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Risk factors related to nosocomial pneumonia in pediatric patients undergoing heart surgery

How to cite this article: Fortanelli-Rodríguez RE, Gómez-Delgado A, Vera-Canelo JM, Alvarado-Diez MÁ, Miranda-Novales G, Yuriko Furuya ME, Solórzano-Santos F, Vázquez-Rosales JG. Risk factors related to nosocomial pneumonia in pediatric patients undergoing heart surgery. Rev Med Inst Mex Seguro Soc. 2015;53 Suppl 3:S316-23.



Received: August 14th 2014

Accepted: September 1st 2015

Risk factors related to nosocomial pneumonia in pediatric patients undergoing heart surgery

Rocío Elvira Fortanelli-Rodríguez,a Alejandro Gómez-Delgado,b José Manuel Vera-Canelo,c Miguel Ángel Alvarado-Diez,d Guadalupe Miranda-Novales,e María Elena Yuriko Furuya,f Fortino Solórzano-Santos,g José Guillermo Vázquez-Rosalesa

aServicio de Infectología

bUnidad de Investigación en Epidemiología

cServicio de Cardiocirugía

dUnidad de Terapia Intensiva

eUnidad de Investigación en Infecciones Nosocomiales

fUnidad de Investigación Médica en Enfermedades Respiratorias

gDirección Médica

a,c,d,gHospital de Pediatría

b,e,fCoordinación de Investigación en Salud

Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Distrito Federal, México

Communication with: José Guillermo Vázquez-Rosales

Telephone: (55) 5627 6900, extensión 22462

Correos electrónicos:

Background: Procalcitonin is a diagnostic marker useful to discern infections and non-infectious complications in heart surgeries. The aim is to describe risk factors related to nosocomial pneumonia and the predictive value of serum procalcitonin in pediatric patients undergoing heart surgery.
Methods: During a year a nested case-control study was carried out in a third level hospital. All patients undergoing open-heart surgery were followed and clinical data searching for pneumonia were registered every day. Blood samples for determination of procalcitonin were taken 48 hours after surgery. Those patients who developed pneumonia based on CDC clinical criteria were defined as cases; and controls were those patients who did not developed pneumonia.
Results: 188 patients underwent heart surgery (15 % developed pneumonia). Ninety-seven patients were submitted to open-heart surgery: 24 cases and 73 controls. Seventy-eight % of cases developed pneumonia between second and fifth day after surgery. The average time of surgery, extracorporial bypass, aortic cross-clamp, and mechanical ventilation were greater in control patients. The frequency of open sternotomy, reintubation, and surgical wound infections was greater in case patients.
Conclusions: Some of the events related to heart surgery and their subsequent management are associated significantly to the development of hospital-acquired pneumonia.

Keywords: Procalcitonin, Thoracic surgery, Risk factors, Pediatrics.


It is considered that in developed countries congenital heart disease is the leading cause of death between 1 and 12 months of age. About two thirds of these malformations require surgery at some point in their development, since without it one third of patients develop critically and die in the first year of life.1

Moreover, nosocomial infections are a serious problem among surgical patients, with lower respiratory tract infections being among the most frequently reported complications in patients who have these procedures and have to stay in the intensive care unit (ICU).2-3 In adult subjects the hospital stay in the ICU is longer in patients undergoing cardiac surgery who develop pneumonia, and it is probably the most frequent and severe cause of infection in this group of patients, associated with a higher mortality rate than other nosocomial infections such as those of the urinary tract or surgical wound.4 The global mortality attributed to nosocomial pneumonia in children has been estimated at 11%.5

Pediatric patients undergoing heart surgery are a population at high risk for developing ventilator-associated pneumonia, but information on this topic is scarce. Risk factors involved in the development of nosocomial pneumonia in this patient group (mechanical ventilation, antibiotics) are common to other groups of patients; however, there are particular factors such as duration of surgery, aortic clamping, extracorporeal circulation, prior administration of antibiotics, etc.5

A prospective study reported reintubation (OR 62.5), presence of nasogastric tube (OR 19.7), prior use of broad-spectrum antibiotics (OR 6.6), and blood transfusion (OR 12.8) as risk factors for the development of nosocomial pneumonia after heart surgery.6 Mandakini et al. further describe the presence of chronic lung disease, emergency surgery, and steroid use.7 A multivariate analysis from Fischer et al. found that pneumonia after heart surgery is associated with a delay in extubation greater than 3.7 days.8

The presence of upper respiratory infection after cardiac surgery was associated with an increased incidence of respiratory complications, as well as stay in the pediatric intensive care unit, so it was a predictor of postoperative infection.9 However, the results of a study to determine the frequency and etiology of pneumonia in adult patients with major cardiac surgery showed that the value of monitoring cultures of bronchial aspirate for predicting pneumonia in ventilated patients is a diagnostic method that anticipates the etiology of pneumonia in only a small percentage of patients.6

Moreover, cardiac surgery can induce an acute inflammatory response characterized by hemodynamic and respiratory alterations that may cause confusion with an additional infectious process. This response results from a combination of several factors including exposure to non-smooth surfaces, surgical trauma, myocardial ischemia or reperfusion, or endotoxin discharge.10

Procalcitonin (PCT), initially described as a marker of infection, has emerged over the past decade as a specific and sensitive marker associated with bacterial infection.11,12 To determine the value of PCT as a marker of infection after cardiac surgery in adults, it was found that serum PCT is modified by the surgical event itself, with a transient peak of 1 μg/mL.13 In the presence of postoperative fever figures > 1 μg/mL are observed, suggesting systemic infection; change in figures of procalcitonin has also been observed in patients previously managed with antibiotics.14 Arkader et al. conducted a study in children and evaluated the behavior of PCT and C-reactive protein in patients undergoing cardiovascular surgery; they found that both rise after surgery with the difference that PCT decreases in the first day after surgery, while C-reactive protein may be elevated up to three days after surgery in pediatric patients who do not develop infection.15 PCT consequently has been investigated in several studies as a prognostic marker in heart surgery with a focus on the ability to predict or discriminate between infection and noninfectious complications.  

The aim of this study was to identify preoperative, intraoperative, and postoperative risk factors associated with the development of nosocomial pneumonia in pediatric patients undergoing cardiac surgery and to identify if PCT elevation in the postoperative period predicts the development of this complication.


After approval by the Research Committee, a prospective nested case-control study in a cohort was carried out at the Hospital de Pediatría del Centro Médico Nacional Siglo XXI. All patients admitted to the hospital scheduled for cardiovascular surgery were included. Study information was given to the patient's family, and signed informed consent was requested. Preoperative factors were obtained from medical records. Once in the pediatric unit intensive care unit (PICU) for postoperative recovery, clinical conditions were monitored daily and intraoperative (postoperative and anesthesia notes) and postoperative (nursing sheets and medical progress notes) factors were identified. Patients were tracked from admission to 72 hours after removal of cardiac devices (mediastinal catheters, pacemakers, etc.). A data record was made which was emptied into an SPSS database for analysis. Serum samples were collected to determine procalcitonin levels at 48 hours after surgery. Serum samples were kept at -72 °C for storage and were processed together at the end of the study.

A case was defined as a patient undergoing cardiac surgery admitted to the PICU who developed nosocomial pneumonia according to the Centers for Disease Control and Prevention (CDC) criteria. A control was defined as a patient undergoing cardiac surgery during the same study period admitted to the PICU, who did not develop nosocomial pneumonia. Patients who died within 48 hours of surgery were discarded. Pneumonia was defined as pulmonary infection acquired in the hospital 48 hours after PICU admission, according to the CDC criteria. The preoperative factors recorded included sex, age, nutritional status, immunocompromised status, hospital stay before surgery, and presence of upper respiratory tract infection. The intraoperative factors recorded were: durations of surgery, extracorporeal circulation, and aortic clamping, and blood transfusion. Postoperative factors recorded were surgical reoperation, time with mediastinal and pleural catheters in place, and appropriate use of antimicrobial prophylaxis. PCT determination was performed using BRAHMS PCT LIA (Hennigsdorf, Germany), a quantitative assay with a measuring range of 0.3 to 500 μg/mL with results in about two hours.

Descriptive statistics were used for the analysis of demographic variables, which were expressed as mean and standard deviation or median and ranges, according to their distribution. Chi-squared test was used to compare proportions between two groups. Student’s t test was applied for comparison of quantitative variables between groups, considered statistically significant at p < 0.05. ROC curves were used to choose the best cutoff value of procalcitonin determination. Univariate and multivariate analysis was used to identify risk factors significantly associated with nosocomial pneumonia. Data were analyzed with statistical program in the social sciences (SPSS) version 14.


Cohort description

188 patients undergoing cardiovascular surgery were included during the study period; eight were excluded for not meeting inclusion criteria. 52% were male. The age range was from one month to 84 months, and the average was 21 months. 44% of patients had chronic malnutrition and 16% severe malnutrition.

The main cardiological diagnoses were ventricular septal defect (16%), patent ductus arteriosus (13%), tetralogy of Fallot (11%) and atrial septal defect (9%). In 53% of patients the surgical procedure was open (sternotomy and extracorporeal circulation), and the rest of the procedures were closed (thoracotomy without extracorporeal circulation). The main surgical procedures performed in these patients were VSD closure (21.1%), ductus arteriosus closure (20%), and systemic-pulmonary fistula (16.7%).

72.8% of patients were given preoperative antimicrobial prophylaxis considered appropriate, and only one patient received third-generation cephalosporins before surgery. Upper respiratory tract infection was documented in two patients before surgery. 97 patients (53%) underwent extracorporeal circulation. 97.8% of patients required mechanical ventilation, and tracheal cannula remained in place an average of 36 hours; 10% of patients required reintubation. The average hospital stay before surgery was 1.9 days. Less than 2% of patients required reoperation, and in 4.4% sternotomy had to be left open after surgery. 65% of patients required transfusion with globular packages, with an average of 1.4 packages administered per patient. Mortality in the study cohort was 5%.

Frequency of nosocomial pneumonia in the cohort

After surgery, 27 patients developed pneumonia (15%), and the male to female ratio for the development of this complication was 2: 1, with predominance in the 1-29 month age group (21 cases).

78% of cases were diagnosed between two and five days after surgery. The frequency was higher in those who underwent complex surgical procedures: total correction of tetralogy of Fallot 60% (3/5), CAVP total correction 55% (6/11), Senning 100% (2/2).

100% of patients who developed pneumonia had received mechanical ventilation with an average of 120 hours, and 33% required reintubation. Of the three patients who had surgery for the second time, two developed pneumonia, as did all patients with a history of sternotomy left open after surgery.

There was microbiological recovery in blood cultures in only four cases of pneumonia; the recovered microorganisms were S. sanguis, S. aureus, E. coli, and P. aeruginosa. Mortality in the group of patients who developed pneumonia was 14%.

Risk factors for the development of pneumonia

To establish the risk factors of nosocomial pneumonia, only patients undergoing extracorporeal circulation were studied, since these patients have different factors than those who are not subject to this procedure; therefore, 83 patients were discarded, leaving 97, of whom 24 developed pneumonia (24.7%) (Figure 1).

Figure 1 Distribution of 180 patients subject to cardiovascular surgery, according to their clinical course, time of extracorporeal circulation, and procalcitonin determination. ECC = extracorporeal circulation; Tx = time; PCT = procalcitonin; no = no determination

Differences in the variables of gender, age, and nutritional status were not significant between patients with and without pneumonia. The frequency of open sternotomy, reintubation, and surgical wound infection was higher in the case group (p < 0.001), as shown in Table I.

The following factors were found statistically associated with risk of developing a pneumonic process: mediastinal catheter left in place more than five days: OR 3.63, 95% CI: 1.17-11.40; chest tube in place more than 5.25 days: OR 9.45, 95% CI: 2.61-35.7; surgery time (ST) higher than average (225 min): OR 6.77, 95% CI: 1.91-26.3; extracorporeal circulation time (ECCT) higher than average (89 min): OR 4.36, 95% CI: 1.65-15.42. 

Of the 97 patients included in the analysis, procalcitonin at 48 hours post-surgery to could only be determined in 63, of whom 21 belonged to the group of patients who developed pneumonia, and 42 to the group without pneumonia, with a median serum procalcitonin concentration of 4.42 mg/mL in the first group, which was significantly different (p < 0.05) from that of the second group (median of 0.45 mg/mL). Using ROC curve analysis, the cutoff of a concentration ≥ 1.7 mg/mL was taken as suggestive of pneumonic process. The sensitivity of the test to predict the development of a pneumonic process was 72% (95% CI: 50-93), specificity was 79% (95% CI: 65-92), with a positive predictive value of 63% (95% CI: 41-84), and a negative predictive value of 85% (95% CI: 72-97). In univariate analysis, procalcitonin concentration equal to or greater than the estimated cutoff value was associated significantly with the development of pneumonia (Table I).

Table I Univariate data analysis
Variable Pneumonia Without pneumonia OR CI (95%) p
Mean ± SD Mean ± SD
Age (in months) 23 ± 18.7 28.2 ± 17.4 0.576
Mechanical ventilation (in hours) 110 ± 136 23 ± 27 3.22 0.75-15.2 < 0.001 *
Surgery time (in min) 253 ± 77 163 ± 66 6.77 1.91-26.3 < 0.001 *
ECC time (in min) 106 ± 58 38 ± 50 4.96 1.65-15.42 < 0.001 *
AC time (in min) 53 ± 34 17 ± 25 2.64 0.89-8.04 < 0.001 *
PC time in place (in days) 5 ± 10 2 ± 7 9.45 2.61-35.7 < 0.001 *
MC time in place (in days) 5 ± 12 4 ± 9 3.63 1.17-11.4 < 0001 *
n % n %
Sex: male 15 62 38 52 0.480
Malnutrition 18 75 36 49 0.145
Appropriate surgical prophylaxis 21 87 57 78 0.244
Open sternotomy 8 33 0 0 < 0.001?
Reintubation 6 25 1 1 < 0.001?
Reoperation 2 8 1 1 0.150
Bacteremia 3 12.5 6 8 0.392
Surgical wound infection 3 12.5 1 1 0.046?
Procalcitonin ≥ 1.7 μg/mL 15 62.5 10 13.69 < 0.001?
*Student's twas used; ? Chi-squared was used
OR = odds ratio; CI = confidence interval; ECC = extracorporeal circulation; AC = aortic clamp; PC = pleural catheter;
MC = mediastinal catheter;

Of the variables subjected to univariate analysis, only a history of open sternotomy and serum procalcitonin concentration equal to or greater than 1.7 mg/mL were independently associated with the development of pneumonia when subjected to multivariate analysis (Table II).

Table II Predictors of nosocomial pneumonia in patients undergoing cardiovascular surgery. Multivariate logistic regression analysis
Variables p RR CI
Procalcitonin ≥ 1. 7 μg/mL 0.023 1.22 1.05 2.22
Open sternotomy 0.024 1.07 1 2.03
RR = risk ratio; CI = confidence interval


Although there are well-established clinical criteria for the diagnosis of nosocomial pneumonia in patients undergoing cardiovascular surgery in the first postoperative days, it is sometimes difficult to perform them, due to systemic inflammatory response secondary to the surgical trauma, including presence of fever within the first 24 to 48 hours, hemodynamic instability, and even difficulty in interpreting radiology.

The purpose of this study was to evaluate risk factors associated with the development of nosocomial pneumonia, including determination of serum procalcitonin at 48 hours post-surgery, in a homogeneous group of pediatric patients who underwent a cardiovascular surgery. Prior studies have been reported in adult subjects and some pre- and postoperative risk factors have been established;16 however, in the group of children requiring heart surgery, there are few reports on risk factors before, during, and after surgery.

The frequency of nosocomial pneumonia developed after cardiovascular surgery observed in our study was higher than those reported by Bongo and Jashiashvili in the Philippines and Georgia, respectively, which were < 5%.17,18 This increase can be explained by the differences in the populations studied, as those studies involved school-age and adolescent patients unlike this one, where infants predominate, who, due to incomplete immune system development and nutritional deficits in most of them, would be expected to have increased frequency of infections in general.

Our study showed that intraoperative risk factors were the main factors associated with the development of pneumonia.

History of having undergone extracorporeal circulation divided the study cohort into two groups. Those who were not subjected to this procedure had a low frequency of pneumonia, unlike those who had undergone this event, who presented eight times the infection rate. The mere fact of undergoing cardiovascular surgery such as extracorporeal circulation leads to a stress response manifested by evidence of systemic inflammatory response and release of stress hormones. One mechanism is by activation of the immune system, which behaves differently in children than it does in adults, immune response varying and with it the vulnerability to developing infections.19   

Pulmonary endothelial damage in patients undergoing thoracotomy without extracorporeal circulation has already been described, with the consequent development of local inflammation and subsequent infection.

Moreover, the mere fact of having a prolonged surgery with extensive tissue trauma facilitates contamination of the surgical field and the development of infection. While cardiovascular surgery is characterized by its complexity, and the time needed to complete it is higher than other surgeries, there are risk factors described in adults for the development of pneumonia, most of them postoperative, including reintubation, management with globular packages, and use of nasogastric tube. These factors may have relevance in pneumonic processes developed late in the postoperative period; however, in pneumonias developed between the second and fifth day after surgery it is likely that other factors involved during it are important. In our study the times during surgery, especially surgical time and extracorporeal circulation time, were risk factors associated with pneumonia, even though they were not significant in the multivariate analysis. In studies similar to ours (retrospective and prospective, and also in children), it has been found that ECCT and aortic clamping time are risk factors for developing pneumonia after cardiovascular surgery.20,21

New risk factors, such as history of open sternotomy and surgical wound infection, are described in this study, which may relate to the extent of surgical trauma.

History of being under mechanical ventilation makes this type of patient susceptible to development of pneumonia. There are reports in which this is mentioned as a risk factor for its development;22 however, we found no significant association: 70% of patients developed the pneumonic process in the first days after undergoing the surgical procedure and, therefore, it appears to be a consequence and not a cause of infectious process.

As previously mentioned, it is difficult to differentiate between inflammation and infection soon after cardiovascular surgery; therefore, the behavior of procalcitonin serum levels was evaluated as part of the risk factors for developing pneumonia. Aouifi et al.13 reported values ​​of 1.36 mg/mL in adults subject to cardiovascular surgery in the immediate postoperative period; these values ​​declined in the next three days, as in our patients subject to extracorporeal circulation without development of pneumonia, in whom the average was 0.45 g/mL at 48 hours post-surgery. The same report claims a concentration of this marker of 4.85 mg/mL in patients who developed bacteremia or pneumonia, similar to that found in our group of pediatric patients with pneumonia (4.42 mg/mL). 

Elevated procalcitonin levels have been associated with prolonged surgical procedures, as well as with the intraoperative development. It is reported that these levels may persist until the third day in children. In our study, most patients with a high level of procalcitonin underwent prolonged surgery such as total correction of tetralogy of Fallot or Senning.

It is likely that a high concentration of procalcitonin the second postoperative day depends on the peak level at 24 hours from the initial surgical trauma and, since the half-life is constant (18-24 hours), this level will be different in each patient. Moreover, if an infectious process is added, that level can increase. In our study, several patients developed pneumonias belatedly, with high initial procalcitonin numbers, which highlights the importance of severe initial inflammatory reaction predisposing to the development of a pneumonic process.

A recent systematic literature review on the behavior of procalcitonin levels in postoperative cardiac surgery patients indicates that the kinetics of this molecule in the first postoperative days seems to be more useful for identifying infectious complications than an isolated value. However, in the current report, the sensitivity and specificity to predict a pneumonic process using only one determination at 48 hours after surgery were not very different from those reported by other authors for detecting an infectious process.23

Moreover, other factors such as the host’s genetic constitution can influence both susceptibility to infection and response to surgical trauma, which could make procalcitonin values​​ between individuals different.


In this study we observed that time of extracorporeal circulation analyzed in conjunction with procalcitonin values can provide early diagnostic help: we note that these two parameters being elevated helps detect almost 60% of patients with nosocomial pneumonia complications and, therefore, to establish early or preventative antimicrobial therapy; however, new prospective studies with homogenized study populations are necessary to confirm or establish new risk factors and to propose early treatments to reduce the frequency of this type of pneumonia in pediatric patients.

Important note
This protocol competed and obtained funding in the 2005 second call for applications of the IMSS Fondo de Fomento a la Investigación with the number 2005/1/I/180. It was registered with the Local Research Committee under No. 2005/3603/081.
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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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