Abstract
Background
There is limited information about the incidence and risk factors of surgical site infections (SSIs) after coronary artery bypass (CABG) surgeries in the Omani population.
Aim
To estimate the prevalence and describe possible risk factors of SSIs after CABG surgeries in Oman.
Method
A retrospective nested case–control design was used to screen 596 patients who underwent CABG surgeries over 2 years (2016–2017) in two tertiary hospitals in Oman. The CDC definition for SSIs was used to identify the infected cases.
Results
Prevalence rate of SSIs was 17.4% and 17.5% in 2016 and 2017, respectively. The most isolated microorganism was Gram-positive bacteria (45.2%). Risk factors of SSIs include female gender (OR = 3.2, p < 0.001), diabetes (OR = 5.83, p < 0.001), overweight or obese (OR = 2.14, p < 0.05) and shaving technique [using razor shaving] (OR = 8.4, p < 0.001). Readmission rate for the case group was 44.2%.
Conclusion
The infection rate of SSIs after CABG surgeries in developing countries, such as Oman, is considerably high. There is an urgent need to establish SSIs preventive program at the national level. Frequent and systematic assessment of infection control practices before and after CABG surgeries is fundamental and priority strategy to prevent SSIs.
Keywords: Surgical site infection, infection prevention, infection control, surveillance
Introduction
Coronary artery bypass surgery (CABG) is considered one of the standard treatment options for coronary artery disease (CAD) since late 1960s and to date (Palmerini et al., 2017). According to the Society of Thoracic Surgeons (STS), more than 400 CABG procedures performed daily in the USA (D’Agostino et al., 2017). However, CABG surgeries are associated with many complications, of which the most commonly reported are surgical site infections (SSIs) (CDC, 2014).
Surgical site infections are increasingly recognized as a serious worldwide public health concern. According to the Centre for Disease Prevention and Control (CDC), SSIs are the second most common infection among surgical patients (CDC, 2014). Surgical site infection is defined as an infection occurs at the surgical incision site or in the implant organ within 30 days after invasive surgical procedure (CDC, 2008).
Previous research showed varying incidence rate of SSIs after CABG surgeries among different countries around the globe. In the USA, the reported rate ranged from 0.37% (Haley et al., 2012) to 3% (Gulack et al., 2018). Compared to Europe, where the overall reported rate is 2.6 (ECDC, 2017), within the Middle East region, the reported prevalence rates ranged from 2.1% in Kuwait (Nair et al., 2019) to 23.3% in Egypt (Hafez et al., 2012).
The impact of SSIs on the healthcare system is tremendous as SSIs are associated with increased mortality rates, length of stay (LOS), readmission and healthcare cost. In the USA, it was estimated that SSIs are contributing to extra 406,730 hospital days with an extra healthcare cost that can reach up to US$ 900 million (De Lissovoy et al., 2009). Further, SSIs were responsible for an increase of readmission by 91,613 readmissions bringing the number of LOS in the hospitals to 521,933 days (De Lissovoy et al., 2009). Although SSI rate has always been considered as a healthcare quality indicator (Biscione, 2009), little information about SSIs is available within Oman. Indeed, there are no previous studies that have reported the incidence and risk factors of SSIs after CABG surgeries in Oman. Therefore, the purpose of this study was to describe the incidence and the associated risk factors of SSIs after CABG surgeries in Oman.
Method
The current study utilized the retrospective, nested case–control design where the cases were identified from an existing well-defined population, with known sample size, and the controls were randomly sampled from the same population (Biesheuvel et al., 2008). The study involved reviewing healthcare medical records for patients underwent CABG surgeries in two referral tertiary hospitals in Oman during the period of 2016–2017. These hospitals are considered the only centres that performed CABG surgeries in Oman until 2016, and to date, only few cases are performed outside these hospitals. Consensus review was used to review all possible patients in the accessible population. Simple random sampling technique was used to select the control group on a base of 1:4 ratios. The study protocol was ethically approved by the participating hospitals as well as by the IRB approval bodies in the institution of the principle investigator.
Case finding method
The data were collected by including all the patients underwent CABG surgeries from the period of 1st of January 2016 until 31st of December 2017 in the participating hospitals. As shown in Figure 1, 613 CABG surgeries were performed during the study period. Non-Omani patients (n = 17) were excluded from the current study based on the assumption that non-Omani patients are mostly self-sponsored patients as compared to Omanis who are covered by the governmental universal health insurance and free of charge healthcare services. This may affect their treatment options and their length of stay. All the remaining patients’ files (n = 596) were screened for evidence of SSI according to the CDC definition of SSIs (CDC, 2008), in which positive wound culture within 30 days of the surgery and/or documented in medical record the diagnosis of incisional SSI by the attending physician and/or documented of purulent drainage from incisional SSI and/or surgical incision is deliberately opened by surgeon were considered the base for the case finding. Positive swab culture results were checked for presence of antibiotic resistance. Documented resistance for two antibiotics or more is considered as multidrug resistance. Therefore, physician’s notes, wound care notes, nursing notes and laboratory findings in the patient’s medical record were critically reviewed for evidences of SSI that match the CDC defection.
Figure 1.
Filtration phases of patients’ medical records.
Data analysis
Data were analysed using SPSS (version 23) statistical software. Descriptive analyses such as frequency, percentage, mean and standard deviation were used to describe the study sample. Mantel-Haenszel Common Odds Ratio Estimate was used to calculate unadjusted odds ratio for possible risk factors, whereas logistic regression analysis was used to calculate the adjusted odds ratio and identify the significant predictors of SSIs. Statistical assumptions such as normality and multicollinearity were examined before conducting the appropriate statistical procedures. Unconditional logistic regression is the typical statistical analysis for unmatched case–control studies (Pearce, 2016; Suárez et al., 2017). With logistic regression, it is possible to estimate the magnitude of the association between the exposure (i.e. risk factors) and the outcome (CLBSIs). Besides estimating the strength of the relationship, logistic regression allows controlling the effect of the confounding variables on the outcome under the study (Suárez et al., 2017).
Results
All medical records of the CABG patients (n = 596) were scanned for the CDC definition and wound culture results. Of the total 104 identified cases, 76.0% (n = 79) were confirmed by meeting the CDC definition as documented in medical record and positive swab culture and the rest cases, 24.0% (n = 25), were identified based on documented physician’s and/or wound care notes, but no evidence of positive swab culture was found in the patients’ medical records. For all positive wound culture cases (n = 79), the infection was also confirmed by the physician’s and or wound care notes. The SSI sites for the case group were as follows: 64 (61.5%) cases were the sternal wound, 34 (32.7%) were the harvesting wound and 6 (5.8%) were both sternal and harvesting wounds.
According to the CDC definition of the SSIs, 59.6% (n = 62) of the SSI were classified as superficial infections, whereas the rest (40.4%, n = 42) were deep tissue infections. A random sample of 404 uninfected cases was selected as the control group resulting in a total sample of 508 patients. For the case group, more than half (61.5%, n = 64) of the patients had only sternal SSIs, 32.7% (n = 34) had leg SSIs and 5.6% (n = 6) had both sternal and leg SSIs. The mean age for the infected patients was 62.3 (SD = 8.6) years, compared to 63.8 (SD = 9.2) for the controls, (p = 0.13). Based on the standard equation, the calculated incidence rate of SSIs was 17.4 and 17.5 per 100 CABG surgeries in 2016 and 2017, respectively.
Most of the patients in the case group (88%) had elective CABG surgeries compared to 94.3% for the control group. Most of the patients (70.2%, 65.8%) were within the age group of 50–69 years for the case and control groups, respectively. Likewise, most of the patients in the case (59.6%) and control groups (81%) were males. Of the total case group, 82.3% were obese or overweighed compared to 60.2% for the control group. More than three quarters (86.5%) of patients in the case group were diabetic compared with less than half (49.1%) of patients in the control group. More than half (61.5%, n = 64) of the infected patients had only sternal SSIs and 32.7% (n = 34) had leg SSIs. Of those infected cases, the majority had at least one antibiotic resistance pathogen (71.1%, n = 74). For the wound management, almost (80%) of wounds were managed with daily dressing and about 4% patients experienced wound debridement in the operating theatre (Table 1).
Table 1.
Sample characteristics and calculated unadjusted odds ratio for possible risk factors (N = 508).
| Variable a | Cases, n =
104 n (%) |
Controls, n =
404 n (%) |
X 2 | Odds ratio | 95% CI | p |
|---|---|---|---|---|---|---|
| Age group, years | ||||||
| <65 | 58 (55.8) | 209 (51.7) | 0.54 | 0.85 | 0.55–1.30 | 0.500 |
| ≥65 | 46 (44.2) | 195 (48.3) | ||||
| Gender | ||||||
| Male | 62 (59.6) | 327 (80.9) | 21.0 | 2.90 | 1.80–4.60 | <0.001 |
| Female | 42 (40.4) | 77 (19.1) | ||||
| Body mass index | ||||||
| Normal weight | 18 (17.6) | 155 (39.6) | 17.2 | 3.10 | 1.80–5.30 | <0.001 |
| Overweight or obese | 84 (82.4) | 236 (60.4) | ||||
| Diabetes mellitus | ||||||
| No | 14 (13.5) | 205 (50.9) | 47.0 | 6.70 | 3.70–12.1 | <0.001 |
| Yes | 90 (86.5) | 198 (49.1) | ||||
| Hypertension | ||||||
| No | 27 (26) | 153 (38) | 5.20 | 1.70 | 1.10–2.80 | 0.030 |
| Yes | 77 (74) | 250 (62) | ||||
| Smoking | ||||||
| No | 98 (94.2) | 348 (86.4) | 4.85 | 0.40 | 0.16–0.93 | 0.030 |
| Yes | 6 (5.8) | 55 (13.6) | ||||
| History of myocardial infarction | ||||||
| No | 65 (62.5) | 291 (72.2) | 3.73 | 1.60 | 1.0–2.50 | 0.070 |
| Yes | 39 (37.5) | 112 (27.8) | ||||
| History of renal disease | ||||||
| No | 80 (76.9) | 352 (87.3) | 7.12 | 2.10 | 1.20–3.60 | 0.012 |
| Yes | 24 (23.1) | 51 (12.7) | ||||
| Hair removal technique | ||||||
| Clipping | 6 (5.8) | 131 (32.4) | 31.3 | 8.30 | 3.52–19.5 | <0.001 |
| Shaving | 86 (82.7) | 227 (56.2) | ||||
| Type of surgery | ||||||
| Elective | 91 (87.5) | 381 (94.3) | 5.82 | 2.40 | 1.16–4.85 | 0.030 |
| Emergency | 13 (12.5) | 23 (5.7) | ||||
| Use of bypass pump | ||||||
| No | 0 (0) | 11 (2.7) | 2.90 | — | — | — |
| Yes | 104 (100) | 393 (97.3) | ||||
| Harvesting site | ||||||
| Others | 4 (3.8) | 57 (14.1) | 8.24 | 4.10 | 1.46–11.6 | 0.003 |
| Mammary artery and saphenous vein | 100 (96.2) | 347 (85.6) | ||||
aMissing data in the controls were as follows: 13 for body mass index; 1 for diabetes mellitus, hypertension, smoking and myocardial infraction; 1 renal disease and 46 for hair removal technique. Missing data for cases were as follows: 2 for body mass index and 12 hair removal technique.
For the positive culture swab, the most prevalent microorganisms among the Gram-positive bacteria were Staphylococcus epidermidis (23.7%, n = 22), of which 45.5% (n = 10) were isolated from deep wound and the rest were from superficial wound, followed by Staphylococcus aureus (15%, n = 14), of which 57.1% (n = 8) were isolated from deep wound and the rest were from superficial wound. However, the most prevalent microorganism among Gram-negative bacteria was Escherichia coli (10.7%, n = 10), of which 40% (n = 4) were isolated from deep wound and the rest were from superficial wound (Table 2).
Table 2.
Types of isolated microorganisms from infected cases (n = 93).
| Type of microorganism | n (%) |
|---|---|
| No growth | 14 (15.0) |
| Gram-positive bacteria | 42 (45.2) |
| Staphylococcus epidermidis | 22 (23.7) |
| Staphylococcus aureus | 14 (15.0) |
| Methicillin-resistant Staphylococcus aureus | 4 (4.3) |
| Enterococcus faecalis | 2 (2.2) |
| Gram-negative bacteria | 36 (38.7) |
| Escherichia coli | 10 (10.7) |
| Klebsiella pneumonia | 8 (8.6) |
| Pseudomonas aeruginosa | 8 (8.6) |
| Enterobacter cloacae | 5 (5.4) |
| Serratia marcescens | 4 (4.3) |
| Citrobacter koseri | 1 (1.1) |
| Fungi | 1 (1.1%) |
| Candida albicans | 1 (1.1) |
A binary logistic regression analysis was used to identify significant risk factors of developing SSIs after CABG surgery using the following variables: gender, age (below or above 65), smoking, diabetes, hypertension, kidney disease, cerebrovascular disease, old myocardial infraction, valvular heart disease, dyslipidemia, body mass index categories (obese vs. normal weight) and hair removal method (shaving vs. electric clipping). The enter method was used to test for significant predictors. The full model was tested against a constant only model and was statistically significant (χ2 = 131.4, p < 0.001). The total Nagelkerke R2 for the model was 0.371. The final model showed that gender, hair removal method, having diabetes and the body mass index category were significant predictors of developing SSIs after CABG surgery (Table 3).
Table 3.
Predictors of surgical site infections after coronary artery bypass graft surgery.
| 95% CI | |||||||
|---|---|---|---|---|---|---|---|
| Variable a | B | S.E. | Wald | p | Exp (B) | Lower | Upper |
| Gender | 1.153 | 0.305 | 14.40 | <0.001 | 3.20 | 1.74 | 5.80 |
| Age (>65 vs. < 65) | −0.269 | 0.287 | 0.879 | 0.349 | 0.76 | 0.44 | 1.34 |
| Smoking | −0.542 | 0.506 | 1.147 | 0.284 | 0.58 | 0.22 | 1.60 |
| Diabetes | 1.763 | 0.363 | 23.64 | <0.001 | 5.83 | 2.90 | 11.90 |
| Hypertension | 0.104 | 0.327 | 0.101 | 0.751 | 1.11 | 0.59 | 2.11 |
| Kidney disease | 0.517 | 0.363 | 2.031 | 0.154 | 1.70 | 0.82 | 3.42 |
| Cerebrovascular disease | 0.671 | 0.771 | 0.758 | 0.384 | 1.96 | 0.43 | 8.90 |
| Old myocardial infraction | 0.510 | 0.300 | 2.883 | 0.090 | 1.70 | 0.92 | 3.0 |
| Valvular heart disease | −18.5 | 6944.4 | 0.000 | 0.998 | 0.000 | 0.00 | 0.00 |
| Dyslipidemia | −0.345 | 0.334 | 1.069 | 0.301 | 0.71 | 0.37 | 1.36 |
| BMI category b | 0.758 | 0.337 | 5.049 | 0.025 | 2.14 | 1.107 | 4.14 |
| Hair removal | 2.125 | 0.461 | 21.24 | <0.001 | 8.40 | 3.40 | 20.70 |
| Constant | −6.42 | 0.791 | 65.83 | <0.001 | 0.002 | — | — |
CI: confidence interval.
aReference group of significant predictors are male gender, > 65 years, no diabetes, normal weight and electric clipping hair removal.
bBMI: body mass index category (normal weight vs. obese or overweight).
Discussion
Findings from the current study showed that the overall incidence rate of SSIs after CABG surgeries in Oman is 17.5%. Regionally, the current study showed that the infection rate in Oman is less than the reported rates from Egypt (23.3%) (Hafez et al., 2012) and Jordan (21.6%) (Al-Zaru et al., 2010). On the other hand, the reported rate in the current study is higher than the rates from Bahrain (17.0%) (Ahmed Abdulaziz et al., 2015) and Kuwait (2.1%) (Nair et al., 2019). At the international level, most of the multicenter and large-scale studies have reported incidence rates much lower than the rate reported in the current study. For example, the overall incidence rate of SSIs after CABG surgeries in Europe is 2.6% (ECDC, 2017). Likewise, the incidence rate in USA studies ranged from 0.37% (Haley et al., 2012) to 3% (Gulack et al., 2018).
Although the variation in the incidence rate among these countries can be largely attributed to infection control measures and healthcare quality, there are other factors that may be contributed to this variation such as the study setting, design, case finding method and the period of the study. For example, retrospective studies done in Bahrain (Ahmed Abdulaziz et al., 2015) and Jordan (Al-Zaru et al., 2010) are both used a single setting. On the other hand, studies conducted in the USA (Haley et al., 2012) and Europe (ECDC, 2017) were conducted at a larger scale and involved data collection from a large number of hospitals. Therefore, it is important to interpret the incidence rate from the single setting studies carefully, as the results might not be generalizable to the whole country, compared to the multisite studies. Nevertheless, the rate in the current study is substantially higher than rates reported in studies from developed countries. Therefore, this study is considered an alarming study for further investigating the root cause of this inflated rate. Possible clinical practices pre-, intra-, and postoperatively need a critical review in the study settings to identify possible causes of this high rate.
In the current study, the most prevalent microorganisms among the Gram-positive bacteria were S. epidermidis (21.2%), followed by S. aureus (15%). The results of the current study were consistent with previous studies (ECDC, 2017; WHO, 2018) where Gram-positive bacteria especially S. aureus and S. epidermidis were the most common isolated microorganisms after CABG surgeries. Although these pathogens could be isolated from the patients’ normal skin flora, they also can be transmitted through cross-transmission from the hands of the healthcare workers. This may pose concerns about the compliance of healthcare workers with hand hygiene guidelines. Therefore, conducting observational studies can give more insight into the role of compliance level with hand hygiene and infection control guidelines in the inflated infection rate in the current study settings.
In the study settings, all patients undergoing CABG surgeries receive antibiotic prophylaxis with first generation cephalosporin (cefazolin). The cefazolin dose of 2 g was given three times a day for 48 h. The first dose of cefazolin was given 30 min intraoperatively before the incision. Previous studies (Sommerstein et al., 2019) have shown that prophylaxis cefazolin administration significantly reduces the incidence of SSIs after CABG surgeries. Further, previous research has demonstrated that administration of cefazolin 30 min before incision with a dose concentration >104 mg/litre at closure time significantly reduces the SSIs after CABG surgeries (Zelenitsky et al., 2018). Since the study is retrospective, it was not possible to assess the antibiotics prophylaxis data accurately. It was not possible to assess accurately the role of the antibiotic prophylaxis protocol on the incidence of SSIs after CABG surgeries. Future prospective studies may reveal better insight about this role.
Further, infection control guidelines suggested screening for methicillin-resistant Staphylococcus aureus (MRSA) before CABG surgeries, as a preoperative preventive measure. However, the current study did not evaluate the patients for MRSA preoperatively. Future prospective studies may consider this screening for better understanding of the causative agents of SSIs after CABG surgeries in Oman.
In the current study, nine variables were found to be significant unadjusted risk factors for SSIs after CABG surgeries, which include female gender, obesity, diabetes mellitus (DM), hypertension, smoking, renal impairment, type of shaving (razor vs electric clipping), type of the surgery (emergency vs elective) and vein harvesting site. In the multivariate analyses, four variables were identified as significant predictors for SSIs after CABG surgeries, which include female gender, DM, obesity and type of preoperative shaving.
The association of female gender with increasing risk of SSIs after CABG surgeries is not fully clear. Different research efforts have been done to clarify the relationship between the female gender and the increased risk of SSI after CABG surgeries. For example, in a large-scale study in Germany (Aghdassi et al., 2019), researchers suggested that the increased risk for female patients can be attributed to re-vascularization of arterial occlusion. Other studies (Arnaoutakis et al., 2017; Vuorisalo et al., 1998) suggested that differences in fat distribution between men and women might explain the increased risk among females. Researchers suggested that since women have more fat tissue in their chest and thighs, this might delay the wound healing process and increase the risk of SSI.
In the current study, diabetic patients are approximately six times at higher risk for SSIs than non-diabetic patients. Diabetes mellitus is an independent risk factor of SSIs as documented in many regional (Al-Zaru et al., 2010) and international studies (Haley et al., 2012). The relationship between DM and development of SSIs is complex. Diabetic hyperglycemia have been found to be major factor in delaying wound healing by disturbing the function of the immune system (Jafar et al., 2016) and delay of granulation tissue (Berlanga-Acosta et al., 2013). The impact of DM on the risk of SSIs within the Omani population becomes more significant when the diabetic self-management is already suboptimal (Al-Hadhrami et al., 2020).
In the current study, obese patients are two times more likely to develop SSIs than patients of normal body weight. This finding was previously reported (Gulack et al., 2018). The excessive adipose tissue at skin layer mainly subcutaneously found to delay the healing process of the wound and result in a hypoperfusion which means less blood supply to the wound, less oxygen and nutrients needed for wound healing process (Pierpont et al., 2014). Further, the interaction between obesity and DM is very well documented in the literature (Bustamante-Munguira et al., 2019). In the current study, the majority of diabetic patients (83.1%) were obese (42.7%) or overweight (40.4%).
In the current study, patients who are prepared for the surgery using razor shaving were more than eight times at higher risk to develop SSIs than those who were prepared by electric clipping technique. Using a razor blade may cause micro-injuries at the operation site, which was found to increase the risk of developing SSIs (WHO, 2018). According to the WHO guidelines, for preventing SSIs, using electric clippers for hair removal should be the standard procedure for skin preparation of the surgery site (WHO, 2018). In the current study settings, it seems little attention was given to these guidelines and razor shaving is still the practice procedure for skin preparation for the CABG surgery.
Although this study has valuable results, there were some limitations that are worth to refer to. Firstly, this study collected data based on a retrospective design. The data used in this study were originally collected for clinical use and not for research purposes. Therefore, future research may consider using a prospective design to enhance reliability and data accuracy. Second, although the study explored many clinical variables, there are some variables that were not included in the current study such as preoperative nutritional status, intraoperative hypothermia and postoperative wound assessment and reoperation. This limitation can be overcome by using the prospective data collection as well as by having more comprehensive surveillance database for SSIs after CABG surgeries at the hospital and national levels.
Conclusion
The current study revealed very important findings and implication that can be used to inform clinicians and decision maker in Oman and similar countries. Although the results from the current study are very generalizable and applicable to Oman healthcare system, the implications of results are very applicable to similar regional and international healthcare systems, especially in other developing countries where following standard infection control measures is suboptimal (Al-Rawajfah and Tubaishat, 2017; Al-Rawajfah et al., 2013). Results from the current study can inform clinicians in Oman and worldwide regarding practices that can prevent and control SSIs. The results from the current study are consistent with the recommendations by the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines for CABG surgery (Hillis et al., 2011). Further, the results supported the WHO recommendation for preventive measure of SSIs especially the skin preparation recommendations (WHO, 2018). Further, the identified predictors in the current study, such as DM, obesity, hypertension and other comorbidities, are global factors. Interventions directed to control these factors are likely to improve patient’s outcome including preventing and controlling SSIs.
Although the incidence of SSIs after CABG surgeries in Oman is within the regional expectation, it is still much higher than the international rates. This necessitates establishment of preventive program at the national level. Previous experiences demonstrated that establishment of preventive program at the national level, such as the National Surgical Quality Improvement Program in the USA (Fuchshuber et al., 2012), has resulted in a substantial reduction of the infection rates in many hospitals (Hawn et al., 2011). Enforcing implementing standard guidelines to prevent SSIs at the hospital level is a high priority for healthcare decision maker and infection control practitioners.
Acknowledgements
The authors would like to thank Sultan Qaboos University Hospital and Ministry of Health and their staff for facilitating the data collection.
Footnotes
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iDs
Omar M AL-Rawajfah https://orcid.org/0000-0002-2427-8969
Fatma M Al Riyami https://orcid.org/0000-0001-9293-5716
Sulaiman Al Sabei https://orcid.org/0000-0002-3436-8757
Hilal A Al Sabti https://orcid.org/0000-0001-6270-9013
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