What Art the Dermatologic Morphologic Terms for a Bedsore
J Spinal Cord Med. March, 2015; 38(two): 147–160.
Bacteriology of force per unit area ulcers in individuals with spinal cord injury: What we know and what we should know
Ali N. Dana
iDermatology Service, James J. Peters VA Medical Center, Bronx, NY, USA
2Department of Dermatology, Columbia University School of Medicine, New York, NY, The states
William A. Bauman
3Department of Veterans Affairs Rehabilitation Research & Development Service'south National Center of Excellence for the Medical Consequences of Spinal String Injury, James J. Peters Veterans Affairs Medical Heart, Bronx, NY, USA
4Medical Service, James J. Peters VA Medical Heart, Bronx, NY, USA
5Section of Medicine and Rehabilitation Medicine, Ichan Schoolhouse of Medicine at Mount Sinai, New York, NY, USA
Abstract
Individuals with spinal string injury (SCI) are at increased risk for the development of pressure ulcers. These chronic wounds are debilitating and contribute to prolonged hospitalization and worse medical outcome. However, the species of bacteria and the part that specific species may play in delaying the healing of chronic pressure ulcers in the SCI population has not been well characterized. This report will review the literature regarding what is known currently virtually the bacteriology of pressure level ulcers in individuals with SCI. An electronic literature search of MEDLINE (1966 to February 2014) was performed. Xi studies detailing bacterial cultures of pressure level ulcers in the SCI population met inclusion criteria and were selected for review. Among these studies, bacterial cultures were often polymicrobial with both aerobic and anaerobic bacteria identified with civilization techniques that varied significantly. The most common organisms identified in pressure ulcers were Staphylococcus aureus, Proteus mirabilis, Pseudomonas aeruginosa, and Enterococcus faecalis. In general, wounds were poorly characterized with minimal to no physical description and/or location provided. Our nowadays understanding of factors that may alter the microbiome of pressure ulcers in individuals with SCI is quite rudimentary, at all-time. Well-designed studies are needed to appraise appropriate wound culture technique, the touch on of bacterial limerick on wound healing, development of infection, and the optimum medical and surgical approaches to wound care.
Keywords: Pressure ulcer, Spinal cord injury, Bacteria, Bacteriology, Wound care
Introduction
Individuals with paralysis following spinal cord injury (SCI), also as others who have medical or neurological conditions that predispose to prolonged immobilization, are at significant chance for the development of skin breakup. The crusade of these localized wounds (due east.g. force per unit area sores, pressure ulcers, decubitus ulcers, or bedsores) may exist due to force per unit area over a bony prominence that results in shearing and/or ischemia of the overlying pare, leading to tissue breakdown.ane However, it is at present generally accepted that external pressure compromises skeletal muscle, likewise every bit cutaneous microvascular blood menstruum, resulting in the development of pressure ulcers that actually arise from deeper tissue beds. As such, many wounds initially result from deep tissue ischemia and necrosis prior to the appearance of skin breakdown.two Skin breakdown in patients with SCI will be referred to every bit pressure ulcers in this review because the defect typically occurs at a site of prolonged and unrelieved pressure.
Compared with the general population, individuals with SCI are at meaning risk of developing a pressure level ulcer. In contempo years, the prevalence of force per unit area ulcers in individuals with SCI has increased.3 In the literature, prevalence rates of pressure ulcers vary due to differences in study methodology, only more than recent studies suggest that betwixt 25 and 50% of veterans with SCI are estimated to receive treatment for pressure ulcers.3–5 Pressure level ulcers not only pose a significant medical brunt, but they likewise are associated with loftier costs of care. The annual price of treating pressure ulcers in the SCI population has been projected to be $i.three billion.6 Healthcare costs for individuals with SCI and pressure ulcers significantly exceed the costs for individuals without pressure ulcers.7 The boilerplate cost per hospitalization is estimated to be about $150 000 for the treatment of a pressure ulcer in an individual with SCI.iv
Complications arising from pressure ulcers are associated with significant morbidity and mortality. Bacterial infection is the nearly mutual complexity associated with pressure ulcers. Infection of a pressure level ulcer may effect in soft tissue and os infections: cellulitis, abscess formation, bursitis, and osteomyelitis of bone underlying the wound bed.8 Pressure level ulcers are a common source of bacteremia in individuals with SCI.9 However, in general, the relationship between bacterial colonization, infection, and wound healing is not well characterized.
To begin to understand the influence of bacteria on the development of disease states, meaning effort has focused on identifying the mutualistic microorganisms that reside in the human being microbiome. Using standard culture methods, Corynebacterium species, Propionibacterium acnes, and coagulase-negative staphylococcus have been identified every bit resident flora of the skin.10 Newer molecular studies have demonstrated that in improver to these commensals, there is a vast complexity of organisms that comprise the cutaneous microflora. Studies using 16sRNA sequencing have shown that the bulk of these leaner belong to the 4 phyla: Actinobacteria, Firmicutes, Bacteroidetes, and Proteobacteria.xi–sixteen Many of these species had non been associated with the resident flora of the pare and have typically accounted for <1% of the total flora in any distinct area. In a normal host, commensal bacteria are considered non-pathogenic and may beneficially influence the host immune response to serve to decrease colonization of potentially more pathogenic species. For instance, the presence of commensal Staphylococcus epidermidis prevents nasal colonization with the more pathogenic species Staphylococcus aureus. 17 Just if the epithelium is compromised, depending on the type and number of organisms, resident flora may contribute to delayed wound healing or the evolution of local or systemic infection.18,19 Recent areas of inquiry have focused on understanding how communities of bacteria positively and negatively bear on wound healing. In diabetic mice with wounds, the temporal shift in limerick of microflora is accompanied by changes in local host immunoregulation.xx This review focuses on the bacteriology of pressure ulcers in individuals with SCI. The aim of this review is to compile available bacteriological data of chronic pressure ulcers in the spinal cord injured. A better agreement of bacterial colonization and wound infection of chronic pressure level ulcers may be expected to provide insight into new therapeutic interventions that may prevent or reduce morbidity and bloodshed.
Methods
Identification of articles
An electronic search of MEDLINE (1966 to Feb 2014) was performed using the post-obit combination of keywords ("pressure level ulcer*" OR "pressure sore*" OR "bedsore*" "decubitus") AND ("bacter*" OR "civilization" OR "micro*") AND ("spinal cord injur*" OR "?plegia"). Studies called were limited to the English linguistic communication. All titles and abstracts identified by the above search strategy were screened for relevance to the inclusion criteria. If relevance could non be ascertained from the title and abstract alone, the full text of the article was reviewed for possible inclusion. Full texts of manufactures that were initially considered to be potentially relevant were reviewed for possible inclusion. In addition, cited literature of relevant articles was examined for farther meaningful content.
Studies were included if the patient accomplice had SCI and if bacteriological data for more than than one pressure ulcer was available. Studies with mixed populations were included only if information for >80% subjects with SCI could be identified. Similarly, studies with bacteriological data for treated or manipulated force per unit area ulcers were included only if civilization data were unequivocally from chronic force per unit area ulcers and non from mail service-operative wounds in individuals with SCI. Studies were non included if results of bacterial cultures were non adequately specified. Case reports and reviews were excluded from our analysis.
For the purpose of this review, "pressure ulcer" will be term that will be used for other common terms to place this condition—that is, for pressure sores, pressure ulcers, decubitus ulcers, or bedsores. In addition, the relationship between bacteria and the wound substrate is circuitous, and considered an ill-defined continuum. This review focuses on bacterial presence within chronic pressure level ulcers, and not the identification of bacterial species that are recognized to be potentially pathologic. Studies were included even if they did not present all information on bacterial culture past the willful exclusion of the reporting of the presence of peel commensals.
Study characteristics
From the articles that met the inclusion and exclusion criteria, bachelor data were extracted, including patient number and sexual activity, number of pressure ulcers included in the study, number of pressure ulcers from which bacterial samples were obtained, number of bacterial cultures obtained from pressure level ulcers, type of bacterial civilization performed, the number of polymicrobial cultures, and blazon and incidence of bacterial species identified. Information about the pressure ulcers studied was also extracted, such as ulcer stage and size, and whether or not the patient or the pressure ulcer was treated prior to bacterial sampling of the pressure ulcer. In addition, data concerning concrete characteristics of force per unit area ulcers were collected including the presence of osteomyelitis, malodor, tissue necrosis, and exudate.
Due to inconsistencies in the level of speciation inside each commodity, the bacterial species recorded in each study were sorted into broad categories based on the characteristics of cell wall structure, morphology, and cellular metabolism. Using the incidences of bacterial species identified, the relative frequency of each category (aerobic vs. anaerobic, Gram positive vs. negative, cocci vs. rods) was calculated and graphed for each report. Similarly, bacterial species were classified into genera and the frequencies of unique genera were charted. The anatomic sites and frequency of pressure ulcers affecting these sites were recorded; anatomic sites were classified into four main categories: pelvis, buttock/thigh/leg, talocrural joint/foot, and other) and frequencies of pressure level ulcers affecting these sites were calculated if the number and physical location of cultured pressure ulcers were reported in the study.
Results
Literature search
The electronic literature search returned 51 articles. We screened the titles and abstracts of all of these articles for relevance. If an article was considered relevant, the literature cited within the study was too screened for relevance. The eligibility of relevant manufactures for inclusion in the review was determined past evaluating the total text to define if inclusion or exclusion criteria were satisfied (Fig.i). A total of 11 studies were identified for inclusion in this review.
Flow diagram of the literature review.
Report characteristics
We identified 11 articles with information on species of bacteria cultured from pressure ulcers in the spinal cord injured.9,21–30 The characteristics of these studies were tabulated (Table1), including authors and date of publication, purpose of written report, number of patients and ulcers included in the study, number and type of bacterial cultures obtained from pressure ulcers, and number of polymicrobial cultures. Among the manufactures included in this review, the number of patients with SCI and pressure level ulcers that were sampled ranged from 12 to 101 (boilerplate 32 ± 26). The number of pressure level ulcers sampled ranged from 5 to 47 (average 23 ± 13), and the number of bacterial cultures obtained ranged from 12 to 168 (average 51 ± 59). Among the 11 studies, bacterial sampling methods were not standardized and included needle aspiration, surgical drainage, cotton swab, tissue biopsy, or a combination of these techniques. At least seven studies indicated whether aerobic and anaerobic cultures were performed (Table1).21,23–26,28,29
Tabular array 1
Characteristics of the 11 studies included in our review that examined the bacteriology of pressure ulcers in individuals with SCI
| Galpin et al. 23 | Vaziri et al. 29 | Sugarman et al.27 | Sapico et al. 26 | Thornhill-Joynes et al. 28 | Montgomerie et al. 25 | Biering-Sorensen et al. 21 | Waites et al. 30 | Wall et al. nine | Heym et al. 24 | Biglari et al. 22 | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Written report focus | Bacteriology of PU associated with sepsis | Infections in patients undergoing hemodialysis | Osteomyelitis beneath pressure sores | Microbiology of PU in dissimilar stages of healing | Evaluation of the frequency of osteomyelitis in patients with SCI and PU | Mortality amid patients with bacteremia | Bacterial contagion of bath water | Bacteremia after SCI during hospitalization | Chance factors for mortality from bacteremia in individuals with SCI | Bacteriology of PU and impact on antibody therapy | Utilize of Medihoney as non-surgical therapy for PU |
| Number of patients | 21 (14 M, seven F) | 43 (43 M) | 19 (NA) | 25 (21 M, four F) | 40 (35 Thousand, v F) | 93 (74 Thou, 19 F) | 18 (NA) | 59 (48 Thou, eleven F) | 63 (62 M, 1 F) | 101 (68 M, 33 F) | 20 (13 M, seven F) |
| Number of patients with PU | 21 | 27 | 19 | 25 | 40 | xviii | 12 | NA | 36 | 101 | xx |
| Number of PU cultured | 47 | NA | 22 | 25 | 35 | NA | 12 | v | 21 | NA | twenty |
| Number of cultures | NA | NA | NA | 49 | 38 | 20 | 12 | NA | NA | 168 | 20 |
| Sampling method | Needle aspiration, surgical drainage, or cotton wool swab | Needle aspirate or cotton swab | NA | Cotton wool swab or tissue biopsy; debridement prior to sampling | Cotton fiber swab | NA | Cotton fiber swab culture | NA | NA | Tissue biopsy, needle aspiration, surgical drainage, or cotton swab; debridement prior to sampling | Cotton swab |
| Type of cultures | Aerobic and anaerobic | Aerobic and anaerobic | NA | Aerobic and anaerobic | Aerobic and anaerobic | Aerobic and anaerobic | Aerobic | NA | NA | Aerobic and anaerobic | NA |
| Per centum polymicrobial cultures | NA | 55% (≥two spp.) | xvi% (1 spp.) | NA | NA | NA | 75% (1 spp.) | NA | NA | 69% (≤ two spp.) | 70% (one spp.) |
| 16% (two spp.) | 25% (2 spp.) | 21% (3 spp.) | 15% (2 spp.) | ||||||||
| 21% (3 spp.) | eight% (≥four spp.) | x% (3 spp.) | |||||||||
| 31% (4 spp.) | 5% (4 spp.) | ||||||||||
| 15% (≥5 spp.) | |||||||||||
| Predominant organism (percentage of bacterial isolates) | P. mirabilis (xviii%) | P. mirabilis (17%) | P. mirabilis (17%), P. aeruginosa (17%) | S. aureus (11%) P. aeruginosa (11%) | S. aureus (16%) | Due south. aureus (20%) | S. aureus (30%), E. faecalis (xxx%) | S. aureus (50%) | S. aureus (57%) | South. aureus (23%) | South. aureus (30%) |
Bacteriology of force per unit area ulcers
The anaerobic and aerobic bacterial composition of wounds too seems to be similar amidst studies that provided bacteriological data for pressure ulcers in patients with SCI. A non-redundant list of unique aerobic and anaerobic bacteria identified in the 11 articles was compiled (Tableii). More unique species of aerobic bacteria (30 unique species) were identified when compared with anaerobic species (22 unique species). The aerobic Gram-negative rod category contained the greatest number of unique bacterial genera (eighteen unique genera). The relative frequency of isolation of each of the bacterial categories for each study reviewed herein has been provided (Fig.2). Aerobic Gram-negative rods and aerobic Gram-positive cocci were the bacterial categories most commonly isolated. Anaerobes typically deemed for less than ane-3rd of bacterial isolates (Fig.ii). The pct of aerobic organisms isolated appears greater for studies performed after the year 2000, but this may merely reflect sampling methods. The predominant bacterial species and frequency for each of the eleven studies have been provided (Table1). In the before studies, Proteus mirabilis was the about frequently identified bacterium, but there is a tendency for the predominance of S. aureus to be increasingly identified from bacterial cultures in subsequently studies.nine,21–30 A composite of all bacterial genera and the frequency of their identification amidst all of the eleven studies have been presented (Fig.three). The about common genus of bacteria identified was Staphylococcus (23% of all genera identified) followed by Proteus (14% of all genera identified) (Fig.three).ix,21–thirty 8 studies identified S. aureus as the most predominant organism, one of which likewise isolated an equal number of Enterococcus faecalis isolates and another study had an equivalent frequency of Pseudomonas aeruginosa (Table1).9,21,22,24–26,28,30 Three other studies had identified P. mirabilis as the most common organism, with one report identifying an equal number of P. aeruginosa.23,27,29 Thus, information technology appears that the predominant organism identified in pressure ulcers is highly variable, and largely dependent upon the report population.
Percentages of bacterial type identified in chronic force per unit area ulcers in individuals with SCI for each study of the 11 publications included in our review. GPC, Gram-positive cocci; GPR, Gram-positive rod; GNR, Gram-negative rod.
Bacterial species as a percentage of total leaner identified in chronic pressure ulcers in individuals with SCI among the 11 studies included in our review.
Table ii
Composite list of unique bacterial isolates identified in chronic force per unit area ulcers in individuals with SCI among the xi studies included in our review
| Aerobic bacterial organisms | Anaerobic bacterial organisms | |
|---|---|---|
| Gram-negative rod | Acinetobacter anitratus | Bacteroides assacharalyticus |
| Acinetobacter baumanii | Bacteroides corrodans | |
| Acinetobacter calcoaceticus | Bacteroides distasonis | |
| Citrobacter diversus | Bacteroides fragilis | |
| Enterobacter cloacae | Bacteroides Group 3452A | |
| Escherichia coli | Bacteroides mealaninogenicus | |
| Flavobacterium spp. | Bacteroides oralis | |
| Haemophilus spp. | Bacteroides thetaiotaomicron | |
| Klebsiella oxytoca | Bacteroides uniformis | |
| Klebsiella pneumoniae | Bacteroides urealyticus | |
| Morganella morganii | Bacteroides vulgatus | |
| Proteus mirabilis | Eggerthella lentum | |
| Proteus rettgeri | Fusobacterium necophorum | |
| Proteus vulgaris | Fusobacterium nucleatum | |
| Proteus spp., other | ||
| Providencia stuarti | ||
| Pseudomonas aeruginosa | ||
| Pseudomonas spp., other | ||
| Gram-positive cocci | Enterococcus faecalis | Clostridium bifermentans |
| Staphylococcus aureus | Clostridium clostridiiforme | |
| Staphylococcus epidermidis | Clostridium difficile | |
| Streptococcus Group A | Microaerophilic streptococcus spp. | |
| Streptococcus Group B | Peptostreptococcus assacharolyticus | |
| Streptococcus Group D | Peptostreptococcus magnus | |
| (non-enterococcal) | Peptostreptococcus prevotii | |
| Streptococcus Group G | ||
| Streptococcus Group F | ||
| Streptococcus viridans | ||
| Streptococcus intermedius | ||
| Gram-positive rod | Corynebacterium spp. | Lactobacillus spp. |
| Bacillus spp. |
Only v studies indicated whether or not bacterial cultures grew more than one species of bacteria, or were polymicrobial (Tableane).21,22,24,27,29 Of the limited number of studies that provided detailed data on the microbial complexity of pressure ulcers, 10–21% of bacterial cultures grew more three bacterial species per culture.22,24,27 In this review, three studies provided data from which the boilerplate number of organisms cultured per wound could be calculated. Biglari et al. 22 identified 1.five bacterial species per wound, Biering-Sorensen et al. 21 cultured one.25 bacterial species per wound, and Sugarman et al. 27 identified 3.3 bacterial species per wound.
Pressure level ulcer characteristics
The percentages of pressure level ulcers sampled from a particular anatomic region have been provided (Fig.4). Of the half dozen studies that were reviewed which included data of the anatomic location of the pressure ulcer, more than half of all pressure level ulcers were located in the pelvic region (i.east. sacral, ischial, perineal, and trochanteric regions).21–23,26–28 The next most common area was the buttock and/or legs. Information concerning the physical characteristics of the sampled pressure level ulcers accept been provided (Table3). At that place is a paucity of data concerning the physical characteristics of the pressure ulcers sampled among the studies included in this review. Six studies included at to the lowest degree i wound characteristic for the pressure ulcers sampled,21–23,26–28 with only three studies reporting pressure ulcer size and21,22,26 one study reporting force per unit area ulcer staging.22
Frequency of anatomic site affected past chronic force per unit area ulcers in individuals with SCI from six studies that detailed anatomic location amongst the xi studies included in our review.
Table 3
Wound characteristics amidst studies examining pressure ulcers in individuals with SCI from the xi studies included in our review
| Galpin et al. 23 | Vaziri et al. 29 | Sugarman et al.27 | Sapico et al. 26 | Thornhill-Joynes et al. 28 | Montgomerie et al. 25 | Biering-Sorensen et al. 28 | Waites et al. 30 | Wall et al. nine | Heym et al. 24 | Biglari et al. 22 | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Presence of osteomyelitis | eight individuals (38%) | NA | 3 individuals (16%) | eight individuals (32%) | 25 PU of 38 sampled in 24 patients (66%) | NA | 1 private (8%) | NA | NA | NA | NA |
| Presence of malodor | 13 individuals (62%) | NA | NA | 8 individuals (16%) | NA | NA | NA | NA | NA | NA | NA |
| Presence of tissue necrosis | eighteen individuals (86%) | NA | NA | 17 individuals (68%) | NA | NA | NA | NA | NA | NA | five individuals (25%) |
| Presence of exudate | NA | NA | NA | NA | 13 PU sampled in 24 patients (62–68%) | NA | 5 individuals (42%) | NA | NA | NA | NA |
| Ulcer staging performed | NA | NA | NA | Capricious categorization of healing stages | NA | NA | NA | NA | NA | NA | 5 individuals (25%) with grade Four |
| fifteen individuals (75%) with class 3 | |||||||||||
| Ulcer size | NA | NA | NA | Ave l cm2 | NA | NA | 5 mm to 6 cm undermining | NA | NA | NA | Boilerplate 21.7 cmtwo |
| Range 4–225 cm2 | Range viii–fourscore cm2 | ||||||||||
| Treatment of PU before sampling | 62% of patients receiving antibiotics | NA | 26% of patients received antibiotics prior to sampling | 38% of tissue biopsies obtained while receiving antibiotics; 47% of tissue biopsies obtained while receiving local wound care | NA | NA | NA | NA | NA | Patient received antibiotics later PU sampling | Patient received local wound care with Medihoney after PU sampling |
Word
This study reviews the available bacterial culture data available for pressure ulcers in the SCI population. Bacterial constituents of pressure ulcers in individuals with SCI are quite varied and can include both aerobic and anaerobic leaner. Fifty-two unique species of bacteria were identified (22 unique genera), of which near half were anaerobic (Table2).ix,21–thirty This number of genera may underestimate the quantity of unique bacteria due to variations in anaerobic civilisation methods and inability to grow fastidious organisms. Many organisms take complex nutritional growth requirements, and ofttimes are not identified using traditional culture methods. Fewer than half of studies in this review performed both aerobic and anaerobic cultures, and the majority did non detail specific methods of the culture technique employed. A prior study that identified leaner in chronic pressure ulcers in individuals without SCI using traditional civilisation methods isolated an average of 1.2–5.8 organisms per culture.31 This is similar to the boilerplate of one.25–iii.3 organisms per civilisation identified from pressure ulcers in the spinal cord injured. More recently, studies of chronic wounds employing molecular techniques have demonstrated that microbiomes of wounds are more complex than previously determined.32–34 Using molecular techniques, Dowd et al. 35 constitute that the bacterial population in pressure ulcers in individuals without SCI is represented by 28 singled-out genera and mainly comprised by obligate anaerobes (62%). Toll et al. 32 used large-calibration sequencing to place an average of x bacterial families that had residence in a chronic wound, which is several times greater than estimated past traditional culture methods. Compared with traditional culture methods, molecular methods may permit more comprehensive analysis of bacterial populations in wounds.
Although the most predominant organism was constitute to be different among reports, it should exist appreciated that the virtually prevalent bacterial species really varied relatively little amidst the bacteria isolated from chronic force per unit area ulcers. Prior studies evaluating the microbiology of force per unit area ulcers in the full general population accept identified S. aureus, S. epidermidis, P. mirabilis, and P. aeruginosa every bit common bacterial species identified from ulcers.36–38 In an extensive clinical compilation of 2500 cases of chronic pressure level ulcers in patients with SCI, El-Toraei et al. 39 identified the following bacteria and their prevalence: S. aureus (35%), Proteus spp. (19%), P. aeruginosa (13%), Escherichia coli (10%), Acinetobacter spp. (viii%), Providencia spp. (6%), Klebsiella spp. (4%), and other species (v%). These findings are reflected in all of the studies reviewed herein that examined the bacteriology or pressure ulcers in individuals with SCI. Resident bacterial flora may business relationship for the predominance of enterobacteria in chronic pressure ulcers of individuals with SCI. Due to skin breakdown, chronic wounds tin be colonized by microbial flora that may originate from the external environment, contiguous skin, gastrointestinal tract, and/or the urogenital mucosa.
In full general, chronic pressure ulcers are colonized and infected with normal cutaneous and enteric commensal bacteria, but the bacterial constituents of microbial flora tin modify depending on host immunity and ecology factors. Individuals with SCI are more than likely to develop Gram-negative leaner as part of their normal flora as compared to individuals without SCI. Factors that may influence Gram-negative bacteria colonization of the perineum include the presence of neurogenic bladder dysfunction, external safety catheter use, changes in skin pH, and bacteriuria.40–43 Studies of peel flora in the male person genital region have identified several bacterial isolates: Pseudomonas spp., Klebsiella spp., E. coli, Acinetobacter spp., Proteus spp., Enterobacter spp., and Citrobacter freundii.40 In a report of genital skin flora, Gram-positive cocci and diphtheroids accounted for 93.7% of bacterial isolates from the skin in controls, whereas Gram-negative enteric organisms and enterococci deemed for 54% of bacterial isolates from males with SCI.43 In particular, the perineal region in individuals with SCI is more likely to become colonized with Pseudomonas and Klebsiella, with rates of colonization ranging from twenty to lxxx%.40,44–48 Colonization with Klebsiella has been shown to persist as long as 55 days and for Pseudomonas, 120 days during hospitalization.45,49 These prior described changes in skin flora may be anticipated to touch the bacterial composition of pressure ulcers in individuals with SCI.
Overall changes in the leaner isolated from chronic pressure level ulcers may reflect changes in the microbiome of the skin. In the earlier studies in this review, P. mirabilis was more commonly identified, but studies after 1986 started to identify Due south. aureus more ofttimes. The predominance of S. aureus may exist due to the increasing prevalence of methicillin-resistant S. aureus (MRSA) in the customs. An emerging pathogen, MRSA has become ubiquitous in the infirmary and customs settings. MRSA has been identified as the virtually common multi-drug-resistant organism colonizing patients with SCI.50 Individuals with SCI are at increased chance of becoming colonized or infected with MRSA because they often require lengthy infirmary stays and are routinely transferred betwixt skilled nursing facilities and rehabilitation centers where nosocomial transmission more ofttimes occurs.51,52 Community-acquired MRSA is becoming more prevalent than MRSA acquisition from nosocomial transmission.53,54 Previously, rates of colonization varied widely, and ranged from <five to >lxx% of individuals with SCI in a infirmary setting or specialized SCI center.53,55 In 2013, MRSA was identified in 38.half-dozen% of individuals with SCI inside 48 hours of admission to an acute intendance facility.56 In those with SCI and MRSA, the bacterium may typically be isolated from three or more body sites, but most frequently from pressure ulcers.l,51,54 Wounds that are colonized with MRSA may remain colonized despite antibacterial treatment and other decolonization measures.54,57 Non simply has MRSA colonization been associated with prolonged infirmary stays for individuals with SCI, but too the predisposition to the development of pressure ulcers and nosocomial infections.9,50,54,58 Because of the prevalence of MRSA in the community and among individuals with SCI, the identification of MRSA in pressure ulcers will probable simply increase over time.
Chronic wounds are complex, and typically incorporate more than ane bacterial species. 3 of the studies reviewed herein identified >10% of bacterial cultures that grew more than than three bacterial species per civilisation. Thus, molecular techniques may also identify larger numbers of distinct leaner from wounds every bit compared to conventional civilization methods and, as such, application of these more than sophisticated techniques may provide a useful clinical tool in the analysis of wound flora of chronic pressure ulcers in the SCI population. However, standardization is lacking in how bacterial cultures are obtained from wounds, and differences in bacterial sampling may occur as a result. In general, the methods of bacterial identification vary and include superficial and deep tissue biopsy, curette, superficial and deep swab culture, needle aspiration, surgical drainage, and molecular studies. Traditionally, aerobic and anaerobic bacterial cultures of deep tissue biopsies have been considered the gold standard for the identification of wound bacteria. Several studies accept suggested that the swab technique, such as the Levine technique, in which a cotton Q-tip twirled for five seconds on an surface area of an open wound measuring at least 1 cmii in size with sufficient pressure to incite minimal bleeding of the underlying wound bed, may be considered a viable sampling culling to tissue biopsy.59 In a prior review of five studies in which swab technique was described and compared with tissue biopsy, the swab technique yielded a sensitivity of 93.5–100%, and a specificity of 76.3–94.2%.60 The studies reviewed herein by and large used swab cultures, although several researchers used a combination of sampling methods, including needle aspiration, surgical drainage, and/or tissue biopsy. Simply two of the studies of SCI cohorts that nosotros reviewed addressed rates of concordance between the two sampling methods.24,26 In a study that examined 25 chronic pressure ulcers in 25 patients with SCI during different stages of healing, the hateful quantitative cyclopedia of swab cultures to biopsy cultures was 74.five%.26 Whereas in a comparing of bacterial cultures from chronic pressure ulcers in individuals with SCI obtained by swab civilisation on admission and tissue sampling at the stop of surgical intervention, only 28 (36%) of the 77 patients had like bacterial cultures.24 In both of these studies, the ulcer bed was debrided prior to tissue biopsies, a technique that would be anticipated to decrease the number of unique bacterial isolates due to removal of bacterial colonizers.
There appears to be a trend for less anaerobic organisms being cultured over fourth dimension, but this may merely be a reflection of variability in civilisation methods employed. Another possibility to consider is that differences exist in the location and physical characteristics of pressure ulcers existence sampled amid the unlike studies comprising our review. The association of enteric bacteria with pelvic wounds would suggest that the presence of particular microbes in a pressure level ulcer depends on the locale of the afflicted site. Previous studies that have examined the bacterial composition on normal intact peel accept shown that the presence of certain bacteria differs widely amid unlike sites of the trunk.61,62 A recent 16S rRNA gene sequence analysis of the microbial multifariousness amid twenty distinct skin sites of healthy humans demonstrated that physiologically similar sites (sebaceous, moist, and dry out) retain comparable bacterial communities but that these communities demonstrated pregnant variation in composite species.15,16,63 How these bacterial communities influence the bacterial colonization of chronic wounds is notwithstanding to be determined.
Although an individual with an SCI may develop an ulcer in any location, chronic wounds accept a predilection for certain sites, which tend to depend upon the duration of injury. Early afterward becoming paralyzed, the anatomic areas involved are ofttimes the sacrum, trochanterics, ischia, heads of fibula, and calcaneal prominences. In those with chronic SCI, the most common region for pressure ulcers is the pelvis; nonetheless, in those individuals with increased spasticity, ulcers will also develop with increased frequency in the areas of patellae, medial tibial prominence, and medial malleoli.64 Of the six studies discussed in this review that provided the locations of the pressure ulcers, only i report provided bacterial data and site of location for pressure ulcers, only the limited data in this one written report does non let for whatever determination to exist drawn concerning prevalence of leaner based on anatomic location (data not shown).22 Thus, the extent to which normal flora of adjacent sites impact the microbiota within a wound based on pressure level ulcer location has not been established.
Regardless of the location of the pressure ulcer, microbial variety within an individual wound is also largely unknown. In an evaluation of tissue culture from opposing rims in xi chronic wounds and from the center of 8 of these wounds, sampling yielded the same organisms in 90–94.seven% of the wounds.33 In a report of chronic venous leg ulcers from 14 pare graft operations, quantitative polymerase chain reaction demonstrated large variations in bacterial numbers, and molecular methods demonstrated differences in bacterial species identification based on spatial distribution inside a wound, specially with regard to anaerobic pathogens, which were not detected by routine anaerobic culture methods.65 Just one written report involving force per unit area ulcer healing in individuals with SCI examined spatial differences in bacterial composition by location within a wound; sampling a pressure ulcer from the periphery and the center had a hateful quantitative concordance of 63%.26 The difference in civilisation findings demonstrates that variability exists in cultures obtained from unlike areas of the same ulcer. This is non surprising given that fluorescent in situ hybridization techniques have adamant that structural organization of bacteria within the eye of a chronic wound is non-random and heterogeneous: P. aeruginosa aggregates as microcolonies in a polymicrobial biofilm, whereas S. aureus localizes to the surface of the wound.66 These findings would suggest that in that location are spatial differences and microenvironmental factors that influence microbial diverseness.
Other factors, in addition to wound location and associated microflora, may have the potential to affect bacterial composition of pressure ulcers. For example, location of a pressure ulcer may non have every bit much impact on the bacterial colonizers as the physical factors of the wound. Epidemiological studies have shown that bacterial species in a wound differ as a function of the type of chronic wound. Depending on whether the etiology of a wound is due to underlying venous illness, diabetes, or pressure, the ratio of aerobic to anaerobic bacteria varies.35 Sapico et al. 26 demonstrated that the ratio of anaerobic to aerobic leaner in 25 patients with SCI who had chronic pressure ulcers was correlated with the amount of tissue necrosis in the wound; although comparable numbers of aerobic and anaerobic bacteria were isolated from pressure ulcers with tissue necrosis, the presence of anaerobes significantly decreased as the ulcer healed and malodor abated. Bacteroides spp., Eastward. coli, Proteus spp., group D streptococci, and anaerobic streptococci were the most prominent organisms in pressure ulcers with necrotic tissue, whereas P. aeruginosa and S. aureus were most frequently isolated from healing wounds.26
Other than tissue necrosis, specific wound characteristics that may be predictive of sure microbial organisms or communities have not been identified just may include the moistness or aridity of a wound. For instance, Gram-negative bacilli exercise not typically colonize intact epithelium due to the aridity of the peel.67 In all of these studies examining microbial species in pressure ulcers affecting individuals with SCI, the wounds are typically poorly characterized with no physical description (i.e. dimensions, the presence of necrosis, etc.) provided. In addition, the impact of local and systemic antibiotics in conjunction with local wound care on bacterial composition has not been adamant. Thus, hereafter studies are needed to assess how wound characteristics, the potential evolution of resistant pathologic strains with systemic antibiotic usage, and routine or more experimental approach to wound care impact the microbiome of pressure ulcers in patients with SCI.
Bacterial composition of pressure ulcers may vary depending on concomitant soft tissue or bone infections. In a report of infected pressure level ulcers (purulent exudate present), the most mutual organisms identified were Enterobacteriaceae, Pseudomonas, Bacteroides, and Streptococcus faecalis, with Staphylococcus less frequently identified.68 Gram-negative bacilli and anaerobes (fecal flora) were most ordinarily identified in infected pressure ulcers with concurrent soft tissue abscesses and osteomyelitis.69,70 Necrotizing soft tissue infections (i.e. myonecrosis, Fournier'due south gangrene, necrotizing fasciitis) are characterized by fulminant and progressive necrosis of fascia, subcutaneous tissue, and/or muscle often with systemic signs of sepsis. Mutual characteristics between necrotizing soft tissue infections in individuals with and without SCI are that the perineal region is virtually often affected, and the infection is typically polymicrobial with every bit many as iv unlike species of leaner identified by routine bacterial methods.71–74 In individuals with necrotizing fasciitis without SCI, streptococcal species was the most common bacteria identified, which were followed by Bacteroides, staphylococci, and enterococci.73 Similarly, in studies of individuals with SCI with necrotizing fasciitis or Fournier's gangrene, streptococci was about usually identified.75 However, P. aeruginosa was as well commonly identified in individuals with necrotizing fasciitis and SCI, an organism non typically identified in individuals without SCI.71,76 Individuals with grade III and form IV pressure level ulcers, characterized past full thickness tissue loss and the presence of not-viable tissue, are at increased run a risk of developing necrotizing soft tissue infections.75,76
Oft, pressure ulcers associated with osteomyelitis are cultured positive for Gram-negative bacilli and anaerobes.27,70 Notwithstanding, bone cultures may differ significantly from wound cultures obtained from the overlying pressure ulcers. In another written report of pressure ulcers associated with osteomyelitis, Sugarman77 constitute that bone cultures often contained fewer organisms than wound culture; the organisms identified from os cultures were oftentimes different than those identified from cultures obtained from the surface of the pressure ulcer, with these cultures institute to be concordant in only 25% of the cases. This work strongly indicates the need for bone biopsies to be performed surgically nether sterile conditions to differentiate skin flora and/or the more superficial infection from the offending organism that is responsible for the osteomyelitis, which will then ensure initiation of the appropriate antibiotic coverage.
In that location are many factors that may influence the microbial ecology of chronic wounds. The bear on of each of these factors is difficult to appraise given that each study has varying aims and methodologies. The power to compare the studies presented in this review was limited due to lack of wound clarification, including those of size, location, presence of necrosis and/or malodor, underlying osteomyelitis, and staging. In addition, sampling, bacteriological, and reporting methods were non standardized. These studies likewise differed in the number of cultures per ulcer procured and the number of wounds studied per patient. The data were, in part, skewed due to differences in the aims of the studies, and thus differences in methodology employed (i.e. bacteriology of pressure ulcers were reported only if congruent with blood cultures in bacteremic patients, exclusion of the reporting of pare commensals, lack of anaerobic data, as well equally other factors). Yet, despite these limitations, information technology is apparent that our agreement of the wound microbiome in pressure ulcers of individuals with SCI is rudimentary.
Conclusions
In general, the characterization of bacterial presence as colonizing bystanders vs. invasive pathogens that impede wound healing in chronic force per unit area ulcers is non well divers. Depending on the bacterial species present in a wound, both beneficial and detrimental furnishings take been associated with wound colonization.19 In addition, the concept of bacterial pathogenicity is evolving from identification of a single species of leaner that cause illness to defining microbial ecologies that influence health states, although the clinical value of this more than global microbiological arroyo to pressure ulcer care has not been proven. Previously standard culture methods accept been used to define the microbial environment of wounds, but typically only several species of bacteria are identified using this methodology due to inherent limitations of growing bacteria in cultures. Unfortunately, <1% of bacterial species tin can be identified by culture technique using routine laboratory conditions.78 Recent molecular studies take shown that the microbiome of wounds is far more than complex than previously thought.32,35,79–81 With the advent of molecular assay, vast numbers of different bacterial species are being identified within a single wound.
At that place are many questions that still remain to be addressed. Does the diversity of the cutaneous microbiome influence the microbial environmental and pathogenicity of a wound? Do certain populations of leaner provide any do good to the healing of a wound, i.eastward. probiotics? How does the complexity of bacterial surroundings influence the local host immune responses? Are the physical characteristics of a wound and/or its anatomic location predictive of a predominant organism, or vice versa? Tin identification of a wound'due south microflora predict concomitant or future development of soft tissue or bone infection? Studies using molecular methods to identify the microbial diversity of pressure ulcers in correlation with wound physical characteristics, anatomic location, and stage of healing are needed to understand the impact of different species of bacterial colonization.
The role of routine bacterial culture is unclear given the lack of standard methods of collection and interpretation of culture data. Understanding changes in the microbiome of a wound before and later systemic antibiotics or surgical debridement will assist to place successful treatment approaches to wound healing. Does the administration of topical and/or systemic antibiotics adversely affect the microbial flora in a wound with the emergence of antibody-resistant organisms that then have deleterious impact on wound healing? For instance, Price et al. 32 demonstrated that recent antibody use was associated with increased wound colonization with Pseudomonas bacteria. Depending on the answers to these questions, the clinical approach to chronic wounds may alter apropos appropriateness of the apply of topical anti-microbial agents and/or systemic or local antibody therapy, aggressiveness of debridement (available evidence would propose the vigorous removal of necrotic tissue), and the awarding of various physical adjunctive therapies, such equally negative pressure, electric stimulation, ultraviolet or laser, hyperbaric oxygen, or ultrasound.
A more comprehensive evaluation of pressure level ulcers and the bacteria that inhabit the wounds in individuals with SCI is needed to improve our insight into the consequence of colonization or pathogenic leaner equally it relates to the charge per unit of wound healing and associated complications, also every bit consideration of the effect of current approaches to wound care on microflora and the generally recognized pathogenic species of organisms.
Disclaimer statements
Contributors All authors contributed equally.
Conflicts of interest None.
Ethics approval None required.
Funding Support for this work was provided past the James J. Peters Veterans Affairs Medical Center and the Section of Veterans Affairs Rehabilitation Enquiry and Development Service (#B2468-C, #B4162-C) and the James J. Peters Veterans Affairs Medical Center.
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