Letters in Applied Microbiology ISSN 0266-8254

UNDER THE MICROSCOPE

The benefits of silver in hygiene, personal care and

healthcare
V. Edwards-Jones
Manchester Metropolitan University, Manchester, UK

Keywords Abstract
healthcare, hygiene, nanoparticles, silver.
Silver has been used for centuries as an antimicrobial agent to reduce biobur-
Correspondence den and prevent infection. Its usage diminished when antibiotics were intro-
Valerie Edwards-Jones, Professor of Medical duced but remained one of the most popular agents for wound infections,
Microbiology, Acting Director of Research, especially in burned patients. Incorporation of silver into a range of hygiene
Enterprise and Development, Manchester
and healthcare applications has increased, and this has raised concerns over
Metropolitan University, Manchester, UK.
E-mail: [email protected]
the development of silver resistance, toxicity, methods of testing products and
evidence of efficacy. The published evidence for resistance and toxicity is lim-
2009 ⁄ 0414: received 4 March 2009, revised ited and associated with frequent and high levels of silver used. Increasing evi-
11 April 2009 and accepted 12 April 2009 dence of improved antimicrobial activity of nanoparticles of silver and
possible dual immunomodulatory effects are exciting. This may lead to further
doi:10.1111/j.1472-765X.2009.02648.x product development as potential alternative preservatives as some currently
available preservatives have an increasing incidence of allergic reactions.
Acknowledging the role of the carrier is important, and as silver is active when
in solution, opens a window of opportunity in personal hygiene area. This is
important in an age when multiple antibiotic–resistant bacteria are becoming
prevalent.

Introduction Historical use of silver

The use of silver (Ag) as a broad-spectrum antimicrobial The first report of lunar caustic or lapis infernalis (silver
agent is well documented in the literature. A systematic nitrate) dates back to the middle ages. The Surgeon’s Mate
search conducted on Medline using the key words antimi- by John Woodhall (1613) describes silver as an essential
crobial-silver, hygiene healthcare retrieved a study by Will- multipurpose medicinal product (Klasen 2000). In the
cockson and Cox (1953). This reported the comparison early 17th century, Angelus Sola used systemic silver
of the antimicrobial effect of silver nitrate against terra- nitrate to treat epilepsy and cholera. Argyria (blue skin
mycin and terramycin–polymyxin-B. Since then, there discolouration because of deposits of silver sulfide) was
have been over 1000 referred journal articles, with later described by Gettler et al. (1927).
increasing numbers focusing on applications in hygiene, In the 19th century, 0Æ5% AgNO3 was used for the
personal care and healthcare. These range from silver treatment of Ophthalmia neonatorum, by the German
coatings on hard surfaces (e.g. computer keyboards) to obstetrician Carl Crede, and for the prevention of infec-
colloidal silver used at 30 parts per million (ppm) as a tion in burns by the Austrian surgeon Johann Nepomuk
spray for prevention and treatment of sore throats. The Rust. Further detailed sequential history on the use of Ag
natural antimicrobial properties of silver, very limited is reported in two excellent reviews (Klasen 2000; White
examples of resistance and sensitization emerging prob- 2001).
lems of prevention and treatment of multiple antibiotic– AgNO3 soaks became routinely used for in burned
resistant bacterial strains such as MRSA have encouraged patients (Moyer 1965; Moyer et al. 1965) and are still in
its use. use today by some plastic surgeons prior to grafting. Fox

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Journal compilation ª 2009 The Society for Applied Microbiology, Letters in Applied Microbiology 49 (2009) 147–152 147
Silver in hygiene, personal care and health V. Edwards-Jones

(1968) introduced 1% silver sulfadiazine (AgSD) to 2. Inorganic complexes – e.g. AgSD, AgNO3 and silver
prevent burn wound infection. AgSD is less soluble than chloride, each with varying solubility.
AgNO3 and releases Ag+ into the wound bed over a longer 3. Organic complexes – colloidal silvers, silver proteins
period. Ag+ ions complex with chloride ions present in (Lansdown and Williams 2004).
the wound bed, inactivating the antimicrobial Ag+ and Different chemical forms of silver are used in a range
blackening the wound by precipitation of AgCl. In addi- of products and solubility; ultimately releasing Ag+ deter-
tion, the frequent additions of the topical cream result in mines the longevity of activity. Nanocrystals or Ag+ nano-
the formation of a pseudoeschar, which can create prob- particles are produced by the chemical reduction of silver.
lems with assessment of the wound bed. Despite these The physical, biochemical and antimicrobial properties of
minor problems, 1% AgSD cream remains a popular treat- different size and shapes of Ag+ nanoparticles have been
ment in a large number of burn units worldwide. extensively investigated and in solution, portray different
optical, magnetic and catalytic properties. Ag+ nanoparti-
cles are produced in different sizes in a controlled manner
Mode of action of silver
using laser ablation of pure Ag (Zhao et al. 2006).
Silver can be found in four oxidative states and produce Improved antibacterial activity is dependent on both the
ions: Ag0, Ag+, Ag++ and Ag+++. size and the shape of the nanoparticles, with triangular
The two latter states produce complexes that are insolu- nanoparticles displaying more activity than rod-shaped or
ble or less antimicrobial than the former. The antimicrobial spherical nanoparticles (Pal et al. 2007). These have been
action of silver is dependent upon the bioavailability of the applied to a number of surfaces or suspended in various
silver ion (Ag+). Silver compounds ionize in the presence carriers for a variety of applications in both hygiene and
of water, bodily fluids and other exudates. It has a broad healthcare.
spectrum of activity interacting with the cell membrane
resulting in uncoupling of the respiratory electron
Immunomodulatory action of silver
transport system from oxidative phosphorylation, also
interfering with membrane permeability and the proton Wright et al. (2002) described how nanocrystalline
motive force (Schreurs and Rosenberg 1982; Dibrov et al. Ag+-inhibited matrix metalloproteases known to prevent
2002), inhibiting respiratory chain enzymes (Chappell and wound healing and postulated that Ag+ may promote
Greville 1954; Semeykina and Skulachev 1990), inhibiting wound healing. Ag+ was also shown to bind metallothi-
intracellular enzymes reacting with electron donor groups, oneins that contribute to tissue repair (Lansdown 2006)
especially sulphydral groups and interchelation with DNA and appeared to modulate the immune system in a benefi-
(Rosenkranz and Rosenkranz 1972; Modak and Fox 1973; cial way. In animal studies, a topical antimicrobial cream
Teng et al. 2000). containing 1% (w ⁄ w) nanocrystalline silver suppressed
Biologically active Ag+ is released from a number of two proinflammatory cytokines, IL 12 and TNF a, known
silver salts and is dependent upon solubility (Richards et al. to be involved in allergic skin diseases such as contact
1991). 45% of Ag+ rapidly binds to protein resulting in dermatitis (Bhol et al. 2004; Bhol and Schechter 2005).
partial inactivation (Dollery 1991). Also, Ag+ complexes Dermatological conditions, such as toxic epidermal
with free chloride, phosphate and sulfate ions all frequently necrolysis and Steven Johnson syndrome, have shown
found in tissues. Therefore, to sustain antimicrobial improvement when treated with a topical nanocrystalline
activity, Ag+ should be released slowly and continuously. Ag+ dressing compared to traditional Vaseline gauze, and
Ag+ inhibits bacterial growth between 8 and 80 ppm, continue to support increasing evidence of a beneficial
with Gram-negative bacteria having lower MICs than immunomodulatory effect (Asz et al. 2006; Dalli et al.
Gram-positive bacteria (Hamilton-Miller et al. 1993). A 2007). In studies using a pig model, inflammation was
standard antimicrobial susceptibility testing method for induced with dinitrochlorobenzene, and wounds treated
Ag+ has not yet been agreed although is essential as the daily with nanocrystalline Ag+ dressings, 0Æ5% AgNO3 or
use of silver increases in a wide range of applications saline. Erythema, oedema and histological data showed
(Chopra 2007). that nanocrystalline Ag+-treated pigs had near normal skin
after 72 h, whilst the other treatment groups remained
inflamed. This was associated with increased inflammatory
Different forms of silver – the silver nanoparticle
cell apoptosis, a decreased expression of proinflammatory
There are three general groupings of silver products avail- cytokines, and decreased gelatinase activity (Nadworthy
able. These are et al. 2008). Other animal studies have shown that 1%
1. Elemental or metallic silver in a natural crystalline nanocrystalline Ag+ incorporated into catheters and placed
state or as nanoparticles. intravesically into female rat bladders significantly

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148 Journal compilation ª 2009 The Society for Applied Microbiology, Letters in Applied Microbiology 49 (2009) 147–152
V. Edwards-Jones Silver in hygiene, personal care and health

decreased bladder inflammation and mast cell activation There are reported products containing Ag+ nanoparti-
for up to 4 days poststimulation (Boucher et al. 2008). cles-embedded antimicrobial paints based on vegetable
oil, Ag+-doped bioactive glass-coated sutures for tissue
engineering, stainless steel surfaces coated with Ag+ and
Personal care
zinc-containing zeolites and Ag+ incorporated into
Healthy human skin is colonized by nonpathogenic bacteria dental resins. Silver is used in water purification for the
including coagulase negative Staphylococci, Diphtheroids prevention of water-associated infection and formation of
and Propionibacteria (Elsner 2006). The distribution biofilms, replacing traditional chemicals such as chlorine
and density of normal flora is dependent on age, sebum and bromine. In a major response to hospital-associated
secretion, occlusion, temperature and humidity. Odour Legionnaires’ disease, many water filters and other mech-
production in the axilla is attributed to Corynebacterium sp. anisms within their water purification systems now incor-
and S. epidermidis decomposing natural secretions contain- porate silver into the surfaces of the device. There are a
ing short chain fatty acids, sulfur compounds and steroids number of nonclinical hygienic uses of nanosilver for
and producing malodorous volatile compounds, for exam- example in linings of washing machines, dishwashers,
ple isovaleric acid (Taylor et al. 2003). Foot and scalp refrigerators and toilet seats. Samsung Electronics use
malodor are often attributed to similar compounds nanosilver widely on their computer keyboards. Research
(Katsutoshi et al. 2006). Antimicrobials are incorporated has seen incorporation of silver into fabrics to reduce the
into a range of deodorants to help reduce the density of risk of healthcare-associated infections. Trials at Queen’s
skin flora, but they do not completely eliminate it. In Medical Centre, Nottingham University Hospitals, have
addition, some antimicrobials cause irritation and allergic indicated a reduction in environmental contamination
contact dermatitis (Elsner 2006). Conventional underarm with MRSA compared to cotton curtains, and further
deodorants suppress the process of odour production by studies are being undertaken to determine their full
reduction in number of bacteria, suppression of perspira- potential.
tion, deodorization and masking odour. Research under-
taken as early as 1996 saw the potential for the use of silver
Healthcare applications
as a preservative and antimicrobial in personal care
products. A silver chloride titanium dioxide composite The use of silver as an antimicrobial agent in medical
allowed a controlled release of silver and inhibited skin flora devices has expanded rapidly and alongside an increased
associated with odour at low concentrations (50 ppm) cost. A meta-analysis reported in 2007 on the use of silver
without associated toxicity or hypersensitivity (Corbett dressings in leg ulcers approximated that over £23m was
1996). Incorporation of Ag+ nanoparticles into personal spent on the use of silver dressings in wound care by the
care products has been described and offers an exciting new NHS in the United Kingdom in 2006 compared to £858k
application. A dose–response study of Ag+-zeolite powder in the same period in 2004 (Chambers et al. 2007).
spray (0–40% w ⁄ w) in 39 volunteers demonstrated at 10% However, if benefits of the use of silver dressings can be
(w ⁄ w), which showed an antimicrobial effect against demonstrated and justified, then it should be used. For
skin-resident bacteria. A further study, comparing Ag+- example, a systematic audit on a burns unit in Australia,
zeolite powder spray at 10% (w ⁄ w) with triclosan 0Æ2% reported by Fong et al. (2005), showed that the use of a
(w ⁄ w), showed that one application of Ag+-zeolite inhib- nanocrystalline Ag+ dressing (Acticoat; Smith & Nephew
ited bacterial growth for 24 h and was more effective than Ltd, Hull, UK) reduced the cost by decreasing dressing
triclosan (Nakane et al. 2006). changes, nursing time and the use of antibiotics com-
Ag+ nanoparticles have been incorporated into foot pared to conventional treatment with AgSD ⁄ chlorhexidine
powders, sprays, soaps, socks, shoe insoles and a wide cream (Silvazine; Smith & Nephew Ltd, Melbourne,
range of fabrics used for pyjamas, briefs, undergarments Australia). Nanocrystalline Ag+ is used to prevent infec-
and pillows. The role of the carrier is very important, and tion in large, total body surface area burns, as the sequa-
incorporation into fabrics will only show effect when lae of infection and the costs associated with the dressings
there is moisture, as Ag+ is only active in solution. are outweighed by the successes achieved. The use of sil-
ver alloy-coated Foley catheters for the prevention of
urinary tract infection in patients with short-term cathe-
Hygiene and prevention of infection in solid
terization has been reviewed by the Health Protection
surfaces
Agency rapid review panel, and awarded a level 1 recom-
Applications of Ag+ incorporated into solid surfaces have mendation. As urinary tract infections cost £124 million
increased following the concern over healthcare-associated per year, with each UTI costing on average £1327, these
infection caused by multiple antibiotic–resistant bacteria. catheters could potentially save a 600-bedded hospital

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Journal compilation ª 2009 The Society for Applied Microbiology, Letters in Applied Microbiology 49 (2009) 147–152 149
Silver in hygiene, personal care and health V. Edwards-Jones

£180K per annum, even though they are initially more

Discussion
expensive than the nonsilver catheters (Seymour 2006).
There are other medical devices being used in healthcare Exciting developments in personal care, hygiene and
including endotracheal tubes. healthcare offer major opportunities for development of a
range of applications arising from the latest research into
the antimicrobial properties of silver. The limited resis-
Toxicity
tance, sensitization and toxicity considering the frequency
Reported cases of silver toxicity are limited, and of use have offered a new solution to problems of reducing
after 50 years of intensive use in burns, silver toxicity is bioburden across a range of industries. Silver also offers
insignificant compared to the benefits of use and in a broad-spectrum antimicrobial agent with the added
comparison with other antimicrobials. A number of benefits of slow and sustained release in the form of
documented cases of systemic silver toxicity with argyria nanocrystalline or nanoparticles of silver.
were reported in the early 1960s when uncontrolled levels Silver affects multiple targets sites within the bacterial
of silver from AgNO3 were used. There have only been cell, so the development of resistance through mutation is
occasional reports of silver toxicity in recent years usually unlikely; however, the chance of acquiring silver resistance
associated with ingested silver. Arygria is the commonest may still occur. There are sporadic reports of plasmid-
manifestation of toxicity (Payne et al. 1992; Tomi et al. mediated silver resistance in Gram-negative bacteria from
2004), but it can also be seen as silver deposition in the the healthcare environment (Percival et al., 2005), and
liver and kidneys (Lansdown 2006). Sensitization to silver intrinsically resistant strains originating from areas near
is rarely described and at a lower incidence compared to silver mines have also been isolated. Silver resistance
other topical antimicrobials used in personal care and encoded by the sil gene is mediated through an efflux
wound dressings. The safety of silver in wound care has mechanism or reduced membrane permeability (Silver
been raised, and most manufacturers state the levels in et al. 2006) and can be determined by molecular detec-
ppm of silver released over time. These are discussed by tion of the sil gene. Standardized antimicrobial testing
Lansdown and Williams (2004). Toxicity is dependent methods need to be developed to monitor the patterns of
upon levels absorbed into the body over time, and levels silver susceptibility over time, to ensure whether any
absorbed across intact skin are less than those across open demonstrable change is recognized quickly and allow for
wounds. In a study in 1991, silver levels were determined intervention. In one study undertaken in 2003, more than
in serum, urine and tissues of 22 patients treated with 10% of enteric isolates had sil genes detected (Silver
AgSD. Serum concentration peaked at 6 h, and urine lev- 2003).
els were between 100 ⁄ 400 times higher (Coombs et al. Silver is used extensively in wound care, and the num-
1992). In healthy volunteers across intact skin, silver levels ber of dressings available with different chemical forms of
were barely above normal (Wan et al. 1991). In 2007, a silver and different physical properties creates confusion
systematic prospective study of 30 patients with burns for the nursing staff using them. Additionally, dressings
treated with nanocrystalline Ag+ dressings showed that and medical devices are purchased from procurement
the maximum serum level was 230 lg ml)1 with a med- hubs, and cost may play a more important role in the use
ian of 56Æ8 lg ml)1. This usually correlated to the size of rather than efficacy. More evidence through robust clini-
the burn and subsequent exposure to silver. Within cal trials, full cost-benefit analysis of pre- and postusage,
6 months post-treatment, serum silver levels return to quality of life, comfort for the patient, frequency of dress-
normal, demonstrating no long-term effects (Vlachon ing changes and days to healing needs to be reported to
et al. 2007). inform through evidence appropriate use.
In the environment, silver is usually associated with The anti-inflammatory effect of nanocrystalline silver,
sulfide minerals and released into soil and surface water especially in dermatological conditions and wounds, offers
through weathering. However, in areas where silver levels exciting new applications. Nanocrystalline silver has been
are high, toxicity to fish and marine life has been noted. used with great success in Australia for the prevention of
Uncontrolled release of silver into the water supply infection in large burns (especially in paediatric patients).
from wastewater treatment plants and accumulation in Infected burns can produce poor scars and a poor cosmetic
waste products may have a secondary effect on animals effect.
and plants that may have long-term effects e.g. affecting Silver does have other additional benefits. Nevertheless,
the food chain, so this needs close monitoring (Pelkonen William Conrad Roentgen in 1895 used activated silver
et al. 2003). However, it would be expected that these halide crystals and revolutionized medical diagnosis
effects would have become apparent by now, as silver has through X-rays. Silver halide crystals are also incorporated
been used for centuries. into lenses to produce UV-reactive sunglasses.

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150 Journal compilation ª 2009 The Society for Applied Microbiology, Letters in Applied Microbiology 49 (2009) 147–152
V. Edwards-Jones Silver in hygiene, personal care and health

Conclusions Elsner, P. (2006) Antimicrobials and the skin physiological and

pathological flora. Curr Probl Dermatol 33, 35–41.
Silver has already proved itself as a powerful inorganic Fong, J., Wood, F. and Fowler, B. (2005) A silver coated
compound, and can if used correctly, prevent infection. As dressing reduces the incidence of early burn wound
a broad-spectrum agent, it kills a wide range of micro- cellulitis and associated costs of inpatient treatment:
organisms in low levels without associated toxicity. comparative patient care audits. Burns 31, 562–567.
Currently, the usage has increased dramatically in the Fox, C.L. (1968) Silver sulfadiazine-a new topical therapy for
developed world across a huge range of applications, but Pseudomonas in burns. Arch Surg 96, 184–188.
the impact has not reached the areas of developing world, Gettler, A.O., Rhaods, C.P. and Weiss, S. (1927) A contribu-
where the greatest impact could be seen through incorpora- tion to the pathology of generalized argyria with a discus-
tion into applications associated with the production of sion on the fate of silver in the human body. Am J Pathol
uncontaminated food and water. 3, 631–651.
Hamilton-Miller, J.M., Shah, S. and Smith, C. (1993) Silver
sulphadiazine; a comprehensive in vitro reassessment.
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