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 ~  Abstract
 ~ Introduction
 ~  Materials and Me...
 ~ Results
 ~ Discussion
 ~ Conclusion
 ~  References
 ~  Article Figures
 ~  Article Tables

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  Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 38  |  Issue : 3  |  Page : 371-378
 

Antimicrobial activity of biosynthesised silver nanoparticles against multidrug-resistant microbes isolated from cancer patients with bacteraemia and candidaemia


1 Department of Botany and Microbiology, Faculty Science (Boys), Al-Azhar University, Cairo, Egypt
2 Department of Microbiology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt
3 Department of Clinical Pathology, National Cancer Institute, Cairo University, Giza, Egypt

Date of Submission30-Jun-2020
Date of Decision12-Jul-2020
Date of Acceptance25-Jul-2020
Date of Web Publication4-Nov-2020

Correspondence Address:
Dr. Gamal Mohamed El-Sherbiny
Department of Botany and Microbiology, Faculty Science (Boys), Al-Azhar University, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_20_299

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 ~ Abstract 


Background: In the past years, saprophytic bacteria and candida have been emerging as potential human pathogens causing life-threatening infections in patients with cancer. This study was designed to determine the bacteria and candida species, causing bloodstream infections in cancer patients and the assessment of their susceptibility to antibiotics and biosynthesised silver nanoparticles. Materials and Methods: Ninety-seven microbial pathogens recovered from blood samples of cancer patients were included in the present study. The microbial isolates were collected in a duration period extending from December 2016 to July 2018 at National Cancer Institute, Cairo, Egypt. The clinical samples were collected using microbiological methods and were cultivated on MacConkey agar, blood agar media and Sabouraud dextrose agar media. The microbial isolates were identified using both standard microbiological methods and VITEK 2 compact automated system. The antibiotic resistance pattern was determined by the VITEK 2 compact automatic system and disk diffusion method, according to the Clinical and Laboratory Standards Institute. The characterisation of nanoparticles was carried out using ultraviolet spectroscopy and electron microscope. The antimicrobial activity of bio (AgNPs) was evaluated. Results: A total of 97 microbial isolates recovered from collected blood samples from cancer patients were included in the study. Pathogenic bacteria and Candida were represented by 74 isolates (76.22%) and 23 isolates (23.69), respectively. Among the 74 bacterial isolates, Escherichia coli constituted (27.81%), Klebsiella pneumoniae (24.72%), Acinetobacter baummannii (11.33%), Pseudomonas aeruginosa (4.12%), Enterobacter spp. (3.09%) and) Staphylococcus aureus (2.06%). Cedecea davisae (1.03%), Burkholderia cepacia (1.03%) and Pantoea agglomerans (1.03%). Among the 23 Candida isolates, Candida tropicalis constituted (9.27%), Candida albicans (5.15%), Candida glabrata (5.15%) and Candida krusei (4.12%) from the total microbial isolates. The antibiotic susceptibility results revealed that amikacin and gentamycin were the most effective antibiotics against Gram-negative bacteria, while vancomycin and linezolid were most effective against S. aureus. Caspofungin was the most effective against candida species. The obtained stable biosynthesised silver nanoparticles ranged in size from 10 nm to 100 nm and were mostly spherical in shape. These biosilver nanoparticles showed the highest antimicrobial activity against most of the microbial isolates (bacteria and Candida). The in vitro cytotoxicity of biosynthesised AgNPs on HeLa cell lines revealed a dose-dependent potential. The IC50 value of AgNPs was found 6 and 5.6 μg/ml, respectively. Conclusion: The present study revealed a significant distribution of multidrug-resistant microbes, which may increase the burden of healthcare to prevent infections in cancer patients. Biosilver nanoparticles exhibit antimicrobial activity against multidrug-resistant microbes and could be considered as effective agents against these strains.


Keywords: Antibiotic resistance, Bacteria, cancer patients sliver nanoparticles, Candida


How to cite this article:
El-Sherbiny GM, Lila MK, Shetaia YM, F. Elswify MM, Mohamed SS. Antimicrobial activity of biosynthesised silver nanoparticles against multidrug-resistant microbes isolated from cancer patients with bacteraemia and candidaemia. Indian J Med Microbiol 2020;38:371-8

How to cite this URL:
El-Sherbiny GM, Lila MK, Shetaia YM, F. Elswify MM, Mohamed SS. Antimicrobial activity of biosynthesised silver nanoparticles against multidrug-resistant microbes isolated from cancer patients with bacteraemia and candidaemia. Indian J Med Microbiol [serial online] 2020 [cited 2020 Nov 24];38:371-8. Available from: https://www.ijmm.org/text.asp?2020/38/3/371/299829





 ~ Introduction Top


Chronic diseases, especially cancer, is usually minimising immunity. Patients with cancer are highly susceptible to many types of microbial infections.[1] Infections in cancer patients could happen either endogenously from normal flora at the wound and operative site or exogenously from the hospital staff, inanimate environment, air and medical equipment.[2],[3] Many factors increase the susceptibility of immunosuppressed cancer patients to infection, such as neutropenia during aggressive therapy, shift of normal flora because of frequent antibiotic administration, disruption of skin and damage of epithelial surfaces by cytotoxic agents.[4],[5] The treatment of multidrug-resistant (MDR) bacteria represents a global health challenge since they resulted in increased morbidity and mortality rates worldwide. Infection with (MDR) bacteria represented the main cause of death of >700.000 people annually worldwide, and that may rise to ~10 million by 2050.[6],[7] According to the WHO, MDR bacteria are considered those were belonging to the ESKAPE group (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter, Pseudomonas aeruginosa and Enterobacter), and they were highly causing dangerous infections.[8] Infections due to Gram-negative bacilli are common in cancer patients during aggressive therapy.[9] Data from several large surveillance's studies were conducted at major cancer centers both in the United States and Europe. They indicated that Enterobacteriaceae were the cause of approximately 65%–80% of documented Gram-negative infections in cancer patients.[10],[11]Candida species are very often present as commensal organisms in the human body and represent part of the normal microbial flora. However, under immunosuppressive treatment (chemo-radiotherapy), Candida species may transform from commensal to a pathogen in patients with cancer. Candida was the most common invasive fungal pathogen, leading to candidaemia, the cause of morbidity and mortality in hospitalised patients.[12],[13] Nanotechnology holds promising application in antimicrobial agents and drug delivery biosensing and cancer therapy. Biological systems such as bacteria and fungi for the synthesis of noble nanoparticles are easy, inexpensive and eco-friendly. Bio nanoparticles have physicochemical nature, possess biologically active properties such as antimicrobial activity against MDR bacteria and cancer therapy.[14] Therefore, the aim of the present study was to assess the antimicrobial activity of nanoparticles in combating MDR bacteria and Candida isolated from cancer patients admitted at the National Cancer Institute (NCI), Cairo, Egypt.


 ~ Materials and Methods Top


Ninety-seven microbial isolates recovered from positive blood cultures of cancer patients were included in this study. The microbial isolates were collected in a duration period extending from December 2016 to July 2018 at NCI, Cairo, Egypt. The collected samples were processed by standard microbiological methods and were cultivated on MacConkey agar, blood agar and Sabouraud dextrose agar media. All media were readily obtained from (Oxoid, England).

Assessment and Purification of Microbial Isolates

The plates containing MacConkey agar, blood agar, Sabouraud dextrose media were inoculated with the collected clinical samples and were incubated at 35°C for 24 and 48 h. The grown colonies were selected, picked up, purified and then transferred to agar slants containing the same medium. The purified microbial isolates were subjected to a scheme of experimental identification.

Identification of microbial isolates

The pure cultures were identified based on morphological, physiological and biochemical characteristics using Microbiological Methods 8th,[15] Bergey's Manual of Systematic Bacteriology.[16] Identification was confirmed by VITEK 2 compact automated system (Biomerieux Inc., Marcy I'Etoile, France). Candida isolates were identified using chromogenic agar media.[17]

Antibiotic susceptibility testing

Susceptibility of microbial isolates to antibiotics was performed with a VITEK 2 compact automated system (Biomerieux Inc., Marcy I'Etoile, France) and disk diffusion method according to the Clinical and Laboratory Standards Institute recommendation in 2015.[18],[19],[20],[21]

Biosynthesis of silver nanoparticles

Aspergillus fumigatus (ATCC1922) was obtained from Botany and Microbiology Department, Faculty of Science, Al-Azhar University, Cairo, Egypt and was used for the biosynthesis of the AgNPs, 150 ml of yeast malt (ISP2) broth medium was prepared and was inoculated with a fresh culture of A. fumigatus. The inoculated flasks were incubated in an orbital shaker at 30°C, 150 rpm for 8 days. At the end of the incubation period, centrifugation was carried out at 1200 g for 10 min. The supernatant was then combined with 1 mM AgNO3 (1:1, v/v) and was incubated at 30°C in a shaking incubator for 5 days in the dark. Biosynthesised AgNPs were preliminary detected by colour change from yellow colour to dark brown and then confirmed by ultraviolet (UV)–Visible spectroscopy analysis. After the end period, biosynthesised AgNPs were treated with NaCl solution (1% v/v) to remove unreacted Ag ions. The separation of AgNPs present in the solution was centrifuged at 12,000 ×g for 30 min. The biosynthesised AgNPs were purified by one, two, three cycles of precipitation-redissolution in deionised water, respectively, and dried at 40°C. Mass of purified biosynthesised AgNPs was estimated and maintained at 4°C, according to Buszewski et al., (2018).[22]

Characterisation of the biosynthesised sliver nanoparticles

Ultraviolet-visible spectroscopy

The extracellular biosynthesised silver nanoparticles were primarily monitored using UV–Vis spectrophotometer 6800 JENWAY) at a wavelength from 190 to 900 nm.

X-ray diffraction

The morphology and composition of the silver nanoparticles were examined by X-ray diffraction (XRD) analysis (Advance Powder X-ray diffraction meter, Bruker, Germany model D8), Atomic Force Microscopy (Hitachi S4800).

Transmission electron microscopy

The morphology and size of sliver nanoparticles determined using transmission electron microscopy (TEM) in the Center of Biotechnology and Mycology, Al-Azhar University, Cairo, Egypt.

Assessment of antimicrobial activity of biosynthesised silver nanoparticles

Antimicrobial activity of the biosynthesised nanoparticles was expressed as the diameter of the inhibition zones using the agar plate diffusion method.[18] Sterile standard antibiotic discs with a diameter of 6 mm were used to evaluate the activity after loading of 100 μl from synthesised nanoparticles. The resistant microbial isolates were subculture on Muller-Hinton (Oxoid) broth for bacterial isolates at 37°C and on Sabouraud broth for Candida isolates at 30°C in a rotary shaker at 180 rpm. Each microbial isolate was swabbed uniformly onto the individual plates using sterile cotton swabs and was incubated at optimum conditions for tested bacteria and candida. Discs loaded with sliver nanoparticles were aseptically placed on Muller-Hinton agar and Sabouraud dextrose agar plates. At the end of the incubation period, the diameters of the inhibition zones were measured as (mm).[23]

Cytotoxicity of silver nanoparticles

The cytotoxic activity of biosynthesised AgNPs was evaluated in vitro, using the mouse 3T3 fibroblasts and HeLa cell line in triplicate, according to Wypij et al.[24]


 ~ Results Top


In this study, a total of 97 microbial isolates recovered from positive blood cultures from cancer patients were included in the analysis. Sixty-one blood cultures were collected from adults and 36 blood cultures were collected from children. Fifty-seven patients were male and forty patients were female (the male-to-female ratio was 1.42:1). Out of the 97 included microbial isolates, pathogenic bacteria and Candida were represented by 74 (76.22%) and 23 (23.69%) isolates, respectively. Out of the 74 bacterial isolates, 49 (50.47) isolates were recovered from adult patients and 25 (25.75) isolates were recovered from children. Out of the 23 Candida isolates; 12 (12.36) isolates were recovered from adult patients and 11 (11.33) isolates were recovered from children.

Among the 74 bacterial isolates, Escherichia coli constituted (27.81%), K. pneumoniae (24.72%), Acinetobacter baummannii (11.33%), P. aeruginosa (4.12%), Enterobacter spp. (3.09%), S. aureus (2.06%), Cedecea davisae (1.03%), Burkholderia cepacia (1.03%) and Pantoea agglomerans (1.03%). Among the 23 Candida isolates, Candida tropicalis constituted (9.27%), Candida albicans (5.15%), Candida glabrata (5.15%) and Candida krusei (4.12%) from the total microbial isolates [Table 1].
Table 1: Number and percentage of microbial isolates included in the study

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The antibiotic resistance patterns of different Gram-negative bacterial species isolated from blood samples of cancer patients showed that these bacterial isolates were highly resistant to ampicillin, cefazolin, cefotaxime, ceftriaxone, ceftazidime, amoxicillin/clavulanic acid, cefepime and cefoxitin with the ratio of (96.60%), (94.38%) (92.99%), (91.60%),

(91.60%), (89.70%), (88.82%) and (86.05%), respectively. While, they were sensitive to amikacin and gentamycin with a ratio of (55.42%) and (39.42%), respectively [Figure 1]. The two S. aureus isolates were resistant to oxacillin, tetracycline and trimethoprim/sulfamethoxazole, while both isolates were sensitive to vancomycin, linezolid, clindamycin, cefoxitin, ciprofloxacin, nitrofurantoin, meropenem and tigecycline [Figure 2].
Figure 1: Antibiotic susceptibility profile of included Gram-negative bacteria isolated from blood samples of cancer patients

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Figure 2: Antibiotic susceptibility profile of included Staphylococcus aureus isolated from blood samples of cancer patient

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Most of Candida isolates were susceptible to caspofungin with a ratio of 91.14%, followed by miconazole and fluorocytosine with a ratio of 39.06% and 34.72%, respectively. All isolates of C. krusei were resistant to itraconazole, fluconazole and fluorocytosine [Table 2].
Table 2: Antifungal susceptibility profile of included Candida species isolated from blood samples of cancer patients

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The incubation of filtrate of A. fumigatus with silver ion (1 mM) for 24 h. in the dark in shaking incubator showed gradual change into brown colour, while the control cell filtrate without silver ion showed no change in colour. The color intensity increased during the period of incubation [Figure 3]a and [Figure 3]b. The solution of biosynthesised nanoparticles remained as hydrosol, and no precipitation was observed even after 72 h. of incubation. The obtained light absorption of silver nanoparticles indicated a strong surface plasmon resonance band maximum at 445 nm with a characteristic peak for silver nanoparticles [Figure 3]c. Purification of biosynthesised AgNPs by treated with NaCl solution (1% v/v) to remove unreacted Ag ions and centrifuged at 12,000 ×g for 30 min. The mass of purified biosynthesised AgNPs was estimated with 1.2 g/l and dissolving in sterile deionised water. The XRD pattern [Figure 3]d showed four intense peaks at 38.45, 46.35, 64.75 and 78.05 in the whole spectrum ranging from 20 to 80.2 θ. The TEM showed spherical-shaped nanoparticles, and the size of the particles ranged from 10 to 100 nm [Figure 3]e.
Figure 3: Biosynthesis and characterization of silver nanoparticles (a) Filtrate of Aspergillus fumigatus with silver ion (1 mM) at the beginning of the reaction, (b) after 48h of reaction, (c) UV-spectroscopy, (d) X-ray diffraction pattern and (e) TEM image of silver nanoparticles

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The results of antimicrobial activity of the biosynthesised silver nanoparticles against the isolated microbes from blood samples of cancer patients showed activity against all microbial isolates with an inhibition zone ranged from (15–20) to (17–21) mm in case of bacterial and candida isolates, respectively [Table 3], [Table 4], [Table 5].
Table 3: Antibacterial activity of biosynthesized sliver nanoparticles against some bacterial species isolated from blood samples of cancer patients

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Table 4: Antimicrobial activity of biosynthesized sliver nanoparticles against some Candida species isolated from blood samples of cancer patients

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Table 5: Current available medical products containing sliver nanoparticles

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Cytotoxic activity of biosynthesized AgNPs

The biosynthesised AgNPs from A. fumigatus (ATCC1022) were subjected to cytotoxicity against HeLa cell line. HeLa cells viability after treatment with 1, 2, 4, 6, 8, 10, 20 and 40 μg/ml of AgNPs was found to be 96.3, 85.2, 73.1, 64.5, 42.0, 35.2, 24.5 and 15.0%, respectively [Figure 4]. The IC50 value of AgNPs was found to be 6 and 5.6 μg/ml,
Figure 4: Cytotoxic activity of biosynthesized AgNPs from Aspergillus fumigatus HeLa cell line

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 ~ Discussion Top


Ninety-seven microbial isolates were included in the present study. The microbial isolates were recovered from blood samples obtained from cancer patients at NCI, Cairo, Egypt. Seventy-four (76.22%) bacterial isolates and 23 (23.69%) Candida isolates were included in the study. Among the 74 bacterial isolates, Gram-negative bacteria were presented by 74.16% (72/97), whereas Gram-positive bacteria were presented by 2.06% (2/97) of total microbial isolates. Carenav et al., (2020) reported that Gram-negative rods causing bacteremia accounted for 66% of the total cohort of bacteremia of cancer patients.[25] Among the 74 bacterial isolates, E. coli constituted (27.81%), K. pneumoniae (24.72%), A. baummannii (11.33%), P. aeruginosa (4.12%), Enterobacter spp.(3.09%), S. aureus (2.06%). C. davisae (1.03%), B. cepacia (1.03%) and P. agglomerans (1.03%). Among the 23 Candida isolates, Candida tropicalis constituted (9.27%), C. albicans (5.15%), C. glabrata (5.15%) and C. krusei (4.12%) from the total microbial isolates. Eldomany and Abdelaziz reported that E. coli was the main isolated Gram-negative bacteria from all clinical samples (30%) followed by P. aeruginosa (24.5%) and by A. baumannii (18.7%).[26] Another study found that most frequent isolates among patients with leukemia and solid tumors were K. pneumoniae (31.2%), followed by E. coli (22.2%).[27] In a study performed by Hassan et al., the most common isolated microorganisms from febrile neutropenia cancer patients were Gram-negative bacteria (180/212: 84.9%). Escherichia coli was the most frequently isolated pathogen (38.68%), followed by Klebsiella sp. (14.15%) and Acinetobacter sp. (11.32℅).[28] Trecarichi and Tumbarello reported that the rate of Gram-negative bacteria recovery from cancer patients ranged from 24.7% to 75.8%. E. coli represented the most common species (mean frequency of isolation 32.1%).[29]

According to the susceptibility of Gram-negative bacilli to available antibiotics, we found high resistance to ampicillin, cefazolin, cefotaxime, ceftriaxone and ceftazidime while sensitivity to amikacin and gentamycin was (55.42%) and (39.42%), respectively. The two S. aureus isolates included in the study were resistant to oxacillin, tetracycline and trimethoprim/sulphamethoxazole, while both were sensitive to vancomycin, linezolid, clindamycin, cefoxitin, ciprofloxacin, nitrofurantoin, meropenem and tigecycline. Antibiotic resistance of the major pathogens increased gradually.[30] Eldomany and Abdelaziz reported that Gram-negative isolated from cancer patients were highly resistant to cefotaxime and ceftazidime. Acinetobacter sp. exhibited 84.1% and 81.2% resistance to cefotaxime and ceftazidime, respectively.[26] The percentage of resistance to ceftazidime and cefotaxime was also high in Klebsiella, Escherichia, Pseudomonas and Enterobacter species. In addition, simultaneous resistance to ceftazidime and cefotaxime was evident in E. coli, Enterobacter and Klebsiella species at the following respective percentages, 54.4%, 95.8% and 57.9%, respectively. The decreased susceptibility to most tested antibiotics, including non-β-lactam antibiotics such as aminoglycosides (gentamicin) and quinolones (ciprofloxacin, levofloxacin) was observed in isolates of E. coli, Enterobacter, Klebsiella, Pseudomonas and Acinetobacter species.[31] MDR Gram-negative rods represent a growing threat for cancer patients.[25]Candida species are ubiquitous yeasts that cause superficial and invasive diseases in humans.[32],[33] Twenty-three Candida isolates were included in the present study. Candida tropicalis was the most prevalent Candida species isolated from clinical samples, followed by C. albicans, C. glabrata and C. krusei. This result agreed with Indian studies, Candida tropicalis was the most common isolated species followed by C. albicans.[34] The most common Candida species emerging as fungal cause of bloodstream infections are C. albicans, C. tropicalis, C. glabrata, C. krusei and C. parapsilosis.[35] The distributions of Candida species are different in various studies and regions, like 50% C. albicans, 24.7% C. glabrata and 1% C. parapsilosis in other studies.[36] Candidaemia is rarely present in healthy individuals but is common in chronic patients' diseases, including diabetes mellitus, indwelling urinary catheters, immunosuppression, cancer patients and exposure to antimicrobials.[37],[38] The antifungal susceptibility testing of pathogenic candida revealed increasing resistance of Candida species, due to long-term use of antifungals. These results were in agreement with Badiee and Alborzi 2011.[39] Blackbird and Alem isolated Candida species from blood cultures of patients with invasive candidiasis that showed resistance to azole antibiotics.[40] Caspofungin was active against most of Candida isolates with a ratio of 91.14%; this finding was in agreement with Amran et al. 2011.[41] Nanoparticles are considered to be a viable substitute or combined with antibiotics and appeared to have a high potential to solve the problem of the increasing of microbial multidrug resistance.[42] Nanoparticles are synthesized by physical, chemical and biological methods. Bhainsa and Souza in used A. fumigatus for the synthesis of silver nanoparticles.[43] Similarly, in the present study, A. fumigatus was also used for the synthesis of silver nanoparticles. The biosynthesised sliver nanoparticles can be primarily confirmed through observation of the change of yellow colour into dark brown due to the excitation of surface plasmon vibration. The XRD analysis was carried out to confirm the crystalline nature of the bio (AgNPs). TEM analysis of the dried particles measured the size of bio (AgNPs) as 100 nm. Spherical nanoparticles with a size range of 10–100 nm were synthesised by cell filtrate of Streptomyces sp.[44] In this study, biosynthesised silver nanoparticles exhibited antimicrobial activity against multidrug resistance microbes isolated from blood samples of cancer patients with an inhibition zone ranged from (15–21 mm). Wypij et al., reported the antimicrobial activity of silver nanoparticles against all tested bacteria and yeasts.[24] The antimicrobial activity of nanoparticles was dependent on their shape and size.[45] Nasrollahi et al., in (2011), reported the higher antifungal activity of AgNPs against C. albicans compared to fluconazole and amphotericin B.[46] The biosynthesised (AgNPs) attacked Gram-negative bacteria by penetrating the cell wall and changing cell membrane permeability.[47] The mode of action of (AgNPs) was associated with the formation of free radicals that induce cell membrane damage. Interaction of AgNPs with DNA were preventing replication of nucleic acid, cell division and leading to cell death.[48] Silver nanoparticles have anticancer activity against five different tumours cell lines.[49] Thein vitro study of cytotoxic efficacy of biosynthesised AgNPs on HeLa cell line was high IC50 about 6 μg/ml. However, other authors reported that the concentration of AgNPs reduction in viability by 50% HeLa cells was 100 μg/ml.[50] Rathod et al., in (2016), reported the lower cytotoxic effect of AgNPs (IC50 value of 64.5 μg/ml) against mouse fibroblasts (L929 cell line).[51],[52] The cyto- and geno-toxic effect of Ag-NPs is dependent on their concentration, size, exposure time and environmental factors. Furthermore, Majeed et al., in (2016), found that silver nanoparticles exhibit anticancer activity against breast cancer cell line.[53]

In the last few years, there has been a steadily growing interest in using silver nanoparticles in different biomedical applications such as targeted drug delivery, photoablation therapy, hyperthermia, bioimaging and biosensors. The product of silver nanoparticles used to treatment cardiovascular implants, wounds, burns, ulcers, catheters, cancer, bone cement, antiviral, antifungal and antibacterial.[54],[55]


 ~ Conclusion Top


The results of this study indicated that microbial isolates with high multidrug resistance represent a life-threatening condition to patients with cancer. A. fumigatus can be used for the biosynthesis of AgNPs using an inexpensive and eco-friendly method.

Acknowledgements

We would like to thank staff members of the Microbiology unit at the NCI, Cairo, Egypt, for providing the clinical samples.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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2004 - Indian Journal of Medical Microbiology
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