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Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals

  • Tamene Milkessa Jiru EMAIL logo and Ewunetu Ayanaw
Published/Copyright: September 11, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

This study aimed to investigate the presence of antibiotic susceptibility patterns and bacterial profiles of some multi-drug-resistant bacteria isolated from the effluents of Kolladiba and Debark Hospitals. Sixteen samples were collected from Kolladiba and Debark Hospitals in North Gondar, Ethiopia, to investigate the presence of multi-drug-resistant bacteria. To assess susceptibility patterns, well-isolated bacterial colonies were subjected to seven antibiotics. The selected resistant isolates were characterized using morphological and biochemical tests. Plasmid DNA analysis of the isolates was also performed. Out of a total of 28 bacterial isolates, 12 were found to be multi-drug resistant. Among the tested antibiotics, erythromycin was the most resistant antibiotic, while novobiocin was the most effective antibiotic. A plasmid profile study of the isolates revealed both the presence and absence of plasmids. The number of plasmids ranged from zero to four, with plasmid sizes of 100, 900, 1,000, 1,400, 1,500, and 1,800 base pairs. This study concluded that effluents from both hospitals have high number of multi-drug-resistant isolates. The genes responsible for multi-drug resistance in bacterial isolates under this study could be either plasmid-mediated or chromosomal DNA-mediated. The presence of multi-drug-resistant bacteria in these effluents should not be overlooked.

Keywords: antimicrobial susceptibility; bacterial profile; effluents; plasmid profile

1 Introduction

Serious infections caused by pathogenic bacteria that have become resistant to commonly used broad-spectrum antibiotics have become major global healthcare issues in the current century, and also, the growth of antibiotic-resistant bacteria in hospital setups is becoming a serious problem. Such emerging antibiotic resistance is threatening the management and control of bacterial infections. Although antibiotic resistance as an environmental problem is increasing from time to time, it has largely been overlooked, and prevention and containment have received far too little attention. As a result, the increasing incidence of resistance to a wide range of antibiotics by a variety of pathogenic organisms is a major concern facing modern medicine. Furthermore, antibiotic resistance has resulted in increased healthcare costs, morbidity, and mortality among patients with infectious diseases [1].

In Africa, including Ethiopia, many hospitals and clinics are major sources/reservoirs for large numbers of disease-causing bacteria, and such bacterial strains are introduced into the public environment [2]. The spread of antibiotic-resistant bacteria from hospitals to the environment can occur through various mechanisms, such as discharged antibiotics that are excreted through feces and urine of patients, discharged patients and health-care workers, accidental spilling of different antibiotics, and discarding expired drugs without burning. Overuse and misuse of antibiotics have accelerated antibiotic resistance. Uncontrolled and unrestricted uses of different antibiotics by the community also cause a rise in antibiotic resistance and result in the spread of resistance genes in hospital effluents. These multiple antibiotic-resistant pathogenic bacteria entering into an environment mainly through effluents are causing a serious public health impact. Bacteria resistant to these antibiotics, which carry the transmissible gene, have the ability to transfer such transmissible genes to other normal non-resistant bacterial communities. Such infections caused by the transferred resistance gene of bacteria are habitually difficult to treat [3]. It also minimizes the power of the antibiotic pool for handling bacterial infections [3]. Hence, hospital effluents could raise a number of common antibiotic-resistant bacteria in the recipient environment both by the mechanisms of introduction and selection pressure [4]. It is also true that hospitals provide an environment conducive to multi-drug bacteria, making the treatment options limited and expensive [5].

Genes coding for antibiotic resistance and virulence may share common features of being located in the bacterial chromosome, as well as on plasmids. The genes they carry may be expressed under stressed conditions and are considered to be living organisms in their simple structure since they are the main elements of a continuous lineage with every individual’s evolutionary history [6]. Many pathogenic bacteria have plasmids that carry antibiotic resistance encoding genes, which contribute to the emergence of multi-drug resistance [7,8]. These plasmids also encode virulence factors.

In the study areas, there is a lack of information on whether hospital effluents carrying antibiotics could contribute to the development of antibiotic-resistant microorganisms in the environment or not. The current study was designed to assess the antimicrobial susceptibility pattern of bacteria isolated from the effluents of two hospitals in North Gondar, Amhara Region, Ethiopia, against commonly used antibiotics. The study also aimed to analyze the plasmid profile of the multi-drug-resistant isolates. The purpose of studying the plasmid profile was to check whether the resistance is plasmid-mediated or chromosome-mediated. The findings of this study therefore would help to make public health authorities aware of the dissemination of drug-resistant bacteria in the hospital environments for proper management of effluents.

2 Materials and methods

2.1 Description of the study areas

The study was carried out in Debark and Kolladiba hospitals of North Gondar, Amhara Region, Ethiopia. Debark is located in the northern part of Gondar town near Ras Dashen mountain. The town has 13°08′N latitude and 37°54′E longitude with an elevation of 2,850 m above sea level. Conversely, Kolladiba is 16 km far from Gondar town in the southwestern part. Kolladiba town has 12°40′N latitude and 37°10′E longitude with an elevation of 2,146 m above sea level. The distances from Addis Ababa to Kolladiba and Debark are 729 and 835.3 km, respectively. Maps of both study areas are depicted in Figures 1 and 2.

Figure 1 Map showing study area – Debark district (Debark town) [9].
Figure 1

Map showing study area – Debark district (Debark town) [9].

Figure 2 Map showing Dembia district (Kolladiba town).
Figure 2

Map showing Dembia district (Kolladiba town).

2.2 Sample collection and isolation of bacteria

A cross-sectional study was used to conduct this research. A total of 16 effluent samples were collected from Debark and Kolladiba hospitals in North Gondar, Amhara Region, Ethiopia. They were taken from different sites of the two hospitals (around the drug store, laboratory, shower, surgical room, and patient bedding room) and finally at the sites where all the hospital effluents collectively enter into the septic tank. The samples were collected using sterilized plastic bags. The collected samples were transported to the Microbial Laboratory, Department of Biotechnology, Institute of Biotechnology, University of Gondar. Then, the samples were preserved at 4°C in a refrigerator for further analysis.

Bacteria were isolated by a serial dilution method. Stock solution was prepared by diluting 1 mL of the effluent sample in 9 mL of distilled water and shaken using a vortex mixer. From the stock solution, 1 mL was used to prepare the final volume of 10−4, 10−5, 10−6, and 10−7 and distributed on Mueller Hinton agar medium aseptically. Then, the plates were incubated at 37°C for 48 h. Distinct bacterial colonies that were grown well on each plate were observed. Distinct representative colonies were sub-cultured on differential and selective media such as mannitol salt agar (Staphylococcus sp. confirmation test), MacConkey agar (Escherichia coli isolation test), Salmonela–Shigella agar (Salmonella and Shigella confirmation test), pseudomonas agar (Pseudomonas sp. confirmation test), and XLD (xylose lysine deoxycholate) agar media (Salmonella confirmation test) [10].

2.3 Morphological and biochemical characterization tests

The selected isolates underwent morphological and biochemical analysis [11].

2.4 Morphological tests

The morphology of growing bacterial colonies, such as size, color, shape, margin, elevation, texture, appearance, and opacity of each isolate, was tested and used for identification purposes [11].

2.5 Biochemical characterization

Isolates were characterized using various biochemical tests following the procedures set in Bergey’s Manual of Systematic Bacteriology and Determinative Bacteriology [11], including Gram straining, motility and catalase tests, citrate utilization tests, coagulase and urease production tests, indole production tests, oxidase tests, and Methyl Red–Voges Proskauer (MR–VP) tests.

2.6 Antibiotic susceptibility test

The antimicrobial susceptibility profile of isolates was assessed using the standard Kirby Bauer disk diffusion assay [12]. The inoculum of each bacterium was prepared by suspending the freshly grown bacteria in 5 mL sterile nutrient broth, and the turbidity was adjusted to an approximate value of 0.5 McFarland standard. Then, the antibiotic discs were placed over Mueller Hinton agar plates seeded with each bacterial isolate. The common antibiotics used for susceptibility tests were ampicillin (AMP, 10 µg), tetracycline (TET, 30 µg), gentamycin (GEN, 10 µg), amoxicillin (AMX, 10 µg), novobiocin (NV, 30 µg), erythromycin (E, 15 µg), and cotrimoxazole (COT, 25 µg). The Petri plates were incubated at 37°C for 24 h. The zone of growth inhibition around each disc was measured, and the results were interpreted according to the guidelines from the Clinical and Laboratory Standards Institute [13]. All experiments were done in triplicates. The experimental results were expressed as the mean of three replicates.

2.7 Plasmid DNA isolation and analysis

Those selected antibiotic-resistant isolates were subjected to plasmid analysis [14]. The isolates were grown in 10 mL of nutrient broth in test tubes and incubated at 37°C for 18–24 h. After incubation, 1,500 µL of each culture was transferred into 2 mL Eppendorf tubes for plasmid extraction, and glycerol was added to the remaining culture and stored at 4°C. The 1,500 µL bacterial culture in the Eppendorf tubes was centrifuged at 6,000 rpm for 8–10 min and placed in ice. Then, the supernatant was carefully removed using a fine-tip micropipette, and the pellet was thoroughly re-suspended in 100 µL of ice-cold solution I (containing sucrose and Tris–ethylene diamine tetra acetic acid). The suspension was vortexed gently, placed in ice for 5 min, and then shifted to room temperature.

After that, 200 µL of solution II (containing sodium hydroxide and sodium dodecyl sulfate) was added to the suspension containing pellets and solution I. Those pellet–suspension mixtures were mixed by inverting the mixture six to seven times, and the tube was maintained for 1 min at 0°C.

Then, 150 µL of solution III (containing acetic acid and potassium acetate) was added from the ice box to the sample containing test tubes. The content of each tube was gently mixed by inverting the tubes for five to six times and maintained at 0°C for 5 min. The tubes were centrifuged for 10 min at 6,000–8,000 rpm to yield a clear supernatant. This fractionation step separates the plasmid DNA from the cellular debris and chromosomal DNA in the pellet. Plasmid DNA renatures and remains in solution. Other components get precipitated. The supernatant was removed carefully without disturbing the pellet from each tube and transferred into new Eppendorf tubes, and 200 µL of ethanol was added to it. The precipitate was collected using centrifugation at 10,000 rpm for 20 min. Then, the supernatant was decanted, and the Eppendorf tube was inverted on bloating paper to drain left over, which was still stuck to the Eppendorf tube at the bottom side. The inverted tube was dried for about 10–15 min at room temperature. The dried pellet was suspended with 50 µL of 1× TE buffer and mixed by tapping by finger; the extracted plasmid DNA was quantified using nanodrop, and then the plasmid DNA in solution was applied to an agarose gel for electrophoresis. The samples were processed using horizontal gel electrophoresis to identify the number of plasmid copies present in different isolates of each cell. For this purpose, an agarose gel of 1% was used. Staining of DNA fragments was carried out using ethidium bromide (0.5 μg/mL), and they were visualized by UV-Trans illumination equipment. A standard DNA molecular weight marker was used to estimate the plasmid size. The standard DNA marker was used in this 1 kb ladder with 100 bp ladder gaps. This was done to check whether the isolated bacterial-resistant gene is plasmid-mediated or chromosomal DNA-mediated.

3 Results and discussion

3.1 Bacterial colony isolation and subculture and screening

In this study, a total of 16 effluent samples were collected from Kolladiba and Debark hospitals. Of these samples, 28 bacterial isolates were recovered. The bacterial isolates from Debark hospital effluent samples were designated as SD1, SD2, SD3, SD4, SD5, SD6, SD7, SD8, SD9, SD10, SD11, SD12, SD13, SD14, SD15, and SD16, while that of Kolladiba effluent samples were labeled as SK1, SK2, SK3, SK4, SK5, SK6, SK7, SK8, SK9, SK10, SK11, and SK12. The isolates were sub-cultured using differential and selective media. From these bacterial isolates, 12 (SD1, SD2, SD4, SD7, SD11, SD15, SD16, SK2, SK3, SK5, SK7, and SK8) were found to be multi-drug resistant. By the way, multi-drug resistance is defined as non-susceptibility to at least one agent in three or more classes of antibiotics.

3.2 Morphological and biochemical characteristics of multi-drug resistant bacteria

Colony morphology is the visual culture characteristics of a bacterial colony on an agar media. Observing colony morphology is an important skill used in the microbiology laboratory for the identification of microorganisms. Colonies need to be well isolated from other colonies to observe the characteristic shape, size, color, surface appearance, and texture. The different colony morphology characteristics, i.e., colony shape, size, texture, appearance, etc., were characterized for each of the 12 bacterial isolates. The details are described in Table 1.

Table 1

Colony characteristics of selected bacterial isolate

Isolate Colony characteristics
Size Color Shape Margin Elevation Texture Appearance Opacity
SD1 1.0 mm Bright yellow Circular Entire Convex Mucoid Rough Opaque
SD2 2 mm Grey Circular Entire Convex Shiny Smooth Opaque
SD4 2.2 mm White Irregular Entire Raised Shiny Smooth Transparent
SD7 1.5 mm Yellow Filamentous Entire Raised Shiny Smooth Opaque
SD11 2 mm Pale yellow Circular Entire Convex Shiny Smooth Transparent
SD15 1.8 mm Colorless Circular Undulate Raised Shiny Smooth Opaque
SD16 1.9 mm Yellow Filamentous Entire Convex Mucoid Smooth Transparent
SK2 0.8 m Yellow Spindle Entire Convex Mucoid Smooth Transparent
SK3 2.6 mm Colorless Circular Undulate Raised Shiny Smooth Opaque
SK5 1 mm Golden yellow Circular Entire Convex Mucoid Rough Opaque
SK7 2.5 mm White Circular Entire Convex Mucoid Smooth Opaque
SK8 2.0 m White Circular Entire Raised Shiny Smooth Transparent

In this study, ten biochemical tests were performed against each isolated multi-drug-resistant bacteria from effluent samples. Variations were observed for the different tests across the isolates. Each of the biochemical test results is presented in Table 2.

Table 2

Biochemical test results for bacterial isolates from effluent Debark and Kolladiba hospital sample

Tests SD1 SD2 SD4 SD7 SD11 SD15 SD16 SK2 SK3 SK5 SK7 SK8
Gram staining + − − + − − − − − + − −
Shape Spherical Rod Rod Spherical Rod Rod Rod Rod Rod Spherical Rod Rod
Indole test − − + − − − − − − − − +
Catalase test + + + + + + + + + + + +
Oxidase test + + − + − + + + + + − −
Urease test − − − − − + − − + − − −
Coagulase test + − − + − − − − − + − −
Citrate test + − − + − − + + − + − −
Motility test − + + − − + − − + − + +
Methyl red + − + + + − − − − + + +
VP test + − − − − − + + − + − −
Isolate name Staphylococcus sp. Citrobacter sp. E. coli Staphylococcus sp. Shigella sp. P. aeruginasa K. pneumoniae K. pneumoniae P. aeruginosa Staphylococcus sp. Salmonella sp. E. coli

In this study, different bacterial colonies were isolated from hospital effluents and identified using morphological characteristics (shape, size, color, texture, margin, and elevation of the colony) and different biochemical tests (Gram staining, urease, catalase, motility, oxidase, indole production, coagulase, citrate, and MR-VP tests) [11]. Based on the morphological and biochemical test results, isolates were assigned as Staphylococcus sp. (SD1, SD7, and SK5), Citrobacter sp. (SD2), E. coli (SD4 and SK8), Shigella sp. (SD11), P. aeruginosa (SD15 and SK3), K. pneumoniae (SD16 and SK2), and Salmonella sp. (SK7).

3.3 Antibiotic susceptibility tests

The 28 bacterial isolates that were recovered from effluent samples were subjected to antibiotic susceptibility tests using seven commonly used antibiotics. Almost all of the commonly used antibiotics that were tested in this study failed to inhibit all 12 bacterial isolates, while the rest isolates were sensitive to all 7 antibiotics (Table 3).

Table 3

Resistance rate of bacterial isolates from Debark and Kolladiba Hospital effluent samples against commonly used antibiotics

Bacterial isolates Antibiotic resistance N (%)
AMP AMX COT GEN NV TET E
Staphylococcus sp. (n = 3) 3(100) 2(66.7) 3(100) 3(100) 3(0) 2(66.7) 3(100)
E. coli (n = 2) 1(50) 1(50) 1(100) 1(50) 1(50) 2(100) 2(100)
P. aeruginosa (n = 2) 2(100) 2(100) 1(50) 1(50) 1(50) 2(100) 2(100)
Salmonella sp. (n = 1) 1(0) 1(0) 1(0) 1(100 1(0) 1(100) 1(100)
Citrobacter sp. (n = 1) 1(0) 1(100) 1(100) 1(0) 1(100) 1(0) 1(100)
Shigella sp. (n = 1) 1(100) 1(100) 1(100) 1(100) 1(0) 1(0) 1(100)
K. pneumoniae (n = 2) 2(100) 2(100) 2(0) 2(100) 2(100) 2(100) 2(100)

AMP: Ampicillin, TET: Tetracycline, GEN: Gentamycin, AMX: Amoxicillin, NV: Novobiocin, E: Erythromycin, COT: Cotrimoxazole.

Susceptibility to antibiotics result presented a varying degree of resistance to the different antibiotics tested against the tested bacteria. However, all isolates were sensitive to at least one of the seven antibiotics except against erythromycin (100% resistance). One isolate of E. coli (SK8) was 100% resistant to all the tested antibiotics. When we take into consideration about isolates showing resistant to more than five antibiotics, the distribution of multi-drug-resistant isolates in Debark and Kolladiba hospitals is still found to be high.

Antibiotic resistance is a major public health threat, and the presence of resistant organisms in environmental wastewaters/effluents is an emerging concern around the world. In this study, high incidences of antibiotics-resistant bacteria were isolated from Kolladiba and Debark Hospitals effluents. Out of 28 isolates, 12 were found to be resistant to at least one to seven tested antibiotics. This appeared to be analogous to what was predicted in many reports by researchers in Ethiopia that there is clear evidence of abuse of antibiotics for which the emergence of multi-drug-resistant bacteria is continuously increasing from time to time [15,16]. The indiscriminate use of antibiotics (misuse and overuse of antibiotics) currently has resulted in the increase of occurrence of antibiotic-resistant bacteria in the hospital effluents. The presence of a high rate of multi-drug-resistant bacteria in the hospital effluent is an alarm to take measures. This is because it may further result in disease spread and treatment failure. Similar results have been reported by Praveenkumarreddy et al. [17] in India and Molla et al. [18] in Gondar, Ethiopia. In this study, the antimicrobial susceptibility pattern shows that the isolates were highly resistant to the most commonly used antibiotics. One isolate of E. coli (SK8), which was isolated from the Kolladiba Hospital effluent sample, was 100% resistant to all the tested antibiotics (Table 3). Conversely, there was a high degree of resistance to erythromycin (100% resistance). The most effective antibiotic was novobiocin, with 58.3% inhibition effectiveness against the tested bacteria. A similar result was reported by Teshome et al. [19] in eastern Ethiopia, who isolated samples from hospital effluents. Study results by Osadebe and Okounim [20] also demonstrated that waste effluent from hospital environments contains a wide range of multi-drug-resistant bacteria.

3.4 Plasmid isolation and bacterial profile

Plasmid isolation and profiling of the 12 bacterial isolates that were resistant to the commonly used broad-spectrum antibiotics were performed. Plasmid profiles for the bacterial isolates revealed that some possessed four plasmids, just a few had single plasmid, and two of them had no plasmid. Isolates SD1 (L111), SK5 (L2), SD15 (L3), SK7(L5), SK3 (L6), SD11 (L9), SD2 (L10), SK2 (L11), and SD16 (L12) were having plasmid(s). Conversely, isolates SK8 (L4), SD4 (L7), and SD7 (L8) do not possess any plasmid when exposed to the horizontal gel electrophoresis, and it means that the multi-drug-resistant gene is not plasmid mediated but it may be chromosomal DNA-mediated. Therefore, the multi-drug resistance in these isolates may be plasmid or chromosomal DNA-mediated. The plasmid sizes for the isolates were found to have different base pair sizes (bps). SD1 (L1), SK7 (L5), and SK2 (L11) had one plasmid with a size of 100 bp, while SK5 (L2), SD15 (L3), SK3 (L6), and SD11 (L9) had two plasmid fragments of 100 bp and approximately 1,500 bp. SD16 (L12) had four plasmid sizes of 100, 900, 1,000, and approximately 1,500 bp, while SD2 (L10) contains two plasmids with sizes of 100 and approximately 1,800 bp. The result of the plasmid profile of the isolates is shown in Figure 3.

Figure 3 Plasmid size determination and a band size of 12 multi-drug-resistant bacteria. Key: M-Marker, L1-SD1, L2-SK5, L3-SD15, L4-SK8, L5-SK7, L6-SK3, L7-SD4, L8-SD7, L9-SD11, L10-SD2, L11-SK2, L12-SD16.
Figure 3

Plasmid size determination and a band size of 12 multi-drug-resistant bacteria. Key: M-Marker, L1-SD1, L2-SK5, L3-SD15, L4-SK8, L5-SK7, L6-SK3, L7-SD4, L8-SD7, L9-SD11, L10-SD2, L11-SK2, L12-SD16.

Plasmid profile studies are widely used for epidemiological studies, and the role of plasmids in drug resistance is well understood. In this study, the presence, number, and molecular size of plasmids were analyzed for the 12 multi-drug-resistant bacterial isolates. The isolates were found to contain various numbers of plasmids (1–4) with different sizes (from 100 to 1,800 bp) (Figure 1). The most common plasmid sizes encountered were 100 and 1,500 bps. These different-sized plasmids were responsible for the presence of multi-drug resistance. The isolates might acquire genetic elements (plasmids) from other bacteria. Large mobile genetic elements appear to encode both antibiotic-resistant factors and proteins that are responsible for the increase in virulence, thus giving the organism the ability to adapt to the selective pressure of antibiotics. This study correlates with the study done by Ojo et al. [21] and Olawale et al. [22]. The analysis of the plasmid profile makes it possible to estimate the dependence between antibiotic susceptibility and the presence of plasmids with respect to a particular isolate [20,22]. It can be said that resistance mediated by plasmid which has been observed in various studies such as Ojo et al. [21], Olawale et al. [22], Jaran [23], Agrahari et al. [24], Nmesirionye et al. [25], and Olorunfemi et al. [26] may be responsible for the differences observed in treatment by clinicians. The gene responsible for multi-drug resistance that occurred in bacterial isolates under this study may be grouped into chromosomal mediated [(SK8 (L4), SD4 (L7), and SD7 (L8)] and plasmid-mediated (the rest isolates).

3.5 Limitation of this study

The limitation of our study was the small number of sample sizes collected due to lack of resources.

4 Conclusions

This study aimed to investigate the presence of antibiotic resistance patterns and bacterial profiles of some multi-drug-resistant bacteria isolated from effluents of Kolladiba and Debark Hospitals. The findings reveal that effluents of Kolladiba and Debark Hospitals have a high incidence of multi-drug-resistant bacteria. From a total of 28 bacterial isolates, 12 were found to be multi-drug resistant. Among the tested antibiotics, erythromycin was the most resisted antibiotic, while novobiocin was the most effective antibiotic. A plasmid profile study of the isolates revealed both the presence and absence of plasmids. The number of plasmids ranged from zero to four, with plasmid sizes of 100, 900, 1,000, 1,400, 1,500, and 1,800 base pairs. Most of multi-drug resistances could be due to plasmid genes. To reduce the incidence of drug resistance, the unwise use of antibiotics by individuals whose health is impaired should be discouraged. In order to reduce the impact of hospital effluents on the spread of antimicrobial resistance in the community, a proper effluent treatment mechanism should be devised.

Acknowledgements

Both authors would like to acknowledge University of Gondar.

  1. Funding information: Authors state no funding involved.

  2. Author contributions: E.A. performed the experiments as part of his master’s thesis work. This work was carried out under the supervision of T.M.J. T.M.J. helped in editing the manuscript. Both authors read and approved the final manuscript.

  3. Conflict of interest: Authors state no conflicts 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: 2024-03-11
Revised: 2024-08-17
Accepted: 2024-08-19
Published Online: 2024-09-11

© 2024 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

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
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  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
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  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
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  25. Current state of research on copper complexes in the treatment of breast cancer
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  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
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https://doi.org/10.1515/biol-2022-0960
Keywords for this article
antimicrobial susceptibility; bacterial profile; effluents; plasmid profile
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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