Journal of Respiratory and Lung Diseases

Clinical Outcomes of Pulmonary Hypertension in Children with Pneumonia and Respiratory Failure

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Pubslished Date: May 15, 2017

Clinical Outcomes of Pulmonary Hypertension in Children with Pneumonia and Respiratory Failure

María C. Guzmán1,2,4, Ledys M. Izquierdo2,3,4, Darling Carvajal4, Beatriz Duque4, and Carlos Rodriguez-Martinez1,5

1Department of Pediatrics and Critical Care Pediatric El Bosque, University of Bogota, Colombia

2Pediatric Intensive Care Unit, Santa Clara Hospital Bogota, Colombia

3Intensive Care Unit, Central Military Hospital Bogota, Colombia

4Pediatrician Intensivist El Bosque University Bogota-Colombia

5Department of Pediatrics, School of Medicine, National University of Colombia, Central Military Unit Research Hospital, Bogota, Colombia

*Corresponding author: Ledys M. Izquierdo, Department of Pulmonary and Critical Care Pediatric El Bosque, University of Colombia, Tel: 571- 348-6868 ext. 5125; E-mail: ledysmai@gmail.com.

Citation: Guzmán MC, Izquierdo LM, Carvajal D, Duque B, Rodriguez-Martinez MC (2017) Clinical Outcomes of Pulmonary Hypertension in Children with Pneumonia and Respiratory Failure. J Resp Dis 1(1): 107.

 

Abstract

 

Background: Pulmonary hypertension (PH) is a disease with increasing prevalence (5–25 cases/million inhabitants) and an incidence of 1–2.4 cases/year/million inhabitants [1]. The association between pulmonary arterial hypertension and acute respiratory diseases is less clear. The principal objective of this study is to investigate the association between PH and mortality, duration of hospital stay, and incidence of Multiple Organ Dysfunction Syndrome (MODS) in children with lower respiratory tract infection and respiratory failure.

Methods: This was a prospective observational cohort study conducted over a period of three years. All pediatric patients were included if required mechanical ventilation, secondary to acute respiratory infection, for more than 24 hours and if they were admitted to the Pediatric Intensive Care Unit (PICU).

A Receiver Operating Characteristic (ROC) curve was used to determine the best cut-off point of Pulmonary Artery Systolic Pressure value (PASP) and to differentiate between patients with and without mortality.

Results: Of the 631 patients admitted to the PICU during the study period, only 120 met the inclusion criteria. Of these, 82.5% (99) were diagnosed with PH, and 97.9% (97) fulfilled the Berlin criteria for Acute Respiratory Distress Syndrome (ARDS). The overall mortality rate was 10.1%. The ROC analysis revealed an optimal threshold value of PASP of 54 mmHg (area under the ROC curve: 0.855; 95% CI: 0.768–0.943) for discriminating between patients with and without mortality. The length of stay in the PICU, the incidence of MODS, and the mortality rate were higher in patients with PH than without PH.

Conclusions: The incidence of PH in children with lower respiratory tract infection, respiratory insufficiency, and ARDS is high and affects several clinical outcomes, such as mortality, PICU stay, duration of mechanical ventilation, and MODS.

Keywords: Pulmonary Hypertension; Pneumonia; Bordetella Pertussis; Right-Sided Heart Failure, Respiratory Insufficiency

Abbreviations

 

PH: Pulmonary Hypertension; ARDS: Acute Respiratory Distress Syndrome; PICU: Pediatric Intensive Care Unit; MODS: Multiple Organ Dysfunction Syndrome; PASP: Pulmonary Artery Systolic Pressure value.

Introduction

 

Pulmonary hypertension (PH) is an elevation in pulmonary artery pressure, usually due to small pulmonary artery disease, is hemodynamically defined as the presence of a mean pulmonary artery pressure (PAPm) ≥ 25 mmHg at rest, with a pulmonary capillary wedge pressure of ≤15 mmHg [2]. It has been associated with acute respiratory distress syndrome (ARDS) since 1977, when Zapol and Snider [3,4] reported increased pulmonary vascular resistance and PH in all of the ARDS patients in their series. They also noted that the survivors had a progressive decrease in pulmonary vascular resistance over the evolution of the disease, whereas the non-survivors tended to have stable or increased pulmonary vascular resistance [5].

For several years, the literature has reported cases of PH associated with acute respiratory diseases via mechanisms that include hypoxic pulmonary vasoconstriction, respiratory and metabolic acidosis, changes in lung volume, increased viscosity, compression by edema, and remodeling of the vessel walls, which directly affect pulmonary vascular resistance [6,7]. Most of these reports have highlighted associations between PH and Bordetella pertussis infection, acute bronchiolitis, or pneumonia; however, these associations correspond to a small series of cases and lack sufficient strength for forming recommendations [8].

Now, due to the introduction of echocardiography in pediatric intensive care units (PICUs) [9], it is possible that reports of PH will increase and the effects of PH on prognosis and outcomes can be better described [9,10].

In Colombia, an association between ARDS and PH in the PICU was reported in a study by Izquierdo et al [11], who described statistically significant associations between PH and mortality and the development of hematologic failure. The main objective of the present study was to investigate the associations between PH and mortality, duration of hospital stay, and incidence of multiple organ dysfunction syndrome (MODS) in children with lower respiratory tract infection and respiratory failure.

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Methods

 

Design

This was a prospective observational cohort study.

Study Population

All patients were greater than 42-week corrected gestational age and less than 18 years old. The pediatric patients who were included in this study were admitted to the PICU of Santa Clara Hospital (a referral center for respiratory diseases with an 8-bed capacity that is located in the city of Bogota at 2,600 meters above sea level) between January 2011 and January 2014. The patients included, also presented with respiratory failure defined as a need for endotracheal intubation and a requirement for mechanical ventilation for over 24 hours. Patients with respiratory malformations (upper or lower airway diseases, post-operative lung pathology, etc), cyanotic heart disease or who had limitation of therapeutic effort orders were excluded. Non-probability sequential convenience sampling was used. The study was approved by the Ethics Committee on Human Research of Santa Clara Hospital.

Data Collection

The data collection method was non-participant direct observation, and a database was created where the processing of the collection form and data storage were performed in an Excel® spreadsheet (Microsoft Corporation, Redmond, WA) that contained epidemiological, demographic, clinical, and paraclinical data. The severity of disease was measured using the Pediatric Risk of Mortality (PRISM) scale [12] within the first 24 hours of admission to the PICU. Ventilatory parameters were assessed at two points: At the time of the echocardiogram and the worst ventilatory parameters that the patient would have had during their stay in PICU. Arterial and/or venous blood gases were analyzed to evaluate the diagnostic criteria of ARDS according to the Berlin definition [13]. For patients with no arterial catheter, saturation/FiO2 was analyzed instead with adjustments for the altitude of Bogota (PaO2/FiO2 (barometric pressure/760)). The presence of MODS was determined by screening for dysfunction of the cardiovascular, respiratory, hematologic, hepatic, renal, neurologic, and gastrointestinal organ systems was defined according to the 2005 Goldstein et al criteria [14], in the International Consensus Conference on Pediatric Sepsis: definitions for sepsis and organ dysfunction in pediatrics [14,15]

The impact of PH associated with acute respiratory infection in the study population was evaluated in terms of mortality at PICU discharge, length of stay in the PICU, fit to PICU discharge 24 hours post extubation or withdrawal of inotropic and / or vasoactive support if they were stable, and MODS [14].

PH Definition

PH was considered when the pulmonary artery systolic pressure (PASP) exceeded 35 mmHg; mild PH was defined as PASP less than 45 mmHg, moderate PH as PASP between 45 and 70 mmHg, and severe PH when PASP higher than 70 mmHg [16,17]. A complete pediatric echocardiography study was performed in the first three days after admission to the PICU, and a control echocardiogram was performed according to the clinical course of the patient. The echocardiography was performed by the pediatric cardiologist of the institution (two operators, with extensive experience in pediatric echocardiography), who systematically evaluated PASP during the procedure using transthoracic echocardiography with an HP Philips Sonos 4500 ultrasound machine equipped with a pediatric transducer. The method used by the pediatric cardiologist involved the quantification of tricuspid insufficiency by 2D and Doppler echocardiography in the four-chamber view during systole. The continuous wave Doppler sample was located at the tricuspid valve as parallel to the regurgitant flow as possible to minimize the angle between the ultrasound beam and the regurgitant flow (16). The central venous pressure (CVP) value was used to determine the pressure of the right atrium (RA) and add it to the gradient of the regurgitant flow [17,18]. The presence of indirect signs of PH (size of the right chambers paradoxical movement of the septum, flattening of the interventricular septum) was taken into account to support the diagnosis [19,20].

Outcomes

The primary outcome, mortality at PICU discharge. Secondary outcomes included the duration of PICU stay and MODS.

Statistical Analysis

Data were analyzed using STATA (version 12.1; College Station, TX). Data are presented as medians with interquartile ranges for continuous variables and frequencies with proportions for categorical variables. Comparisons between groups were performed using the Kolmogorov-smirnov normality test and the Wilcoxon tests for related samples and Mann Witney -Student’s t-test for independent samples. Differences between categorical variables according to the presence or absence of PH were analyzed using the chi-square test or Fisher's exact test. The outcomes that were measured in the multivariate analysis were mortality, length of stay in the PICU, and MODS. Several logistic regression models were used for estimating the odds ratios (ORs), with their respective 95% confidence intervals for identifying independent risk factors and predictors of mortality. A receiver operating characteristic (ROC) curve was used to determine the best cut-off point for pulmonary pressure to discriminate between patients with and without mortality.

Interventions: none.

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Results

 

Among all the patients admitted to the PICU during the study period, 631 were included in the PICU database (only patients with mechanical ventilation and or inotropic or vasoactive support), 206 had respiratory failure of different etiologies and 120 fulfilled the inclusion criteria (Figure 1). Of these patients, 82.5% (99) were diagnosed with PH, and 97.9% (97) met the consensus criteria ARDS [13] (Table 1). A description of the patients is presented in Table 1. The overall mortality was 10%, and there was no mortality among patients without PH or ARDS. The most common cause of respiratory infection was bronchiolitis, followed by pertussis-like syndrome and pneumonia. More than 57% of patients had 3 or more organ dysfunction, being, the hematological and renal dysfunction statistically more frequent in patients with PH (Table 1).

Figure 1: Patients Selection.

 

Table 1: Patients Characteristics PH: Pulmonary Hypertension; PRISM: Pediatricrisk Of Mortality scale; IQR: Interquartile ranges; %: Percentage; PICU: Pediatric Intensive Care Unit; ARDS: Acute Respiratory Distress Syndrome; MODS: Multiple organ dysfunction Syndromes

 

The ROC curve analysis revealed that, for discriminating between patients with and without mortality, the optimal threshold value of pulmonary pressure was 54 mmHg (area under the ROC curve: 0.855, 95% CI: 0768–0943) (Figure 2).

Figure 2: ROC Curve

 

The  bivariate analysis with a cutoff value of 54 mmhg for the PSAP according to the ROC curve, showed a longer PICU stay (OR 95% CI: 4.6 (1.77–11.9)), higher mortality   (OR 95% CI: 7.55 (1.79–31.8)), a longer duration of mechanical ventilation (OR 95% CI: 2.8 (1.09–7.13)), and a higher incidence of  hematologic, renal, and hepatic dysfunction (OR 95% CI: 6.2 (1.73–22.2), 27.86 (8.33–93.12), and 15.2 (1.68–135.08), respectively). These associations all had a p-value of < 0.05 (Table 2). There was no difference in the oxygenation variables (PaO2, PaO2/Fio2, Saturation/fio2 and Oxygenation index, OI) in patients with or without PH at any of the two cut off values of PSAP, 35 and 54mmhg.

Table 2: Bivariate analysis between variables analyzed in the study and the value of pulmonary systolic pressure categorized according to result obtained ROC Curve Systolic Pulmonary (MODS: Multiple organ dysfunction Syndromes; %: Percentage; ROC: Receiver Operating Characteristic Curve;PICU: Pediatric Intensive Care Unit).

 

The values of PEEP (Positive end-expiratory pressure), PIP (peak inspiratory pressure), and P plateau (pressure plateau), which were assessed when the echocardiogram was performed, did not differ significantly between patients with and without PH (Table 3). No difference was found either when the cut-off value used was (PEEP: 5.70 vs. 6.01, p = 0.127; PIP: 20.4 vs. 21.1, p = 0.272; P plateau: 17.5 vs. 18.4, p = 0.187, respectively) (Table 3).

Table 3: Ventilation Parameters found in the first Echocardiogram in patients with and without pulmonary hypertension according to ROC curve point (ROC: Receiver Operating Characteristic Curve; PH: Pulmonary Hypertension; PIP: Peak Inspiratory Pressure ; PEEP: Positive End-Expiratory Pressure; Pplateau: Pressure Plateau , FIO2: Fraction Of Inspired Oxygen ; RR: Rate Respiratory)

 

A direct relationship was found between PaCO2 (Partial pressure of carbon dioxide) and pulmonary pressure: the mean PaCO2 value was higher in patients with PH than in those without PH, with the two cut-off values, 35 and 54mmhg, and it increased as the pulmonary pressure increased (p < 0.05) (Table 4).

Table 4: Average PCO2 values associated without PH and with PH, according to values PASP major of 35 mmHg and according to ROC curve point 54 mmHg PASP. (PH: Pulmonary Hypertension; PASP: Pulmonary Artery Systolic Pressure; PaCO2: Partial pressure of carbon dioxide)

 

A report of the control echocardiogram was found in only 30 patients (25%), with this small number is difficult to draw any conclusion, but there was as a decrease in the PSAP in patients who survived of a mean of 14 mmhg and no decreased or increase in patients who died. Only three patients who died had the control echocardiogram reported in the record, mean decrease of 0.6 mmhg of the PSAP.

Table 5: Multivariate analysis between the variables analyzed in the study and the value of systolic pulmonary artery categorized with the highest value of 54mmHg PASP. (PASP: Pulmonary Artery Systolic Pressure)

 

The multivariate analysis revealed that, after adjusting for age and PRISM score, patients with PASP values higher than 54 mmHg had a significantly longer duration of mechanical ventilation and a higher probability of dying compared to patients with PASP values less than 54 mmHg (coefficient = 5.70, CI 2.91–8.49, p < 0.001; and OR = 8.4; 95% CI: 1.95–36.4, p < 0.001, respectively) (Table 5).

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Discussion

 

Among patients with PH admitted to PICU, moderate to severe PH was associated with worse MODS, more length of PICU stay and high overall mortality as compared with patients without PH. The PH was present in approximately 82% pediatric patients with ARDS and was independently associated with poor outcomes. Children with PH (PASP values higher than 54 mmHg)-associated ARDS, had more than double the odds of death at PICU and had a significantly longer duration of mechanical ventilation than children without PH. Our results suggest that the patients who survive reduce PH compared to those who die. The aim of this study was not to evaluate the type of therapy performed, although we think subjectively that low mortality in these critical patients is due to timely diagnosis and aggressive management of PH and right ventricular dysfunction frequently present in these critical patients.

Respiratory diseases are the leading cause of admission to PICUs [11]. In our area, respiratory diseases secondary to infection continue to be a public health problem associated with considerable mortality [11]. The progress of an infection to respiratory failure is frequently accompanied by systemic inflammatory compromise, sepsis, diffuse alveolar damage, and ARDS with progression to MODS, which significantly increases mortality [21]. Although we believe that the altitude can influence the presentation of PH in patients with acute respiratory infections, due to a lower oxygen inspiratory pressure, we did not compare the frequency or the outcome of children in other altitudes.

Our data confirm that PH is an important risk factor and has a strong independent association with worse outcomes. Future efforts are required to evaluate, if a reduction in PH improves survival, identify factors associated with the development of PH and prospectively test interventions.

Our findings on the association of respiratory failure and PH with worse outcomes confirm what has been described in adult PH studies. As reported by Bull et al (22), on patients with ARDS, pulmonary vascular failure is an independent risk factor for higher mortality at 60 days, decreased number of ventilation-free days, longer intensive care unit stay, and greater need for cardiovascular support.

This study showed a high incidence of PH and MODS in children with acute respiratory infection and respiratory failure not dependent on the ventilator parameters, as well as a strong association between the severity of hypertension and the outcome. MODS has been demonstrated to be correlated with risk of mortality in both adults [23] and children [24,25]. A study by Rossi et al [24] demonstrated that MODS involving three or more dysfunctional organs were associated with a mortality rate of 90%. In our study, MODS was very common and was significantly associated to PH., when, renal and hematologic dysfunction was present.

The pathophysiology of ARDS involves both alveolar and capillary compromise [22]; however, ARDS therapy and research have generally focused on mechanical ventilation strategies and anti-inflammatory therapies (and sometimes coagulation inhibition) but have not addressed as much, the management therapy of PH, right ventricular dysfunction, and its consequences. Clinical observations, pathology findings, echocardiogram findings, and, in particular, evolution have led to the suggestion that pulmonary vascular injury produced by an imbalance between vasodilators (nitric oxide, prostacyclin, normoxemia, and normocarbia) and vasoconstrictors (such as hypoxic vasoconstriction, hypercapnia, alveolar collapse, thromboxane A2, and endothelin) is a determining factor in the clinical picture and evolution of these patients, especially in children younger than 4 months, whose pulmonary vascular resistance has not decreased to the level of older children and adults [22,26].

The degree of PH showed a direct relationship with the level of PaCO2, which is correlated with the pathophysiology of pulmonary vascular injury or pulmonary vascular dysfunction, a term that encompasses all phenomena that occur in the pulmonary vessels due to multiple causes [26]. Because hypercapnia can be due to vascular collapse or alveolar over distention and often considered benign or even beneficial during mechanical ventilation, these findings may have important clinical implications, because  PH with  deteriorated right ventricle (RV) function, need a lung-protective ventilation that gradually adapt and limit hypercapnia and RV overload [27–29]. This concept can be summarized in the advice that physicians should consider management strategies that promote "what it is good for the RV and good for the lungs" [29].

However the study by Mekontso [27] found that more than 60% of patients with PH and low PEEP had an RV/LV end-diastolic area ratio greater than 0.6, which was closely associated with RV systolic overload than with the PEEP levels. This finding indicates that ventilator parameters not always influence the presence of PH. A pulmonary volume that tends to the collapse also is accompanied of a high vascular resistance.

This effect of the ventilator parameters, in the pulmonary vasculature was not seen in the present study, probably because they were in the protective ventilation range; no differences in ventilator parameters assessed at the time of echocardiography, were found between patients with and without PH. This results leads to the following questions: in the era of protective ventilation, can PH be due to vascular injury rather than ventilator pressure?

The level of PSAP did not correlate with the levels of oxygenation measures, but it did with the level of PCO2 which correlates with the pulmonary vascular dysfunction.

Strengths

 

To our knowledge, this is the first study with these characteristics which has been conducted in Colombia. This study will be used as a basis for designing future studies to track patients and observe the frequency and evolution of PH. This work will also serve as a basis for designing other studies to identify the course of ARDS, including the evaluation of therapeutic strategies that can be applied in a timely manner to potentially decrease the morbidity and mortality of patients. The results found in our study are consistent with those reported in the literature, which we believe strengthens the internal validity of our study. Also, most of the studies have been done in the adult population, whilst this is a Pediatric study.

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Limitations

 

The limitations of this study were the use of a sample of 120 patients from a single center and the observational study design, which prevents the evaluation of the effects of management strategies used during the illness and other factors such as the high altitude might be influencing the incidence of PH and were not evaluated.

Conclusions

 

The incidence of PH in children with low respiratory infection that progress to respiratory insufficiency and ARDS, is high and has an impact on several clinical outcomes, such as mortality, length of PICU stay, duration of mechanical ventilation, and MODS. The causes of PH are multiple can be detected as an increase in dead space. Pulmonary pressure that does not improve is associated with increased mortality. Although we believe that altitude can influence the presentation of PH in patients with acute respiratory infections, studies conducted at different altitudes are needed to assess the impact of this factor. The identification and treatment of PH in patients with respiratory pathologies can reduce morbidity and mortality.

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References

 

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Copyright: © 2017 Guzmán MC, et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.