic data of the patients were published earlier [15]. The JAK2 V617F mutant allele was present in 71.4% of PMF patients, 87.8% of PV and 61.7% of ET patients. Thrombotic complications were present in 59 (54.6%) subjects of those with MPN. The patients with thrombotic complications were older than those without thrombotic complications, 66.98 (SD = 13.42) years and 60.17 (SD = 15.58) years (p = 0.016). There were no gender differences between the groups. LA was present in nine (8.3%) MPN patients. Solid phase aPLA were detected in 18 (16.7%) MPN patients. Patients with positive aPLA were older than those without aPLA (72.5 and 63.0 years; p = 0.017). PV patients were more likely to have aPLA than ET or PMF patients (66.7, 27.8, and 5.6%; p = 0.6). Distribution of different aPLA classes in MPN patients with thrombosis and without thrombosis is shown in Table 1.

Table 1

Distribution of aPLA classes in MPN patients with thrombosis compared to patients without thrombosis

aPLA No thrombosis, n (%) With thrombosis, n (%) p value
aCL IgM 1 (2.0) 3 (5.1) 0.41
aCL IgG 8 (13.6)
anti-β2 GPI IgM 1 (2.0) 2 (3.4) 0.67
anti-β2 GPI IgG 2 (4.1) 7 (11.9) 0.14

aPLA – antiphospholipid antibodies; aCL – cardiolipin antibodies, anti-β2 GP1 – anti-glycoprotein 1 antibodies.

aPLA were significantly more frequently found in MPN patients with thrombosis than in patients without thrombosis (25.4 and 6.1%; p = 0.007) (Figure 1).

Figure 1 
               aPLA in MPN patients (n = 108). χ
                  2 – chi-square test. *Data are presented as % in the thrombosis group. #Data are presented as % in the no thrombosis group.
Figure 1

aPLA in MPN patients (n = 108). χ 2 – chi-square test. *Data are presented as % in the thrombosis group. #Data are presented as % in the no thrombosis group.

MPN patients with arterial thrombotic complications were significantly more frequently positive for aPLA compared to those without arterial thrombosis (38.8 and 11.9%; p = 0.001) (Figure 2).

Figure 2 
               aPLA and LA in MPN patients (n = 108). χ
                  2 – chi-square test. *Data are presented as % within thrombosis group patients. #Data are presented as % within group of patients without thrombosis.
Figure 2

aPLA and LA in MPN patients (n = 108). χ 2 – chi-square test. *Data are presented as % within thrombosis group patients. #Data are presented as % within group of patients without thrombosis.

MPN patients with thrombotic complications were significantly more frequently positive with aPLA and had platelet receptor GP Ia/IIa c.807C>T CT/TT genotypes compared to MPN patients without thrombotic complications (18.6 and 2.0%; p = 0.006) (Figure 3).

Figure 3 
               Distribution of the aPLA together with platelet receptor GP Ia/IIa c.807C>T CT/TT genotypes in MPN patients (n = 108). aFisher‘s exact test. *Data are presented as % in the thrombosis group. #Data are presented as % in the no thrombosis group.
Figure 3

Distribution of the aPLA together with platelet receptor GP Ia/IIa c.807C>T CT/TT genotypes in MPN patients (n = 108). aFisher‘s exact test. *Data are presented as % in the thrombosis group. #Data are presented as % in the no thrombosis group.

aPLA were significantly more frequently found in patients with cerebrovascular events (ischaemic stroke and TIA) compared to MPN patients with other thrombotic complications or MPN patients with no thrombosis, respectively (39.3, 6.1 and 12.9%; p < 0.001).

4 Discussion

The main objective of this study was to evaluate whether aPLA could be associated with the risk of thrombosis alone or with the other risk factors in patients with MPNs.

Circulating aPLA and lupus anticoagulant are found in patients with malignancies, in APS and in patients with arterial and venous thrombosis [16]. It is known that the formation of aPLA on the cell membrane affects them not only directly but also via various cofactors, such as platelet receptor beta-2 (β2) glycoprotein-1 [10].

In our patient’s blood samples, we found a higher incidence of aPLA in older patients than in younger patients, and this was consistent with data reported in the literature [17].

Analyzing data from patients with different MPN, we found that aPLA is more commonly detected in PV than in patients with ET or PMF, although this difference was not statistically significant in our research. Bidot et al. also found a relationship between thrombotic complications and aPLA in ET patients [12]. In the study of the Schwarz et al., aPLA were significantly related to thrombosis [13]. Our study found that the aPLA increased the risk of thrombotic complications.

When we separated patients with arterial thrombosis according to different arterial circulation regions, we found that aPLA were statistically significantly more common in patients with ischemic stroke and TIA than in subjects who had not experienced thrombotic complications or experienced other thrombotic complications. Djokovic et al. found that APS subjects who experienced cerebrovascular thrombotic complications were more likely to be diagnosed with IgG β2GP1 antibodies than those who had not experienced these complications [18]. Carmel-Neiderman et al. who studied patients with the stroke and aPLA compared these data with the healthy control group. They also found a tendency for IgG-class aPLA to be more common in the ishaemic stroke group than in healthy people [19]. Meta-analysis that was done by Sciascia et al. included 5,215 patients from 43 clinical trials; it was found that the presence of aPLA increased the risk of ishaemic stroke and TIA in subjects under 50 years of age [20]. Our results support the data that aPLA could be associated with developing ischemic stroke and TIA in patients with MPN.

Analyzing the separate classes of aCL and anti-β2GPI, we found that IgG-class aCL and anti-β2 IgG aPLA were found more frequently than anti-β2 IgM aPL antibodies or aCL in patients with thrombotic complications.

In our research, we analyzed the synergism of aPLA antibodies and platelet receptor SNP effect on thrombosis. We described earlier platelet receptor and coagulation factor SNP impact on thrombosis [15]. Analyzing MPN subjects who had experienced thrombotic complications, we found that these subjects were more likely to be positive for aPLA antibodies in combination with GP Ia/IIa c.807 CT or TT genotype (T allele) than subjects without thrombosis. The c.807C>T T allele of the platelet receptor GP Ia/IIa (ITGA2 gene) has been shown to be associated with higher receptor density and an increased risk of thrombotic development [21]. On this basis, it can be assumed that platelets with this SNP are more active, while concomitant aPLA antibodies may activate them even more by binding to the platelet, creating favorable conditions for thrombosis. Therefore, we can hypothesize that these patients with MPN who are positive with aPLA and have platelet receptor GP Ia/IIa c.807 CT or TT genotype may be linked with more frequent thrombotic complications.

The results of our study show that aPLA alone or in combination with the platelet receptor GP Ia/IIa c.807 CT or TT genotype increased the risk of thrombotic complications in patients who are diagnosed with MPNs.


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Acknowledgments

The authors would like to thank medical biologists at the Institute of Oncology Scientific Laboratory for performing molecular genetic analysis.

  1. Funding information: Authors state no funding involved.

  2. Author contributions: Conceptualization, R.D. and R.G.; methodology, E.J. and D.R.; software, R.P.; validation, R.D.; formal analysis, R.P.; investigation, R.D., A.V., E.S., and D.R.; resources, A.V. and E.S.; data curation, M.R. and I.Z.; writing – original draft preparation, R.D.; writing – review and editing, R.G.; visualization, R.D.; supervision, E.J.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2022-10-03
Revised: 2022-11-19
Accepted: 2022-12-14
Published Online: 2023-02-07

© 2023 the author(s), published by De Gruyter

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

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  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
  105. Effects of physical exercise on biomarkers of oxidative stress in healthy subjects: A meta-analysis of randomized controlled trials
  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
  112. CXCL12/CXCR4/CXCR7 axis in placenta tissues of patients with placenta previa
  113. Association between thyroid stimulating hormone levels and papillary thyroid cancer risk: A meta-analysis
  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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