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Risk Factors for Surgical Site Infection in Minor Dermatological Surgery

A Systematic Review

Delpachitra, Meth Ruvinda, MBBS (Hons), BMedSci (Hons); Heal, Clare, PhD, MBChB, DRANZCOG, DipGUMed, FRACGP, MPHTM; Banks, Jennifer, PhD, MBS, BBS; Divakaran, Pranav, MBBS; Pawar, Mrinal, MBBS

Advances in Skin & Wound Care: May 2019 - Volume 32 - Issue 5 - p 217–226
doi: 10.1097/01.ASW.0000546118.25057.1a

OBJECTIVE: To identify patient- and procedure-related risk factors for surgical site infection following minor dermatological surgery.

DATA SOURCES: The MEDLINE, Cumulative Index of Nursing and Allied Health Literature, Informit, and Scopus databases were searched for relevant literature on patient populations receiving minor surgery, where risk factors for surgical site infection were explicitly stated.

STUDY SELECTION: Studies involving major dermatological surgery were excluded. The preliminary search yielded 820 studies after removing duplicates; 210 abstracts were screened, and 42 full texts were assessed for eligibility. A total of 13 articles were included. Studies were appraised using the Newcastle-Ottawa Quality Assessment Scale.

DATA EXTRACTION: An electronic data collection tool was constructed to extract information from the eligible studies, and this information was distributed to participating authors.

DATA SYNTHESIS: Risk factors identified included age, sex, diabetes mellitus, chronic obstructive pulmonary disease, use of antihypertensive or corticosteroid medications, smoking, surgery on the lower or upper extremities, excision of nonmelanocytic skin cancers, large skin excisions, and complex surgical techniques. No more than two studies agreed on any given risk factor, and there were insufficient studies for meta-analysis.

CONCLUSIONS: Re-excision of skin cancer, below-knee excisions, and intraoperative hemorrhagic complications were predictive for infection in more than one study. More high-quality studies are required to accurately identify risk factors so they can be reliably used in clinical guidelines.

At the James Cook University College of Medicine and Dentistry in Brisbane, Queensland, Australia, Meth Ruvinda Delpachitra, MBBS (Hons), BMedSci (Hons), is a Resident Medical Officer (Royal Brisbane & Women’s Hospital); Clare Heal, PhD, MBChB, DRANZCOG, DipGUMed, FRACGP, MPHTM, is Professor of General Practice and Rural Medicine; Jennifer Banks, PhD, MBS, BBS, is Senior Research Officer; Pranav Divakaran, MBBS, is a Resident Medical Officer (Mackay Base Hospital); and Mrinal Pawar, MBBS, is a Resident Medical Officer.

Acknowledgments: The authors thank Mr Stephen Anderson for his assistance with systematic literature searches. The authors have disclosed no financial relationships related to this article. Submitted November 14, 2017; accepted in revised form May 14, 2018.

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Surgical site infection (SSI) following dermatological surgery is associated with prolonged wound healing, lengthened recovery time, poor cosmesis, and overall increased costs to the health system.1 Both patient and clinician concerns regarding these adverse outcomes result in an anticipatory safety net of inappropriate antibiotic prophylaxis, which promotes undesirable antibiotic resistance.2 A key recommendation from the antibiotic stewardship guidelines from the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America is that antibiotic therapy should be based on patient-specific factors.3 Therefore, an ability to differentiate patients who are at higher risk of SSI is necessary to encourage more judicious antibiotic prescribing.

To accurately define patient groups predisposed to developing an SSI, a comprehensive understanding of patient, procedural, and provider risk factors is necessary. Extensive clinical studies have investigated these risk factors in small to large cohorts; however, few studies have presented a large systematic review of all possible risk factors that contribute to an individual’s overall risk of infection.

This review aims to systematically appraise the current evidence of risk factors for SSI in minor dermatological surgery and identify where further research may be required.

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The study was registered in the PROSPERO international prospective register of systematic reviews (ID CRD42016045830).

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Eligibility Criteria

Two eligibility criteria were applied in this review. The first was based on a population, intervention, comparison, and outcome (PICO) strategy (Table 1). Eligible articles examined populations of patients undergoing minor dermatological surgical procedures (from 1990 onward) and described relevant risk factors for SSI in sufficient detail for data extraction.

Minor dermatological surgery was defined as any small surgical procedure carried out on the skin in an outpatient setting. The definition did not account for the size of the lesion excised. Although skin flaps could be considered to be a more complex surgery, they were included because they are often carried out in a primary care outpatient setting in Australia. Graft and Mohs procedures were included if they were a component of a study that included simple skin excisions, but data on individual procedures could not be extracted. Major surgeries (which were excluded) were defined as larger plastic surgery procedures such as mammoplasties, abdominoplasties, and gluteoplasties, as well as burns, graft procedures, and major oncological surgeries involving structures other than the skin (eg, removal of head and neck cancer).

The second criterion regarded the study design. Only cohort or case-control studies in the English language were eligible for inclusion. Interventional studies, case studies, commentaries, letters, editorials, and reviews were excluded. Randomized controlled trials were included only when the authors performed a secondary data analysis to define risk factors for SSI.

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Information Sources

The Ovid MEDLINE, Cumulative Index of Nursing and Allied Health Literature, Scopus, and Informit databases were searched to identify relevant literature, from January 1, 1990, to the date of search. The search was conducted in May 2016, and repeated in August 2017. Reference lists of identified articles were also searched for additional studies.

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A search strategy based on the PICO format described in Table 1 was used, using the search terms “dermatological surgical procedures,” “minor surgical procedures,” “surgical wound infection,” “skin neoplasms,” “plastic surgery,” and variations (as suggested by the MESH headings), combined with Boolean search terms “AND” and “OR” as appropriate. Specifiers within each term’s subject tree were used to narrow down the search. The MESH terms and their alternative terms were used in databases that could not be searched using subject headings.

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Study Selection

Following removal of duplicates, title scanning for relevance resulted in the removal of a number of articles from consideration, whereas titles that were ambiguous were included for abstract screening. The remaining abstracts were then perused to identify articles relevant to the topic, followed by full-text screening, using the PICO criteria described in Table 1. An author and two independent assessors screened all articles.

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Data Collection Process

A data collection tool was constructed to extract information from the eligible studies. This tool comprised the following fields: “author,” “year,” “country,” “study type,” “population,” “setting,” “sample size,” “methods used,” “surgical procedures done,” “definition of infection,” “infections,” “risk factors for infection,” “secondary outcomes,” “key conclusions,” and “source of funding.’ Infections were expressed as absolute and relative frequencies.

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Risk of Bias in Individual Studies

Articles were evaluated with the Newcastle-Ottawa Quality Assessment Scales to determine the quality of each study. Those found to be of low quality were interpreted with caution.

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Summary Measures

The ideal summary measure for this review was relative risk (RR). If RR was not available, then odds ratios (ORs) were presented. If neither was available, proportions of infection in each risk factor group were presented, with confidence intervals (CIs) and statistical significance if available.

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Synthesis of Results

The risk factors identified were highly variable and expressed via different summary measures, so a meta-analysis was not performed because of the heterogeneity of the data.

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Study Selection

The literature search retrieved 892 articles. Following elimination of 72 duplicates, 610 articles were excluded after title screening. Abstracts of the remaining 210 eligible articles were reviewed, and 42 full texts were screened. A total of 13 studies were included. The full screening process is presented in the Figure.



Table 1

Table 1

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Study characteristics and results of individual studies have been combined into one single section below.

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Risk of Bias Within Studies

The quality of the studies is presented in Table 2. Only one quality assessment scale was required. Most studies were representative of the “true exposed cohort” because they followed all patients from the start of the study until its endpoint and excluded patients only if they significantly altered the results (ie, were already taking antibiotics).

Table 2

Table 2

The main source of bias arose from assessment of the primary outcome. The diagnosis of SSI is subjective, and although several different definitions exist, there is a need for a more validated, reliable, and standardized definition of SSI.4 For this review, the Centers for Disease Control and Prevention (CDC) criteria for SSI were used because they are currently considered to be the criterion standard, although still prone to subjectivity.5 The time period involved for defining infection varied among studies from time of hospital discharge to time of suture removal, or 30 days after operation (the CDC guidelines use up to 30 days). Further, in all but one study, the outcomes were self-reported either by the investigators or a separate clinician. The study that did not self-report outcomes enlisted a pathologist to blindly report whether infection was present in laboratory results.6

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Results of Individual Studies

Results of individual studies are summarized in Table 3. Two studies consisted of total procedures rather than total patients, which raised the issue of having multiple wounds per patient. These studies are marked accordingly in Table 3.

Table 3

Table 3

Infection rates ranged from 1.3% to 27.0%, but the overall incidence of infection was low. Exceptions were studies carried out in general practice settings in Australia and another study with a small sample size.7–9 Demographic, social/environmental, medical, preoperative, and intraoperative risk factors were described in the studies. Only two articles reported their results with an RR.

Demographic Factors. Only one study of 1,000 patients reported older age (>50 years) as a risk factor (OR, 5.5; 95% CI, 1.9–16.0).10 Men had a higher risk of infection than women in the same study (OR, 5.1; 95% CI, 1.7–15.9) and in another large prospective study when reconstructive procedures were involved (OR, 5.46; 95% CI, 1.12–26.54; P = .04).10,11

Patient Medical Comorbidities. A large hospital study found diabetes mellitus (OR, 2.54; 95% CI, 1.10–5.87; P = .03) and chronic obstructive pulmonary disease (COPD; OR 2.52; 95% CI, 1.06–5.97; P = .04) were significantly associated with infection.12 A smaller general practice study in Australia also found that diabetes mellitus predisposed to infection (RR, 1.7; 95% CI, 1.4–2.2; P < .001).7

Medication-/Treatment-Related Factors. Use of antihypertensives was associated with infection (OR, 2.5; 95% CI, 1.4–4.2; P = .006) in a large Australian study. A small British study (with a high infection rate) found 63% of patients on corticosteroids developed an infection compared with 21% who were not taking the medication (95% CI difference, 19%–66%; P < .001).9

Smoking. Ex-smokers were found to have a higher risk of infection in a general practice setting (RR, 1.7; 95% CI, 1.1–2.6; P = .02).8 In a small prospective hospital study, 63% of smokers developed an infection compared with 12% of nonsmokers (95% CI difference, 34%–70%; P < .001).9

Location of Lesion and Surgical Site. Procedures below the waist were associated with an increased risk of SSI. In one study, 48% of patients who had a “below-waist” procedure developed an infection, compared with 23% of those who received their procedure above the waist (95% CI difference, 4%–47%).9 In general practice, there was a higher risk of infection in procedures on the thighs (RR, 2.2; 95% CI, 1.3–3.6; P = .002) and legs/feet (RR, 1.9; 95% CI, 1.1–3.1; P = .02) in one study,7 and “lower extremities” (RR, 3.7; 95% CI, 1.9–6.9; P < .001) in the other.8 A private hospital study reported similar findings, as 6.92% of their surgical wounds below the knee (P < .001) and 10% around the groin (P = .03) became infected.13 An American study supported these findings, with procedures on the leg having increased odds of infection (OR, 4.28; P = .03).6

The trunk (OR, 4.49; P = .005), scalp (OR, 4.33; P = .01),6 and upper extremities (RR, 3.2; 95% CI, 2.3–4.4; P < .001) were high-risk surgical sites for infection.8 A smaller study also found 6.5% of patients receiving surgery on the nose and 5.2% on the ear developed an infection, with no statistical inference.

Surgical Factors: Complexity and Size of Procedure. The type of procedure was reported to be a significant risk factor. In a private surgery setting, 8.57% of patients receiving wedge resections (lip/ear) and 8.7% of patients receiving graft procedures developed an infection (P < .001).13 Flap repairs had the highest proportion of infections (15.5%; P < .001) in another private, surgery-based study in Australia.14 This finding was supported by a small German study (P = .009); however, this result was not quantified.15 “Complex surgical wounds” (flap and graft procedures) were also risk factors for infection in a British study.16

The same study found excisions larger than 20 mm in length conferred an increased risk of infection (RR, 2.4; 95% CI, 1.7–3.4; P < .001). In a small study of 100 patients, 7.5% of patients who had an excision larger than the median defect length (>30 mm) developed an infection, compared with 1.4% in the group without this exposure.

Histology of Lesion. Excision of nonmelanocytic skin cancers (NMSCs), specifically squamous cell carcinomas (SCCs) and basal cell carcinomas (BCCs), were risk factors. This finding was demonstrated in two studies performed in a general practice setting, with one study reporting a higher risk of infection if a BCC (RR, 2.1; 95% CI, 1.3–3.4; P = .004) or SCC (RR, 1.8; 95% CI, 1.3–2.6; P < .001) was excised.7 The second study found that, conversely, SCC excisions (RR, 2.3; 95% CI, 1.1–4.6) held a higher risk of infection compared with BCC excision (RR, 2.1; 95% CI, 1.4–3.2; P = .001), both posing a significant risk compared with those who were not having an NMSC excised.8 Another study reported a 12.0% infection rate in a population undergoing skin cancer removal, compared with 0.8% in those who underwent non–cancer-related procedures.16 Re-excision of skin cancer was also strongly predictive of infection (RR, 14.8; 95% CI, 4.5–28.5; P < .001).8

Hemorrhagic and Anesthetic Complications. Hemorrhagic complications were uncontrolled bleeding around the time of surgery or development of a hematoma shortly after, and anesthetic complications comprised vasovagal syncope, clinical signs of drug reaction, or neurological signs of overdose. One study found both hemorrhagic (OR, 7.59, 95% 3.95–14.61; P < .001) and anesthetic complications (OR, 4.58; 95% CI, 1.61–13.00; P < .004) carried increased odds of infection.17 Another study carried out separate analyses for reconstructive procedures and simple excisions, and hemorrhagic complications were a risk factor for infection in both (ORs, 11.29 [95% CI, 3.43–37.16; P < .001] and 6.6 [95% CI, 2.52–17.30; P < .001], respectively).11

Other. Receiving preoperative radiotherapy (OR, 20.35; 95% CI, 5.37–77.17; P < .001) and the insertion of a surgical drain (OR, 3.02; 95% CI, 1.64–5.57; P < .001) were associated with increased odds of developing an infection in one Italian study.12 In an audit article, 28.5% of patients whose surgery involved the cartilage developed an infection, compared with 5.9% of the group where the surgery was above the level of the cartilage. Mohs surgery on the ear was also a risk factor, (12.5% vs 1.45% in the “nonear” group).18 One of the studies carried out in a private surgical setting in Australia found ulceration of the wound/lesion was a risk factor (OR, 3.15; 95% CI, 1.8–5.7; P = .008), as was keeping the wound dry (OR, 2.1; 95% CI, 1.1–3.8; P = .018).14 A small British study reported that the location of the operation (53% infected in ward vs 17% in operating theater; 95% CI, difference 17%–55%; P < .001) and experience of the surgeon were associated with infection (33% infected in patients operated on by senior house officer and 14% operated on by a specialist registrar and consultant [95% CI difference 2%–37%; P = .03]).9

Aseptic Technique. The use of nonsterile gloves was identified as a risk factor for infection (OR, 0.18; 95% CI, 0.05–0.65; P = .009) in a French study with the OR in favor of sterile gloves, but only in a subgroup of more complex procedures.11

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This systematic review identified 13 articles that measured risk factors for SSI in minor dermatological surgery. Two studies were assessed to be of high quality, two were moderate-high, two moderate, four low-moderate, and three studies were of low quality.

Although study settings varied from outpatient clinics/examination rooms to hospital operating theaters, it is difficult to assess whether this had an impact, because data heterogeneity did not allow us to analyze infection by setting. The one study that formally assessed this was underpowered and of poor quality.9

Although no restrictions were placed on the country of origin, all included articles were published in developed Western countries. Surgical site infection is low after dermatological surgery as evidenced in this review and associated with low morbidity and mortality. Indeed, the applications of this study are more concerned with improving outcomes relevant in Western settings, such as costs to the health system, maintaining cosmetic appearance, and antibiotic resistance. Such issues are minor in comparison to the more pressing public health concerns in developing countries.

Infection rates in most studies were between 1% and 5%, consistent with the CDC-accepted rate of infection following clean minor surgery (<5%).19 Exceptions were three Australian studies, conducted in a tropical setting, reporting infection rates between 7.25% and 8.70%.

Only one study identified age older than 50 years as a risk factor on multivariate analysis; however, a direct relationship is unlikely because of the number of confounding factors associated with older age that might lead to vascular compromise, poorer wound healing, and greater risk of infection. Male sex was a risk factor in two low-moderate quality studies with large sample sizes.10,11 This relationship has been identified in nondermatological studies20 and is likely because of inherent health behaviors and practices of males regarding wound care and postsurgical management.

Although two large studies demonstrated that diabetes mellitus was a risk factor, the authors of the latter study confirmed that this parameter was underrecorded.7,12 Diabetes mellitus may be associated with infection because of its immunological and vascular complications.21 However, the sparsity and poor level of evidence across the dermatological literature make it difficult to draw any definite conclusions in this population. Further, COPD is a plausible risk factor because affected patients have impaired innate immunity.22 It is also possible that COPD is associated with infection because of the inherent risks of smoking (see below) and concomitant steroid use.

Antihypertensive medication and corticosteroid use were also risk factors.13 The immunosuppressive effects of corticosteroid use are well recognized in the medical literature; why antihypertensive medication predisposes patients to wound infection is less clear. Because Penington14 did not control for medical comorbidities, it is possible that underlying vascular defects (causing hypertension) were responsible for impaired wound healing. Hypertension itself (rather than the use of antihypertensive medication) is a possible risk factor in nondermatological surgery populations.23

The effect of smoking on SSI is contentious. Although generally believed to be a contributor to infection because of its adverse effects on perfusion, coagulation, capillary oxygen transfer, and collagenesis,24 only two studies reported an association. One study had poor methodology, and the other claimed that the status of “ex-smoker” rather than “current smoker” conferred an increased risk. This result should be interpreted with caution, however, because the time between quitting smoking and involvement in the study was not specified, and it is unclear how having previously smoked would impart a greater risk of infection than being a current smoker.

Several studies identified an increased incidence of infection when procedures were performed on the extremities of the upper and lower limbs (particularly below the knee). Procedures on the ear and nose were also more likely to become infected. Although facial wounds have a lower infection rate because of high vascularity,16 sites such as the ear and nose have been previously noted as high-risk areas for infection because of increased moisture and higher concentrations of local flora and sebaceous glands.25 It is likely that the higher risk of infection in the extremities is also attributable to the reduced perfusion at these locations, implying a substandard healing process compared with a wound with ample perfusion.

The impact of the type of the procedure was similarly well documented. The high rates of infection after flap and graft procedures are plausible because of the degree of skin damage inflicted. Flap surgery is a larger and more complex procedure compared with a simple skin incision, and although designed to reduce wound tension, it still has a higher overall tension compared with smaller closures, making it more susceptible to breakage and opening.26 Skin grafts are required for wounds too large to be closed by simple techniques; however, unlike flap surgery, grafted skin lacks adequate blood supply. The authors of the present review postulate that with more complex wound closure and compromised blood flow comes higher risk of wound reopening and poor vascular access, creating a portal for infection as well as an ideal environment for bacterial growth. This may clarify why wound size was also a significant risk factor for infection.

Excisions of SCCs and BCCs were risk factors for infection in several studies.7,8,16 As NMSCs are often excised from the nose and ear,27 it is possible that it is the location on which NMSCs arise that have a higher risk of developing wound infection, rather than the lesion itself. However, BCC and SCC were still a risk factor when body site was controlled on multivariate analysis, and it is likely that oncological surgery is itself a risk factor, possibly because of the increased risk of ulceration and the viability of surrounding skin.

Hemorrhagic complications were associated with developing an infection in two studies, as was an anesthetic complication. Hemorrhagic complications during surgery might indicate a deeper underlying pathology causing abnormal bleeding, and this may be the indirect cause of increased risk. Failure to execute a normal inflammatory response followed by rapid tissue remodeling after a surgical injury could therefore provide ideal environmental conditions for bacterial colonization and subsequent SSI. Why anesthetic complications increase infection risk is unclear but may be a result of favoring resuscitative action (to manage syncope, drug reactions, or overdose) over aseptic technique. However, such risk factors are not relevant in the outpatient setting in which minor dermatological surgery is typically performed.

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This review had several limitations. Wound infection is a subjective diagnosis and subject to intra- and interobserver variability.28 Standardized diagnostic criteria exist,5 although many studies did not use them. Second, few studies examined the same risk factors. This also meant that a meta-analysis was not possible because of the heterogeneity of the data collected. It would be preferable to study more risk factors pertaining to the patient and staff, preoperative skin preparation, and other intraoperative variables; however, this review was limited by the variables presented in the studies collected. Last, although this review was limited to the English language, including other articles would have only increased findings by one study.

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Identifying risk factors for SSI guides evidence-based and judicious antibiotic prophylaxis. This systematic review aimed to comprehensively present the current known risk factors for SSI following minor dermatological surgery.

The risk factors identified were re-excision of skin cancer, below-knee excisions, lesion histology, developing a hemorrhagic complication during surgery, and receiving preoperative radiotherapy; that said, the latter two of these risk factors may not be relevant to the outpatient setting in which most minor dermatological surgery is performed.

The results of this review promote assessing patient risk factors for SSI when considering potential candidates for prophylaxis, although the low power of the studies involved highlights the need for larger and adequately powered studies in this field. It is hoped that the results of this study will encourage further research regarding risk factors for SSI to contribute to clinical practice guidelines regarding antibiotic prophylaxis.

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dermatological surgery; dermatology; minor surgery; Newcastle-Ottawa Quality Assessment Scale; risk factors; SSI; surgical site infection; wound infection

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