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Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”

  • Miroslava Kačániová EMAIL logo , Margarita Terentjeva , Simona Kunová , Peter Haščík , Przemysław Łukasz Kowalczewski and Jana Štefániková
Published/Copyright: March 23, 2021
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Open Life Sciences
From the journal Open Life Sciences Volume 16 Issue 1

Abstract

“Bryndza” cheese is an important Slovak traditional regional product. New knowledge on the role of microorganisms involved the “Bryndza” ripening process may provide valuable data on its quality and safety. In our study, the “Bryndza” made from pasteurized ewes milk was studied towards total count of bacteria, coliforms bacteria, enterococci, lactic acid bacteria, and microscopic filamentous fungi. All those groups of microbiota were detected using classical microbiological methods and identified using mass spectrometry. A total of 3,758 isolates were identified with score higher than 2.00. Altogether, 13 families, 24 genus, and 44 species of microbiota were identified in Slovak cheese “Bryndza.” The most often isolated species were yeasts Yarrowia lipolitica and Dipodascus geotrichum and the lactic acid bacteria Lactobacillus paracasei subsp. paracasei.

Keywords: gram-positive and gram-negative bacteria; microscopic filamentous fungi; sheep farms; ewes milk cheese “Bryndza”; mass spectrometry; microbiota identification

1 Introduction

Sheep herding and ewes milk production are important sectors of Slovak agriculture. The well-known product of ewes milk is a Slovak cheese named “Bryndza” or “Oštiepok” [1,2]. “Bryndza” was granted the Protected Geographic Indication (PGI) as it is produced in a defined mountainous regions of Slovakia [3,4]. “Bryndza” is a type of natural white, mature, and spreadable cheese made from matured 100% sheep lump cheese or mixed with up to 50% of cow lump cheese. First, ewes milk is sweetened. This raw material is then allowed to dry on the mountain hut to form lump sheep’s cheese. It is then transferred to a bryndziarna (cheese “Bryndza” production), where it is sorted and washed with water and then left to mature at 20°C in a cheese bath. The rind is then removed from the cheese, the excess liquid (whey) is expelled, and the cheese is crushed. The pulp is salted and spread on rollers to form a “Bryndza” [5]. The manufacturing has been done according to the traditional method. “Bryndza” is produced from raw ewes milk at 29–31°C for 30 min with chymosin or chymosin-identical enzymes [6]. In 2019, the production of ewes milk in Slovakia reached 13,524 tons, which is the highest level since joining the European Union. The annual production of “Bryndza” in Slovakia is almost 4,000 tons, whereas Slovaks consume about 0.6 kg of “Bryndza” per capita per year. The characteristics of the produced “Bryndza” cheese may vary under the climatic conditions and may be influenced by the feeding meant. The botanical composition of the plants in the sheep diet during pasture may affect the quality parameters of the milk used for production of the “Bryndza” cheese. Carpathian Mountains in Slovakia thus represent a specific habitat for sheep milk production by affecting the quality of raw milk [7] and the differences in ambient temperatures influence the ripening microbiota at the early cheese production steps [8]. In Slovak “Bryndza,” Hafnia alvei and Klebsiella oxytoca were the most abundant Gram-negative bacteria, whereas Lactococcus lactis and Lactobacillus paracasei the most abundant Gram-positive bacteria. Lactobacillus, Lactococcus, and Pediococcus were the main representatives of the lactic acid bacteria [8]. The aim of this study was to characterize microbiological variability of “Bryndza” cheese produced in summer of 2016–2019 in various geographical areas in Slovakia.

2 Materials and methods

2.1 “Bryndza” cheese samples

Samples of 80 unpasteurized ewes’ cheese “Bryndza” were provided by eight producers representing eight Slovak farms (F1 to F8). Slovak “Bryndza” is produced in the same way throughout the defined area. The same breed of sheep grazes in the defined area – Native Wallachian sheep, Improved Wallachian sheep, Domestic Tsigai, and East Friesian on pastures with the same flora and climatic conditions, which results in the same quality of the basic raw material – ewes milk [4]. The samples were collected between the end of April and August in the years 2016 to 2019. All samples were transported to the laboratory at 4°C and were analyzed immediately after delivery. Each sample was analyzed for total count of bacteria, coliform bacteria, enterococci, lactic acid bacteria, microscopic fungi, and yeasts MFF (microscopic filamentous fungi). The serial dilutions of the milk products in 0.89% sterile saline were made for plating out the sample material.

2.2 Microbiological analysis

The determination of total count of bacteria, coliforms, enterococci, lactic acid bacteria and fungi, and yeasts has been previously published [9,10]. The colonies from total count of bacteria, coliforms bacteria, enterococci, lactic acid bacteria, MFF, and yeasts were selected for further confirmation with MALDI-TOF MS Biotyper. Selected colonies were subcultured overnight on TSA agar aerobically or anaerobically and were used for identification.

2.3 Identification of bacteria and yeasts with MALDI-TOF MS Biotyper

Microbial isolates for MALDI-TOF MS Biotyper analysis were prepared in accordance with extraction procedure provided by the manufacturer (Bruker Daltonics, Bremen, Germany). The detailed procedure was previously published [11].

2.4 Identification of microscopic filamentous fungi with MALDI-TOF MS Biotyper

The detailed procedure of identification of fungal isolates was previously published [12]. Identification was done by MALDI-TOF MS Biotypes (Bruker Daltonics, Bremen, Germany) with Flex Control 3.4 software and Biotyper Realtime Classification 3.1 with BC specific software (Bruker Daltonics, Germany).

2.5 Krona charts

Krona charts showing automatically the taxonomic identification and relative abundance of the most abundant bacteria or microscopic filamentous fungi.

2.6 Statistical analysis

For microbial counts, lactic acid bacteria count, coliform bacteria, and microscopic filamentous fungi counts, the means and standard deviations were calculated. Krone diagrams were used for visualization of the relatedness of the identified microbial isolates.

3 Results

The number of coliform bacteria ranged from 3.67 in F1 to 3.84 log cfu/g in F2 and enterococci from 2.29 in F6 to 2.64 log cfu/g in F4. Total count of bacteria were from 4.38 in F1 to 4.73 log cfu/g in F4. The higher lactic acid bacteria counts were found in F7 (3.62 log cfu/g) and microscopic filamentous fungi in F6 (2.61 log cfu/g) (Table 1).

Table 1

Microbial counts in sheep cheese “Bryndza” (average ± SD log cfu/g)

Farm CB E TCB LAB MFF
F1 3.67 ± 0.15 2.46 ± 0.13 4.38 ± 0.15 3.25 ± 0.12 2.42 ± 0.13
F2 3.81 ± 0.19 2.42 ± 0.12 4.66 ± 0.11 3.37 ± 0.15 2.36 ± 0.12
F3 3.79 ± 0.20 2.27 ± 0.17 4.64 ± 0.17 3.42 ± 0.17 2.15 ± 0.11
F4 3.81 ± 0.19 2.64 ± 0.11 4.73 ± 0.12 3.43 ± 0.12 2.26 ± 0.12
F5 3.76 ± 0.12 2.36 ± 0.10 4.48 ± 0.11 3.37 ± 0.15 2.41 ± 0.15
F6 3.72 ± 0.12 2.29 ± 0.14 4.81 ± 0.12 3.26 ± 0.11 2.61 ± 0.12
F7 3.74 ± 0.11 2.32 ± 0.11 4.64 ± 0.15 3.62 ± 0.12 2.41 ± 0.12
F8 3.84 ± 0.14 2.46 ± 0.15 4.72 ± 0.13 3.38 ± 0.11 2.35 ± 0.15

CB – coliforms bacteria, E – enterococci, TCB – total count of bacteria, LAB – lactic acid bacteria, MFF – microscopic filamentous fungi, SD – standard deviation.

A total of 3,758 isolates from cheese “Bryndza” were identified using MALDI-TOF Biotyper (Table 2). The most abundant microbial species isolated from cheese were Yarrowia lipolitica (254 isolates), Lactobacillus paracasei subsp. paracasei (252 isolates), and Dipodascus geotrichum (Geotrichum candidum, 227 isolates). The most abundant family of cheese “Bryndza” was Lactobacillaceae (25.24%).

Table 2

Number of isolated species from F1 to F8

Species F1 F2 F3 F4 F5 F6 F7 F8 Total
Acinetobacter baumannii 10 14 15 18 12 11 9 13 102
Acinetobacter tandoii 15 18 10 16 15 14 11 10 109
Aspergillus fumigatus 12 15 14 18 10 12 16 13 110
Bacillus pumilus 8 9 7 8 6 8 7 9 62
Candida catenulata 4 6 5 8 9 11 12 8 63
Candida krusei 6 8 5 7 4 8 9 5 52
Candida lusitaniae 15 15 16 11 15 17 10 15 114
Candida rugosa 6 8 9 9 9 7 10 11 69
Candida utilis 8 5 8 5 9 6 8 10 59
Citrobacter braakii 8 6 6 8 7 8 5 5 53
Citrobacter koseri 5 6 8 9 5 4 5 6 48
Dipodascus geotrichum 25 30 28 32 26 28 30 28 227
Dipodascus silvicola 6 5 7 4 5 4 3 5 39
Enterobacter cloacae 2 4 8 9 5 6 4 10 48
Enterobacter ludwigii 8 9 7 5 6 8 9 5 57
Enterococcus faecalis 6 11 5 8 9 9 7 8 63
Enterococcus faecium 10 15 25 24 21 15 12 18 140
Enterococcus hirae 15 6 18 7 9 10 14 11 90
Escherichia coli 14 10 12 8 10 12 16 10 92
Hafnia alvei 5 6 8 7 8 9 10 8 61
Klebsiella oxytoca 10 5 6 8 9 7 6 8 59
Klebsiella pneumoniae ssp. ozaenae 6 4 8 7 8 8 5 6 52
Klebsiella pneumoniae ssp. pneumoniae 5 6 7 8 7 8 9 5 55
Lactobacillus brevis 12 15 18 21 16 18 21 18 139
Lactobacillus harbinensis 8 9 10 8 9 15 12 16 87
Lactobacillus johnsonii 5 8 8 6 12 4 11 8 62
Lactobacillus plantarum 23 21 25 18 26 22 20 32 187
Lactobacillus paracasei ssp. paracasei 28 31 39 45 36 15 28 30 252
Lactobacillus paraplantarum 8 15 15 16 15 17 14 10 110
Lactobacillus suebicus 5 4 6 5 8 7 9 6 50
Lactococcus lactis ssp. lactis 18 22 25 19 16 8 15 21 144
Lactococcus lactis 15 10 10 12 14 10 18 14 103
Microbacterium liquefaciens 8 9 8 9 11 6 4 5 60
Mucor circinelloides 8 4 6 10 9 8 7 9 61
Pediococcus acidilactici 6 4 8 11 10 5 8 9 61
Penicillium sp. 7 5 8 8 6 4 5 8 51
Pichia cactophila 4 5 6 6 7 8 5 6 47
Raoultella ornithinolytica 5 7 8 9 10 12 8 5 64
Rhizopus sp. 8 7 5 4 2 4 6 5 41
Serratia liquefaciens 6 7 5 8 5 4 6 5 46
Staphylococcus aureus ssp. aureus 6 2 5 4 5 3 4 6 35
Staphylococcus pasteuri 2 4 6 7 5 4 6 3 37
Stenotrophomonas maltophilia 5 4 6 5 8 6 4 5 43
Yarrowia lipolytica 25 28 30 28 39 45 28 31 254
Total 421 442 499 503 493 455 466 479 3,758

In our study, Gram-negative, Gram-positive bacteria, and microscopic filamentous fungi accounted for majority of the identified microbiota in “Bryndza.” The Enterobacteriaceae family was the most abundant family of Gram-negative bacteria isolated. Percentage of all isolated family, genera, and species indicates Krona (Figure 1). Altogether 889 isolates belonged to Gram-negative bacteria group. The Lactobacillaceae family was the most abundant among Gram-positive bacteria (Figure 2). Altogether 1,682 isolates of Gram-positive bacteria were identified. Yarrowia lipolitica was the most abundant microscopic fungi (21%) (Figures 3 and 4).

Figure 1 Diversity microorganisms isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).
Figure 1

Diversity microorganisms isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).

Figure 2 Diversity of Gram-negative bacteria isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).
Figure 2

Diversity of Gram-negative bacteria isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).

Figure 3 Diversity of Gram-positive bacteria isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).
Figure 3

Diversity of Gram-positive bacteria isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).

Figure 4 Krona chart for microscopic filamentous fungi isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).
Figure 4

Krona chart for microscopic filamentous fungi isolated from ewes’ cheese “Bryndza” (outermost ring: species, middle ring: genus, innermost ring: family).

4 Discussion

The total count of bacteria in ewes’ cheese “Bryndza” samples was from 4.38 ± 0.15 log cfu/g for F1 to 4.81 ± 0.12 log cfu/g for F6 total count of bacteria. The microbial counts similar to detected here were described previously for ewes’ cheese “Bryndza,” where number of total count of bacteria ranged from 3.87 to 4.32 log cfu/g [10]. Our findings on coliform bacteria counts (3.84 log cfu/g) were in line with Pangallo et al. [13] who reported their counts in the spring “Bryndza” at 3.87 log cfu/g. The counts of coliform and Staphylococcus spp. in Šaková et al.’s [3] study reached 105 to 106 cfu/g in “Bryndza” cheese; moreover, the majority of Staphylococcus spp. isolates were coagulase-positive (104 cfu/g). Within this study, the coliforms counts were less than 105 cfu/g. Coliforms were frequently identified in dairy products and contamination of dairy products may occur during milk storage, transportation, and processing, if the hygienic requirements are not met [14,15,16,17]. Intrinsic and extrinsic factors such as low pH, salt concentration, and water activity all affect the survival of coliforms and a decline in coliforms counts was detected during the ripening of other cheese types [18,19,20]. Escherichia coli, Klebsiella sp., and Enterobacter sp. were isolated from local Nigerian soft and semisoft cheese [21], whereas Citrobacter braakii, Enterobacter sakazakii, and E. coli were identified in the local Italian cheese [22,23]. High microbial counts of 9.0 log cfu/g were detected in raw ewes milk after 30 days of maturation [24]. The most important bacteria for ripening of ewes’ cheese are lactic acid bacteria and several these bacteria in “Bryndza” were considered as potentially probiotic in character [25]. Lactic acid bacteria up to 10.95 log cfu/g in “Bryndza” was reported previously [13] in comparison to 3.62 log cfu/g identified in our study. The microbiological quality of dairy products can be improved by adding a starter culture such as lactic acid bacteria, which will prevent the growth of pathogenic microorganisms [26].

Yeasts counts (2.61 log cfu/g) and Enterococcus counts (2.64 log cfu/g) in our study were lower than 5.97 log cfu/g and 7–8 log cfu/g, respectively, detected in other studies [13,14]. Yeasts belong to the natural microbiota of “Bryndza” cheese and contribute to the ripening of the cheese. The differences in yeasts counts in “Bryndza” cheese from raw and pasteurized milk were not significant. Dipodascus geotrichum was the predominant yeast identified in the present study in “Bryndza cheese.” The functional significance of this yeast is related to a breakdown of sugars, milk fat, and proteins [27,28]. Some strains of Dipodascus geotrichum were reported to form esters and sulfur compounds, important for the development of typical aroma and other characteristics of cheese [29].

Candida catenulata, C. krusei, C. lusitaniae, C. rugosa, C. utilis, Dipodascus geotrichum, D. silvicola, Pichia cactophila, and Yarrowia lipolitica were isolated in the present study. Galactomyces/Geotrichum (Dipodascus geotrichum) was reported in “Bryndza” of Slovak origin [30]. Yeasts as compounds of the milk microbiota are important in the agri-food industry as they are involved in biodegradation and depollution, may act as contaminants. Dipodascus geotrichum was found as a commensal of gut of humans and animals [31] and is important for milk production since it is naturally present in raw milk [32,33,34,35].

A total of 3758 isolates were identified to species level in cheese “Bryndza” and the most frequently isolated species were Yarrowia lipolitica, Lactobacillus paracasei subsp. paracasei, and Dipodascus geotrichum (Geotrichum candidum). Lactobacillaceae (25.24%) was the most frequently isolated family of the cheese “Bryndza.” Among the isolates, 889 were Gram-negative, 1,682 were Gram-positive, and 1,187 were microscopic filamentous fungi. In other study [10], a total of 1,175 isolates were identified by mass spectrometry and included Gram-negative bacteria, Gram-positive bacteria, and microscopic filamentous fungi. In the same study [10], 199 isolates were isolated and identified from Gram-negative, 599 isolates from Gram-positive, and 377 isolates of yeast and molds.

Beside the abundance of Lactobacillaceae (25.24%), other isolated families were Bacillaceae (1.65%), Dipodascaceae (13.84%), Enterobacteriaceae (16.89%), Enterococaceae (7.8%), Microbacteriaceae (1.6%), Moraxellaceae (5.61%), Mucoraceae (2.71%), ‎Saccharomycetaceae (10.75%), Staphylococcaceae (1.91%), Streptococaceae (6.57%), Trichocomaceae (4.29%), and Xanthomonadaceae (1.14%). Similar results of identified genera were found [10].

In our study, 44 microbial species representing 24 genera were identified using MALDI-TOF MS Biotyper with score higher than 2.00. Lactobacillus paracasei subsp. paracasei was identified as most often identified species in the present study. Lactococcus, Lactobacillus, Streptococcus, Leuconostoc, and Enterococcus were members of lactic acid bacteria group commonly found in cheeses [36]. Needs for characterization of complex population and discovery of new lactic acid bacteria strains facilitate the research on the microbiota present in raw milk cheese and other traditional dairy products [37]. The genus Enterococcus was frequently isolated from cheese and identified as the prevalent among the lactic acid bacteria isolated from Coalho cheese in Brazil [38]. Several species of Enterococcus genus such as E. faecium, E. faecalis, E. italicus, E. durans, E. casseliflavus, and E. gallinarum were isolated from raw milk and cheese [38,39]. The dominant group of bacteria in “Bryndza” was lactic acid bacteria, mainly Lactobacillus species [10]. Lactococcus, Pediococcus, Enterococcus, and Streptococcus were abundant in “Bryndza” from different Slovak regions [3,40,41]. Previous study [42] identified Klebsiella (65%), Escherichia (20%), Serratia (10%), and Enterobacter (5%) in cheese samples. Klebsiella oxytoca, K. pneumoniae and K. ornithinolytica, and E. coli were identified among Enterobacteriaceae.

Aspergilus fumigatus, Mucor circeneloides, Rhizopus sp., and Penicillium sp. from micromycetes were isolated in “Bryndza” in our study. “Bryndza” could serve as a natural habitat for microscopic fungi, but their role in cheese ripening needs to be studied. Mucor spp. has been occasionally isolated from sheep cheese, accompanied by recognized human and plant pathogens [43,44,45,46]. Various applications of M. circinelloides were reported previously: starter cultures in China and Vietnam, and a contributor to organoleptic proprieties in study in Poland [47,48]. Mucor strains are accumulated in lipid bodies rich in polyunsaturated fatty acids [49].

In contrast to industrial food products, traditional cheese is of particular interest to consumers who care about the nature, origin, and nutritional value of foods [50]. Much of their reputation is attributed to the unique organoleptic properties and to the indigenous microorganisms living in raw milk or natural starters [51]. However, raw milk can also contain pathogenic microorganisms that have been raising public health concerns since the beginnings of the dairy industry [27].

5 Conclusion

The microbiota of traditional ewes’ cheese produced in Slovakia include diverse families of Bacillaceae, Dipodascaceae, Enterobacteriaceae, Enterococaceae, Lactobacillaceae, Microbacteriaceae, Moraxellaceae, Mucoraceae, ‎Saccharomycetaceae, Staphylococcaceae, Streptococaceae, Trichocomaceae, and Xanthomonadaceae. The most abundant microbial species were Yarrowia lipolitica, Lactobacillus paracasei subsp. paracasei, and Dipodascus geotrichum. The unique sensory properties of the Slovak “Bryndza” are believed to be attributed to microbial activity of the microbiota primary present in the lump ewes’ cheese – Lactobacillus spp., Lactococcus spp., Streptococcus spp., Enterococcus spp., Kluyveromyces marxianus, and Dipodascus geotrichum. The results of this study contribute to better understanding of the microbiota of the local cheese produced in Slovakia. The study of “Bryndza” microbiota is important for development of processing technology and improvements in safety of products.

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Acknowledgments

Dr. Marcin Nowicki (University of Tennessee, Knoxville, TN) is gratefully acknowledged for critical reading and linguistic copy editing of an early version of this study’s report.

  1. Author contributions: Conceptualization, M.K. and S.K.; methodology, M.K. and S.K.; validation, M.K., M.T., S.K., P.H., and J.Š.; formal analysis, M.K., M.T., S.K., and J.Š.; investigation, M.K., and S.K; resources, M.K., S.K., and J.Š; data curation, M.K., S.K., and J.Š.; writing – original draft preparation, M.K., M.T., S.K., J.Š., P.H., and P.Ł.K.; writing – review and editing, M.T., and P.Ł.K.; visualization, P.Ł.K.; supervision, M.K. All authors have read and agreed to the published version of the manuscript.

  2. Funding: This publication was supported by the Operational Program Integrated Infrastructure within the projects: Sustainable smart farming systems taking into account the future challenges 313011W112, co-financed by the European Regional Development Fund and Demand-driven research for the sustainable and innovative food, Drive4SIFood 313011V336, co-financed by the European Regional Development Fund.

  3. Conflict of interest: Przemysław Łukasz Kowalczewski who is the co-author of this article is a current Editorial Board member of Open Life Sciences. This fact did not affect the peer-review process.

  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: 2020-11-25
Revised: 2021-01-26
Accepted: 2021-02-10
Published Online: 2021-03-23

© 2021 Miroslava Kačániová et al., published by De Gruyter

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

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https://doi.org/10.1515/biol-2021-0038
Keywords for this article
gram-positive and gram-negative bacteria; microscopic filamentous fungi; sheep farms; ewes milk cheese “Bryndza”; mass spectrometry; microbiota identification
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
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  55. Therapeutic potential of anticoagulant therapy in association with cytokine storm inhibition in severe cases of COVID-19: A case report
  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
  57. Rufinamide (RUF) suppresses inflammation and maintains the integrity of the blood–brain barrier during kainic acid-induced brain damage
  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
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