Annals of Clinical Cardiology

ORIGINAL ARTICLE
Year
: 2019  |  Volume : 1  |  Issue : 1  |  Page : 30--36

Microbiological and clinical characteristics of sternal wound infections following cardiac surgery in a teaching hospital in Kuwait: A 5-year retrospective study


Deepthi Nair1, Mustafa Firoz Singapurwala2, Khalifa Al-Benwan3,  
1 Department of Microbiology, Al-Amiri Hospital, Kuwait City, Kuwait
2 Department of Cardiac Surgery, SACC, Al-Amiri Hospital, Kuwait City, Kuwait
3 Department of Microbiology, Al-Amiri Hospital; Department of Microbiology, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait

Correspondence Address:
Dr. Deepthi Nair
MD, DipRCPath (UK), Specialist, Department of Microbiology, Al-Amiri Hospital, Kuwait, P.O.Box 4077, Code:13041 Safat, State of Kuwait
Kuwait

Abstract

Background: Sternal wound infections (SWI) following cardiac surgery are health-care-associated infections which have to be prevented as the morbidity and mortality attributed to SWI are high. Objective: The aim is to study incidence, microbial etiology, risk factors, and outcome of SWI that followed cardiac surgery in our hospital. Methods: A retrospective, single-center study involving 833 patients who underwent cardiac surgery from January 2012 to December 2016 was conducted in Al-Amiri hospital in collaboration with the Cardiac Coronary Care Unit, Sabah Al Ahmed Cardiac Centre, Kuwait. Microbiological data were retrieved from laboratory computers, and clinical details from patient files. Age, sex, microbial etiology, risk factors, and outcome were analyzed. A statistical study was done using the SPSS statistical package. Results: The incidence of SWI was 2.1%. Predominant microorganisms isolated were Staphylococcus epidermidis (27.7%) and Pseudomonas aeruginosa (27.7%). The most common risk factor was diabetes mellitus, 88.9% cases. About 50% cases were obese and 72.2% cases had a hospital stay for more than 10 days, with the median length of stay being 13.50 days. 30-day mortality outcome was zero. Conclusion: SWI lead to bacteremia, sepsis and extended hospital stay placing the patient at risk of further hospital acquired infections, and increased cost. Preoperative blood sugar control and weight reduction are important. Infection control measures such as nasal screen for Staphylococcus aureus and rectal screen for multidrug-resistant Gram-negative bacilli have to be considered. Based on the most common organisms isolated, ceftazidime with vancomycin could be a better option for surgical antibiotic prophylaxis in our center.



How to cite this article:
Nair D, Singapurwala MF, Al-Benwan K. Microbiological and clinical characteristics of sternal wound infections following cardiac surgery in a teaching hospital in Kuwait: A 5-year retrospective study.Ann Clin Cardiol 2019;1:30-36


How to cite this URL:
Nair D, Singapurwala MF, Al-Benwan K. Microbiological and clinical characteristics of sternal wound infections following cardiac surgery in a teaching hospital in Kuwait: A 5-year retrospective study. Ann Clin Cardiol [serial online] 2019 [cited 2020 Feb 23 ];1:30-36
Available from: http://www.onlineacc.org/text.asp?2019/1/1/30/273000


Full Text



 Introduction



Sternal wound infection (SWI) is a significant postoperative complication of sternotomy-based cardiac surgery which has to be prevented. The incidence of SWI worldwide is low and is reported to range from 0.4% to 4%.[1],[2],[3],[4] SWI are categorized under surgical site infections (SSIs) which account for up to 16% of all health-care-associated infections.[5]

In this study, the incidence, microbial etiology, risk factors, and the outcome of cases with SWI were analyzed.

 Methods



A retrospective review of 833 patients who underwent sternotomy during cardiac surgery from January 2012 to December 2016 was done. The single-center study was conducted in Al-Amiri hospital in collaboration with the Cardiac Coronary Care Unit, Sabah Al-Ahmed Cardiac Center, Kuwait. The microbiological data of the cases were collected from the laboratory computer system, and the clinical and surgical details were retrieved from the medical files of the patients.

Organism identification and antimicrobial susceptibility testing

Wound swabs and tissue samples were cultured on the appropriate laboratory media and incubated at 37°C under aerobic and anaerobic conditions for 24–48 h. Vitek 2 automated system was used in the identification and antimicrobial susceptibility testing of the isolates. The Clinical and Laboratory Standards Institute guidelines were followed in testing and reporting of antibiotic susceptibility.

Case analysis

The medical records of cases with SWI were retrospectively reviewed and the data were spread on an excel sheet. The cases were analyzed with respect to age, sex, risk factors, time to SWI postsurgery, related septicemia, length of postinfection hospital stay, and 30-day mortality outcome. The cases were grouped into superficial SWI (SSWI) and deep SWI (DSWI).

The definition for SWI was based on the Center for Disease Control and Prevention criteria of SSI. SWI was defined as a health-care-associated infection that occurs at the site of incision on the sternum. It may be superficial or deep. SSWI was defined as infection that involves only skin and subcutaneous tissue of incision along with one of the followings: purulent drainage, organism isolated in culture, signs or symptoms of infection such as pain, redness or swelling, and diagnosis by a surgeon. DSWI was defined as infection at the incision site that involves fascia and muscle with or without involvement of the sternum and the mediastinum. The other criteria for DSWI included one the followings: purulent discharge, spontaneous wound dehiscence, diagnosis by surgeon, isolation of organism in culture, and the presence of an abscess diagnosed by direct examination/reoperation/histopathology/radiology.

We studied the incidence of SWI in our center. The microbial etiology of the infections was looked into and compared to previous studies on SWI. The infections were classified as monomicrobial and polymicrobial, and their antibiotic susceptibility patterns were studied. Cases with concomitant bacteremia were noted.

Procedures like the preoperative nasal screen for Staphylococcus aureus and subsequent administration of nasal mupirocin, whether performed were looked into.

Various risk factors known to cause SWI were studied. Risk factors were classified into patient risk factors and surgical factors. Patient risk factors included obesity (BMI ≥30 kg/m2 as per the WHO definition), cardiac failure, chronic obstructive pulmonary disease (COPD), diabetes mellitus (DM), DM Type 1 (T1DM), prolonged preoperative hospital stay (pre-OHS), preoperative antibiotics within 30 days. Those with controlled and uncontrolled diabetes were listed, and the HbA1C levels and blood sugar trends during clinic visits, during procedure, and during hospital stay were monitored.

Surgical factors included type of surgery (coronary artery bypass graft [CABG], valvular or combined), use of internal mammary artery (IMA), packed red cell transfusion, IMA harvest method used, use of pump, cross-clamp time, mechanical ventilation > 48 h, re-exploration, and re-intubation.

The time elapsed from the procedure to infection diagnosis and the outcome following infection in terms of 30-day mortality and the length of postinfection hospital stay (post-IHS) were analyzed.

Procedure for obtaining preoperative skin antisepsis and the antiseptic employed were noted.

White blood cell count (WBC), inflammatory markers such as C-Reactive Protein (CRP) and serum procalcitonin (PCT) values were checked.

Statistical analysis was performed with SPSS statistical package (IBM SPSS Statistics for Windows, Version 25. 0. Armonk, NY: IBM Corp).

 Results



Incidence

Eight hundred and thirty-three patients underwent cardiac surgery through a median sternotomy from January 2012 to December 2016. Eighteen out of eight hundred and thirty three cases were diagnosed to have SWI. The incidence of SWI in our group of patients was 2.1%. The incidence of SSWI was 0.8% (7 cases, 38.9%) and DSWI 1.3% (11 cases, 61.1%).

The mean age was 59.61 ± standard deviation 5.75 years (with a minimum 51 years and maximum 71 years). Eleven cases (61.1%) of SWI were in the 51–60 years age group followed by six (33.3%) in 61–70 years age group and one (5.6%) in 71–80 years group. The SWIs were more in females (10, 55.55%) compared to males (eight, 44.44%).

Five (27.7%) cases of SWI were associated with positive blood cultures: four out of eleven (36.4%) in patients with DSWI and one out of seven (14.3%) in patients with SSWI.

Inflammatory markers related to SSWI and DSWI are shown in [Table 1]A and [Table 1]B.{Table 1}

Microbial etiology

Thirteen cases (72.2%) were monomicrobial, and five cases (27.8%) were polymicrobial. The organisms isolated from the SWIs were: Staphylococcus epidermidis (5 cases, 27.8%), Pseudomonas aeruginosa (5 cases, 27.8%); Proteus mirabilis, Klebsiella pneumonia, and Serratia marcescens (three cases each (16.7%); S. aureus (2 cases, 11.1%), the other microorganisms were Candida albicans (1 case, 5.6%) Acinetobacter baumannii (1 case, 5.6%), Enterobacter cloacae (1 case, 5.6%), Bacteroides species (1 case, 5.6%) [Bar Chart 1] and [Table 2].{Table 2}[INLINE:1]

The antimicrobial susceptibility patterns of the microbial isolates are shown in [Table 3]A, [Table 3]B, [Table 3]C, [Table 3]D. Both S. aureus isolates were methicillin sensitive. There were no multidrug-resistant (MDR) strains of P. aeruginosa. Two out of three isolates of K. pneumoniae were extended-spectrum Beta-lactamase (ESBL) producers. There were no carbapenem-resistant strains of K. pneumoniae, S. marcescens, E. cloacae, or P. mirabilis. The isolate of A. baumannii was a MDR strain, sensitive only to colistin.{Table 3}

Five cases (27.8%) of SWI (4 cases DSWI and 1 case SSWI) developed concomitant bloodstream infection. The organisms responsible were methicillin-sensitive S. aureus (MSSA) in 2 cases, K. pneumoniae (ESBL), C. albicans and S. epidermidis, 1 case each. Four cases with DSWI had bacteremia, whereas one case with SSWI had fungemia. Comparatively, similar proportion of BSI was observed among SSWI and DSWI (P > 0.05) [Table 4].{Table 4}

Risk factors

The various patient and surgical factors in the study group are shown in [Table 5].{Table 5}

Patient factors

Nine (50%) patients were obese. Five (27.8%) of eighteen cases had COPD.

Sixteen (88.8%) cases had DM, ten cases (62.5%) uncontrolled DM, six cases (38.5%) controlled DM. Thirteen (72.2%) cases were T1DM. HbA1C levels ranged from 7.1% to 11.5%. Blood sugar levels in diabetic cases in pre-operative, intra-operative, and postoperative periods ranged from 6.2 to 14.7 mmol/L, 6.7 to 19.1 mmol/L, and 5.0 to 14.6 mmol/L, respectively. All cases with high HbA1C were treated with continuous infusion of insulin till postoperative period day 2–3. Cases whose HbA1C were normal preoperative were put on insulin infusion in the operating room and then continued till day 2–3 postoperative. All patients with high and normal HbA1C continued to be on subcutaneous insulin postoperative for 2 months after surgery as per diabetologist advice and were followed up by the diabetologist.

Two (11.1%) out of 18 cases had an infection within 30 days before surgery. Regarding preoperative hospital stay (PreOHS), eight (44.4%) cases had PreOHS <15 days, four (22.2%) had 16–30 days, and one (5.5%) had PreOHS for more than 30 days. Hence, 13 (72.2%) of 18 cases had a PreOHS, the number of days ranging from 3 to 34 days. The remaining five cases had 0–1 day stay in hospital preoperatively.

Surgical factors

With respect to the type of surgery, sixteen cases (88.9%) had CABG and two (11.1%) had combined CABG and valve surgery. None of the 18 cases had infective endocarditis.

Two (11.1%) out of eighteen cases did not use IMA for grafting while two (11.1%) had bilateral IMA. Unilateral IMA was used in the remaining cases. The method of IMA harvest was skeletonized in all cases except in three cases where it was harvested as a pedicled graft.

Fourteen cases (77.7%) were on-pump during surgery, while four (22.2%) were off-pump. Cross-clamp time ranged from 53 to 272 min.

All the 18 cases (100%) underwent mechanical ventilation for <48 h.

With regard to the time of onset of infection, seven cases (38.8%) developed SWI within 2 weeks from surgery and five (27.7%) in 15–30 days. Five cases (27.7%) developed SWI in the 2nd month of surgery, while one case (5.5%) had SWI in the 3rd month following surgery. The median length of time to infection postsurgery was 19.50 days [Table 6]. Two cases (11.1%) had reintubation and two cases (11.1%) underwent reexploration.{Table 6}

Only eleven cases (61.1%) received 1–2 packed red cell transfusions.

Preoperative skin preparation was as follows: whole-body shaving (except back) was done first. The patient was then advised to take shower with Hibiscrub solution. After the scrub, the whole body was poured over with Betadine solution diluted in water, then washed with clean water and dried. This was the preparation done the night before surgery, in the ward.

In the operating room, chlorhexidine solution 0.5% was applied all over the body and left for 3 min to dry, after which the patient was draped in the standard procedure for the surgery.

Preoperative surgical prophylaxis was administered to all patients with cefuroxime 1.5 g intravenous (IV) just before incision, and it was continued for 3 days postoperatively at the dose of 1.5 g IV 8th hourly.

Preoperative nasal screen for S. aureus was not done as a routine, and nasal mupirocin was not applied.

Two (11.1%) cases were treated with antibiotics preoperatively for various infections. Twelve (66.6%) cases received antibiotics intraoperatively.

Following the SWI, five (27.7%) cases had a postinfection hospital stay for <10 days, six (33.3%) cases from 10 to 15 days, four (22.2%) cases for 16–30 days, and three (16.6%) for >30 days. The median length of postinfection hospital stay by descriptive statistics was 13.50 days [Table 6] and [Figure 1].{Figure 1}

Thirty-day mortality outcome was zero.

 Discussion



The total population of Kuwait is approximately 4.5 million.[6] The expected need of CABG in Kuwait is on an average 30 cases every 100,000 persons/year due to the young age prevalence in the population. This brings the expected number of CABG in Kuwait to around 1350 cases/year. Hence, our center SACC deals with just a fraction of the total of these patients.

The incidence of SWI in our study was 2.1%; SSWI 0.8%, DSWI 1.3%. The results are approximately similar to the findings in other studies.[1],[7],[8] SWIs were more in the age group of 51–60 years and females (55.6%) were more affected.

Several studies have reported S. epidermidis as the most common organism isolated from SWI, while others have P. aeruginosa as the most common sternal wound isolate.[8],[9],[10] In our study, however, the microorganism predominance in culture of sternal wound samples was equally shared by S. epidermidis (27.8%) and P. aeruginosa (27.8%). Isolation of the MDR strain of A. baumannii in one case (5.6%) shows the changeover of the antibiotic susceptibility pattern of microorganisms from the sensitive to the more difficult-to-treat resistant pattern. A recently published study on DSWI shows similar MDR strain of A. baumannii isolated from the sternal site.[11] MDR organisms pose a threat to the treatment of wound infections due to the lack of antibiotics needed to treat the same and in addition, due to the side effects of nephrotoxicity and neurotoxicity associated with drugs like colistin which remain the sole choice in the antibiotic pipeline to treat these organisms.

Only five cases (27.8%) of SWI developed bloodstream infections. This could be due to prompt care of the wound and treatment with the appropriate antibiotic following microbiologist advice. S. aureus (MSSA) constituted 40% of bloodstream isolates, pointing to the need for preoperative nasal screen and application of nasal mupirocin. About 80% of positive blood cultures were associated with DSWI. Comparatively, similar proportion of BSI was observed among SSWI and DSWI (P > 0.05).

CRP and PCT help in the diagnosis and prognosis of infection. In various cases, disparity was observed in the levels of CRP and PCT. CRP is a nonspecific marker of inflammation and PCT levels mostly co-relate with the severity of infection. Fungal infections may show a high CRP but a low PCT. Therefore, it would be wise to order both the tests to detect and monitor the severity and progress of infection. WBC was, however, elevated in all cases, excepting one, at the time of infection. In a few cases in our study, PCT was not available due to the lack of supply of reagent for the test.

The most common risk factor was DM. Diabetic patients are at increased risk of SSIs. Preoperative control of blood sugar is an important factor in controlling SSIs. HbA1C levels and blood sugar trends have to be monitored. Depending on blood sugar levels, a long-acting basal insulin by subcutaneous route along with bolus of a short-acting insulin analog should be considered preoperatively, insulin infusion to be given during the procedure and for 2–3 days postoperative. For up to 2 months after surgery, patients may be continued on subcutaneous insulin. During follow-up, patients can resume oral or oral plus parenteral hypoglycemic drugs, which they were on before surgery.

Risk factors for SWI after cardiac surgery are said to vary with the type of surgical procedure.[12] Several studies have shown diabetes, obesity, and insulin dependence as independent risk factors for SWI.[13],[14],[15],[16]

Fifty percent cases were obese. Obesity can cause sternal dehiscence and impair healing due to reduced subcutaneous tissue oxygenation.[17] Prophylactic antibiotics do not reach sufficient tissue levels in obese individuals. Preventive measures such as weight reduction before surgery by exercise and diet control, prophylactic sternal reinforcement, and appropriate dosing of antibiotics based on the bodyweight of individuals should be considered.

The median time to infection postsurgery in our study was 19.50 days. Median time of 7 days with 67% of patients presenting with SWI within 14 days of surgery was observed in a study by Bor et al.[18] Delayed presentation of SWI 6 months after cardiac surgery in a 56-year-old male was reported by Stuesse et al.[19]

The postinfection hospital stay extended beyond 10 days in 72.2% cases, which included hospital stay for >30 days in 16.6% cases. The median length of postinfection hospital stay was 13.50 days. The effect of prolonged hospital stay in increasing the morbidity, hospital expenses, and the risk of further infection with hospital pathogens have been documented in several studies.[20],[21]

Mortality in previous studies has ranged from 0% to 40%.[8],[22],[23] 30-day mortality in our group of patients was zero. This could be due to the early identification and treatment of SWI with the appropriate antibiotic following a good communication between the microbiologist and the cardiac surgeon, and good infection control measures being followed in the hospital.

 Conclusion



Although the incidence is low, the morbidity due to septicemia and prolonged hospital stay in these patients are high. Blood sugar control and weight reduction before surgery are very important. Depending on blood sugar levels, a long-acting basal insulin by subcutaneous route plus bolus of a short-acting insulin analog should be considered preoperatively, insulin infusion to be given during the procedure and for 2–3 days postoperative. For up to 2 months after surgery, patients may be continued on subcutaneous insulin. During follow-up, patients may be put back on their original treatment, which may be oral or oral plus parenteral hypoglycemic drugs. Weight reduction measures through diet control and exercise have to be advised and bodyweight controlled before surgery.

Infection control measures like the nasal screen for S. aureus, use of nasal mupirocin, and rectal screen for MDR Gram-negative bacilli can be considered preoperatively. In view of the most common organisms isolated, ceftazidime with vancomycin could be a better option for surgical antibiotic prophylaxis at our cardiac center.

Acknowledgment

We are grateful for the statistical assistance given to us by the Faculty of Medicine, Jabriya, Kuwait.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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