key: cord-0762858-lqf383dl
authors: Sahtoe, Anouschka P.H.; Duraku, Liron S.; van der Oest, Mark J.W.; Hundepool, Caroline A.; de Kraker, Marjolein; Bode, Lonneke G.M.; Zuidam, J. Michiel
title: Warm Weather and Surgical Site Infections: A Meta-analysis
date: 2021-07-27
journal: Plast Reconstr Surg Glob Open
DOI: 10.1097/gox.0000000000003705
sha: 9f93be594c17ea107704398159759be86c82e5ff
doc_id: 762858
cord_uid: lqf383dl

Seasonal variability, in terms of warm weather, has been demonstrated to be a significant risk factor for surgical site infections (SSIs). However, this remains an underexposed risk factor for SSIs, and many clinicians are not aware of this. Therefore, a systematic review and meta-analysis has been conducted to investigate and quantify this matter. METHODS: Articles were searched in Embase, Medline Ovid, Web of Science, Cochrane Central, and Google Scholar, and data were extracted from relevant studies. Meta-analysis used random effects models to estimate and compare the pooled odds ratios (OR) and corresponding confidence intervals (CIs) of surgery performed during the warmest period of the year and the colder period of the year. RESULTS: The systematic review included 20 studies (58,599,475 patients), of which 14 studies (58,441,420 patients) were included for meta-analysis. Various types of surgical procedures across different geographic regions were included. The warmest period of the year was associated with a statistically significant increase in the risk of SSIs (OR 1.39, 95%CI: [1.34–1.45], P < 0.0001). Selection of specific types of surgical procedures (eg, orthopedic or spinal surgery) significantly altered this increased risk. CONCLUSIONS: The current meta-analysis showed that warm weather seasons are associated with a statistically significant risk increasement of 39% in developing SSIs. This significant risk factor might aid clinicians in preoperative patient information, possible surgical planning adjustment for high risk patients, and potentially specific antibiotic treatments during the warmer weather seasons that could result in decrease of SSIs.

Surgical site infections (SSIs) are a common complication of surgery and hospitalization, occurring in 2%-5% of patients undergoing surgical procedures in the United States, and representing 160,000 to 300,000 SSIs each year. [1] [2] [3] [4] The definition of SSIs are infections located at or near the area of incision and/or deeper underlying tissue spaces and organs which present within 30 days, or when prosthetics are implanted, 90 days postoperatively. 5 SSIs are becoming more common and more challenging to treat due to the number of surgical procedures being performed worldwide, more complex comorbidities of our patients, and the rise of antimicrobial resistance in pathogens. 6 Consequently, the growing incidence of SSIs leads to a substantial increase in healthcare costs, accounting for the third most costly healthcare-associated infection, with estimated mean attributable costs ranging from $10,443 to $25,546 per infection in the United States. [7] [8] [9] [10] [11] [12] Costs can exceed up to $90,000 per infection when SSIs involve prosthetic joint implants or antimicrobial resistance. [13] [14] [15] [16] Seasonal variability, in terms of warm weather, has been shown to be a significant risk factor for SSIs with an odds ratio (OR) of up to 2.16. 17, 18 When compared with other well-known risk factors like preoperative weight loss more than 4.5 kg (OR 2.12), diabetes mellitus (OR 1.53), emergency operations (OR 2.05), and blood loss (EBL) more than 600 ml (OR 2.23), seasonal variability remains a major contributor. [19] [20] [21] A recent cohort study that investigated the seasonal impact on surgical-site infections in body contouring surgery showed that seasonal variability had a more significant impact on SSIs than age, duration of surgery, hospitalization time, BMI, and smoking. 22 Proposed theories explaining the association between warmer weather conditions and SSIs are increased colonization of pathogens like Staphylococcus aureus, increased skin-to-skin contact with a higher transmission chance, and skin disruptions (ulcers and sores), which are more common in the summer. [22] [23] [24] Despite the multitude 17, [25] [26] [27] of proposed studies that show the significance of seasonal variability as a risk factor for SSIs, many clinicians are not aware of this association. Consequently, patients are not informed of this increased risk especially for the elective planned surgical cases. Therefore, our main goal was to first conduct a systematic review and investigate how significant the impact of seasonal variability on SSIs is and subsequently perform a meta-analysis to quantify this association. Second, we investigated if a specific type of surgery was more prone to SSIs during the warmer weather conditions. Third, we described the relationship between warmer weather conditions and type of microbial pathogen causing SSIs. By understanding the magnitude of the effect and the specific microbial pathogens involved, we aimed to create more awareness among clinicians, possibly producing additional preoperative patient information, adjusted surgical planning of high-risk patients, and administration of potentially specific antibiotic treatments during the warmer months. Through this, we aim to achieve a decrease in SSIs. The Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) guidelines were followed, and the checklist is available in the online supplements of this article. (See SDC1B. http://links.lww.com/PRSGO/B713.) 28 

Two reviewers (APHS and LSD) performed a manual secondary selection based on the following inclusion criteria for our primary and secondary outcome measures. The reviewers screened titles, abstracts, and full-text articles reporting potentially eligible studies. Differences between reviewers were resolved by consensus. Eligibility criteria were formulated to select articles with comparable, preferably standardized, measures of seasonality (Table 1) .

The two reviewers independently extracted the following data from each article using a standardized study form: (1) study information; (2) patient characteristics;

(3) climate information according to geographic location; (4) primary outcomes, including data for calculating risk of SSIs during the warmest period of the year compared with the colder period of the year; (5) secondary outcomes, including data on types of microbial pathogen cultured from SSIs during the warmest period of the year compared with the colder period of the year (Table 2) .

Bias was assessed using the Newcastle-Ottawa scale for assessing the quality of nonrandomized studies in meta-analyses. 43 

Our primary aim was to analyze the risk of SSIs during the warmest period of the year compared with the colder Thirdly, we analyzed the incidence of different types of microbial pathogen cultured from SSIs during the warmest period of the year compared with the remainder of the year. Therefore, the corresponding OR or prevalence rate ratio (PRR) was extracted when available.

A systematic literature search in databases (such as Embase.com, Medline Ovid, Web of Science, and Cochrane Central) and Google revealed a total of 1733 articles. After automated removal of 510 duplicate articles, 1223 articles remained. After screening the article abstracts, a total of 1191 records were excluded, with the following reasons: no research regarding the association between change in weather conditions and incidence of SSIs, change in weather conditions did not demonstrate a seasonal pattern, the language was other than English, the title referred to a conference abstract. The remaining 32 full-text articles were then reviewed. After exclusion of 12 full-text articles (with reasons of no data regarding the influence of seasonality on the incidence of SSIs was found, and the term "seasonality" did not refer to factors regarding climate), a total of 14 articles remained to be included in quantitative synthesis. There was a low risk of bias in the individual articles. (See SDC 1, Appendix 5. http://links.lww.com/PRSGO/ B713.) Six articles were excluded from meta-analysis, because of insufficient data regarding calculation of risk of SSIs during the warmest period of the year compared with the colder period of the year. 33, 34, [37] [38] [39] [40] Only 14 studies described an OR or provided sufficient data to include in the meta-analysis. 17, 18, 22, [25] [26] [27] [29] [30] [31] [32] 35, 36, 41, 42 ( Table 2) . Most studies were conducted in the Northern Hemisphere, mainly in North America, with climate conditions divided into four distinct seasons (summer, fall, winter, and spring). The number of included patients varied greatly across studies, ranging from 602 to 55,665,828 patients. Several surgical procedures were described, namely orthopedic surgery procedures, spinal surgery procedures, plastic surgery procedures, colorectal surgery procedures, and cataract surgery procedures. The most common type of surgical procedure was orthopedic arthroplasty surgery. Two articles (by Duscher Of the articles included for meta-analysis, four articles regarding orthopedic surgery procedures reported arthroplasties only. 17, 29, 31, 32 Another article reported orthopedic foot and ankle surgery, but the specific type of surgical procedure was not mentioned. 30 Concerning one article by Anthony et al, the results were divided according to the type of arthroplasty, namely total hip arthroplasty and total knee arthroplasty. 17

The risk of SSIs during the warmest period of the year was compared with the coldest period of the year in nine studies and the remainder of the year in five studies. For meta-analysis, the coldest period of the year (nine studies) and the remainder of the year (five studies) were both included in the category named "the colder period of the year." Meta-analysis using a random-effects model, without Hartung and Knapp correction, showed that SSIs are more common during the warmest period of the year, when compared with the colder period of the year (OR 1.39, 95% CI: [1.34-1.45], P < 0.0001) (Fig. 1) .

Subgroup analysis focusing on the comparison between patients receiving orthopedic surgery (which mainly regarded arthroplasties) versus patients receiving other types of surgery showed that the association between warmer weather conditions and a higher incidence of SSIs was significantly less common among 2,098,863 patients receiving orthopedic surgery (P = 0.029) (Fig. 2) . Adversely, subgroup analysis, focusing on the comparison between patients receiving spinal surgery versus patients receiving other types of surgery, showed that the association between warmer weather conditions and a higher incidence of SSIs was significantly more common among 114,697 patients receiving spinal surgery (P = 0.003) (Fig. 3) .

The PRR of different types of bacteria, namely gram positive cocci and gram negative rods, cultured from SSIs during the warmest period of the year compared with the remainder of the year could be extracted from two articles by Durkin et al. 25, 26 One article by Gross et al 40 reported the ORs of gram positive cocci cultured from SSIs during summer, fall, and winter, all compared with the same reported during spring. The low number of articles reporting on microbial pathogen cultured from SSIs precluded statistical analyses of pooled data. Therefore, no meta-analysis was performed.

Of a total of 5398 SSIs among the three aforementioned articles, gram positive cocci were isolated from 3243 SSIs (60%). 25, 26, 40 Gross et al reported gram positive cocci to be cultured from 40.8% of all infections. Concerning the overall incidence of SSIs, the article reported inflatable penile prosthesis (IPP) infections to be more common in IPPs placed during spring (29%) and summer (27%) months when temperature tends to be higher than 55°C, when compared with those during fall (26%) and winter (18%). Infected implants performed in the fall and summer were over three and 2.3 times, respectively, more likely to grow gram positive cocci compared with implants performed in spring (P = 0.004; P = 0.039). The study reported an OR of 3.14 (95% CI: 1.44-6.83, P = 0.004) for gram positive cocci cultured from infections of IPP during fall (52.7%) and an OR of 2.27 (95% CI: 1.04-4.93, P = 0.039) for gram positive cocci cultured from infections of IPPs during summer (44.6%), when compared with during spring (26.2%). The incidence of gram positive cocci cultured from these SSIs during winter (41.5%) was also higher when compared with during spring, with an OR of 1.99 (95% CI: 0.86-4.63, P = 0.11). 40 summer, when compared with those during the remainder of the year. 25,26

We performed a meta-analysis of 58,441,420 patients undergoing different types of surgical procedures during different periods of the year. Summer is a risk factor for developing SSIs. Patients are 39% more likely to develop an infection during the warmest period of the year, when compared with the colder period of the year.

While seasonality of many infections (eg, respiratory infections, tick-and mosquito-borne infections) is considered common knowledge, little attention has been focused on seasonality of healthcare-related infections. 44 Although, some surgical fields extensively studied seasonality of SSIs and different types of microbial pathogen cultured from SSIs, this area remains underexposed, and very little action has been taken to apply this knowledge in the prevention of SSIs. 17, [25] [26] [27] Unlike prior studies, we included a large and more generalized population of patients, undergoing various types of surgery, across different geographic regions, including different climate conditions. Our results demonstrate both statistical and potential clinical significance of this seasonality. As absolute reduction of the amount of surgical procedures performed during warm summer months cannot be expected, healthcare staff should be aware of the increased risk of developing SSIs during this period. We advise this factor to be taken into account regarding surveillance systems and precautionary measures in the prevention and control of SSIs and the timing of elective surgical procedures. Regarding prevention, we suggest extra attention for current measures (ie, preoperative control of comorbidities such as obesity and diabetes mellitus, preoperative antibiotic prophylaxis and screening, and utilizing nasopharyngeal and oropharyngeal swabs in patients at risk for developing SSIs). We also suggest intraoperative strict surveillance, control of patient homeostasis, and postoperative strict compliance to methods ensuring optimal wound hygiene. 45, 46 Also, we recommend that further research on seasonal variations in bacterial colonization of skin and soft tissue, as well as further analyses of the patient population exhibiting this seasonal increase in SSIs, should be performed. 1.56, respectively) . Both display a positive association between the risk of developing SSis and the warmest period of the year. the lowest diamond represents the comparison between both pooled ORs and cis, demonstrating that the positive association between the risk of developing SSis and the warmest period of the year is less common after orthopedic surgery procedures when compared with nonorthopedic surgery procedures as a significant P value is found (OR = 1.39, 95% ci: 1.34-1.45, P = 0.029).

We argue that a better understanding of the association between warm weather conditions and the increased risk of developing SSIs would not only allow prevention of this seasonal increase, but also significantly reduce the corresponding healthcare costs.

Several theories explaining the increase of SSIs during warm summer months have been suggested. These include increased skin-to-skin contact during summer, causing an increase in bacterial transmission and colonization, and the increase in possible portals of entry for bacteria as sores and ulcers have been shown to be more prevalent during summer. [22] [23] [24] One often mentioned theory suggest a higher bacterial colonization rate of skin and soft tissue due to increase in environmental temperature and humidity. 47, 48 Supporting this, Leekha et al performed a systematic review on seasonal variations of S. aureus skin and soft-tissue infections, confirming an association of warm summer months with a higher incidence of infections. 49 of SSIs during all seasons of the year when compared with winter, gram positive cocci were prominently found in SSIs of IPPs placed during fall, followed by SSIs of IPPs placed during summer. Although Gross et al also reported gram positive cocci to display a higher OR during winter when compared with that during spring, this finding was not significant. 40 Also, both articles by Durkin et al reported an increased PRR for SSIs during summer, when compared with the remainder of the year. 25, 26 Furthermore, one article by Durkin et al, regarding different types of surgery, also reported an increased PRR of gram negative rods during the warmest period of the year. 26 Adversely, the other article by Durkin et al, regarding spinal surgery, reported the opposite, but this finding was not significant. 25 We also point out that this article reported on patients undergoing spinal surgery, among whom gram positive cocci, namely S. aureus, is known to be the principal causal agent of SSIs. 50 Our findings suggest the incidence of SSIs increases considerably as soon as winter ends and environmental temperatures start to rise. Concerning the incidence of gram positive cocci found in SSIs, our findings suggest a delayed increase in incidence persisting throughout fall. We found that the seasonal increase in SSIs differs between surgical specialties. In orthopedic surgery more is done to prevent postoperative infection, especially when foreign material is implanted. These surveillance systems and precautionary measures include surgical hand preparation, antibiotic perioperative prophylaxis, use of glycopeptide antibiotics in routine prophylaxis, antibiotic-containing cement for prophylaxis, prophylaxis before dental interventions, screening for S. aureus carriage with subsequent decolonization and preoperative bathing or showering, among others. 51 Our findings show that the increased risk for developing SSIs during warm summer months is significantly lower in patients undergoing orthopedic surgery when compared with patients undergoing nonorthopedic surgery. While this difference may be due to the aforementioned systems and measures, the exact determining factors remain unclear. Adversely, the increased risk for developing SSIs during warm summer months is significantly higher in patients undergoing spinal surgery, when compared with patients undergoing nonspinal surgery. While the continuous expanding complexity and the increasing number of invasive procedures instead of conservative treatment in spinal surgery has been proved to play an important role in the increase of SSIs in general, the exact determining factors of our finding remain unclear and possibly involve an amplification of the aforementioned. 52 Furthermore, when studying current literature, we noticed that the term "seasonality" does not only refer to change in weather conditions, but is also used to describe the "July Effect." This phenomenon refers to the academic year-end changeover and suggests that seasonal increase in SSIs is caused by trainee changeover, due to arrival of inexperienced staff which have higher surgical complication rates. 36, [53] [54] [55] However, studies have shown this to be a false assumption. 25, 32 To substantiate this, studies focused on the difference between teaching and nonteaching hospitals. In teaching hospitals, trainee changeovers take place during specific periods of the year. However, in nonteaching hospitals, arrival of inexperienced staff is not concentrated during specific periods of the year. Durkin et al reported the rate of SSIs following spinal surgery to be higher during summer, while only nonteaching hospitals were included. 25 Rosas et al argued that their finding of periprosthetic joint infections being more common during winter suggests that incoming residents may not be at fault. 32 We also argue that the "July Effect" does not fully explain the seasonal increase in SSIs because studies included in this meta-analysis regard both teaching and nonteaching hospitals, as well as countries where trainee changeover does not take place during warm summer months, thus refuting the "July Effect" as the only cause of seasonal increase in SSIs.

While the individual studies included in this systematic review and meta-analysis do not solely focus on plastic surgery procedures, the importance of our finding to the field of plastic surgery is evident and unavoidable. In addition to plastic surgery procedures, studies included report on surgical procedures regarding bone fractures, prosthetic devices, debridement and deep laceration, all of which are important in the field of plastic surgery. Also, we feel that multiple factors are of importance concerning the cause of the seasonal increase in SSIs found. While operative factors influencing the risk of SSIs in plastic surgery procedures might somewhat differ from other surgical procedures, there is much overlap. Overlapping factors include duration of the surgical scrub, skin antiseptic preparation, length of the operation, antimicrobial prophylaxis, proper ventilation of the operating room, usage of surgical drains, quality of surgical technique, and exposure to hemoglobin. 19 Also, factors such as patient characteristics and physiological states influencing the risk of SSIs are of importance in all surgical procedures.

One of the limitations of this study is the inclusion of surveillance data with limited patient information available. Therefore, we were unable to address multiple known patient-related risk factors, which play a significant role in the development of SSIs. Also, we included surgical procedures with limited information on surgery-related and physiological risk factors for developing SSIs. However, we argue that the variation of studies included for metaanalysis (eg, describing large populations, different types of surgical procedures, and procedures performed in different countries) generate a decreased influence of these factors on the results of this study.

Secondly, the diagnosis of SSIs was not standardized among included articles. SSIs were confirmed either by clinical diagnosis meeting criteria for SSIs according to the CDC guidelines or National Healthcare Safety Network criteria in the United States, or the need for antibiotic treatment, reoperation or revision after wound problems or SSIs. We argue that SSIs were possibly missed or remained undiagnosed, especially when diagnosis of SSIs was based solely on the need for antibiotic treatment, reoperation, or revision after wound problems.

Also, concerning the incidence of SSIs and microbial pathogens cultured from SSIs, there was a variability in the definition of the coldest period of the year. When data on the coldest period of the year were unavailable, data regarding the remainder of the year were used. We argue that this variable definition distorts the outcome, as an exact comparison between the warmest and coldest period of the year would provide a better representation of the association between seasonality and the incidence of SSIs. We recommend further research on this matter, including different factors regarding seasonality (eg, temperature and humidity), comparing all seasons within the concerning geographic area and in search of a threshold temperature regarding the risk of SSIs.

Summer is a risk factor for SSIs. Patients are 39% more likely to develop an infection during warm summer months, compared with the remainder of the year, although the general incidence of 1.9% remains low. This finding differs after selection of orthopedic and spinal surgery procedures and might be caused by gram positive cocci in particular. Due to the absence of trainee changeover during warm summer months in various articles included, we deny the "July Effect" as the only cause of the seasonal increase in SSIs. Instead, our data support the hypothesis of warm weather conditions contributing to a higher rate of SSIs during summer. Based on our analysis, we recommend this factor to be taken into account regarding surveillance systems and precautionary measures in the prevention and control of SSIs and the timing of elective surgical procedures. We also suggest further research should be done on seasonal variations in bacterial colonization of skin and soft tissue, as well as the exact determining factors of the seasonal increase in SSIs.

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