1. Introduction
Copper (Cu, atomic number 29), is not one of the most abundant chemical elements on earth. Yet, its power, functions and application are myriad. Through its integration into ointments, liquid solutions, compression clothing and jewelry (e.g. anti- arthritis bracelets), it has played a key role in folk medicine for decades, and ancient civilizations employed copper to fight microbes long before microbes were known and named (Sorensen, 2012). It is now recognized that copper is essential to the normal development, function and growth of living organisms of all types (Martínez‐Bussenius et al., 2017). However, it is only in recent years that the anti-bacterial properties of copper and its alloys (e.g. bronzes, brasses, and cupronickel) have been systematically investigated, with researchers in healthcare, hospitality and other industrial settings expressing interest in copper’s potential application in a broad range of products and materials. Specifically, it has been found that copper and copper alloys are effective against a range of microorganisms that represent a threat to public health. This includes pathogens as varied as bacteria like Methicillin-Resistant Staphylococcus Aureus (MRSA) and Clostridium difficile, and viral pathogens, such as influenza and adenovirus (Sorensen, 2012; Noyce et al., 2007; Weaver et al., 2007). Drawing on these findings, researchers are interested in exploiting copper and copper-based products for use in a wide range of industrial settings, especially those that involve patient care, the production of medications and the preparation of foods. Before discussing the potential anti-bacterial applications of copper, a scientific overview and brief history of its usages is provided.
2. Scientific Background
2.1 History of Copper
There is some scarce, but clear archeological evidence of the use of copper by human civilizations in Europe and the Middle East dating as far back as the 5th millennium BC (Grass et al., 2011). The beginning of the metallurgic, or Bronze Age (around the 2nd millennium BC) is marked by the invention of smelting as a method of extracting metals from their ore, and copper was soon combined with tin to form bronze. During this time, there is evidence that copper was used as a sterilizing agent; according to Borkow & Gabbay (2009), it was frequently added to water to make it potable, and to treat wounds, as well as being used for general hygiene purposes by ancient Romans, Greeks, Aztecs and other early civilizations. A turning point occurred in the 19th century when multiple outbreaks of cholera (an infectious disease caused by the Vibrio cholerae bacterium which is typically transmitted through food or water) occurred in Paris, France. It was observed that the city’s jewellers, lath workers, goldsmiths, boilermakers and other workers who had frequent and habitual exposure to copper seemed to be immune to the infection (Fraser, 1953). An extensive investigation was carried out by a physician called Burq. He reportedly personally visited 400 Parisian establishments in the copper industry, including organizations that employed just a few workers, as well as those than employed hundreds. He was especially struck by his observations at one electrometallurgic plant, where he found that there had been not one single case of cholera among the workers. In addition, he obtained reports from colleagues as far flung as Sweden, Italy and Spain, who reported similar findings. In the 1865 cholera outbreak [1], of the 1,667,000 inhabitants of the city, 6176 fell victim to the disease – an average of around 3.7 per 1000 citizens. However, of the 30,000 individuals who were estimated to be directly employed in the copper industry, 45 died (1.5 per 1000 persons). Burq argued that deducting those who were not exposed to copper dust in the course of their work meant there were just 12 deaths in the industry, an average of 1 in, 3500 (Fraser, 1953). Burq presented the findings of his observations to the Academy of Science and Medicine, concluding that “copper, or its alloys, brass and bronze, applied literally and pregnantly to the skin the cholera epidemic are effective means of prevention which should not be neglected” (cited in Fraser, 1953, p. 63). He also gave some suggestions as to how copper might be used in the fight against infectious diseases suggesting that it be “scraped and sewed on a supply leather thong – or by tincture (dye) in a vest, chemise or flannel waistband”, burned at home in a lamp or even added to wine (ibid). Following Burq’s and other researchers’ observations, the use of copper as an antibacterial agent grew, at least until antibiotics became commercially and widely available in 1932 (Grass et al., 2011). While antibiotics continue to be the primary tool used to fight pathogens in medical settings, their continued use is under threat. The spread of antibiotic resistance is directly responsible for the emergence of antibiotic resistant bacteria that are now ubiquitous in settings as diverse as animal breeding facilities, food processing plants, care homes and hospitals (Luna et al., 2010). Practicing good hygiene is the other key approach to preventing the transmission of infectious diseases. However, as Dr. Jon Otter, an epidemiologist in Infection Prevention Control at Imperial College London explains, conventional cleaning and disinfection techniques are fraught with risk that may inhibit their ability to halt the spread of infection. For example, studies suggest that disinfection activities often reduce, but do not entirely eliminate pathogens from surfaces (Manian et al., 2013). In one study reported by Otter et al. (2014), after patient rooms in one hospital were cleaned with liquid detergents, MRSA was found to remain on 66% of surfaces. In another paper, Manian et al. (2013) report that after four rounds of disinfection with sodium hypochlorite (bleach) A. baumannii and/or MRSA was still cultured from more than one quarter of rooms surveyed. In any case, multiple applications of bleach, given the time burden, the potential of corrosive damage and risk to the health of the cleaning operator, should be avoided. The problems with conventional cleaning and disinfectant techniques are myriad. One problem, of course, is that viruses and bacteria are dynamic and diverse, and common disinfectants may not be effective on them all (Otter et al., 2014). For instance, the liquid detergents that are typically used in hospital settings are ineffective against norovirus and C. difficile spores, and the efficacy of certain products is inhibited by organic matter present on surfaces. Other challenges include the difficulty in measuring the appropriate amount of a detergent to use, and for how long to use it, the possibility of toxicity to staff or damage to equipment or other materials, and human-related issues (such as lack of time to properly clean, poor compliance with organizational hygiene policies, and contamination of cleaning materials) (Otter et al., 2014). All of these observations point to the need for a more efficacious, less harmful method of preventing the spread of bacteria and viruses on surfaces. A promising solution involves the impregnation of copper on surfaces in hygiene-sensitive areas. In fact, the Environment Protection Agency has registered around 300 different copper surfaces as antimicrobial. So, what’s so special about copper?
2.2 Antimicrobial Properties and Mechanisms of Copper
Research shows that copper, copper compounds, copper containing proteins, alloys and solutions have intrinsic properties that have the power to eliminate microbes like Mycobacterium tuberculosis, Clostridium difficile, Acinetobacter species, Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus species (VRE), and norovirus (Weber & Rutala, 2013). A number of mechanisms of action have been proposed. Reactive hydroxyl radicals may be generated which contribute to the oxidation of lipids, proteins and other cellular molecules (Grass et al., 2011). Copper ions also help in the depletion of sulfhydruls, and while bacteria have evolved[2] to protect themselves from their toxic effects, few microorganisms survive sustained copper ion challenge (Weber & Rutala, 2013). Bacteria that form spores (e.g. Clostridium and Bacillus) are often resilient against germicides that work through contact killing because spores are resistant to radiation, heat, dessication and germicides (Weber & Rutala, 2013). In spite of the robustness of these spores, copper has been found to kill C difficile cells within just 30 minutes of contact (Weaver et al., 2008). One study found that that viable C difficile spores were diminished by 99.8% after spending three hours on a solid copper surface, while another study reported complete inactivation of spores after 48 hours (Weaver et al., 2008; Wheeldon et al., 2008) Equally, it is notoriously difficult to prevent transmission of Escherichia coli O157, more commonly known as E. coli when infected food products come into contact with food production surfaces and materials (Noyce et al., 2006). Furthermore, E. coli microbes can survive on stainless steel surfaces for weeks. However, studies have shown that over 99.9% of these microbes are destroyed after they have been in contact with copper alloy surfaces after around two hours (Wilks et al., 2005). In fact, copper has been found to kill certain microorganisms within just a few seconds of contact (e.g. Saccharomyces cerevisiae (a fungal pathogen which is commonly used in beer brewing and bread making). According to Weber & Rutala (2013), contact with copper alloys will kill even the most copper ion-resistant strains (such as P aeruginosa and Salmonella enterica) within 60 minutes of interaction. In addition to these remarkable properties, there are a number of benefits of copper and copper compounds over alternatives. Firstly, copper is resistant to corrosion, and even if it turns green through oxidation, it continues to be antimicrobial (Sorensen, 2012). This means that it is not necessary to clean it to a high shine (one of the reasons why copper has been thought to have been passed over for stainless steel in surface production is that it is believed to be a challenge to clean). In addition, there is little danger of running out of copper – it is one of the most recycled metals in the world, and even after recycling, it does not lose its microbial properties.
3. Industrial Applications of Copper
Clearly, then, copper has tremendous potential. This raises questions about the kinds of products and settings in which copper can – and has – been used. In fact, copper is found in many different organizational settings, especially in healthcare, hospitality and food production.
Healthcare Settings
In the academic literature, multiple pieces of research point to the efficacy of copper and copper -based biocidal formulations in medical settings that demand sanitary environments, including laboratories and hospitals. Given the nature of the activity that goes on in these organizations, touch surfaces that are commonly found therein (e.g. toilet seats, bed rails, touch plates and door handles) are often highly contaminated with microbes. One study showed that some of the more resilient germs, such as Acinetobacter and Staphylococcus aureus can persist for months on these surfaces (Grass et al., 2011), and research has shown that in spite of frequent sanitation, microbes can never be completely eliminated (Otter et al., 2014). Over the past decade or so, in line with the growth in the application of automated technologies in a wide range of settings, a number of automated decontamination technologies have attracted attention from industrial designers and specialists in infection control (Rutala et al., 2013; Schneider, 2013; Otter et al., 2013). Among the various technologies (e.g. fluorescent dyes, UV-C light) under active investigation, self-disinfecting surfaces have shown the greatest promise (Weber et al., 2013). In the early 1990s, Dr. Robert Weinstein identified the various sources of cross contamination of infections in hospitals, concluding that infection via the hands is responsible for 20 to 40% of cross infections, but that some 20% of infections are transferred via environmental surfaces. In the intervening years, researchers have attempted to identify strategies to reduce cross-contamination of high touch surfaces, with self-sanitizing copper surfaces emerging as a the forerunner in the race to prevent infections. Most equipment and surfaces in hospital settings are made of stainless steel because its resistance to corrosion and its clean and sterile appearance (Grass et al., 2011). However, stainless steel offers no antibacterial properties. In contrast, copper surfaces have self-sanitizing properties which could make a vital contribution to infection management and control (Borkow & Gabbay, 2009). As early as 1983, an empirical study found that compared to stainless steel door knobs which were found to be heavily colonized by E. coli growths, brass door knobs (which are made from copper) hardly had any growths on them at all (Kuhn, 1983). More recently, Warnes et al. (2015) found that human coronavirus 229E was still able to infect a human lung cell after remaining for five days on a range of different materials, such as glass, rubber, stainless steel, Teflon and ceramic. However, the coronavirus was inactivated rapidly after contact with copper alloy surfaces. Trials of copper infused surfaces at hospitals in the United Kingdom, Germany and South Africa have all demonstrated the potent antimicrobial effects of copper when incorporated into high touch surfaces like toilet seats, windowsills, desks and door handles (Grass et al., 2011). Could copper be effective in the fight against SARS-COV2, the virus strain that causes novel coronavirus (COVID-19)? At the time of writing, research into the coronavirus is early and ongoing, and it is still difficult to say with any confidence what is effective and what is not. However, one study, conducted by researchers in China, suggested that the virus was rapidly depleted after exposure to copper. The virus persisted up to three says on stainless steel and plastic, but after exposure to copper, the virus was depleted rapidly (it survived 120 minutes on copper nickels, and just 40 minutes on brass (Ren et al., 2020). The results have been replicated elsewhere, and suggest that copper could play an important role in the halt of this highly infectious disease.
Hospitality Settings
Copper food preparation equipment is certainly aesthetically pleasing, but the benefits go beyond visual appeal. According to research, copper cooking materials (e.g. kettles and pans), may offer better protection against foodborne bacteria than the stainless steel alternatives (Noyce et al., 2006). While stainless steel is often preferred in the food production and processing industry because it does not corrode as easily as copper through the application of chemical cleaning materials), and is believed to be easier to clean, in fact, the use of cast copper alloys during food processing may better help prevent cross-contamination of harmful pathogens such as E. coli. Hospitality settings, such as restaurants and hotels, but also food processing plants, run a major risk of spreading E. coli, especially if they produce beef products, because cattle is one of the major reservoirs of the pathogen. Although ensuring that beef products are well cooked and that the materials used to prepare the foods are properly cleaned, cross-contamination of infected beef with food production materials, however well cleaned, makes it especially challenging to prevent the spread of the disease, and the bacteria has been found to remain viable even after rigorous cleaning and sanitation (Noyce et al., 2006). In order to demonstrate the efficacy of copper, Noyce et al. (2006) exposed E. coli to a series of metals containing varying degrees of copper, and to stainless steel. Some samples also contained beef juice. The findings revealed that stainless steel was ineffective at reducing cell numbers, but when stored at 22 degrees Celsius, the three copper alloys not exposed to beef juice completely killed E. coli microbes, and an alloy of 95% copper was able to completely kill the bacterium containing beef juice at the same temperature. These results, as well as others showing the powerful antimicrobial effects of copper cooking materials on Listeria monocytogenes contamination (Wilks et al. 2006) are further evidence that copper alloys have the potential to aid in food safety.
Industrial and Residential Settings
In addition to being used in healthcare and hospitality settings, copper is already being used in a wide range of industrial and residential contexts. Copper is a common material used in the construction and maintenance of buildings and is known as the plumbers’ friend. Copper beds, copper railings and copper door knobs were all prevalent after the Industrial Revolution, and while in modern buildings, these materials are often passed over in favor of their cheaper alternatives (plastic, aluminum and stainless steel), examples of copper use can be found everywhere. Perhaps the most famous example is the prominent central staircase at New York City’s Grand Central Terminal (built in 1913), which has antimicrobial copper handrails. However, there are more modern applications too. Scotch Distilleries on both sides of the Atlantic prefer copper stills over the more durable stainless steel alternatives because they help to strip whisky (or whiskey) of sulphurous odors and compounds (The Whisky Professor, 2016). The use of copper-8-quinolinolate in construction materials such as air filters in ventilations and in fireproofing is a known strategy for controlling the spread of aspergillosis (a fungal infection) (Haiduven, 2009), and copper-silver ionization is used for the control of Legionella in water supplies (Weber & Rutala, 2013). Given that the risk of transmission of infections is highest in communal areas where people gather, it makes sense that the optimal application of copper products would be in public transportation systems such as train stations, subways and buses, and for products that are readily shared, such as gym equipment. One study indeed found that integrating copper alloys into high-touch athletic center surfaces significantly reduced bacterial burden (Ibrahim et al., 2018). Some organizations are already pioneering the application of copper. At Atlanta airport, for example, 50 water bottle filling stations have been retired replaced with copper-made versions. In practice, however, we are still early in the journey of industrial application of copper and copper solutions.
4. The Production Potential of Copper
Given the considerable benefits and applications of copper and copper-based solutions, it is worth asking whether there exist any logistical or practical considerations associated with the use of this chemical element to fight bacteria and disease in industry, healthcare, hospital and other settings. Of particular importance is whether the professionals in these industries have identified concerns about using copper, or whether any resistance might be expected. Examination of the literature seems to suggest that there are few concerns in this regard, and in fact, copper would often be welcomed, and preferred as an alternative to existing solutions. For example, one observational study conducted in a British general hospital gathered data from healthcare professionals on the performance and preferability of ultramicrofiber cleaning materials which were either used with standard cleaning solutions (e.g. chlorine), or with a novel copper-based biocide (Hall et al., 2011). Staff responses indicated that copper treated cleaning materials (e.g. cloths and mops) were preferred to the chlorine-based cleaning supplies that are standard in UK hospitals, and staff also believed that copper biocide has superior cleaning ability. Furthermore, a study examining the impact of copper-based biocides on Methicillin-Resistant Staphylococcus Aureus (MRSA[3]) isolates reached the conclusion that if hospital surfaces were treated with copper-based biocides, this intervention alone could play a key role in stopping the spread of MRSA in healthcare settings. Those authors also emphasized that copper is preferable compared to alternatives on the market due to its anti-corrosive properties (enabling it to be used on the metal surfaces that are common in hospitals). The toxicity of copper solutions also seems to be of limited concern. Overall, while copper sulphate containing solutions are indeed selectively toxic to bacterial cells (and hence, antimicrobial), even up to concentration of 1000ppm, human cells are unaffected, and overall toxicity of copper is low (Gant et al, 2007).
5. Takeaways
- Common techniques used to disinfect spaces that are required to remain clean and pathogen free are not always successful due to a combination of product and process-related factors. This, and the growing resistance of antibiotics, as well as the observation that 20% of the transmission of pathogens occurs through interaction with surfaces, increases the importance of finding new ways to tackle the spread of infectious diseases.
- Copper has inherent antimicrobial properties which can kill even the most resilient fungus spores in as little as a few seconds
- In addition, the antibacterial properties survive over time, even if copper is recycled, and this material is in plentiful supply
- Application of copper in high traffic, high touch areas has potential in halting the transmission of infectious diseases
- There are few concerns among professionals about the usefulness and efficacy of copper -based solutions and treatments. Overall, toxicity is low and the anti-corrosive properties of copper make it especially suitable for use in settings where there are many metal surfaces which require continuous disinfecting, such as restaurant kitchens and hospitals.
- While copper certainly has antibacterial and disease fighting properties appropriate actions should be taken to ensure full efficacy. For example, most of the research assessing the value of copper in healthcare settings pointed out that long contact times are necessary to realize its benefits. This has implications for industrial application, as products that are designed to have only minimal contact with surfaces (e.g. single use wipes), may be unsuitable.
References Borkow, G., & Gabbay, J. (2009). Copper, an ancient remedy returning to fight microbial, fungal and viral infections. Current Chemical Biology, 3(3), 272-278. Fraser, T. (1953). Information Circular 7660. US Department of the Interior, Bureau of Mines. Gant, V. A., Wren, M. W., Rollins, M. S., Jeanes, A., Hickok, S. S., & Hall, T. J. (2007). Three novel highly charged copper-based biocides: safety and efficacy against healthcare-associated organisms. Journal of Antimicrobial Chemotherapy, 60(2), 294-299. Grass, G., Rensing, C., & Solioz, M. (2011). Metallic copper as an antimicrobial surface. Appl. Environmental. Microbiology., 77(5), 1541-1547. Haiduven, D. (2009). Nosocomial aspergillosis and building construction. Medical Mycology, 47(Supplement_1), S210-S216. Hall, T. J., Jeanes, A., McKain, L. W., Jepson, M. J., Coen, P. G., Hickok, S. S., & Gant, V. A. (2011). A UK district general hospital cleaning study: a comparison of the performance of ultramicrofibre technology with or without addition of a novel copper-based biocide with standard hypochlorite-based cleaning. Journal of Infection Prevention, 12(6), 232-237. Ibrahim, Z., Petrusan, A. J., Hooke, P., & Hinsa-Leasure, S. M. (2018). Reduction of bacterial burden by copper alloys on high-touch athletic center surfaces. American journal of infection control, 46(2), 197-201. Kuhn, P. J. (1983). Doorknobs: a source of nosocomial infection. Diagnostic Medicine, 6(8), 62-63. Luna, V. A., Hall, T. J., King, D. S., & Cannons, A. C. (2010). Susceptibility of 169 USA300 methicillin-resistant Staphylococcus aureus isolates to two copper-based biocides, CuAL42 and CuWB50. Journal of antimicrobial chemotherapy, 65(5), 939-941. Manian, F. A., Griesnauer, S., & Senkel, D. (2013). Impact of terminal cleaning and disinfection on isolation of Acinetobacter baumannii complex from inanimate surfaces of hospital rooms by quantitative and qualitative methods. American journal of infection control, 41(4), 384-385. Martínez‐Bussenius, C., Navarro, C. A., & Jerez, C. A. (2017). Microbial copper resistance: importance in biohydrometallurgy. Microbial Biotechnology, 10(2), 279-295. Noyce, J. O., Michels, H., & Keevil, C. W. (2006). Use of copper cast alloys to control Escherichia coli O157 cross-contamination during food processing. Applied. Environmental. Microbiology., 72(6), 4239-4244. Noyce, J. O., Michels, H., & Keevil, C. W. (2007). Inactivation of influenza A virus on copper versus stainless steel surfaces. Applied Environmental Microbiology., 73(8), 2748-2750. Otter, J. A., Yezli, S., Perl, T. M., Barbut, F., & French, G. L. (2014). A guide to no-touch automated room disinfection (NTD) systems. In Decontamination in hospitals and healthcare (pp. 413-460). Woodhead Publishing. Ren, S. Y., Wang, W. B., Hao, Y. G., Zhang, H. R., Wang, Z. C., Chen, Y. L., & Gao, R. D. (2020). Stability and infectivity of coronaviruses in inanimate environments. World Journal of Clinical Cases, 8(8), 1391. Rutala, W. A., & Weber, D. J. (2013). Disinfectants used for environmental disinfection and new room decontamination technology. American Journal of Infection Control, 41(5), S36-S41. Schneider, P. M. (2013). New technologies and trends in sterilization and disinfection. American Journal of Infection Control, 41(5), S81-S86. Sorenson, J. R. (2012). Inflammatory Diseases and Copper: The Metabolic and Therapeutic Roles of Copper and Other Essential Metalloelements in Humans (Vol. 2). Springer Science & Business Media. Suman, R., Javaid, M., Haleem, A., Vaishya, R., Bahl, S., & Nandan, D. (2020). Sustainability of Coronavirus on different surfaces. Journal of Clinical and Experimental Hepatology. The Whisky Professor (2016). Why are whisky stills made from copper? Retrieved from https://scotchwhisky.com/magazine/ask-the-professor/9685/why-are-whisky-stills-made-from-copper/ Warnes, S. L., Little, Z. R., & Keevil, C. W. (2015). Human coronavirus 229E remains infectious on common touch surface materials. MBio, 6(6), e01697-15. Weaver, L., Michels, H. T., & Keevil, C. W. (2008). Survival of Clostridium difficile on copper and steel: futuristic options for hospital hygiene. Journal of Hospital Infection, 68(2), 145-151. Wheeldon, L. J., Worthington, T., Lambert, P. A., Hilton, A. C., Lowden, C. J., & Elliott, T. S. J. (2008). Antimicrobial efficacy of copper surfaces against spores and vegetative cells of Clostridium difficile: the germination theory. Journal of Antimicrobial Chemotherapy, 62(3), 522-525. Wilks, S. A., Michels, H., & Keevil, C. W. (2005). The survival of Escherichia coli O157 on a range of metal surfaces. International Journal of Food Microbiology, 105(3), 445-454. Wilks, S. A., Michels, H. T., & Keevil, C. W. (2006). Survival of Listeria monocytogenes Scott A on metal surfaces: implications for cross-contamination. International Journal of Food Microbiology, 111(2), 93-98. Weber, D. J., & Rutala, W. A. (2013). Self-disinfecting surfaces. Infection Control & Hospital Epidemiology, 33(1), 10-13. [1] There were also outbreaks in 1832, 1849 and 1852. [2] According to Weber & Rutala (2013), the protective mechanisms that have evolved to protect microorganisms from copper ion challenge include intra- and extracellular sequestration, permeability barriers, enzymatic detoxification, efflux pumps, and reduction in the sensitivity of cellular targets to copper ions. [3] MRSA is a particularly virulent type of bacteria that is resistant to conventional antibiotics and responsible for a number of difficult-to-treat infections in humans. MRSA outbreaks are relatively common in hospital settings, and thus infection control professionals are actively seeking antibacterial and disinfectant solutions that demonstrate high efficacy against MRSA.
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