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Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series

  • Na Wang , Zhichao Gao , Shuai He , Mengzhen Han , Wenjie Han , Xiaolin Liu , Hui Cao , Mingxi Jing , Tao Sun and Junnan Xu EMAIL logo
Published/Copyright: July 17, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

A lung abscess is a necrotizing infection caused by microbiomes that lead to the loss of healthy lung tissue. The routine culture is a waste of time and yields false-negative results, and clinicians could only choose empiric therapy or use broad‐spectrum antibiotics, which could significantly contribute to the problem of resistance or aggravate the condition. We report three patients with a routine-culture-negative lung abscess. The presenting symptoms included fever, cough, dyspnea, and chest pain, and a computed tomography scan revealed a lesion in the lungs. The bronchoalveolar lavage fluid and pleural fluid were tested for pathogens using metagenome next-generation sequencing (mNGS), and the results revealed Fusobacterium nucleatum and Streptococcus spp. (S. constellatus, S. intermedius) as the most represented microbial pathogens. Our data demonstrated that mNGS could be a promising alternative diagnostic tool for pathogen detection, and the pathogen lists indicate that it will be important to focus on the Streptococcus genus rather than the dominant Streptococcus spp. in terms of co-infection of pathogen determined by shotgun mNGS.

Graphical abstract

The aim of this article was to employ shotgun mNGS for pathogen diagnosis in three patients with lung abscesses. The pleural fluid or bronchoalveolar lavage fluid from patients was sent to traditional culture and the shotgun mNGS test. Laboratory culture tested negative and shotgun mNGS analysis revealed a co-infection caused by Fusobacterium nucleatum and Streptococcus spp. After standard treatment of co-infection, patients gradually improved and were discharged. This figure is drawn by Figdraw.

Keywords: co-infection; Fusobacterium nucleatum ; lung abscess; shotgun metagenome next-generation sequencing; Streptococcus spp.

1 Introduction

Lung abscess is defined as a microbial infection in lung parenchyma, and typically exhibits a cavity (more than 2 cm) containing necrotic debris or fluid [1]. It continues to be a fatal disease, despite significant progress made in percutaneous drainage and antibiotic therapy. Based on the species of pathogenic microorganisms, lung abscesses could be divided into mono-microbial and polymicrobial infections, which have major differences in antibiotic therapy and prognosis [2]. Mono-microbial lung abscess is caused by Streptococci, Staphylococcus aureus, Acinetobacter baumannii, Klebsiella pneumoniae, Pseudomonas aeruginosa, and so on [3]; while polymicrobial infection is common and is up to 72.2% [4], containing multiple anaerobic bacteria. Fusobacterium nucleatum (Fn) and Bacteroides spp. are predominant among all anaerobes. For known microbial pathogens, different pathogens may be treated with different antibiotics. For example, vancomycin or linezolid are preferred for methicillin-resistant S. aureus infection, while for Legionella micdadei the choice is the macrolide antibiotic. Metronidazole, as a single therapy, does not appear to be particularly useful due to polymicrobial flora [3]. There is evidence that adhesion and invasion protein can influence bacterial co-aggregation, resulting in increased chances of co-infection [4]. Early diagnosis of pathogens contributes to facilitating prompt antibiotic treatment, while virulence gene analysis contributes to the understanding of the precise mechanism of co-infection.

Currently, clinical microbial pathogen detection is still dominated by traditional methods such as culture, staining microscopy, and PCR, which have limitations such as long culture cycles and low sensitivity. For example, the identification of mycobacterium strains takes up to 30 days, while some anaerobic bacteria and viruses have extremely strict requirements on culture conditions, and even cannot be cultured. Although PCR-based molecular diagnostic technology has solved the above problems of pathogen identification, it is difficult to solve the detection problem of unknown microorganisms because primers cannot be designed for nucleic acid sequences of unknown microorganisms [5]. Metagenome next-generation sequencing (mNGS) has the ability to overcome the limitations of these traditional microbial pathogen detection methods and can be directly sequenced and identified without relying on known nucleic acid sequences [6]. As an unbiased pathogen detection method, mNGS can be used in many diseases caused by infection, including central nervous system infections, bloodstream infections, and ocular infections [7–9].

The presence of commensal oral flora organisms, which in some cases may also be pathogens, further complicate pathogen diagnosis in respiratory infections. One of the most striking advantages of mNGS is the ability to distinguish infection from colonization. Furthermore, the administration of broad-spectrum antimicrobial agents may render it difficult to routine culture microorganisms, impairing pathogen diagnosis. mNGS is also capable of overcoming the limitations of this traditional culture. Another advantage of mNGS is that it enables the unbiased and rapid detection of high numbers of pathogens, ranging from bacteria to fungi, viruses, and parasites, addressing the limitation of missed detections. Clinical guidelines and expert consensus have also confirmed that mNGS has greatly enhanced our ability to diagnose, interrogate, and track infectious diseases, as well as these techniques allow researchers to investigate variation in the microbial community structure in a culture-independent manner [10,11]. Lung abscess co-infection is always culture-negative and the possibility of missed detection is also present in clinical setting, which mainly relies on empiric therapy. Herein, we report three cases of lung abscesses caused by Fn combined with Streptococcus (including S. constellatus and S. intermedius) using shotgun mNGS, as well as detecting the presence of virulence genes FadA and RadD, which may be useful to search co-infectious mechanism.

2 Patients and methods

2.1 Patients

This study enrolled three patients with lung abscesses of Fn and Streptococcus co-infection who were admitted to Liaoning Cancer Hospital between April 2021 and June 2021. The criteria for patient inclusion were the following: (1) the patient presented with symptoms including fever, cough, dyspnea, and chest pain; (2) imaging examination showed that the lungs appear as cavitary lesions with infiltrates; (3) Fn and Streptococcus were detected by mNGS with relative abundance in the top 2, and no other pathogenic bacteria that could cause lung abscesses such as Klebsiella pneumonia, S. aureus, and Mycobacterium were detected in the top 10 or their abundance was less than 1%; and (4) the subjects gave their permission for this study within the informed consent form.

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

  2. Ethical approval: The research related to human use complied with all the relevant national regulations, institutional policies, and is in accordance with the tenets of the Helsinki Declaration, and has been approved by the Ethics Committee of Liaoning Cancer Hospital (20201135K).

2.2 DNA extraction, library preparation, and sequencing

Total DNA from BALF and pleural fluid were extracted using the nucleic acid extracted kit (51304, QIAGEN, Germany) and purified using DNA Purification Magnetic Beads (Vazyme, China). DNA libraries were then constructed using the DNA Library Prep Kit (NDM617, Vazyme, China) and sequenced with a 100 bp single-end protocol on an MGISEQ-2000RS sequencing platform.

2.3 Quality control of reads and removal of human reads

Multiple open-source and private software packages were employed to process the raw sequences. Accordingly, sequences were deduplicated, quality trimmed, and adapter-removed using clumpify from the BBTools suite and fastp. The sequences that were mapped to the human reference genome GRCh38 were eliminated using Bowtie2 with options p 16. A secondary analysis of sequences was undertaken using BMTagger software in order to further exclude human host reads. A FASTQ file was then generated from reads, which did not align using Samtools (view -b -f 4, -F 256).

2.4 Taxonomic classification and verification

The FASTQ file was analyzed using two different classifiers: KMA (v 1.3.6) and Blastn (v 2.10.1). The two software packages were chosen to ensure the objectivity and accuracy of our research. KMA was run against the laboratory-developed microbial databases that included 16,959 bacteria, 314 fungi, 9,010 viruses, 173 parasites, 208 mycobacteria, and 162 mycoplasma/chlamydia to determine pathogens and their relative abundance. Blastn was run using options -max_target_seqs 5, -num_threads 10, -outfmt 6 and -evalue 1 × 10−10 on the NCBI-nt database. Principal component analysis (PCA) biplots were generated from the pathogen data using the PCA online analysis website (http://www.ehbio.com/Cloud_Platform/front/).

2.5 Prediction of virulence genes for Fn

The completed reference sequences of Fn were downloaded from the NCBI database to identify virulence genes FadA and RadD. The coverage and depth of Fn and its FadA and RadD genes in the three patients were generated and the formulae are as follows: Coverage = (# area covered by mapped reads)/(# area of reference) and Depth = (# of bases mapping to the locus)/(size of locus). Fn reads were assembled by SPAdes (v3.15.2) with default parameters, except for kmer sizes (kmer = 35). Scaffolds of short (<500 bp) were filtered out. The quality of genome assembly was assessed using the QUAST version 5.0.2 with default parameters. The known FadA signal peptide protein sequences (MKKFLLLAVLAVSASAFA) as queries to search gene models of Fn were determined using BLASTP (v2.10.1), with an e-value threshold of 1 × 10−5.

3 Clinical presentation

3.1 Case 1

A 76-year-old female was transferred to us with chest distress, chest pain for 1 month, severe cough, and expectoration to last 3 days. The patient was in poor physical condition and had a past medical history of hypertension and diabetes for over 15 years and pulmonary fibrosis for 3 years. The initial analysis revealed the following: white blood cell (WBC) count of 8.0 × 109/L, neutrophil proportion of 71.0%, lymphocyte proportion of 23.4%, C-reactive protein (CRP) of 16.4 mg/L, and pro-calcitonin (PCT) of 0.05 μg/L. Thoracic computed tomography (CT) scanning indicated a 56 mm × 41 mm cavitary lesion in the lower lobe of the left lung, and spots, patches, and solid shadows surrounded the mass. A left lower lobe lesion with soft tissue density and pleural effusion was present (Figure 1a). The patient was diagnosed with a pulmonary abscess, treated with intravenous mezlocillin and ornidazole for 4 days, and the disease progressed. The patient underwent CT-guided percutaneous drainage and approximately 30 mL of thick pus was removed; the pleural fluid was sent for culture and for the shotgun mNGS test. The laboratory culture results were negative. Shotgun mNGS analysis revealed that Fn has 72,426 reads and the abundance was 19.0%; the 288,845 reads corresponded to the Streptococcus genus, in which S. constellatus was up to 54.8% (Figure 2a and 2b). Fn and S. constellatus were considered potential pathogens. Virulence genes FadA and RadD were detected because the former is the best-characterized virulence gene of Fn and the latter possesses the ability to bond with the Streptococcus spp. The coverage of FadA was only 7.2% and no signal peptides were detected, while the RadD gene coverage was 66.5%. Streptococcus spp. was excluded from virulence genes analysis because of high homology results in multiple mapping. The symptoms were gradually relieved when the patient was switched to piperacillin-tazobactam; the patient was discharged after 10 days.

Figure 1 (a) Chest CT revealed cavitary lesion (56 mm × 41 mm) in the lower lobe of the left lung in case 1. (b) Chest-enhanced CT of case 2 showing a mass in the upper lobe of the left lung (about 45 × 34 mm). (c) A ches- enhanced CT scan revealed a soft tissue mass shadow in the upper lobe of the left lung in case 3.
Figure 1

(a) Chest CT revealed cavitary lesion (56 mm × 41 mm) in the lower lobe of the left lung in case 1. (b) Chest-enhanced CT of case 2 showing a mass in the upper lobe of the left lung (about 45 × 34 mm). (c) A ches- enhanced CT scan revealed a soft tissue mass shadow in the upper lobe of the left lung in case 3.

Figure 2 Read numbers and relative abundance of pathogens in three patients using two different taxonomic software. (a) The read numbers of pathogens at the genus level. (b) Taxonomic composition and relative abundance of pathogens at the species level.
Figure 2

Read numbers and relative abundance of pathogens in three patients using two different taxonomic software. (a) The read numbers of pathogens at the genus level. (b) Taxonomic composition and relative abundance of pathogens at the species level.

3.2 Case 2

A 40-year-old female experienced pain in the right sternocostal part for 4 days. Chest enhanced CT showed a mass in the upper lobe of the left lung, about 45 mm × 34 mm in size. After enhanced CT scan, no enhanced areas was visible inside, and aerated bronchus sign inside the lesion. The lesion spans the interlobular fissure to the dorsal segment of the left lower lobe of the lung, and no obvious mass was present on the chest wall (Figure 1b). The laboratory test showed a WBC count of 11.4 × 109/L, 74.2% neutrophils, 17.2% lymphocytes, 127.2 mg/L CRP, and 0.07 μg/L PCT. She was treated with levofloxacin. After 2 days, she developed an intermittent high fever, which was up to 39.5℃. The sputum culture grew a normal oral microbiome, and the analysis of BALF with shotgun mNGS reported Fn (554,856 reads, abundance: 55.7%) and Streptococcus genus (410,708 reads, abundance: 41.3%). S. intermedius was the most frequent species, which was up to 94.4% (Figure 2c and 2d). Virulence genes FadA of Fn had 50.8% coverage, with complete signal peptides (coverage 100%) and RadD coverage was 59.7%. The antibiotic treatment was changed to biapenem. Her chest discomfort diminished and her stomach upset symptoms improved. After 4 days, the blood test showed a WBC count of 6.7 × 109/L, 45.3% neutrophils, 43.5% lymphocytes, 0.8 mg/L CRP, and 0.04 μg/L PCT. The patient was symptomatically better and discharged.

3.3 Case 3

A 59-year-old male presented with sustained fever and chest pain for 3 days. The highest body temperature was up to 39℃. A chest-enhanced CT scan revealed a soft tissue mass shadow in the upper lobe of the left lung, a large consolidation shadow in the distal part, and no small nodular shadows were seen around. A few solid shadows in the lower lobes of both lungs were seen (Figure 1c). The blood test showed a WBC count of 9.9 × 109/L, 78.9% neutrophils, 12.7% lymphocytes, 164.0 mg/L CRP, and 0.11 μg/L PCT. He was treated with etimicin for 2 days, but the fever continued. The patient underwent ultrasound-guided percutaneous drainage, and 75 mL of pleural fluid was removed and sent for pathogen testing. The routine culture had no bacteria growth. Shotgun mNGS analysis revealed Fs and Streptococcus genus accounting for 66.2% of the total abundance, and a low amount of diversified microbiomes were detected such as Rhodococcus (6.8%) and Campylobacter (4.6%) (Figure 2e and 2f). It was identified that the patient was co-infected with Fn (11,716 reads, abundance: 31.4%) and Streptococcus genus (10,066 reads, abundance: 27.0%). The patient was excluded from virulence gene analyses because the coverage of Fn was only 35.1% and poor assembly quality may lead to misjudgment. The patient was switched to meropenem for 8 days, and the patient’s body temperature returned to normal gradually and the pain dissipated. The CT scan showed radiological improvement and the patient was discharged. In fact, the chest-enhanced CT scan revealed a soft tissue mass shadow in the upper lobe of the left lung. The clinician suspected the possibility of a tumor and recommended surgery but the patient did not accept it for financial reasons. The basic clinical information and mNGS results in the three patients with lung abscesses are summarized in Table 1.

Table 1

Basic clinical information and mNGS results in three patients with lung abscess

Case Age, gender Potential risk factor Sample type Medication history mNGS result Treatment Outcomes
Fn and Streptococcus (%) Fn and dominant Streptococcus (%)
1 76, F Diabetes Pleural fluid Mezlocillin, ornidazole 95.0 60.6 Piperacillin-tazobactam + percutaneous drainage Good evolution (10 days)
2 40, F None BALF Levofloxacin 97.0 94.7 Biapenem Good evolution (4 days)
3 59, M None Pleural fluid Etimicin 58.4 38.8 Meropenem + percutaneous drainage Good evolution (10 days)

Fn: Fusobacterium nucleatum, BALF: bronchoalveolar lavage fluid.

The patients were followed up by phone call consultation every 2 weeks for a total of 3 months. Cases 1 and 2 showed good tolerability and improved completely without recurrence, and no severe adverse reactions or unanticipated events have been reported. Case 3 was treated with anti-tumor therapy in a higher-grade hospital and additional clinical information is not available.

The standard mNGS protocol is briefly described as follows. It involves a series of DNA extraction, library preparation, sequencing, and data analysis. Total DNA from BALF and pleural fluid were extracted using the nucleic acid extracted kit (51304, QIAGEN, Germany) and purified using DNA Purification Magnetic Beads (Vazyme, China). DNA libraries were then constructed using the DNA Library Prep Kit (NDM617, Vazyme, China) and sequenced with a 100 bp single-end protocol on an MGISEQ-2000RS sequencing platform. Multiple open-source and private software packages were employed to process the raw sequences. Accordingly, sequences were deduplicated, quality trimmed, and adapter-removed using clumpify from the BBTools suite and fastp. The sequences that were mapped to the human reference genomes GRCh38 were eliminated using Bowtie2 with options -p 16. A secondary analysis of sequences was carried out using BMTagger software in order to further exclude human host reads. A FASTQ file was then generated from reads, which did not align using Samtools (view -b -f 4, -F 256). After removing the human sequences, the remaining reads were analyzed using two different classifiers KMA and Blastn to ensure the objectivity and accuracy of our research. KMA was run against a laboratory-developed microbial databases that included 16,959 bacteria, 314 fungi, 9010 viruses, 173 parasites, 208 mycobacteria, and 162 mycoplasma/chlamydia. The parameters of KMA are set as -sam 4, -t_db, -1t1, -t 16, -mem_mode -cge -ef -a. Blastn was run using options -max_target_seqs 5, -num_threads 10, -outfmt 6 and -evalue 1 × 10−10 on the NCBI-nt database. To estimate the microbiome community structure differences in different taxonomic classification methods, a PCA was performed and reflects Fs and Streptococcus consistency in classification, despite particular deviations in relative abundance (Figure 3). The Blastn confirmed the reliability of the analysis by KMA results, so subsequent analysis of the virulence genes was dominated by the KMA result.

Figure 3 PCA of the datasets in the Fusobacterium and Streptococcus genus using KMA and Blastn. The green circles and red-brown triangles represent the Blastn and KMA taxonomic methods, respectively. The PCA results for the two taxonomic methods showed similar results in general, which reflects consistency in classification, despite the different methods used.
Figure 3

PCA of the datasets in the Fusobacterium and Streptococcus genus using KMA and Blastn. The green circles and red-brown triangles represent the Blastn and KMA taxonomic methods, respectively. The PCA results for the two taxonomic methods showed similar results in general, which reflects consistency in classification, despite the different methods used.

4 Discussion

Lung abscess is a severe infection and has a high prevalence worldwide. Early microbial pathogen diagnosis and prompt treatment are crucial for preventing potential fatalities and improving health outcomes. In our study, the most common symptoms in three patients with lung abscesses were fever (66.7%), chest distress, or chest pain (100.0%). These match with those reported in the literature [12]. In addition, the pathogenic microorganisms of lung abscesses have been described in a wide genus species range. For example, Adlakha and Muppala reported a patient with a lung abscess caused by Propionibacterium acnes [13], whereas Hayashi et al. reported a secondary pulmonary abscess caused by Nocardia asiatica in a 78-year-old Japanese man [14]. The clinical symptoms and signs of lung abscesses caused by different pathogens are very similar and are often difficult to identify [12]. Therefore, it is essential to identify the pathogen as soon as possible to choose and optimize antibiotic therapy. However, some anaerobic bacteria or viruses have extremely strict requirements on culture conditions, which will result in false-negative results. A 14-year retrospective cohort study conducted by Fernando et al. showed that the positive rate of conventional blood culture in patients with lung abscesses was only 27.9% [15]. Although interventional methods have increased the detection rate of pathogens responsible for lung abscesses, it is still only 60% [16]. Physicians could only prescribe empirical treatment with broad-spectrum antibiotics if cultures are not available, which could lead to resistance or therapy failure. Herein, we employ shotgun mNGS to diagnose the pathogen of three patients with lung abscesses whose conventional pathogen cultures were negative and identified the co-infection by Fn and Streptococcus spp. Fn and Streptococcus are difficult to culture in the clinic, which makes the diagnosis of lung abscess pathogen at an early time point an intractable problem. Shotgun mNGS, a revolutionized tool in assisting clinical pathogen diagnosis, plays a unique role in identifying novel and rare pathogens such as Pneumocystis jiroveci and Chlamydia psittaci [17,18].

A range of similarities exists in congeneric species, that is, multiple mappings may occur in different species. Our study revealed that the Streptococcus spp. co-infection with Fn is not confined to the same species (S. constellatus in cases 1 and 3, S. intermedius in case 2). The literature review also suggested that various Streptococcus species (S. anginosus, S. pneumoniae, S. viridans) could also cause lung abscesses [19,20]. Because of the sequence similarity, the sequences of Streptococcus are prone to multiple mapping to more than one species rather than fully matching with a dominant species, especially in case 3. Cases 1 and 3 gradually improved after standard treatment of co-infection and percutaneous drainage intervention, and there are certain risks if pathogens are ignored relying solely on the dominant Streptococcus spp. This result gives us a good inspiration: in terms of pathogen determination, the Streptococcus genus should be focused on rather than the dominant Streptococcus spp. to avoid neglecting pathogens.

A previous fundamental study performed in mice indicated that abscesses caused by the combination of Fn and Streptococcus spp. tended to be larger than those caused by mono-bacterial infections. The metabolites substantially of Fn promote Streptococcus spp. growth directly and attenuate the cell-killing abilities of human polymorphonuclear leukocytes on Streptococcus spp. [21,22]. In addition, the virulence factor is integral to bacterial colonization and pathogenesis. For example, hypervirulent K. pneumoniae carries K1 and K2 capsular serotypes, rmpA, rmp2, and magA genes, resulting in disseminated community-acquired severe infection in immunocompetent hosts, and is more aggressive and metastatic [23]. The virulence factor of Fn has a particular emphasis on its adherence and invasion. The protein expressions of FadA and RadD are essential mechanisms for colonization, co-aggregation, and induction of host responses [24,25]. FadA could bind to cadherins, causing the cadherin to migrate from the cell–cell junction to intracellular compartments, increasing the endothelial permeability, and allowing the bacteria to cross the endothelial barrier through loosened junctions [25]. RadD is responsible for arginine-inhibitable adherence in Fn, and Kaplan et al. suggested that gene inactivation mutations in RadD demonstrated decreased co-aggregation with Streptococcus spp. [26]. Both patients of cases 1 and 2 developed a detectable RadD gene, which also provides evidence to favor the co-infection of Fn and Streptococcus spp. In terms of antibiotic therapy, Fn produced a potent β-lactamase, conferring marked resistance to β-lactam antibiotics such as penicillin [27]. Thus, β-lactam/β-lactamase inhibitor combination agents should be the first choice for co-infection of Fn with Streptococcus.

The investigation also faces some limitations. The major limitation is that experimental verification was lacking. All patients suffered from negative culture results, and it was not possible to re-sample for PCR and agarose gel verification from patients due to ethical and moral restrictions, leading to the extent of accuracy on pathogenic microorganisms and virulence genes being difficult to assess. Additionally, we were unable to take samples again after treatment for the identification of microbial pathogens because the patients had recovered and were discharged. Another limitation is the sample size; more cases will need to be investigated to verify our findings and to clarify their significance in pathogen diagnosis in subsequent studies.

To the best of our knowledge, this is the first reported study employing shotgun mNGS to diagnose co-infection with Fn and Streptococcus spp. for lung abscess and tackling the thorny problem of confirming difficult-to-culture pathogens in the clinic. We further analyzed virulence-associated genes for Fn in the hope of providing references for future studies on the mechanisms of co-infection with Fn and Streptococcus spp., as well as new ideas for the choice of antimicrobial agents. Shotgun mNGS is a revolutionary technology that has disrupted traditional clinical diagnostics in terms of time-saving and identification of multiple organisms. Based on this technology, we could further carry out fundamental experimental studies to define inter-bacterial interaction and its relationship with diseases, exploiting novel targets for drug therapy.

# Na Wang and Zhichao Gao contributed equally to this work.

Acknowledgements

The authors wish to thank Professor Liang Y, Department of Respiratory Medicine, and Professor Yan D, Intensive Care Unit, Liaoning Cancer Hospital, for providing help in the diagnosis of lung abscesses and treatment of pathogenic microorganisms in this work.

  1. Funding information: This work was supported by Shenyang Breast Cancer Clinical Medical Research Center (2020-48-3-1, ST), Liaoning Cancer Hospital Yangtse River Scholars Project (ST, XJ), LiaoNing Revitalization Talents Program (XLYC1907160, XJ), Beijing Medical Award Foundation (YXJL-2020-0941-0752, ST, CORP-239-N27, CH), Wu Jieping Medical Foundation (320.6750.2020-12-21, 320.6750.2020-6-30, ST), and the Fundamental Research Funds for the Central Universities (LD202229, ST, LD202230, XJ). All grants were used for metagenomic sequencing.

  2. Author contributions: J.X., T.S., and M.J. conceived and designed the article. N.W. and Z.G. wrote the draft of the paper. S.H., M.H., W.H., and H.C. collected and organized the clinical information of patients. N.W. and X.L. analyzed metagenomics data. J.X., T.S., and M.J. participated in the manuscript revision.

  3. Conflict of interest: Xiaolin Liu is employed by the company Liaoning Kanghui Biotechnology Co., Ltd. All authors declare that they have 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: 2023-02-14
Revised: 2023-05-15
Accepted: 2023-06-05
Published Online: 2023-07-17

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

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

Articles in the same Issue

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  6. A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection
  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
  8. Isoimperatorin alleviates lipopolysaccharide-induced periodontitis by downregulating ERK1/2 and NF-κB pathways
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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-2022-0651
Keywords for this article
co-infection; Fusobacterium nucleatum; lung abscess; shotgun metagenome next-generation sequencing; Streptococcus spp.
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Systemic investigation of inetetamab in combination with small molecules to treat HER2-overexpressing breast and gastric cancers
  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
  4. Identifying two pathogenic variants in a patient with pigmented paravenous retinochoroidal atrophy
  5. Effects of phytoestrogens combined with cold stress on sperm parameters and testicular proteomics in rats
  6. A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection
  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
  8. Isoimperatorin alleviates lipopolysaccharide-induced periodontitis by downregulating ERK1/2 and NF-κB pathways
  9. Immunoregulation of synovial macrophages for the treatment of osteoarthritis
  10. Novel CPLANE1 c.8948dupT (p.P2984Tfs*7) variant in a child patient with Joubert syndrome
  11. Antiphospholipid antibodies and the risk of thrombosis in myeloproliferative neoplasms
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  13. High glucose and high lipid induced mitochondrial dysfunction in JEG-3 cells through oxidative stress
  14. Pharmacological inhibition of the ubiquitin-specific protease 8 effectively suppresses glioblastoma cell growth
  15. Levocarnitine regulates the growth of angiotensin II-induced myocardial fibrosis cells via TIMP-1
  16. Age-related changes in peripheral T-cell subpopulations in elderly individuals: An observational study
  17. Single-cell transcription analysis reveals the tumor origin and heterogeneity of human bilateral renal clear cell carcinoma
  18. Identification of iron metabolism-related genes as diagnostic signatures in sepsis by blood transcriptomic analysis
  19. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation
  20. Surgery, adjuvant immunotherapy plus chemotherapy and radiotherapy for primary malignant melanoma of the parotid gland (PGMM): A case report
  21. Dosimetry comparison with helical tomotherapy, volumetric modulated arc therapy, and intensity-modulated radiotherapy for grade II gliomas: A single‑institution case series
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  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
  24. Meta-analysis of cancer risk among end stage renal disease undergoing maintenance dialysis
  25. 6-Phosphogluconate dehydrogenase inhibition arrests growth and induces apoptosis in gastric cancer via AMPK activation and oxidative stress
  26. Experimental study on the optimization of ANM33 release in foam cells
  27. Primary retroperitoneal angiosarcoma: A case report
  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
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  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
  31. Comparison of immunotherapy combined with stereotactic radiotherapy and targeted therapy for patients with brain metastases: A systemic review and meta-analysis
  32. Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation
  33. Association between the VEGFR-2 -604T/C polymorphism (rs2071559) and type 2 diabetic retinopathy
  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
  35. Triple-negative mouse breast cancer initiating cells show high expression of beta1 integrin and increased malignant features
  36. mNGS facilitates the accurate diagnosis and antibiotic treatment of suspicious critical CNS infection in real practice: A retrospective study
  37. The apatinib and pemetrexed combination has antitumor and antiangiogenic effects against NSCLC
  38. Radiotherapy for primary thyroid adenoid cystic carcinoma
  39. Design and functional preliminary investigation of recombinant antigen EgG1Y162–EgG1Y162 against Echinococcus granulosus
  40. Effects of losartan in patients with NAFLD: A meta-analysis of randomized controlled trial
  41. Bibliometric analysis of METTL3: Current perspectives, highlights, and trending topics
  42. Performance comparison of three scaling algorithms in NMR-based metabolomics analysis
  43. PI3K/AKT/mTOR pathway and its related molecules participate in PROK1 silence-induced anti-tumor effects on pancreatic cancer
  44. The altered expression of cytoskeletal and synaptic remodeling proteins during epilepsy
  45. Effects of pegylated recombinant human granulocyte colony-stimulating factor on lymphocytes and white blood cells of patients with malignant tumor
  46. Prostatitis as initial manifestation of Chlamydia psittaci pneumonia diagnosed by metagenome next-generation sequencing: A case report
  47. NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2
  48. Association of interleukin-10 rs1800896, rs1800872, and interleukin-6 rs1800795 polymorphisms with squamous cell carcinoma risk: A meta-analysis
  49. Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B
  50. Shear stress leads to the dysfunction of endothelial cells through the Cav-1-mediated KLF2/eNOS/ERK signaling pathway under physiological conditions
  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
  52. Meta-analysis of the rs231775 locus polymorphism in the CTLA-4 gene and the susceptibility to Graves’ disease in children
  53. Cloning, subcellular localization and expression of phosphate transporter gene HvPT6 of hulless barley
  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
  56. Whole-exome sequencing applications in prenatal diagnosis of fetal bowel dilatation
  57. Gemella morbillorum infective endocarditis: A case report and literature review
  58. An unusual ectopic thymoma clonal evolution analysis: A case report
  59. Severe cumulative skin toxicity during toripalimab combined with vemurafenib following toripalimab alone
  60. Detection of V. vulnificus septic shock with ARDS using mNGS
  61. Novel rare genetic variants of familial and sporadic pulmonary atresia identified by whole-exome sequencing
  62. The influence and mechanistic action of sperm DNA fragmentation index on the outcomes of assisted reproduction technology
  63. Novel compound heterozygous mutations in TELO2 in an infant with You-Hoover-Fong syndrome: A case report and literature review
  64. ctDNA as a prognostic biomarker in resectable CLM: Systematic review and meta-analysis
  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
  66. Phylogenetic analysis of promoter regions of human Dolichol kinase (DOLK) and orthologous genes using bioinformatics tools
  67. Collagen changes in rabbit conjunctiva after conjunctival crosslinking
  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
  69. Oral nifedipine and phytosterol, intravenous nicardipine, and oral nifedipine only: Three-arm, retrospective, cohort study for management of severe preeclampsia
  70. Case report of hepatic retiform hemangioendothelioma: A rare tumor treated with ultrasound-guided microwave ablation
  71. Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling
  72. Rare presentation of double-clonal Waldenström macroglobulinemia with pulmonary embolism: A case report
  73. Giant duplication of the transverse colon in an adult: A case report and literature review
  74. Ectopic thyroid tissue in the breast: A case report
  75. SDR16C5 promotes proliferation and migration and inhibits apoptosis in pancreatic cancer
  76. Vaginal metastasis from breast cancer: A case report
  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
  99. Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis
  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
  101. Effect of periostin on bone metabolic and autophagy factors during tooth eruption in mice
  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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