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Incidence and risk factors associated with nosocomial infection in pediatric heart surgery

How to cite this article: Duarte-Raya F, Baeza-Zarco FJ. [Incidence and risk factors associated with nosocomial infection in pediatric heart surgery]. Rev Med Inst Mex Seguro Soc. 2016;54(2):190-5.



Received: November 25th 2014

Accepted: January 26th 2015

Incidence and risk factors associated with nosocomial infection in pediatric heart surgery

Fidencia Duarte-Raya,a Fabiola Janet Baeza-Zarcoa

aServicio de Epidemiología Hospitalaria, Hospital de Gineco-Pediatría 48, Instituto Mexicano del Seguro Social, Guanajuato, Guanajuato

Communication with: Fidencia Duarte-Raya

Telephone: (477) 717 4800, extensión 31855


Background: Nosocomial infections are responsible for a high rate of morbidity and mortality in pediatric patients undergoing heart surgery. Our objective was to determine the incidence and associated risk factors to nosocomial infections in this group of patients.

Methods: A descriptive, prospective, clinical study was conducted in a tertiary hospital for a year. We calculated the rate of incidence, accumulated incidence and devices used. Was Applied the EPIDAT 2004 version 3.1 program OPS for obtaining of Chi-square with Yates correction for p with a confidence of 95 %, alpha of 0.05 with a degree of freedom, we calculated odds ratio, besides of the identification of microorganisms, their sensitivity and resistance to antibiotics.

Results: We calculated rates of: 45 % the incidence, 80.6 % cumulative incidence, 7.4 % of mortality, 13.3 % of case-fatality rate of infected and 2.7 % non-infected. The 44.4 % with pneumonia, 74 % associated with mechanical ventilation, 100 % nasogastric tube. The most frequently isolated microorganisms are: Acinetobacter baumanni, Staphylococcus aureus, Staphylococcus epidermidis and Pseudomonas aeruginosa with high resistance to antibiotics.

Conclusions: Pediatric patients undergoing heart surgery have high risk of infection heart disease, cyanogen’s have 5 times more risk. We observed a statistically significant association with infection using nasogastric probe and endotracheal tube, the risk increases to increased hospital stay. Infected patients have 4 times the risk of death.

Keywords: Thoracic surgery; Cross infection; Pediatrics; Disease transmission, infectious

Congenital heart diseases are collectively the most common development anomaly and the leading cause of non-infectious death in newborns around the world;1 it is estimated that 2 to 3% of live births have congenital anomalies, and of these, heart malformations have an incidence ranging from 0.5 to 1.25%. In the United States 44.5% of live births with congenital anomalies who die during the first year of life have some type of congenital heart anomaly.2,3 In Mexico around 5000 children are born with a congenital heart malformation, and nearly half need surgical treatment during the first year of life.4 Patients undergoing cardiovascular surgery have nosocomial infection in half of cases, with an incidence rate of 52 and an even higher case fatality rate in those infected, infected at 21.2 and uninfected at 16.1, as demonstrated in the previous study from our hospital.4

Nosocomial infections are responsible for a high rate of morbidity, mortality, and increased costs in critical pediatric patients due to aggressive cardiopulmonary bypass, the use of invasive procedures, hemodynamic deterioration, prolonged mechanical ventilation, and potential contamination with microbial flora.5 The incidence rate of nosocomial infection subsequent to cardiac surgery in children varies between 10 and 50%. The following have been identified as risk factors for the development of nosocomial infection after cardiac surgery: age, cyanotic heart diseases, prolonged surgical time, reoperation for bleeding, open sternum, invasive procedures, transfusion of blood products, multi-organ dysfunction, and prolonged stay.5 Thus, the presence of these factors complicates the results of cardiac surgery, slows patient rehabilitation, and reduces their quality of life.5,6

Fever is common in the immediate postoperative period, especially in patients undergoing cardiopulmonary bypass; however, fever 48 hours after surgery requires investigation for a possible infectious focus.4,7,8 In the pediatric patient, clinical risk, according to the clinical classification system, is the severity index for patients admitted to the pediatric intensive care unit.8

Intrinsic risk factors are those inherent to the patient that predispose them to infection; they may be present at the time of admission or appear during their stay in the unit: coma, renal failure, respiratory distress, diabetes, malignancy, immunodeficiency, neutropenia, malnutrition, malformations, and others.9,10

Extrinsic risk factors are of exogenous, medical, or hospital origin, and predispose the patient to infection.9,10 The risk of infection in pediatric patients undergoing cardiac surgery is high and proportional to the days of hospital stay in intensive care units, so intrinsic and extrinsic factors should be considered during this time.4,11 In several studies on the incidence and nosocomial infection in pediatric heart surgery, it is concluded that half of the cases have nosocomial infection and a high fatality rate.4,8,12 Mortality risk is 20 times higher in patients who develop infection after cardiac surgery.13

The aim of this study was to determine the incidence of nosocomial infections in patients undergoing pediatric cardiac surgery and associated risk factors.


A descriptive, prospective clinical study was conducted at the Hospital de tercer nivel de Gineco Pediatría 48 in Leon, Guanajuato, from June 1st, 2012 to May 30th, 2013. The sample was composed of 67 patients who underwent cardiac surgery during the study year, with a survival equal to or greater than 48 hours after the surgical procedure. The dependent variable was the presence of nosocomial infection in pediatric heart surgery patients, and independent was the risk factor described with the criteria of the Center for Disease Control in Atlanta (USA), for the definition of nosocomial infection and sites of location. The records were reviewed for patients of the services involved: heart surgery, pediatric intensive care unit (PICU), surgery, epidemiology, and laboratory. The study registered the identification tag, clinical conditions, history and time of diagnosis, weight, size and nutritional status, pump time, and prophylactic treatment. In case of nosocomial infection, the date of infection, microorganism isolated, and antimicrobial sensitivity and resistance was noted. The following definitions were considered for analysis: estimation of clinical risk in pediatric patients, intrinsic risk factors, and extrinsic risk factors. The information was concentrated in the Excel program, the EPIDAT 2004 OPS version 3.1 program was applied to obtain Chi-squared, with Yates correction to obtain p. Data analysis was performed with Chi-squared test with 95% confidence, alpha of 0.05 with one degree of freedom, therefore expecting a tabulated Chi-squared of 3.842. Odds ratio (OR) was estimated to measure the strength of the association between the risk factor and the presence of nosocomial infection, and between mortality and nosocomial infection. The incidence rate was calculated by dividing the number of infected patients by the number of discharges, times 100. In addition, cumulative incidence rate (CI) was calculated, equivalent to the number of infections during the study period divided by the number of admissions during the same period, times 100. The rate of infection related to specific procedures (urinary catheter placement, endotracheal intubation, central catheter placement, arterial line, chest tube) was calculated by dividing the number of infections associated with a specific procedure by the number of procedures made in the same period of time, times 100. The rate of infections from devices used (urinary catheter, mechanical ventilation, central venous catheter, arterial line, chest tube) was calculated by dividing the number of infections associated with the use of said device by the number of days that the device remains in use, times 100. The study registered the microorganisms causing nosocomial infections, and analysis was made of antibiotic sensitivity and resistance. The results were presented with descriptive statistics, rates and percentages, charts and graphs.


67 patients were included from pediatric heart surgery, and two groups were formed: one infected with 30 (45%), 16 males and 14 females, with 4 deaths: 2 males and 2 females. And the other group was uninfected, with 37 patients (55%), 19 males and 18 females, with one death: 1 male.

The distribution by age group was as follows: 42% patients were younger than 1 year, 28% were 1 to 4 years old, 15% were 5 to 9 years old, 12% were 10 to 14, and 3% were older than 15. The average age was 8 months.

The frequency of malnutrition in the sample was as follows: uninfected: mild malnutrition 13%; of those infected, 13.3% had mild malnutrition, 13.3% moderate malnutrition, and 3.3% severe malnutrition.

The incidence of nosocomial infection was 45%, with a mortality rate of 7.4%, the case fatality rate was 13.3% in infected patients, and 2.7% in those uninfected. A total of 54 nosocomial infections were recorded, with a cumulative incidence rate of infection of 80.6%; the localization rate of nosocomial pneumonia infection was 44.4%. Intubated patients were 19 (28%), with mechanical ventilation for an average of 3 days, 14 had nosocomial infections (74%); patients with central catheters were 53 (79%), with an average use of 6 days. Infected patients were 24 (45%), patients with urinary catheter were 44 (65%), lasting 3 days on average, 17 patients (38.6%) had nosocomial infection, arterial line was used in 36 (53%) with an average use of 2 days; patients with nosocomial infection were 17 (39%), with chest tube in 47 (70%) with an average use of 3 days; 28 of these patients (59%) presented infection, with nasogastric tube in 7 (10%) with an average use of 4 days, 100% of infected patients, 2 patients with pericardial tube (3%) with an average use of 2 days and one patient who developed nosocomial infection (50%).

According to the degree of complexity, 65% ​​were simple, 27% were moderately complex, 4% complex, and 4% very complex. Deaths as a function of disease complexity, compared to the total sample, were as follows: 3% simple, 1% moderately complex, and 3% very complex. By type of heart disease: 12 presented cyanotic heart disease (17.9%), and 55 non-cyanotic heart disease (82%). Patient stay prior to surgery was on average 2 days, and 5 days after the event in the PICU. There were 5 deaths, all in the age group under 1 year: 3% had simple heart disease, 3% very complex heart disease, and 1% moderately complex heart disease. As for sex, 3 were male and 2 female. 

Of the most significant data for nosocomial infection, we have cyanotic heart disease with a Chi-squared 5.400, Yates Chi-squared 4.014, p of 0.020; nasogastric tube with a Chi-squared 5.73, Yates Chi-squared 3.965, p of 0.01; and tracheal cannula with a Chi-squared 8.963, Yates Chi-squared 7.405, p of 0.002.

As for the relationship of infection with death, this has a Chi-squared 2.401, Yates Chi-squared 1.255, p of 0.121, and an OR of 4.13 (Table I).

Table I Statistical test with 95% CI, OR with 1 df
Variable Chi-squared p Yates Chi-squared p OR
Cyanotic heart disease and infection 5.4003 0.0201 4.0140 0.0451 4.85
Cyanotic heart disease and death 6.5104 0.0107 3.7843 0.0517 8.83
Gender and infection 0.0261 0.8717 0.0071 0.9327 0.92
Gender and death 0.1304 0.7180 0.0109 0.9170 1.40
Malnutrition and infection 2.7243 0.0988 1.8182 0.1775 2.74
Infection and death 2.4019 0.1212 1.2552 0.2626 4.13
Arterial catheter and infection 0.1883 0.6644 0.0352 0.8512 1.23
Chest tube and infection 2.5174 0.1126 1.7376 0.1874 2.43
Central venous catheters and infection 0.0264 0.8710 0.0195 0.8888 1.10
NGT and infection 5.7326 0.0167 3.9650 0.0465 9.65
Urinary catheter and infection 1.9540 0.1622 1.2976 0.2546 0.48
Tracheal cannula and infection 8.9630 0.0028 7.4054 0.0065 5.60
Pericardial tube and infection 0.0228 0.8801 0.3261 0.5680 1.24

Risk factors associated with nosocomial infection by statistical calculation of odds ratios were: nasogastric tube with an OR of 9.65, mechanical ventilation with an OR of 5.60, cyanotic heart disease with an OR of 4.85, malnutrition with an OR of 2.74, and chest tube with an OR of 2.43. Nosocomial infection as a risk factor associated with death had an OR of 4.13, and cyanotic heart disease as a risk factor associated with death had an OR of 8.83 (Table I).

Type of infection was presented in this order: pneumonia 44.4%, sepsis 40.7%, urinary tract infection 12.9%, and thoracic abscess 1.8%. The number of infectious events per patient were 1 event in 54%, 2 events in 27%, 3 events in 13%, 4 events in 3%, and 6 events in 3% (Table II).

Table II Distribution of number and type of nosocomial infections by sex



Sex Number of nosocomial infections Type

of infection


Male Female
7 3 4 1 Sepsis*
6 4 2 1 Pneumonia*
1 1 0 1 Chest abscess*
1 0 1 1 Sepsis**
1 1 0 1 Pneumonia** Type

of infection

1 1 0 2 Pneumonia* Sepsis*
1 1 0 2 Sepsis* UTI*
1 0 1 2 Pneumonia** Sepsis*
1 1 0 2 Pneumonia* Sepsis**
1 1 0 2 Pneumonia * UTI**
1 0 1 2 Pneumonia** Sepsis**
1 1 0 2 Sepsis** Pneumonia*
1 1 0 2 Pneumonia** Sepsis** Type of infection
1 0 1 3 UTI** Pneumonia** UTI**
1 0 1 3 Sepsis** Pneumonia* Sepsis**
1 0 1 3 UTI** Pneumonia** Pneumonia**
1 0 1 3 Pneumonia** Pneumonia** Sepsis** Type of infection
1 1 0 4 Sepsis* Pneumonia* Sepsis * UTI* Type of infection
Type of infection
1 0 1 6 Pneumonia** UTI** Pneumonia** Pneumonia** Sepsis** Sepsis**
* Without germ isolated. * With germ isolated  

Microorganisms isolated from cultures were: Acinetobacter baumanni haemolyticus 27.8%, Staphylococcus aureus 16.7%, Staphylococcus epidermidis 13.9%, Pseudomonas aeruginosa 13.9%, Escherichia coli 8.3%, Enterococcus faecium 5.5%, Enterobacter cloacae 5.5%, Staphylococcus haemolyticus 2.8%, Staphylococcus hominis 2.8%, and Klebsiella pneumoniae 2.8%. In blood cultures they were: Pseudomonas aeruginosa 25%, Acinetobacter baumanni 25%, Staphylococcus aureus 25%, Staphylococcus epidermidis 12.5% and Staphylococcus hominis 12.5%; in bronchial secretions they were: Acinetobacter baumanni 33.3%, Staphylococcus epidermidis 20%, Staphylococcus aureus 13.3%, Pseudomonas aeruginosa 13.3%, Enterobacter cloacae 13.3%, Escherichia coli 6.7%; from the catheter tip they were: Acinetobacter baumanni 42.8%, Staphylococcus aureus 28.6% Staphylococcus epidermidis 14.3%, and Pseudomonas aeruginosa 14.3%; in urine culture they were: Enterococcus faecium 40%, Staphylococcus haemolyticus 20%, Klebsiella pneumoniae 20%, and Escherichia coli 20%.

100% of patients received prophylaxis prior to surgery with the antibiotic cephalothin (first-generation cephalosporin). To treat nosocomial infection the antibiotic used most was cefotaxime (70%), other antibiotics used were cefepime (33%), vancomycin (33%), amikacin (26%), and dicloxacillin (26%).

Antimicrobial resistance to Gram positive microorganisms was more than 61% for Staphylococcus aureus, which was the most frequent of this group, for the following antibiotics: ampicillin/sulbactam, ampicillin/clavulanate, ceftriaxone, clindamycin, ciprofloxacin, erythromycin, levofloxacin, moxifloxacin, and oxacillin (Table III).

Table III Gram positive microorganisms from cultures, sensitivity and resistance
n Microorganism BLAC Producer Antimicrobial

< 20%


21 to 40%


41 to 60%


> 61%

6 Staphylococcus aureus Penicillin Tetracycline Cefotaxime,

Cefazolin, cefepime, ertapenem,


gentamicin, imipenem


ampicillin/ clavulanic acid, ceftriaxone, clindamycin, ciprofloxacin, erythromycin, levofloxacin, moxifloxacin, oxacillin

5 Staphylococcus epidermidis Ampicillin, penicillin Gentamicin,

levofloxacin, moxifloxacin, rifampicin, synercid, vancomycin


ciprofloxacin, trimethoprim/sulfamethoxazole


Ampicillin/sulbactam, amoxicillin/clavulanic acid, ceftriaxone, erythromycin, oxacillin
2 Enterococcus faecium Levofloxacin,

linelozid, synercid, vancomycin

Ampicillin, ciprofloxacin, erythromycin, penicillin, rifampicin, tetracycline, streptomycin
1 Staphylococcus hominis Ampicillin, penicillin Ampicillin/sulbactam, ampicillin/ clavulanic acid, ceftriaxone, clindamycin, ciprofloxacin, erythromycin, gentamicin, levofloxacin, moxifloxacin, oxacillin, trimethoprim/sulfamethoxazole
1 Staphylococcus haemolyticus Ampicillin, penicillin Ciprofloxacin, tetracycline, clindamycin, erythromycin, penicillin Ampicillin/sulbactam, ampicillin/ clavulanic acid, ceftriaxone, clindamycin, erythromycin, gentamicin, oxacillin, synercid, trimethoprim/sulfamethoxazole, vancomycin
Source: T1 UMAE laboratory results. IMSS 2012-2013

For Gram negative the most common is Acinetobacter baumanni, with resistance greater than 61% to: amikacin, cefepime, cefotaxime, ceftazidime, ceftriaxone, ciprofloxacin, gentamicin, levofloxacin, ticarcillin/clavulanate, tobramycin, and trimethoprim/sulfamethoxazole (Table IV).

Table IV Gram negative microorganisms from cultures, sensitivity and resistance
n Microorganism ESBL producer Antimicrobial

< 20%


21 to 40%


41 to 60%


> 61%

10 Acinetobacter baumanni Piperacillin Ampicillin/sulbactam, meropenem Amikacin, cefepime, cefotaxime, ceftazidime, ceftriaxone, ciprofloxacin, gentamicin, levofloxacin, ticarcillin/clavulanate, tobramycin, trimethoprim/sulfamethoxazole
5 Pseudomonas aeruginosa Ceftazidime, cefepime, imipenem Ceftriaxone, cefotaxime, ticarcillin /clavulanic acid
3 Escherichia coli Aztreonam, ceftriaxone, ceftazidime, cefotaxime Gentamicin, ticarcillin /clavulanic acid Amp/sulbac, ampicillin, cefepime, cefuroxime, cefazolin, levofloxacin, ciprofloxacin, tobramycin, moxifloxacin, trimethoprim/sulfamethoxazole
2 Enterobacter cloacae Ampicillin/sulbactam, ampicillin, cefotaxime, ceftazidime, ceftriaxone, cefuroxime, cefotetan, ticarcillin/clavulanate Tetracycline
1 Klebsiella pnemoniae Aztreonam, ceftriaxone, ceftazidime, cefotaxime Ampicillin, piperacillin, ampicillin/sulbac, trimethoprim/sulfamethoxazole, cefuroxime, ciprofloxacin, cefepime, tobramycin, tetracycline
Source: T1 UMAE laboratory results. IMSS 2012-2013


Comparing this study with a previous one at the hospital, it shows that the incidence of nosocomial infection is 7% lower compared to the earlier study (47% vs. 52%).4 It was held that the high rate of nosocomial infection was because in the first study, the hospital was being renovated, as the most frequently isolated microorganism was Candida albicans (17%);4 in our study the frequency of Candida albicans was 0. Other countries have a much lower incidence rate than ours, including: Spain, reporting an incidence of 29%,14 then Finland with 27.5%,15 Holland with a much lower incidence (25%),16 Cuba with an incidence rate of 18.9% (although the study was conducted in a pediatric cardiac surgery center),17 and Canada with an incidence rate of 3.4%.18

As for the case fatality rate, this was higher in infected patients than in non-infected (13.3% vs. 2.7%), with a mortality risk 4 times higher in infected patients compared with patients who did not develop nosocomial infection. The case fatality rate was lower in this study (16.1%) compared to the previous study (21.2%);4 in Cuba, the fatality rate in infected patients is 42% compared to uninfected (3.5%), and a risk of death is reported 20 times higher in infected patients.17

As for the days of stay in the PICU and total hospital stay, infected patients had a higher average than those uninfected.14 Our study days showed an average stay of: 7 days (infected) over 4 days (uninfected).

In this study, as in others in the literature, age is not defined as a risk factor for the development of nosocomial infection, since it excluded patients operated on during the neonatal period, who are most at risk14,19 because of the immaturity of the immune system.18 Nor was gender a risk factor for infection, since the development of nosocomial infection was the same in both males and females.

Statistically significant risk factors for the development of nosocomial infection were cyanotic heart disease, nasogastric tube, and tracheal cannula. By odds ratio analysis it was nasogastric tube, tracheal cannula, malnutrition, and chest tube. In Colombia the extrinsic risk factors reported were preoperative hospital stay,19 which agrees with a publication from Finland.15 The frequency and severity of complications increases with the complexity of the surgery20 and postoperative stay in the pediatric intensive care unit, mechanical ventilation time, red blood cell transfusion of more than 3 units, and surgical time.19,21

The most frequent nosocomial infection was nosocomial pneumonia, also considered a major cause of morbidity and mortality in the Spanish population;14 as in the previous study from this hospital the most common site of nosocomial infection was pneumonia,4 unlike other studies that report bloodstream infection.17 In other published works, bacteremia is the most common type of nosocomial infection in this group of patients;17 in our study bacteremia was not the most frequent nosocomial infection because of the rapid withdrawal of central venous access, with overall average use of central venous catheter of 6 days and 2 days for arterial lines. Saudi Arabia also reports a higher incidence of ventilator-associated pneumonia, followed by bacteremia.22

The development of nosocomial infections increases morbidity, mortality, and costs,19 so one of the strategies to reduce nosocomial infection is extubating and removing external devices quickly, as they are factors clearly associated with risk of developing nosocomial infection,14 as is observed in our study too.

As for microorganisms, the most commonly isolated in our study were Acinetobacter baumanni and Staphylococcus aureus. However, in the pediatric heart surgery center, the most common organism was coagulase-negative Staphylococcus,7 while in Spain it was Gram positive cocci (Staphylococcus) and Gram negative bacilli (the Enterobacteriaceae family and Pseudomonas).14

In isolates cultured from bronchial secretions, we most often found Acinetobacter baumanni and Staphylococcus epidermidis to be responsible for nosocomial pneumonia due to previous colonization of these pediatric patients, in whom the germ crawls into the lower airways after tracheal intubation. Some authors agree that prior oropharyngeal decontamination of the patient with oral rinses with chlorhexidine appears to reduce nosocomial pneumonia for ventilated patients, although not significantly.14,23-25

Antibiotic prophylaxis is still considered an important factor in preventing surgical wound infection;26 in a study from the United States chlorhexidine was applied to reduce the risk of infection at the infection site by up to 41% compared to the use in most interventions, such as using iodine povidone.27

The time of maximum risk for infection is the surgical incision, so coverage with a first- or second-generation cephalosporin for Gram positive cocci that colonize the skin is considered the most appropriate plan.26 In this hospital all patients undergoing pediatric cardiac surgery were managed with antibiotic prophylaxis with first-generation cephalosporin (cephalothin), although a previous study of this hospital has definitely shown an accelerated increase in antimicrobial resistance of Gram positive and Gram negative bacteria.28 


Pediatric patients undergoing heart surgery are at high risk of infection subsequent to the surgical procedure according to their clinical classification; the risk is 5 times greater in patients with cyanotic heart disease than in patients with non-cyanotic heart disease. As for the devices used, the association of risk factors for infection resemble those reported in the literature worldwide; this study shows an important relationship between infection and the use of nasogastric tube and tracheal cannula, the risk increasing proportionally with longer hospital stay. In patients younger than 1 year, the factors associated with infection were age; malnutrition; use of chest tube, nasogastric tube, and tracheal cannula; and, of course, excessive hospital stay. This study also shows that patient mortality is significantly proportional to the complexity of the heart disease, since it was found that infected patients are at increased risk of death, up to 4 times higher compared with uninfected patients.

It is concluded that the study of nosocomial infections remains a current problem that requires constant attention by the hospital health team. It is necessary to implement and renew strategies to avoid the presence of infections in pediatric heart surgery patients, in order to reduce the incidence of complications, improve prognosis, and reduce the length of hospital stay in our medical unit.

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Conflict of interest statement: The authors have completed and submitted the form translated into Spanish for the declaration of potential conflicts of interest of the International Committee of Medical Journal Editors, and none were reported in relation to this article.

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