Bactericidal, virucidal and fungicidal effect of ZnO, Ag, and ZnO+Ag coatings

doi:10.21203/rs.3.rs-4944515/v1

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Bactericidal, virucidal and fungicidal effect of ZnO, Ag, and ZnO+Ag coatings

https://doi.org/10.21203/rs.3.rs-4944515/v1

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Intensified globalization means the wider spread of pathogenic viruses, bacteria and fungi. Many such microorganisms are transmitted through contact with surfaces polluted with biodeposits as well as through human activity, which greatly increases the risk of infections caused by microbes. Therefore, the search for new effective solutions to inactivate pathogenic microorganisms that ensure safety and improve quality and comfort of life has become a global priority and major challenge. A very effective activity in this area may be the use of surface engineering technologies, which enable the production of coatings with biocidal properties. The very large possibilities of these technologies in terms of shaping the microstructure, chemical composition and phase composition of coatings enable effective shaping of functional properties. The aim of this study was to compare the properties of three types of coatings deposited by HIPIMS characterized by different chemical compositions and microstructures. In this work, all the produced coatings were analyzed in terms of their material, physical and biocidal properties. The authors confirmed the very good biocidal properties of the tested materials against various groups of microorganisms (bacteria, fungi and viruses) at the same time.

Biological sciences/Microbiology/Antimicrobials

Physical sciences/Materials science

Physical sciences/Materials science/Nanoscale materials

Constant human migration causes intense movement of pathogenic viruses, bacteria and fungi, and the observed climate changes create favorable conditions for the migration and development of microorganisms. Currently, the main source of infection involving various types of microorganisms is our immediate surroundings. In modern society, a major problem is the growing number of diseases caused by microorganisms transmitted by various types of frequently touched surfaces in public areas, such as door handles, knobs and grips, sanitary elements, light and lift buttons, and keyboards. In recent years, there has also been an increase in hospital infections (HCAIs) caused by pathogenic microorganisms transmitted through various surfaces. This results in frequent illness, which is accompanied by significant patient mortality. The European Center for Disease Prevention and Control (ECDC) estimates that approximately 4.1 emergency room (ER) patients develop HCAI annually, resulting in 37,000 deaths directly related to HCAI [1]. According to a report by M. Heron et al. [2], hospital-acquired infections lead to 98987 deaths annually in the USA, which is far beyond the number of deaths caused by diabetes and heart failure, with 68504 and 56752 cases, respectively. An increase in hospital infections also causes a significant increase in healthcare costs. Nevertheless, the phenomenon of diseases caused by various types of surfaceborne microbes is unavoidable. While hand hygiene is widely regarded as the most important preventive measure, antimicrobial agents, which can significantly reduce the growth of microorganisms on various types of surfaces, are also essential. Schmidt et al. [3] measured microbial burden by weekly sampling in intensive care units (ICUs) in three hospitals in the USA over 23 months. The average microbial burden of the six studied frequently touched objects was 28 times greater than the safe microbial burden. Subsequently, the objects were replaced with bulk copper alloys, and a significant decrease in the average microbial burden was observed. Nevertheless, it is not possible to use copper alloys in public spaces, mainly due to the high cost of the elements made of these materials and the difficulty in achieving functional and aesthetic value. Thin films (also called coatings) have several advantages over bulk materials, such as reduced material usage or enhanced properties, and they show great flexibility when deposited on a wide range of substrates, including plastics. To date, there has not been successful implementation of antibacterial coatings with proven antibacterial properties during long-term utilization. Therefore, the search for new effective means of deactivating viruses, bacteria or fungi in public spaces is among the priority scientific activities worldwide and is the main challenge for civilization, ensuring the safety and comfort of citizens. The value of the global market for antibacterial coatings in 2019 was USD 3.6 billion, and it is expected to reach USD 8.6 billion by 2027, which confirms the very high demand for these types of solutions [⁴].

In response to such global problems, new solutions are sought that will reduce the transmission of various types of microorganisms and thus reduce the number of diseases caused by them. Surface engineering and the application of PVD coatings in this area are gaining importance. Recently, thin coatings built on basis metals with biocidal properties, such as Ag, Cu, Zr, and W [5–8], have been developed as a new class of materials characterized by antimicrobial activity. Unfortunately, the coatings presented in the literature are typically based on only one metal, which results in selective biocidal properties; i.e., these coatings have bactericidal or fungicidal properties. This is related to the observed mechanisms of microorganism destruction involving individual elements and their compounds. The constant progress of science in the area of biocidal effects of nanoparticles (NPs) has confirmed that different metals affect microorganisms in different ways, mainly through different mechanisms of destruction [9]. Different metallic nanoparticles use several modes of action to do this. NPs have been shown to penetrate the bacterial cell wall and form pores on the surface of the membrane, which in turn causes free radical formation, which can also destroy the cell membrane [10–11]. Ions from NPs can interfere with enzyme production and generate reactive oxygen species (ROS) [12]. DNA transcription has also been shown to be affected [13]. In addition, the possibility of synergistic interactions between two or more types of metallic nanoparticles to eliminate several types of microbes simultaneously was also observed [14–16]. The synergistic interaction of the components in shaping various functional properties of the coatings has already been confirmed [17–19]. Therefore, the combination of PVD technology for shaping materials with nanometric structures with the introduction of several different metals in the coating should also provide synergistic biocidal effects to the corresponding nanoparticles.

The aim of this study was to compare the properties of three types of coatings deposited by HIPIMS characterized by different chemical compositions and microstructures. The tested coatings were deposited on samples made of pure iron (ARMCO). In this work, all the produced coatings were analyzed in terms of their material, physical and biocidal properties. The authors analyzed the impact of the structure of the coatings on the biocidal properties against various microorganisms (viruses, bacteria and fungi) at the same time.

2.1. Coating

All coatings studied were produced on Standard III coating unit by łukasieiwcz – ITEE presented on Fig. 1. The device has two plasma sources located on the wall of the chamber (Fig. 2b). For the process of coating deposition, two types of targets, Ag (99.99% purity) and ZnO (99.99% purity), with the diameter of 100 mm and a thickness of 7 mm, produced by Lesker, were used. The distance between the sample and the plasma source was 200 mm.

The samples were coated at room temperature in a reactive gas atmosphere with an oxygen and argon mixture. The process of coating deposition was carried out at constant pressure, and the variable argon flow, which was adjusted to the thermodynamic conditions of the process, ranged from 290 to 300 sccm. An MKS working atmosphere control system was installed in the Standard 3 device, which enabled precise control of gas flows while maintaining a constant pressure in the working chamber. During the coating deposition process, the rotation (2 rpm) of the substrates in the chamber space was introduced. The coatings were produced without substrate polarization. The detailed parameters of the deposition process are presented in Table 1.

Table 1

PVD coating production process parameters
Material	Atmosphere	Pressure p [mbar]	U_bias [V]	Magnetron source power P [W]	Temperature T [^oC]
Ag	Ar:300 sccm	5.0 x 10^− 3	-	Ag:100		TORUS(Ag)
ZnO	N₂:350 sccm	5.0 x 10^− 3	-	ZnO:260	20	TORUS(ZnO)
Ag + ZnO	N₂:350 sccm	5.0 x 10^− 3	-	Ag:100, ZnO:260		TORUS(Ag) and (ZnO)

Coatings were made on two types of samples for the purpose of the study:

samples made of pure ARMCO with diameter φ = 25 mm, thickness = 6 mm and surface roughness = 0.05 µm were used for the analysis of the chemical composition, phase structure and microstructure of the coatings;
POLYMER samples with a diameter φ = 25 mm, thickness g = 6 mm and surface roughness Ra = 0.05 µm were used for the analysis of antibacterial properties.

2.2. Materials investigations

Microstructure

The surface morphology of the coatings was observed with a Helios 5 PFIB Xe scanning electron microscope with xenon ion sources and a TOF-SIMS detector. A secondary electron (SE) signal was used in the observations. TEM sample preparation and STEM observation at 30 kV were performed with the same equipment (Helios 5 PFIB).

Roughness

Surface roughness and topography tests were carried out for all the PVD coatings produced. To this end, a KEYENCE VHX1000 digital microscope was used.

Chemical composition

Energy-dispersive X-ray spectroscopy (EDS) was applied to analyze the chemical composition of the coatings with the use of the EDAX Octane Elite Super system (Gatan). Measurements were performed at an acceleration voltage of 5 kV and a beam current of 0.8 nA. The surface chemical composition of the Ag + ZnO coating was investigated with the use of a time-of-flight secondary ion mass spectrometry (TOF-SIMS) system (TOF-WERK).

Phase composition

X-ray diffraction was carried out on a Bruker D8 Advance diffractometer (goniometer radius 280 mm) equipped with parallel beam optics and a Cu Kα radiation (λ = 0.154056 nm) source that operates at 40 kV and 40 mA. The scan optics include a Göbel mirror on the incident beam side and twin secondary Soller slits in the diffracted beam. The measurements were performed with a fixed angle of incidence of the primary beam equal to 2° over the 2θ range between 20° and 100°, with a step size of 0.025° and 3 s counting time per step.

2.3. Bactericidal properties

The antimicrobial activity of the ZnO, Ag, and ZnO + Ag coatings on the polypropylene surface was assessed according to the procedure recommended by International Standard ISO 22196 ‘Plastics – Measurement of antibacterial activity on plastic surfaces”, with our own modifications expanding the scope of the test in question to include antifungal (against mold and yeast) and antiviral (against bacteriophage) activities [20]. Seven reference microbial strains were used in this study: Staphylococcus aureus (ATCC 6538P), Bacillus subtilis (ATCC 6633), Escherichia coli (ATCC 13706), and Streptomyces albus (ATCC 3004); Candida albicans (ATCC 10231) and Penicillium melinii (ATCC 10469); and the bacteriophage Phi X174 (ATCC BAA-13706).

Antimicrobial activity tests were carried out according to the abovementioned International Standard ISO 22196 [20]. Briefly, flat specimens of treated and untreated polypropylene materials with a surface area of approximately 127 mm² were placed into separate Petri dishes with the test surface being placed first, inoculated with 0.04 ml of the test microbial inoculum and covered with a piece of polyethylene film that was gently pressed down to spread the inoculum to the edges (while paying attention to the test inoculum not leaking beyond the edges of the cover film). The concentrations of the microbial inocula used were as follows: S. aureus, 2.55×10⁵ cfu/cm³; B. subtilis, 5.80×10⁵ cfu/cm³; E. coli, 1.40×10⁵ cfu/cm³; S. albus, 3.95×10⁵ cfu/cm³; C. albicans, 2.02×10⁵ cfu/cm³; P. melinii, 3.01×10⁵ cfu/cm³; and the bacteriophage Phi X174, 6.25×10⁵ pfu/cm³. Immediately after inoculation, half of the untreated test specimens were processed by adding 1 ml of soybean casein digest broth supplemented with lecithin and polyoxyethylene sorbitan monooleate (SCDLP) to a Petri dish containing the test specimen, and the microorganisms were completely washed from the specimens by using a pipette to collect and release the applied neutralizer at least four times. The second half of the untreated test specimens was incubated together with the inoculated test specimens in Petri dishes at a temperature of 35 ± 1°C and a relative humidity of no less than 90% for 24 ± 1 h. The test specimens were subsequently cultured using the same washing procedure described above. After these steps, viable microorganisms were enumerated by performing 10-fold serial dilutions of the SCDLP in phosphate-buffered physiological saline with subsequent plating of these aliquots on trypticase soy agar (for bacteria) and Sabouraud agar (for fungi) and incubating each of these diluted samples at 35 ± 1°C for 40–48 h. After incubation, the number of microbial colonies was determined for each test specimen in accordance with the following equation:

N = (100 × C × D × V)/A

where N is the number of viable microorganisms recovered per cm² per test specimen;

C – the average plate count for the duplicate plates;

D – the dilution factor for the plates counted;

V – is the volume, in ml, of the SCDLP added to the specimen;

A is the surface area, in mm², of the cover film.

When the test was deemed valid, the antimicrobial activity, R, was calculated using the following equation:

R = (U_t − U₀) − (A_t − U₀) = U_t − A_t

where U₀ is the average of the common logarithm of the number of viable microorganisms, in cfu/cm² or pfu/cm², recovered from the untreated test specimens immediately after inoculation;

U_t is the average of the common logarithm of the number of viable microorganisms, in cfu/cm² or pfu/cm², recovered from the untreated test specimens after 24 h;

_At– is the average of the common logarithm of the number of viable microorganisms, in cfu/cm² or pfu/cm², recovered from the treated test specimens after 24 h.

3.2. Microstructure and chemical composition

SEM photographs of the surfaces and cross-sections of the analyzed coatings are shown in Figs. 2, 3 and 4.

SEM observations revealed that the Ag coating has a homogeneous surface morphology consisting of small spherical grains (Fig. 2a). The average grain size, calculated by counting the number of grains per surface area, was 85,2 nm. A small porosity between the grains is visible. Figure 2b shows the cross-section of the Ag coating prepared by the focused ion beam technique. The total thickness of the coating was 375 nm. The microstructure of the coating consisted of irregularly shaped grains that were elongated toward the growth direction. A relatively good contrast is visible due to the difference in the crystal orientations of the grains. Moreover, grain growth twinning behavior was observed in some grains.

Figure 3 shows the surface morphology (Fig. 3a) and cross-section (Fig. 3b) of the ZnO coating deposited on the ARMCO substrate. Like the Ag coating, the ZnO coating has a homogeneous morphology, which confirms the occurrence of a smooth and optimized deposition process. However, the grain size is much lower than that of the Ag coating. It was difficult to determine the exact diameter of the ZnO grains, but it was in the range of 10–20 nm. The grains also had a spherical shape. Cross-sectional observation revealed that the thickness of the ZnO coating was 235 nm. Thus, the deposition rate of the ZnO coating was lower than that of the Ag coating. Due to the small size of the grains, it was impossible to distinguish grains in the cross section. Nevertheless, it can be concluded that the applied deposition parameters allowed Ag coating to reach equilibrium, while ZnO was in a nonequilibrium state with likely high residual stresses.

Figure 4 shows the morphology and microstructure of the Ag + ZnO composite coatings. The surface is a mixture of Ag and ZnO coatings, which was also confirmed in studies of the phase structure of these coatings. Both a silver phase and a zinc oxide phase were present in the structure of the coating, which confirmed the composite (two-phase) structure of the Ag + ZnO coating (Fig. 5). We observed larger and brighter grains of silver and smaller grains of zinc oxide between them. However, Ag grains have irregular shapes and differences in size. To analyze the microstructure of this composite coating, TEM images were prepared and observed using a STEM3 detector (Fig. 4). The total thickness of the coating was 980 nm. The sample exhibited different microstructures in the surface region and in the core of the coating. Larger silver grains are located only on the surface of the coating. Smaller Ag grains were also observed in the core of the coating. They are arranged along the growth direction. The porosity (darker lines) was also oriented perpendicular to the surface. The rest of the coating comprises very small, nanometric grains of ZnO. A possible explanation for this microstructure-forming process could be as follows. During deposition, the temperature of the coating increases. The residual stress also increased. Under such conditions, the coating (ZnO) grains can “squeeze” silver grains and push them toward the surface. The mechanism of Ag mass transfer from the core to the surface could be plastic flow. A lower pressure in the chamber has a favorable effect on such behavior. Confirmation of this statement requires additional experiments, for example, measuring the temperature increase during the process.

Figure 6 shows the distribution of Ag at the cross-section of the Ag + ZnO coating. It is very difficult to perform quantitative analysis with the TOF-SIMS technique. It was also impossible to determine the sputtering rate of the coating. Thus, the figure shows the number of counts vs. the frame number. Each frame (ion sputtering) leads to greater depths. Nevertheless, the performed measurements confirmed the STEM observations that most of the silver was located at the surface of the coating.

The surface roughness analyses performed at the microscale are shown in Fig. 7. The analyses included a comparison of the Ra, Rz, and Rt values of samples coated with Ag, ZnO and ZnO-Ag coatings.

The samples with one-component ZnO coatings had lower roughnesses than did the other samples. The very high smoothness of this coating is related to its fine-grained structure (Fig. 3). The average grain size of the ZnO coating does not exceed 20 nm. The pure silver coating is composed of grains four times larger in diameter (Fig. 2), which results in increased roughness parameters. Similarly, in the case of the ZnO + Ag coating, a high concentration of silver grains with a larger diameter on the coating surface (Fig. 5) resulted in a significant increase in roughness compared to that of the ZnO coating.

3.4. Bactericidal test

The antimicrobial activities of the ZnO, Ag, and ZnO + Ag coatings on the polypropylene surface against the 7 microbial strains are presented in Table 2. All the tested coatings exhibited antimicrobial activity (R) against all the bacteria, fungi, and bacteriophages. Among the vegetative bacterial cells, the highest R values were noted for S. aureus, against which all 3 tested coating variants (i.e., ZnO, Ag, and ZnO + Ag) were almost equally effective, and the lowest R was recorded for S. albus. However, in the case of this bacterium, the combination of Ag and ZnO was more effective than the pure Ag and ZnO coatings. The observed higher activity of the ZnO + Ag coating (R_ZnO+Ag=1.65) against S. albus than that of the singlecomponent coatings (R_ZnO=1.52, R_Ag=0.8) may indicate the occurrence of synergistic effects. All the tested coatings behaved slightly differently in relation to E. coli, for which the R values were the highest when the ZnO and Ag coatings were separately applied to the polypropylene surface. The combination of ZnO and Ag in the coating did not result in an additive effect. The latter pattern was also observed for antimicrobial activity against C. albicans, P. melinii mold and the Phi X174 bacteriophage, where both the ZnO and Ag coatings were more effective at limiting the survival rate of both of these microorganisms. In turn, for C. albicans and P. melinii, the ZnO coating was much more effective at decreasing the survival rate of these yeast plants than was the other two tested coating variants (i.e., Ag and ZnO + Ag).

Table 2

Antimicrobial activity of ZnO, Ag, and ZnO + Ag coatings on polypropylene surfaces.
Microorganism
	Incubation time [h]	0	24	24	24	24
Staphylococcus aureus ATCC 6538P	Number of viable microorganisms [cfu/cm²]	1.57×10⁵	1.24×10⁴	1.69×10⁰	1.31×10⁰	1.51×10⁰
	Log₁₀	U₀ = 5.20	U_t=4.09	A_t=0.23	A_t=0.12	A_t=0.18
	Antimicrobial activity, R	–	–	3.87	3.98	3.92
Bacillus subtilis ATCC 6633	Number of viable microorganisms [cfu/cm²]	1.09×10⁵	6.46×10³	1.46×10⁰	1.31×10⁰	1.33×10⁰
	Log₁₀	U₀ = 5.04	U_t=3.81	A_t=0.16	A_t=0.12	A_t=0.13
	Antimicrobial activity, R	–	–	3.65	3.69	3.68
Escherichia coli ATCC 13706	Number of viable microorganisms [cfu/cm²]	6.39×10⁴	8.28×10²	1.19×10⁰	3.57×10⁰	1.19×10¹
	Log₁₀	U₀ = 4.81	U_t=2.92	A_t=0.08	A_t=0.55	A_t=1.08
	Antimicrobial activity, R	–	–	2.84	2.37	1.84
Streptomyces albus ATCC 3004	Number of viable microorganisms [cfu/cm²]	4.21×10³	6.55×10¹	1.52×10⁰	1.03×10¹	1.46×10⁰
	Log₁₀	U₀ = 3.62	U_t=1.82	A_t=0.30	A_t=1.01	A_t=0.16
	Antimicrobial activity, R	–	–	1.52	0.80	1.65
Candida albicans ATCC 10231	Number of viable microorganisms [cfu/cm²]	2.43×10⁴	9.46×10²	1.09×10¹	1.09×10¹	2.82×10¹
	Log₁₀	U₀ = 4.39	U_t=2.98	A_t=0.23	A_t=1.04	A_t=1.45
	Antimicrobial activity, R	–	–	2.75	1.94	1.53
Penicillium melinii ATCC 10469	Number of viable microorganisms [cfu/cm²]	1.72×10⁵	1.40×10³	1.85×10⁰	2.64×10⁰	3.92×10¹
	Log₁₀	U₀ = 5.23	U_t=3.15	A_t=0.27	A_t=0.42	A_t=1.59
	Antimicrobial activity, R	–	–	2.88	2.73	1.55
Phi X174 bacteriophage ATCC BAA-13706	Number of viable microorganisms [pfu/cm²]	7.39×10⁴	1.15×10⁴	6.71×10¹	5.04×10¹	3.61×10²
	Log₁₀	U₀ = 4.87	U_t=4.06	A_t=1.83	A_t=1.70	A_t=2.56
	Antimicrobial activity, R	–	–	2.23	2.36	1.50

The observed differences in the microbiological activity of the coatings in relation to the different groups of microorganisms can be explained by the structure of the microorganisms themselves. The lower biocidal activity of the Ag coating in relation to that of gram-negative bacteria and Candida fungi may be due to the difference in the structure of the structures surrounding the cells of gram-positive and gram-negative bacteria [21, 22]. Additionally, gram-negative bacteria have a cell membrane that significantly limits the penetration of hydrophobic molecules with high molecular weights, such as silver. The confirmed lower antifungal activity of silver nanoparticles [23] explains the lower antifungal activity of the silver Ag coating compared to that of the zinc oxide ZnO coating.

The significant reduction in the activity of the ZnO + Ag coating against gram-positive bacteria and fungi compared to that of the ZnO and Ag coatings may be due to the structure of the coating itself. The observed presence of irregularly shaped silver particles on the surface of the ZnO + Ag coating may result in a reduction in microbiological effectiveness compared to that of a pure silver coating, which is composed of spherical silver particles with a regular shape.

The analyses allowed the following general conclusions to be formulated:

The Ag, ZnO and Ag + ZnO coatings are characterized by high microbiological activity but differ in relation to different groups of microorganisms. The observed differences may be related to the features of the different groups of microorganisms, such as cell structure and size. In addition, the microbiological effectiveness may be influenced by the parameters of the coating material, such as the microstructure, chemical composition, and phase structure.

The obtained results showed that the synergistic biocidal effects of coatings with complex chemical compositions are possible. This was confirmed by the greater bactericidal activity of the ZnO + Ag coating against S. albus bacteria than that of the Ag and ZnO coatings. However, no answer was found as to what factor influences the occurrence of this effect.

Future work on the microbiological effectiveness of coatings should focus on analyzing the mechanisms of destruction of microorganisms combined with a detailed material analysis of the coatings, including the microstructure and nanometric phase structure.

The results of these experiments allow us to conclude that thin coatings produced by the magnetron method could be an effective solution for limiting the development of various groups of microorganisms (bacteria, fungi and viruses).

Funding:

This work was supported by the National Centre for Research and Development in Poland and was carried out within the project TECHMATSTRATEG III “Long-life composite filter media for water cleaning and high efficiency separation of gas‒liquid and liquid‒liquid dispersions”, no. Techmatstrateg III/005/2019-00.

Author Contribution

J.K-G. wrote the main manuscript text, prepared figures.J.K.G, J.S. ,A.K. and L. G. projekt rozwiązania materiałowego cienkich powłokJ.K.G projekt oraz realizacja procesu technologicznego osadzania powłok S.S. reazliacja badań chropowatości powierzchni powłokP.W. and H.G realizacja oraz analiza badań mikrostruktury oraz składu fazowego powłokR.G. and A.S-K reazliazja badań właściwości biobójczychAll authors reviewed the manuscrip

Data Availability

The datasets used and analysed during the current study available from the corresponding author on reasonable request.

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No competing interests reported.

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Bactericidal, virucidal and fungicidal effect of ZnO, Ag, and ZnO+Ag coatings

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Abstract

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1. Introduction

2. Materials and methods

2.1. Coating

2.2. Materials investigations

2.3. Bactericidal properties

3. Results and discussion

3.2. Microstructure and chemical composition

3.4. Bactericidal test

4. Conclusions

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Funding:

Author Contribution

Data Availability

References

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