Home Life Sciences The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
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The effect of NK cell therapy on sepsis secondary to lung cancer: A case report

  • Jingling Tang , Lulu Xie , Honglin Liu , Liyun Wu , Xiaoyang Li , Hang Du , Xinjun Wang , Xiaoyun Li and Yuan Yang EMAIL logo
Published/Copyright: August 31, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Patients with sepsis face high mortality rates and a bleak prognosis, prompting the need for advanced therapeutic interventions. A male patient diagnosed with moderately low-differentiated squamous cell carcinoma received diverse treatments, including radiotherapy, chemotherapy, immunotherapy, and targeted therapy to inhibit angiogenesis. Subsequently, he developed sepsis after comprehensive treatment, and conventional antibiotic combinations proved ineffective in combating the infection. As an experimental approach, allogeneic natural killer (NK) cell infusion was administered. Following the NK cell infusion, the patient regained consciousness, and laboratory analyses showed reduced infection-related markers, suppressed serum inflammatory cytokines, and elevated anti-tumor cytokines. However, the therapeutic effect only lasted 2–3 days. In vitro investigations demonstrated that the allogeneic NK cell product reduced interleukin-6 levels in the patient’s serum. Moreover, subsequent co-cultivation of the NK cell product with the patient’s serum resulted in a decrease in the proportion of cytotoxic subpopulations of NK cells and a downregulation of the expression of NK-mediated killing molecules. In conclusion, adoptive transfusion of allogeneic NK cells may improve sepsis symptoms in patients with tumor-related sepsis. In vitro co-culture tests hold promise in providing predictive biomarkers for treatment effectiveness.

Graphical abstract

Keywords: natural killer cell therapy; cytokines; sepsis; lung cancer; case report

1 Introduction

Sepsis represents a critical condition characterized by organ dysfunction, bearing significant morbidity and mortality, arising from an imbalanced immune response by the host to infection [1]. Historically, a majority of research endeavors have focused on inhibiting tumor necrosis factor (TNF) and interleukin-1 to mitigate the inflammatory response [2].

During the course of sepsis, the immune system undergoes excessive activation, leading to heightened levels of circulating cytokines and hyperactivation of immune cells. Consequently, the immune response to the pathogen can contribute to the occurrence of multiorgan dysfunction and, in severe cases, even death [3]. Furthermore, even in instances where patients survive due to immunosuppression, long-term dysfunctional characteristics of immune cells persist, posing a life-threatening risk [4]. In recent years, it has come to light that natural killer (NK) cells hold promise as potential targets for therapeutic intervention, given their role as immune regulators. In this article, we present a case of sepsis secondary to lung cancer wherein the patient was treated with allogeneic NK cells.

2 Case report

A 57-year-old man presented with a persistent cough and hemoptysis persisting for a year and a half, without any prior history of chronic conditions such as diabetes, coronary heart disease, or chronic kidney disease. The patient had a long-standing history of hypertension and hyperuricemia, and the possibility of osteoporosis had been considered a year prior. In April 2019, he was diagnosed with intermediate-low differentiated squamous cell carcinoma of the left upper lung, with metastases observed in the liver, thyroid cartilage, and sternum at our medical facility. Genetic testing revealed negative EGFR, KRAS, BRAF, and PIK3CA mutations, while immunohistochemistry indicated a 5% expression of programmed cell death-ligand 1 (PD-L1) in the tumor tissue. Following multiple sessions of radiotherapy and anti-angiogenic targeted therapy, PD-L1 expression in the tumor tissue escalated to 63%.

In September 2020, the patient underwent a treatment regimen consisting of three doses of anti-tumor immunotherapy (durvalumab) in combination with chemotherapy (albumin paclitaxel) and targeted therapy (bevacizumab), accompanied by platelet-raising and leukocyte-raising measures.

During the course of the anti-tumor treatment, the patient experienced recurrent fever, immune system dysfunction, and unmanageable severe infection, culminating in sepsis and exacerbation of organ functionality impairment. Random blood glucose levels were higher than normal (Figure S1), although a diabetes diagnosis was not established due to the patient’s continued enteral nutrition. Three months later, the patient was admitted to the Intensive Care Unit (ICU) in a comatose state as a consequence of multiple comorbidities, including obstructive jaundice, multiple organ dysfunction syndrome, catheter-related bloodstream infection, intra-abdominal infection, concentrated toxic shock, lactic acidosis, fungal infection-induced necrosis of the thyroid cartilage, a postoperative abscess in the right pyriform fossa, subacute severe liver failure, hepatorenal syndrome, disseminated intravascular coagulation, toxicencephalopathy and hepatic encephalopathy, alimentary tract hemorrhage, severe anemia, and catheter-derived infection (Figure S2). Intermittent dialysis and plasma replacement therapy were initiated to address severe liver failure characterized by intermittent elevation of bilirubin levels, while red blood cell, plasma, and platelet transfusions were administered intermittently to address coagulation dysfunction. Etiological examinations suggested Klebsiella pneumoniae and Enterococcus faecium infections, complicated by refractory mucormycosis infection, which proved resistant to treatment involving multiple antibiotic regimens combined with anti-infective therapy (Tables S1 and S2). Despite treatment, the patient continued to experience recurrent fever, intermittent irritability, impaired consciousness, and progressive elevation of interleukin-6 (IL-6), C-reactive protein (CRP), and procalcitonin (PCT) levels.

Following treatment in ICU, the patient regained consciousness but remained in a critical condition. The effectiveness of anti-infection treatment was unsatisfactory, and the patient’s liver and kidney functions relied on supportive equipment for maintenance. In a multidisciplinary consultation (MDT), oncologists recommended against continuing standard anti-tumor therapy in this case and proposed considering allogeneic NK cell infusion for anti-tumor treatment and immune enhancement. After obtaining informed consent from the patient’s family, a total of seven infusions of NK cells were administered. The details of the NK cell infusion product were as follows: peripheral blood (100 mL) was collected from healthy donors without infectious pathogens. Peripheral blood mononuclear cells were isolated, and the cells were cultured in vitro using NK serum-free medium supplemented with cytokines IL2, IL15, and 5% autologous serum for a duration of 14 days. The release criteria for the product included a cell number of over 5 × 108, cell viability after resuscitation of over 85%, and a proportion of NK cells (CD3-CD56+) of over 75%. The cells were suspended in saline containing 5% human serum albumin. The activation rate, indicated by the percentage of CD16-positive cells to all NK cells (CD3-CD56+ CD16+/CD3-CD56+), was found to be greater than 70% in both cases.

After each cycle of NK cell infusion, the infection markers showed a decrease, and the patient experienced a recovery of consciousness and improved physical performance status. The laboratory data during the administration of NK cell infusions for seven cycles are depicted in Table S5. However, 2–3 days after the injection, the infection markers, including IL-6, CRP, D-dimer, and calcitonin, displayed an upward trend (Figure 1 and Table S3). Additionally, serum cytokine concentrations were measured before and after NK cell therapy. The data indicated that the treatment led to a decrease in serum levels of inflammatory cytokines (IL-6, IL-10, IL-8, and IL-1RA) and an increase in levels of anti-tumor cytokines (IFN-γ and TNF-α) (Figure 2 and Table S4).

Figure 1 Change of serum sepsis biomarkers relative to normal level after NK cell infusion, including IL-6, PCT, CRP, D-dimer. Red arrows show the time of NK cells infusion. Red arrows indicate receipt of NK cell infusion on the same day.
Figure 1

Change of serum sepsis biomarkers relative to normal level after NK cell infusion, including IL-6, PCT, CRP, D-dimer. Red arrows show the time of NK cells infusion. Red arrows indicate receipt of NK cell infusion on the same day.

Figure 2 Alterations in serum levels of inflammatory cytokines (IL-6, IL-10, IL-8, and IL-1RA) and anti-tumor cytokines (IFN-γ and TNF-α) were assessed pre- and post-third NK cell infusion. A total of seven times of NK cells were infused, and the number of cells was 0.8–1 × 109 each time. Serum samples were collected 8–12 h before NK cell infusion and 24–48 h after the last NK cell infusion.
Figure 2

Alterations in serum levels of inflammatory cytokines (IL-6, IL-10, IL-8, and IL-1RA) and anti-tumor cytokines (IFN-γ and TNF-α) were assessed pre- and post-third NK cell infusion. A total of seven times of NK cells were infused, and the number of cells was 0.8–1 × 109 each time. Serum samples were collected 8–12 h before NK cell infusion and 24–48 h after the last NK cell infusion.

Nevertheless, the infection indicators showed resurgence after 2–3 days post-injection. Considering immune hepatitis during a later MDT meeting, the patient was administered methylprednisolone at a daily dose of 40 mg on January 14, 2021, which was subsequently tapered. Following hormone treatment, the patient exhibited a progressive decrease in lymphocyte count (0.46 × 109/L to 0.22 × 109/L) and an increase in leukocyte count (9.2 × 109/L to 13.19 × 109/L). On January 21, the patient developed severe and uncorrectable acidosis, accompanied by a decrease in blood pressure, ultimately leading to demise.

  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 Ethics Committee of Affiliated Hospital of Guizhou Medical University.

3 Discussion

3.1 Sepsis

Sepsis represents a syndrome characterized by the presence of multiple organ dysfunction, resulting from persistently elevated inflammation and immunosuppression [5]. The prevalence of sepsis is higher in individuals with cancer compared to those without, primarily due to the underlying malignancy or its treatment, which can heighten the risk of severe infections. Consequently, cancer patients are deemed to be at a heightened risk of experiencing elevated mortality rates from sepsis [6]. In the case at hand, the patient was in an advanced stage of lung cancer and had undergone radiotherapy, chemotherapy, and immunotherapy utilizing anti-PD-L1 monoclonal antibodies. The anti-tumor therapy inflicted damage upon functional organs, particularly radiation-induced liver injury, while immune system dysregulation and subsequent severe secondary infection further exacerbated organ dysfunction.

Throughout the progression of sepsis, the immune system becomes excessively activated, resulting in the production of excessive levels of cytokines [7]. Cytokines play a pivotal role in modulating the immune response by facilitating protective inflammation. However, when inflammation becomes excessive, it can lead to cellular damage, triggering further activation of the innate immune system and provoking a cascade of inflammation. This, in turn, can result in organ damage and dysfunction [3].

3.2 NK cell-based therapy

NK cells possess immunoregulatory properties that contribute to the maintenance of immune system equilibrium. Previous research indicates that allogeneic NK cells can attenuate graft-versus-host disease while simultaneously exerting a graft-versus-tumor effect [8].

NK cell-based therapies primarily target anti-tumor applications. These cells can directly eliminate tumors through various mechanisms, including cytokine secretion [5], induction of apoptosis [9], and antibody-dependent cell-mediated cytotoxicity [10]. Additionally, they can indirectly exert anti-tumor effects by modulating other immune cells such as T cells, B cells, and dendritic cells [11]. Current investigations in NK cell therapy encompass CAR-NK cell therapy [12] and non-genetically modified NK cell therapy derived from diverse sources, including peripheral blood, cord blood, and induced pluripotent stem cells [13].

While there have been reports of NK cell therapy being employed in the context of COVID-19 [14], there are currently no reports on the use of NK cell therapy for the treatment of severe sepsis. Previous studies have demonstrated that NK cells can be swiftly mobilized by danger signals and are among the earliest cells to reach target organs, including inflamed central nervous system tissues [15]. The role of NK cells in regulating inflammatory responses within different organs is often intricate and occasionally contradictory [16]. It has been observed that upregulation of NK cell activity can result in the downregulation of IL-1β and IL-6 expression [17]. In this particular case, short-term allogeneic NK cell therapy proved effective in normalizing the patient’s cytokine levels, potentially attributable to the reduction in IL-6 levels resulting from the co-cultivation of NK cells. Through in vitro experiments, we confirmed the capacity of allogeneic NK cells to deplete serum IL-6 in patients.

Regarding the cytotoxicity of NK cells, the infusion of unmodified NK cells, devoid of genetic modifications, exhibits a higher level of safety. This can be attributed to the fact that NK cell immune recognition is not restricted by major histocompatibility complex, enabling them to effectively target a broad spectrum of tumors while minimizing immune-related adverse effects [13]. In comparison to CAR-T cell therapy, the utilization of CAR-NK cells also leads to fewer severe side effects, such as cytokine storm and neurotoxicity, typically observed at grades 3–4 [12].

3.3 Case management

This study reports a case in which exploratory NK cell therapy was applied in a severe disease state, leading to temporary symptom relief. The study also explores the potential mechanisms underlying the improvement of symptoms in patients after NK cell therapy. In clinical practice, aggressive or exploratory advanced treatments are typically not employed in cases similar to this report. However, the treatment of this particular patient represents a breakthrough attempt. This case report suggests that NK cell therapy may be a worthwhile approach to consider for late-stage cancer patients with multiorgan failure and sepsis. Further exploration of the reproducibility of treatment effects is warranted, along with efforts to extend the duration of effective treatment through optimization of NK cells infusion and providing a window of time for the patient’s physical recovery. Additionally, the possibility of combining antibiotic therapy and/or anti-tumor treatment should be taken into consideration.

During the course of anti-infection treatment, despite continuous optimization of the antibiotic combination, the effectiveness of the treatment did not manifest prominently. Conversely, following treatment with allogeneic NK cells, the patient’s condition exhibited temporary improvement. Immune factors implicated in tumor development processes, such as IL-6, IL-10, IL-8, and IL-1RA, were suppressed, while anti-cancer immune factors, including IFN-γ and TNF-α, were activated in the patient’s peripheral blood. Furthermore, the levels of infection indicators (IL-6, PCT, CRP, and D-dimer) demonstrated a decline following each infusion. In vitro studies showcased the phenotypic characteristics of allogeneic NK cells, as illustrated in Figure S3a. The patient exhibited an increased proportion of peripheral NK cells subsequent to NK cell treatment (Figure S3b). Following overnight co-incubation of patient serum with allogeneic NK cells in 96-well plates, we assessed changes in IL-6 concentrations in the culture medium, observing that NK cells similarly reduced IL-6 levels in the serum in vitro (Figure S3c). The original therapeutic regimen remained unaltered during the NK cell infusion, thereby indicating a potential correlation between the therapeutic effect and the infusion of NK cells from a repeatability perspective.

Previous studies demonstrated that NK cells regulate alloreactive T cells and prevent the exacerbated immune responses [8,18]. Additionally, we observed a decrease in the absolute value of both helper and killer T cells (Figure S4), along with a tendency toward a decrease in lymphocyte levels (Figure S5) following NK cell treatment. However, as we did not analyze lymphocyte subsets, it is challenging to conclude that NK cells control sepsis through the regulation of T cell levels. Instead, we are inclined to believe that NK cells act as an “absorbent sponge” for inflammatory factors, based on the direct data of cytokine changes. Furthermore, we posit that the use of in vitro co-cultured NK cells with patient serum to detect changes in serum cytokines, as well as alterations in NK cell surface markers, may serve as potential biomarkers for assessing the effectiveness of NK cell therapy in the context of sepsis.

Following treatment with allogeneic NK cells, there was an observed increase in the proportion of activated subsets (cytotoxic subsets) of peripheral blood NK cells in the patient, along with an upregulation in the expression of activation molecules (NKG2D, DNAM-1, and NKP30/46) in peripheral blood NK cells (Figure S6a). Subsequently, we conducted tests to assess the changes in NK cells within the co-culture system using the same panel. Interestingly, the in vitro results contradicted the in vivo findings. The killing function of NK cells may have been impaired after the patient’s plasma treatment, as indicated by the reduction in the proportion of cytotoxic subpopulations and the downregulation of expression of NK-mediated killing molecules (Figure S6b), implying a depletion of NK cell function in the in vitro setting. It is plausible that the activated NK cells observed in the patient’s peripheral blood consisted of a mixture of NK cells derived from the patient himself and allogeneic NK cells, while the expression of functional molecules in allogeneic NK cells diminished during in vitro co-cultivation. We speculate that the infusion of allogeneic NK cells may have contributed to the enhancement of NK cell function in the patient himself. This may help explain the modest effect and limited duration of the NK cell therapy observed in the patient.

Regrettably, the NK cell treatment failed to achieve long-term efficacy. Following hormone therapy with methylprednisolone (40 mg qd, tapered), the patient’s peripheral blood immune cells continued to decrease, resulting in immune system collapse and secondary uncontrollable infection, ultimately leading to the patient’s demise due to uncorrectable acidosis. Pathogenic microbial infections have been shown to impair the function of immune cells, including NK cells and T cells, in patients, resulting in immunosuppression [19]. In fact, next generation sequencing testing identified multiple pathogen infections (Table S1), but we believed that this weakening effect takes a relatively long time to develop, and in this case, the loss of regulatory function within 48 h after allogeneic NK cells infusion was a rapid change. Therefore, we assume that the reasons for the short-term efficacy primarily lie in two aspects. First, the infused NK cells exhibited rapid apoptotic characteristics. During the in vitro culture of NK cells, high doses of IL-2 cytokines (500 IU/mL) were used for expansion, which may have caused the NK cells to become dependent on IL-2. Consequently, when removed from the IL-2 environment, NK cell activity and the expression of effector molecules were affected [20]. In other cases of NK cell-based therapies, subcutaneous injection of IL-2 is routinely performed as an adjuvant to sustain NK cell survival in vivo. However, in this particular case, the patient was critically ill with numerous complications, and we did not utilize IL-2 for maintenance due to safety considerations. This may be a contributing factor to the failure to sustain NK cell survival and activity following infusion into the patient’s body. Second, the duration of NK cell action was short-lived. From our perspective, the inability to maintain the efficacy of allogeneic NK cell infusion was linked to the rapid loss of NK cell numbers and function, which could potentially be improved by adjusting the treatment regimen. In vitro experiments demonstrated reduced NK cell activation, suggesting a similar phenomenon occurring after NK cells entered the patient’s body. This implies that NK cells may lose their function after interacting with inflammatory factors within the body. Therefore, the inability to sustain the efficacy of allogeneic NK cell infusion may be attributed to the rapid loss of NK cell numbers and function, which could be addressed through optimization of the treatment regimen.

The immune response of the host to sepsis undergoes a transition from an initial hyper-inflammatory phase to a prolonged immunosuppressive phase within a few days [21]. Although both proinflammatory and anti-inflammatory processes commence rapidly following the onset of sepsis, the initial hyperinflammatory phase typically prevails, potentially leading to shock, high fever, and multiorgan failure [22]. In patients experiencing sepsis as a secondary effect of oncology treatment, immune depletion accelerates tumor progression and hastens patient mortality [23]. Immunotherapy aimed at stimulating the immune system hold significant potential to reverse sepsis-induced immunosuppression and improve patient outcomes [24]. The modulation of the immune system to restore and reestablish adaptive immunity may emerge as a potent approach for future sepsis treatment [25]. In the present case, the infusion of NK cells is causally associated with the alleviation of sepsis symptoms and the reduction of inflammatory factors.

4 Conclusion

This case indicates that adoptive transfusion of allogeneic NK cells can alleviate symptoms in septic patients secondary to tumors. It may potentially serve as a therapeutic approach for septic patients, particularly those with sepsis related to tumors. However, on the other hand, addressing the issue of short duration of therapeutic efficacy in NK cell therapy and seeking improvement methods is also crucial.

# These authors contributed equally to this work and share first authorship.

  1. Funding information: This work was supported by National Natural Science Foundation of China (82260584), Department of Science & Technology of Guizhou Province ([2022]-193, ZK[2023]-359, [2023]-373), Guiyang Bureau of Science and Technology ([2022] 5-17), and Health Commission of Guizhou Province (GZWKJ2023-041). The funders are not involved in the study design, data collection, analysis, or interpretation of data; and in the decision to submit the article for publication.

  2. Author contributions: J.T. and L.X. conceived the study. H.L., X.L., and X.W. performed data collection and analysis. L.W., X.L., and H.D. performed the cell experiment. Y.Y. supervised and revised the manuscript. All authors have read and approved the manuscript.

  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: 2023-04-20
Revised: 2023-07-19
Accepted: 2023-07-30
Published Online: 2023-08-31

© 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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  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”
https://doi.org/10.1515/biol-2022-0702
Keywords for this article
natural killer cell therapy; cytokines; sepsis; lung cancer; case report
Creative Commons
BY 4.0

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  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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