Download Controlling wound bioburden with a novel silver‐containing

Controlling wound bioburden with a novel silvercontaining Hydrofiber dressing
SAMANTHA A. JONES, BSc; PHILIP G. BOWLER, MPhil; MICHAEL WALKER, PhD; DAVID PARSONS, PhD
Clinicians now recognize that both aerobic and anaerobic microorganisms have the ability to degrade or
damage host tissue at a wound site through the production of a variety of enzymes and toxins. Silver-containing
dressings offer one method for controlling this polymicrobial wound bioburden, and research efforts are currently
ongoing to determine their efficacy against aerobic, anaerobic, and antibiotic-resistant microorganisms. The
current study aimed to determine the antimicrobial activity of a new silver-containing Hydrofiber dressing
(AQUACEL Ag) on both aerobic and anaerobic microorganisms, using the zone-of-inhibition method. This
method provides a measure of the ability of the dressing to make available a sufficient concentration of silver
to have an antimicrobial effect. To some extent this test mimics the clinical use of the dressing and predicts its
microbicidal activity at the wound–dressing interface. The results show that the silver-containing dressing makes
silver available at a dressing–agar interface at a concentration that is effective against a broad range of aerobic,
anaerobic, and antibiotic-resistant microorganisms. In the context of wound healing, the results showing antimicrobial activity against antibiotic-resistant microorganisms are particularly important, as the control and eradication of these organisms is a major concern within the health care profession. (WOUND REP REG 2004;12:288–294)
The moist, warm, and nutritious environment provided
by wounds is conducive to microbial growth. While an
efficient host immune system is usually able to contain
the growth of these microorganisms, in many wounds
(e.g., traumatic, thermal, or chronic wounds) diminished
immune functioning secondary to inadequate wound
perfusion may allow build-up of physical factors such
as devitalized, ischemic, hypoxic, or necrotic tissue and
foreign material, all of which provide an ideal environment for bacterial growth.1–4
How best to treat indolent noninfected and clinically infected wounds is an area of considerable
debate.2 Systemic broad-spectrum antibiotics may be
warranted when clinical signs of systemic infection
exist (where the wound bioburden may have penetrated into deeper tissues). On the other hand, where
From ConvaTec GDC, First Avenue, Deeside Industrial
Park, Deeside, Flintshire, United Kingdom.
Manuscript received: June 25, 2003
Accepted in final form: December 23, 2003
Reprint requests: Samantha Jones, ConvaTec GDC,
First Avenue, Deeside Industrial Park, Deeside,
Flintshire, CH5 2NU, United Kingdom. Email:
[email protected].
Copyright # 2004 by the Wound Healing Society.
ISSN: 1067-1927 $15.00 + 0
288
MRD
MRSA
SHD
TSA
VRE
Maximal recovery diluent
Methicillin-resistant Staphylococcus aureus
Silver-containing Hydrofiber
Tryptone soy agar
Vancomycin-resistant enterococci
the wound bioburden is principally located in the
superficial zone, or when wounds fail to heal but do
not exhibit clinical signs of infection (such as heavily
colonized wounds), topical antimicrobial agents can be
used as an initial treatment tactic.2,5
Therefore, with the emergence and escalation of
bacteria resistant to multiple antibiotics6,7 and the
continuing emphasis on health care costs, previously
out-of-favor topically delivered antiseptic agents are
being increasingly used to control wound bioburden
in the superficial zone, and to prevent infection reaching deeper tissue. These include iodine-releasing agents
(e.g., povidone iodine)8 and silver-releasing agents.
The resurgence in the use of silver-based antiseptics may be linked to their broad-spectrum activity and
far lower propensity to induce bacterial resistance than
antibiotics3,9,10 combined with the availability of new,
advanced dressings impregnated with this antiseptic
agent.11
WOUND REPAIR AND REGENERATION
VOL. 12, NO. 3
Each of the currently available silver-containing
dressings utilizes a different underlying technology to
deliver the silver. However, not all silver dressings provide the benefits of moist wound healing.12,13 Because of
these technological differences, not all of these dressings
are able to respond to the increased levels of wound
exudate associated with increased microbial load in
infected wounds (for example, gauze-type dressings).
Thus, there is still a need for an antimicrobial dressing
that is able to function under all wound conditions,
including highly exuding wounds, because increased
levels of wound exudate are associated with bacterial
infection.14
The ideal antimicrobial dressing would have a
number of key attributes, including provision of a moist
but not saturated environment to enhance healing,13
and broad-spectrum antimicrobial activity (including
activity against antibiotic-resistant bacteria, such as
methicillin-resistant Staphylococcus aureus [MRSA]
and vancomycin-resistant enterococci [VRE]), with low
potential for resistance. The dressing should effectively
deliver antimicrobial activity in a controlled manner to
devitalized tissue that otherwise provides an environment for uninhibited growth; and should be nontoxic
(by ensuring controlled availability of silver), rapid
acting, nonirritant or nonsensitizing, nonadherent,
and effective even in the presence of heavy wound
exudate.
JONES ET AL.
289
A new silver-containing Hydrofiber dressing
(SHD; AQUACEL Ag, ConvaTec, Deeside, UK) was
developed to fulfill these criteria by adding the broadspectrum antimicrobial activity of ionic silver (made
available in a controlled and sustained manner) to the
proven exudate-handling technology of Hydrofiber
(AQUACEL dressing).15,16
We report here the results of a study to investigate
the antimicrobial activity of this new silver-containing
dressing. Specifically, this study used an in vitro standardized agar assay to determine the spectrum and
speed of aerobic and anaerobic antimicrobial activity
of the SHD.
MATERIALS AND METHODS
A variety of aerobic and anaerobic bacteria (including
antibiotic-resistant strains) and yeasts that are often
associated with wound colonization and infection were
included in the study (Table 1). The microorganisms
used were either clinical isolates or standard reference
strains. Test dressings included SHD and a control
dressing that did not contain silver (N-A Gauze, Johnson
& Johnson Wound Management, Somerville, NJ).
Spectrum and speed of antimicrobial activity
Cultures of each challenge organism were separately
prepared on appropriate agar plates. Aerobic bacteria
Table 1. Aerobic and anaerobic isolates included in the study
Aerobic bacteria
Staphylococcus aureus (NCTC 8532)
Staphylococcus aureus (clinical isolate)
Pseudomonas aeruginosa (clinical isolate, · 2 strains)
Enterobacter cloacae (clinical isolate)
Streptococcus pyogenes (clinical isolate)
Klebsiella pneumoniae (clinical isolate, · 3 strains)
Enterococcus faecalis (clinical isolate)
Escherichia coli (NCIMB 8545)
Escherichia coli (NCIMB 10544)
Acinetobacter baumannii (NCIMB 9214)
Yeasts
Candida albicans (NCPF 3179)
Candida albicans (NCPF 3265)
Candida krusei (NCPF 3876)
Antibiotic-resistant bacteria
MRSA (NCTC 10442)
MRSA (NCTC 12232)
MRSA (clinical isolate, · 8 strains)
VRE (NCTC 12201)
VRE (clinical isolate, · 2 strains)
Serratia marcescens (clinical isolate)
Pseudomonas aeruginosa (NCTC 8506)
Anaerobic bacteria
Bacteroides fragilis (clinical isolate)
Bacteroides fragilis (NCTC 9343)
Peptostreptococcus anaerobius (clinical isolate)
Clostridium ramosum (clinical isolate)
Clostridium clostridioforme (clinical isolate)
Clostridium cadaveris (clinical isolate)
Clostridium perfringens (clinical isolate)
Tissierella praeacuta (clinical isolate)
NCIMB ¼ The National Collection of Industrial, Food and Marine Bacteria.
NCPF ¼ The National Collection of Pathogenic Fungi.
NCTC ¼ The National Collection of Type Cultures.
290
WOUND REPAIR AND REGENERATION
MAY–JUNE 2004
JONES ET AL.
and yeasts were cultured on Tryptone Soy Agar
(TSA; Laboratory M, Bury, UK), with the exception
of Streptococcus pyogenes which was cultured on
TSA containing 5 percent defibrinated horse blood,
and anaerobic bacteria were cultured on Fastidious
Anaerobe Agar (Laboratory M) containing 5 percent
defibrinated horse blood.
Suspensions of each challenge organism were subsequently prepared in Maximal Recovery Diluent (MRD;
Laboratory M) at a concentration of approximately
1 · 105 colony forming units/ml. A sterile swab was used
to surface inoculate each organism onto an appropriate
agar plate. Duplicate agar plates were prepared for each
challenge organism. Aerobic bacteria and yeasts were
cultured on TSA (with the exception of Streptococcus
pyogenes, as noted above), and anaerobic bacteria were
cultured on Wilkins Chalgren Agar (Oxoid, Basingstoke,
UK). All inoculated agar plates were incubated for 4 hours
in an appropriate atmosphere at 35 ºC ( 3 ºC) for aerobic
and anaerobic bacteria and at 20–25 ºC for yeasts.
After this period of incubation, each surfaceinoculated plate was divided into two sections. A sample
of the SHD (2.5 cm · 2.5 cm) was aseptically transferred
to each half of the plate and pressed down to ensure
intimate contact with the agar. Dressing samples were
approximately 2.5 cm apart. A negative control plate
(N-A Gauze) for each challenge organism was also
included. Each SHD sample was hydrated with MRD
to simulate wound conditions. Control samples (N-A
Gauze) were not hydrated because given the size and
limited absorption capacity of the gauze, any excess
fluid added (in addition to moisture absorbed from
the agar plates) would saturate the gauze to a point
where the fluid leached beyond the edges onto the
inoculated agar plate. All test plates were performed
in duplicate, with a further control plate containing no
dressing to determine organism viability. All agar plates
were re-incubated under appropriate conditions and
after a 30-minute incubation, one dressing sample
(SHD and N-A Gauze) was removed from each test
plate. This section of the plate was used to observe
the antimicrobial activity (speed of kill) of both the
test and control samples following a 30-minute exposure to the challenge organism. All plates (now containing only one dressing sample) were then re-incubated
under appropriate conditions for a further 24 hours.
After this period of incubation, all plates were observed
to determine the antimicrobial activity of the dressings
over a 30-minute period, and the corrected zones of
inhibition measured using the dressing samples that
remained on the agar plates. A corrected zone of inhibition test allows for any inherent variability in the shape
and size of zones created by the SHD, which changes
in dimension on the agar plate following hydration.
Zones of inhibition were measured horizontally and
vertically (inclusive of the dressing sample) and a
mean value was calculated from the duplicate set of
results. Similarly, a mean dressing size was calculated.
The mean dressing size was then subtracted from the
mean zone of inhibition to determine the corrected zone
of inhibition.17
Depth of penetration assay
VRE (clinical isolate), MRSA (clinical isolate), Pseudomonas aeruginosa (NCTC 8506, multiresistant strain),
and Serratia marcescens (clinical isolate, also a multiresistant strain) were cultured on TSA and Candida
krusei (NCPF 3876) was cultured on Sabouraud Dextrose Agar. Clostridium perfringens (clinical isolate)
and Bacteroides fragilis (NCTC 9343) were cultured
anaerobically on Wilkins Chalgren Agar (Oxoid).
Suspensions of each challenge organism were
separately prepared in MRD (or fluid thioglycollate
medium for anaerobes) and a 1 ml volume of each
suspension was inoculated into molten TSA (precooled
to 40 ºC; or molten Wilkins Chalgren Agar for anaerobes) to give a final concentration of approximately
1 · 103 colony forming units/ml. Duplicate agar plates
were then prepared for each challenge inoculum by
separately pouring a 10 ml volume of the preseeded
molten agar (equivalent to an approximate 1.5 mm
depth) into 90 mm Petri dishes. All seeded agar plates
were allowed to set and then incubated in an appropriate atmosphere at 35 ºC ( 3 ºC) for 4 hours. Following incubation, a 10 ml volume of sterile molten TSA (or
Wilkins Chalgren Agar) was aseptically dispensed over
each seeded agar plate, thereby creating an overlay
plate assay for each challenge organism. Once the
agar layer had solidified, a sample of SHD (5 cm · 5 cm)
was aseptically transferred to each of the seeded plate
assays. A negative control dressing (N-A Gauze) for each
challenge organism was included in the assay. Dressing
samples (including control samples) were fully hydrated
with MRD to simulate wound conditions and then all
plate assays were re-incubated in an appropriate atmosphere at 35 ºC ( 3 ºC) for 24 hours. Following incubation, all plates were observed for growth of colonies
directly beneath the dressing sample.
RESULTS
Figures 1–3 show the corrected zones of inhibition
produced by the SHD for aerobic microorganisms,
antibiotic-resistant bacteria, and anaerobic bacteria. All
microorganisms tested (including antibiotic-resistant
bacteria) were susceptible to the SHD as shown by the
clearly defined zones of inhibition observed around the
dressing. In particular, the SHD showed excellent antimicrobial efficacy against the full range of anaerobic
bacteria tested. However, it should be noted that in
some instances zone sizes were smaller than the original
dressing size (2.5 cm · 2.5 cm). This was due to the SHD
WOUND REPAIR AND REGENERATION
VOL. 12, NO. 3
Antibiotic sensitive micro-organisms (bacteria & yeasts)
18
Anaerobic Bacteria
9.7
9
11
8.2
5
6
9.3
7.75
6.5
8.5
8.5
6
4
4
AQUACEL Ag average zone of inhibition (mm)
25
22.5
22.5
30
12.8
7.5
5.25
3
25
CZOI (mm)
21.25
20
15
11.25
10.5
10
6.5
5
FIGURE 1. Corrected zones of inhibition induced by the SHD
against antibiotic-sensitive bacteria and yeasts.
(CI ¼ Clinical Isolate)
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291
JONES ET AL.
FIGURE 3. Corrected zones of inhibition induced by the SHD
against anaerobic bacteria.
bial effect of the SHD. No depth of penetration was
shown by the control dressing (N-A Gauze).
fibers swelling following hydration and the dressing
sample contracting laterally (from 625 mm2 to 529 mm2,
approximately) and expanding vertically (increase in
thickness). The SHD was also shown to kill all of the
challenge organisms within a 30-minute exposure period,
(an example of which is shown in Figure 4). As expected,
the control dressing (N-A Gauze) did not induce a zone
of inhibition or show killing after a 30-minute exposure
period against any of the microorganisms tested.
Depth of penetration assay
The SHD was shown to be effective at an agar depth
of at least 3 mm against all of the microorganisms
tested. Figure 5 illustrates the depth of penetration
by the SHD against Cl. perfringens (clinical isolate).
The air pockets observed along the outer edge of the
Cl. perfringens test plate were due to the production
of gas by this organism. The lack of growth of the
anaerobe (or associated air pockets) in the center of
the plate was a direct consequence of the antimicro-
DISCUSSION
The present in vitro study clearly shows that the SHD is
effective and rapid acting against commonly encountered wound pathogens, including antibiotic-resistant
bacteria such as MRSA and VRE, anaerobic bacteria,
and yeasts, when in direct and indirect contact with the
microorganisms.
Clinicians have long recognized that aerobic bacteria have the ability to degrade or damage host tissue
through the production of a variety of virulence factors,
enzymes and toxins (e.g., fibrinolysin, hyaluronidase,
hemolysin, leucocidin, exotoxin A).18 However, it is
now appreciated that many anaerobic bacteria
that are commonly found in wounds produce similar
Antibiotic-resistant bacteria
CZOI (mm)
AQUACEL Ag average zone of inhibition (mm)
12
10.25
10
8
7.5
7.25 6.75 6.75
7.25
8
6.5 6.75 7
5.75
6 5.75
5
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4
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0
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(C
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FIGURE 2. Corrected zones of inhibition induced by the SHD
against antibiotic-resistant bacteria.
FIGURE 4. Activity of SHD against B. fragilis after 30 minutes of
exposure (left hand zone) and 24 hour exposure (right hand
exposure).
292
JONES ET AL.
FIGURE 5. Depth of the antimicrobial effect of SHD against
Cl. perfringens.
tissue-degrading enzymes19,20 and that microbial synergy
increases the pathogenic effect.2,19
The incidence of anaerobic bacteria is highly correlated with wound infection. Studies have shown that
anaerobes constitute approximately 38 percent of the
total bacterial load in noninfected wounds and approximately 48 percent in infected wounds.2 As a consequence, most cases of wound infection management
require control of anaerobic as well as aerobic microorganisms. In addition, the emergence of wound pathogens with patterns of multiple antibiotic resistance has
serious consequences in the hospital environment.21
In light of the role of anaerobes and antibioticresistant microorganisms in wounds, the current study
aimed to determine the antimicrobial activity of SHD
against both aerobic and anaerobic microorganisms,
using the zone-of-inhibition method. This provides a
measure of the ability of the SHD to make silver available
at a sufficient concentration to achieve an antimicrobial
effect. To some extent this test mimics the clinical use of
the dressing and may therefore predict its capability of
killing pathogens at the wound–dressing interface. As the
results show (Figures 1–3), SHD makes silver available
at the dressing–agar interface at a concentration that is
effective against a broad range of aerobic, anaerobic, and
antibiotic-resistant microorganisms. In the context of
wound healing, these results showing antimicrobial activity against antibiotic-resistant bacteria are of particular
importance, because these organisms have a significant
clinical impact and are a key concern in health care.12,22
In comparison to SHD, traditional gauze dressings
have no inherent antimicrobial activity, do not prevent
entry of bacteria to wounds,23 and may actually increase
infection risk via air dispersal of bacteria during dressing
changes.24 Furthermore, local reduction in tissue temperature at a wound site, associated with fluid evaporation
through gauze dressings, depresses host immune and
WOUND REPAIR AND REGENERATION
MAY–JUNE 2004
wound healing function via multiple physiological effects
that increase the probability of wound infection.25
Infected wounds can be treated with topical silverbased antiseptic solutions (e.g., silver nitrate) or creams
(e.g., silver sulfadiazine) combined with gauze dressings. However, to maintain microbicidal activity, the
silver must be continuously available in its free ionic
form within an aqueous environment. Because silver
ions react rapidly with many of the ions present in
body fluids (e.g., chloride), topical creams and solutions require multiple daily applications with associated dressing changes and consequent increased
health care costs.26 Furthermore, because of the multiple daily applications, these topical silver agents can
irritate, have astringent effects on tissues, and lead to
discoloration of surrounding tissues.27 In addition, poor
penetration of eschar or, in the case of silver sulfadiazine cream, the pseudoeschar created as the cream
dehydrates, can reduce antimicrobial effect.22 Moreover, silver sulfadiazine is pro-inflammatory, promoting
wound maceration and retarding epithelialization.28,29
SHD combines silver with proven Hydrofiber
technology14,30,31 and was developed to overcome the
difficulties associated with silver solutions and creams.
SHD is designed to provide an effective and long-lasting
concentration of ionic silver at the wound–dressing
interface. The silver cations, which constitute 1.2 percent of the total weight of SHD, are bound to the
individual highly absorbent anionic carboxymethylcellulose fibers of the Hydrofiber dressing. Upon hydration, these silver ions are slowly and continuously
made available for the entire wear time of the dressing.
A chemical equilibrium controls and maintains the concentration of silver ions by exactly balancing the rate of
release of silver in the dressing with the rate of consumption by antimicrobial action or reaction with other
components of the wound fluid. Because the counterions to the silver are the dressing fibers, problems of
toxicity or build-up of pseudoeschar associated with
the counter-ion are avoided. The combination of the
known broad-spectrum antimicrobial activity of silver,10
low risk of inducing antimicrobial resistance,32 and the
moist wound healing environment provided by the
underlying Hydrofiber dressing technology33 may provide optimal conditions for wound healing.
In the current study, the effective antimicrobial
activity against a large range of aerobic, anaerobic,
and antibiotic-resistant microorganisms, following
dressing application, suggests that upon hydration of
the dressing silver ions are rapidly made available at
the interface between the dressing and the agar plate.
In many cases (for example, chronic leg ulcers), the
majority of the bioburden is located in the superficial
zone of the wound. These results suggest a key role
for this antimicrobial dressing in the control of such
bioburden, thus helping prevent microbial infection
WOUND REPAIR AND REGENERATION
VOL. 12, NO. 3
penetrating into deeper tissues. The rapid antimicrobial activity of a silver-containing dressing against
antibiotic-resistant bacteria is particularly significant
given the increasing problems associated with control
and eradication of these organisms within the clinical
environment.22 Other in vitro investigations have
shown that the SHD sustains its antimicrobial activity
for at least 14 days.34
Furthermore, while caution must be exercised
when extrapolating the results of in vitro studies to
the clinical situation, the effectiveness of the antimicrobial activity against microorganisms that are not in
direct contact with the dressing (i.e., beneath the surface of the agar plate), may suggest that the SHD provides some antimicrobial control in regions of the
wound not directly in contact with the dressing—for
example in the devitalized tissue, where the bioburden
is generally high.2
A further advantage of SHD may be its ability to
control the level of wound exudate, although this was
not specifically tested in this study. SHD has a high
fluid-handling capacity provided by the underlying
Hydrofiber technology.14,15,35 This is important
because increased levels of wound exudate are associated with bacterial infection.14 SHD can therefore
manage this exudate and provide antimicrobial activity
against bacteria concomitantly absorbed into the dressing matrix.
The development of wound infection is an ongoing
problem for many patients. Infected wounds may cause
great distress in terms of associated morbidity and mortality, increased length of hospital admission, delayed
wound healing, and increased discomfort, and have
long been known to increase health care costs significantly.36 The present study suggests that this SHD may
offer a solution to the management of infected and
indolent wounds.
ACKNOWLEDGMENTS
This study was supported by ConvaTec Ltd, a BristolMyers Squibb company. AQUACEL and Hydrofiber are
registered trademarks of E.R. Squibb & Sons, L.L.C.
REFERENCES
1. Bowler P. The anaerobic and aerobic microbiology of wounds: a
review. Wounds 1998;10:170–8.
2. Bowler PG, Duerden BI, Armstrong DG. Wound microbiology and
associated approaches to wound management. Clin Microbiol
Rev 2001;14:244–69.
3. White R, Cooper R, Kingsley A. Wound colonization and infection:
the role of topical antimicrobials and guidelines in management.
Br J Nurs 2001;10:563–78.
4. Robson MC. Wound infection. A failure of wound healing caused
by an imbalance of bacteria. Surg Clin North Am 1997;77:637–50.
JONES ET AL.
293
5. EPUAP. European Pressure Ulcer Advisory Panel. Guidelines on
the treatment of pressure ulcers. EPUAP Rev 1999;1:31–3.
6. Normark BH, Normark S. Evolution and spread of antibiotic
resistance. J Intern Med 2002;252:91–106.
7. Hueston WJ, Dickerson L. Antibiotic resistance and the need for
the rational use of antibiotics. J Med Liban 2001;49:246–56.
8. Lawrence JC. The use of iodine as an antiseptic agent. J Wound
Care 1998;7:421–5.
9. Lansdown ABG. Silver 1: its antimicrobial properties and mechanism of action. J Wound Care 2002;11:125–30.
10. Demling RH, DeSanti L. Effects of silver on wound management.
Wounds 2001;13 (Suppl A):A3–A15.
11. Cutting KF. A dedicated follower of fashion? Topical medications
and wounds. Br J Nurs 2001;10:9–16.
12. Thomas S, McCubbin P. A comparison of the antimicrobial effects
of four silver-containing dressings on three organisms. J Wound
Care 2003;12:101–7.
13. Field FK, Kerstein MD. Overview of wound healing in a moist
environment. Am J Surg 1994;167 (1A):2S–6S.
14. Armstrong SH, Ruckley CV. Use of a fibrous dressing in exuding
leg ulcers. J Wound Care 1997;6:322–4.
15. Harding KG, Price P, Robinson B, Thomas S, Hofman D. Cost and
dressing evaluation of hydrofiber and alginate dressings in the
management of community-based patients with chronic leg
ulceration. Wounds 2001;13:229–36.
16. Lydon MJ. The development of Aquacel Hydrofiber dressings. In:
Krieg, T Harding, KG, editors. Aquacel Hydrofiber dressing: the
next step in wound dressing technology. Proceedings of a Satellite Symposium at the Sixth Congress of the European Academy
of Dermatology and Venereology; 1997 Sept 11–15; Dublin, Ireland. London: Churchill Communications, 1998:1–3.
17. Wright JB, Hansen DL, Burrell RE. The comparative efficacy of
two antimicrobial barrier dressings: in vitro examination of two
controlled release silver dressings. Wounds 1998;10:179–88.
18. Heggers JP. Defining infection in chronic wounds: methodology.
J Wound Care 1998;7:452–6.
19. Duerden BI. Virulence factors in anaerobes. Clin Infect Dis
1994;18 (Suppl 4):S253–9.
20. Steffen EK, Hentges DJ. Hydrolytic enzymes of anaerobic bacteria
isolated from human infections. J Clin Microbiol 1981;14:153–6.
21. Morgan M, Evans-Williams D, Salmon R, Hosein I, Looker DN,
Howard A. The population impact of MRSA in a country: the
national survey of MRSA in Wales, 1997. J Hosp Infect 2000;
44:227–39.
22. Wright JB, Lam K, Burrell RE. Wound management in an era of
increasing bacterial antibiotic resistance: a role for topical silver
treatment. Am J Infect Control 1998;26:572–7.
23. Lawrence JC. Dressings and wound infection. Am J Surg 1994;167
(1A):21S–4S.
24. Lawrence JC, Lilly HA, Kidson A. Wound dressings and airborne
dispersal of bacteria. Lancet 1992;339:807.
25. Ovington LG. Hanging wet-to-dry dressings out to dry. Home
Healthc Nurse 2001;19:477–83.
26. Bolton L, van Rijswijk L. Cost effective wound care. CAET J
1999;18:23–5.
27. Greene RM, Su WP. Argyria. Am Fam Physician 1987;36:151–4.
28. Klein DG, Fritsch DE, Amin SG. Wound infection following
trauma and burn injuries. Crit Care Nurs Clin North Am 1995;
7:627–42.
29. Hoekstra MJ, Hupkens P, Dutrieux RP, Bosch MM, Brans TA,
Kreis RW. A comparative burn wound model in the New Yorkshire pig for the histopathological evaluation of local therapeutic
regimens: silver sulfadiazine cream as a standard. Br J Plast Surg
1993;46:585–9.
30. Foster L, Moore P, Clark S. A comparison of hydrofibre and
alginate dressings on open acute surgical wounds. J Wound
Care 2000;9:442–5.
294
JONES ET AL.
31. Vloemans AF, Soesman AM, Kreis RW, Middelkoop E. A newly
developed hydrofibre dressing, in the treatment of partialthickness burns. Burns 2001;27:167–73.
32. Silver S, Novick R, Gupta A. Mechanisms of resistance to heavy
metals and quaternary amines. In: Fischetti, VA, Novick, RP,
Ferretti, JJ, Portnoy, D, Rood, JI, editors. Gram positive pathogens.
Washington, DC: ASM Press, 2000.
33. Williams C. An investigation of the benefits of Aquacel Hydrofiber
wound dressing. Br J Nurs 1999;8:676–7, 80.
WOUND REPAIR AND REGENERATION
MAY–JUNE 2004
34. Bowler PG, Jones SA, Walker M, Parsons D. The microbicidal
properties of a silver-containing Hydrofiber dressing against a
variety of common burn wound pathogens. J Burn Care Rehab
2004;25:192–6.
35. Robinson BJ. The use of a hydrofibre dressing in wound management. J Wound Care 2000;9:32–4.
36. Plowman R. The socio-economic burden of hospital-acquired
infection: executive summary. London: Public Health Laboratory
Service, 1999.