|Year : 2019 | Volume
| Issue : 3 | Page : 1043-1050
Study of lung ultrasonography as a diagnostic tool in childhood pneumonia
Ghada M Elmashad1, Wael A Bahbah1, Waleed A Mousa2, Mostafa M Shalaby3
1 Department of Pediatrics, Faculty of Medicine, Menoufia University, Shibin El-Kom, Egypt
2 Department of Radiology, Faculty of Medicine, Menoufia University, Shibin El-Kom, Egypt
3 Department of Pediatrics, Shibin El-Kom Teaching Hospital, Shibin El-Kom, Egypt
|Date of Submission||25-Nov-2017|
|Date of Acceptance||20-Jan-2018|
|Date of Web Publication||17-Oct-2019|
Mostafa M Shalaby
Department of Pediatrics, Shibin El-Kom Teaching Hospital, Shibin El-Kom, Menoufia 33511
Source of Support: None, Conflict of Interest: None
The aim of this study was to compare chest ultrasonography with chest radiography (CXR) in the diagnosis of children with pneumonia.
In Egypt, pneumonia and other acute respiratory infections were the causes of death in ∼19% of children younger than 5 years. According to current guidelines, pneumonia is diagnosed by clinical history, respiratory rate, fever, respiratory signs, and symptoms.
Patients and methods
A cross-sectional study was conducted on 60 patients with fever and signs of respiratory distress, and they were divided in two groups: group I with pneumonia, which included 45 patients who were finally diagnosed as having clinically evident pneumonia, and group II without pneumonia, which included 15 patients who did not have pneumonia. Full history taken, clinical examination, laboratory investigations, CXR, and chest ultrasonography were done.
There was no statistically significant difference between the two groups regarding age, birth order, weight, residence, parent's education, and employment. C-reactive protein level was higher in pneumonia group than nonpneumonia group (P < 0.001). Lung ultrasonography could detect consolidation in more than one lobe than CXR, which was statistically significant (P = 0.048).
Chest ultrasonography offers an important contribution to the diagnostic procedures of pleuropulmonary disorders in children, such as pneumonia and pleural effusion, with higher sensitivity, specificity, and positive predictive index compared with CXR.
Keywords: pleural effusion, pneumonia, radiographies, respiratory rate, ultrasonography
|How to cite this article:|
Elmashad GM, Bahbah WA, Mousa WA, Shalaby MM. Study of lung ultrasonography as a diagnostic tool in childhood pneumonia. Menoufia Med J 2019;32:1043-50
|How to cite this URL:|
Elmashad GM, Bahbah WA, Mousa WA, Shalaby MM. Study of lung ultrasonography as a diagnostic tool in childhood pneumonia. Menoufia Med J [serial online] 2019 [cited 2019 Nov 12];32:1043-50. Available from: http://www.mmj.eg.net/text.asp?2019/32/3/1043/268849
| Introduction|| |
Respiratory infections have always been considered a worldwide health problem and a major cause of morbidity and mortality, with infants and young children especially susceptible . Among these infections include pneumonia, which is a form of acute respiratory infection that affects the lungs. When a child has pneumonia, the alveoli are filled with pus and fluid, which makes breathing painful and limits oxygen intake . Children with community-acquired pneumonia (CAP) may present with fever, tachypnea, breathlessness or difficulty of breathing, cough, wheeze, or chest pain. They may also present with abdominal pain and/or vomiting and may have headache . Children with upper respiratory tract infection and generalized wheeze with low-grade fever do not have pneumonia .
Pneumonia accounts for almost one million deaths every year, with 922 000 in 2015, which is 16% of total deaths among children younger than 5 years, 5% of which are neonates . This makes it the single most common cause of child deaths worldwide . Despite having made some progress, a 51% decrease in pneumonia from 2000 to 2015, it is nowhere near the greater than 86% decrease in malaria-related under-five mortalities in the same time frame . There is still a significant road ahead to make a marked reduction in the preventable and treatable deaths owing to pneumonia . However, in Egypt, it was estimated that 19% of children deaths below the age of 5 years are likely caused by pneumonia and other acute respiratory infections .
In 1986, Weinberg et al.  described a new method for evaluating CAP, using lung ultrasonography (LUS). For many years, transthoracic ultrasound was limited exclusively to the examination of pleural effusions . However, over the past few years, ultrasonography of the pleural space and lung parenchyma is gaining a wide consensus in different conditions in clinical practice, particularly in emergency conditions ,. Chest ultrasound allows prompt management based upon reproducible data and generates fewer computed tomography examinations, thereby decreasing irradiation, delays, cost, and discomfort to the patient . Point-of-care ultrasound imaging, performed at the patient's bedside, decreases the delays of chest radiography (CXR) in diagnosis of pulmonary diseases . The aim of this work was to compare chest ultrasonography with CXR in the diagnosis of children with pneumonia.
| Patients and Methods|| |
A cross-sectional study was conducted on 60 patients with fever and signs of respiratory distress aged from 12 to 60 months. They were enrolled from patients attending the Pediatric Department, Shibin El-Kom Teaching hospital, Menoufia Governorate, Egypt, during the period between October 2016 and March 2017. All study patients were divided in two groups:
- Group I was the pneumonia group, which included 45 patients who were finally diagnosed as have clinically evident pneumonia
- Group II was the nonpneumonia group, which included 15 age-matched and sex-matched patients who were clinically categorized as the nonpneumonia group (11 patients were diagnosed as having bronchiolitis and four patients were diagnosed as having acute bronchitis).
The study was approved by the Ethical Committee of Menoufia Faculty of Medicine, and oral consent was taken from at least one parent or caregiver of children included in the study. The participants included in this study were selected according to inclusion and exclusion criteria.
The inclusion criteria were presence of fever together with increased respiratory rate more than expected for age and other signs of dyspnea: dyspnea grade I (tachypnea), dyspnea grade II (subcostal and intercostals retraction and working accessory muscles of respiration), dyspnea grade III (grunting), and dyspnea grade IV (cyanosis) .
Patient with co-existing chronic lung disease or predisposing congenital abnormalities were excluded from the study.
All included patients were subjected to the following:
Full history taking, for example, demographic data included age, sex, residence, smoking habits in the families, and history of respiratory illness. Symptoms of respiratory tract infection before hospitalization were recorded upon admission, including the onset and duration of cough, fever, dyspnea, tachypnea, and rhinorrhea. Feeding, hydration status, and urine output were considered.
Complete physical examination including the following:
General examination included vital signs, which comprised assessment of temperature, heart rate, blood pressure, respiratory rate, and capillary refilling time .
Systemic examination included examination of chest, heart, and abdomen.
Standardized clinical assessment was done laying stress on chest examination, which included inspection of both sides of the chest (decreased chest movement on affected side) and chest percussion (dullness over affected part), and chest auscultation, which included air entry (diminished on affected area), breath sound (bronchial breathing on consolidating part), and adventitious sounds (wheeze/crepitations).
On admission, a blood sample was taken for assessment of total white blood cell count with manually verified differential count, hemoglobin, platelet count (Sysmex N1000; Kobe, Hyogo Prefecture, Japan), and quantitative assessment of serum C-reactive protein (CRP) (Copas 6000 analyzer; Roche Diagnostics, Indianapolis, Indiana, USA).
Chest radiography (posteroanterior view)
Posteroanterior CXR were done to patients in supine position and recorded by commercially available radiography machines. In accordance with the British Thoracic Society Guidelines, in children, lateral radiographs were not obtained.
Lung ultrasound immediately was done after plain radiography by a certified pediatric radiologist who was blinded to the CXR. Chest ultrasound is performed using a Toshiba XARio with 3–5 MHz convex transducer, which can visualize deeper lung structures (Toshiba, Minato-ku, Tokyo, Japan). A high-frequency 5–12 MHz linear-array probe is most effective in visualizing the chest wall, pleura, and the lung peripheral parenchyma.
Small infants are easily examined with high frequency (linear transducers), whereas older children require lower frequency transducers (convex transducers). Smaller footprint sector or vector transducers are needed to insonate between ribs, below the diaphragm, or from the suprasternal notch. Linear transducers are valuable for examining chest wall lesions .
Useful acoustic windows are depicted in the relatively unossified thorax of the infant, along with the presence of a relatively large thymus, which allows imaging of the anterior chest and thymus and sternal and costochondral cartilages. Suprasternal or supraclavicular approaches may also be useful in examining the anterior mediastinum and thoracic vessels.
Results were tabulated and statistically analyzed by using a personal computer using Microsoft Excel 2016 and SPSS v. 22 (IBM Corp., Chicago, Illinois, USA). Statistical analysis was done using descriptive measures, for example percentage, mean, and SD for quantitative parametric measures in addition to both number and percentage for categorized data, and analytical measures, for example independent t-test and χ2-test. A value of P less than 0.05 was considered statistically significant.
| Results|| |
Of the total 60 patients who were admitted to the department with suspected pneumonia, 45 patients (29 male and 16 female) were finally diagnosed clinically with pneumonia, with mean age of 24.11 ± 9.42 months (range: 12–60 months), mean weight of 12.66 ± 2.13 kg (range: 9–20 kg), and mean length of 82.04 ± 8.02 cm (range: 53–106 cm). There was no statistically significant difference (P > 0.05) between the pneumonia and nonpneumonia groups regarding age, sex, order of birth, weight, length/height, residence, mother's education, mother's employment, father's education, father's employment, and passive smoking [Table 1].
|Table 1: Demographic and clinical characteristics of all studied patients|
Click here to view
There was no statistically significant difference (P > 0.05) between the pneumonia and nonpneumonia groups regarding hemoglobin, platelets, total leukocyte count, and lymphocyte (%). However, neutrophil count (P = 0.041) and CRP level (P < 0.001) were significantly higher in pneumonia group than nonpneumonia group [Table 2].
|Table 2: Hemoglobin, platelets, total and differential leukocytic counts, and C-reactive protein distribution among the studied cases|
Click here to view
CXR showed that consolidation was diagnosed in 88.9% and effusion in 15.6% of pneumonia cases. However, patients without pneumonia had consolidation in 13.3%, and no pleural effusion was detected. LUS was diagnostic in 95.6% of pneumonia cases, which was statistically highly significant (P < 0.001). Moreover, LUS could detect more obvious findings in pneumonia cases compared with nonpneumonia cases, as seen in 43/45 (95.6%) patients with consolidation [Figure 1] and 39/45 (86.7%) patients with air bronchogram [Figure 2], whereas multiple b-lines in 22/45 (48.9%) patients. In addition, fluid bronchogram finding was positive in 14/45 (31.1%) patients, pleural effusion in 11/45 (24.4%) patients, but pleural line abnormalities in only 8/45 (17.8%) patients. In contrast, LUS detected one case each with subpleural hepatization and pleural line irregularity in nonpneumonia cases [Table 3].
LUS could detect consolidation in more than one lobe than CXR, which was statistically significant (P < 0.05). Moreover, LUS was more specific and sensitive in detection of pneumonia in children than CXR [Table 4] and [Table 5].
|Table 4: Lobar distribution of consolidation among pneumonia group patients|
Click here to view
|Table 5: Diagnostic accuracy of chest radiography and lung ultrasonography in prediction of pneumonia cases|
Click here to view
| Discussion|| |
In the present study, male to female ratio was 1.8 : 1 in patients with pneumonia. The slight predominance of males over females among children with pneumonia was supported by Siziya et al.  who represented 59.7% males among their studied cases. Moreover, Falagas et al.  reported a male predominance in lower respiratory tract infections. Anatomic differences of the respiratory tract may partially explain the different prevalence of infections between males and females. There is also evidence that the peripheral airways are disproportionately narrower during the early years of life in males, which may predispose for lower RTIs. This was in contrast to Montasser et al.  who reported comparable ratio, with slight predominance of females at 51%.
From the studied samples of children with pneumonia, 71.1% were urban inhabitants whereas 28.9% were rural inhabitants. This comes in agreement with the study done in Kenya and Gambia that reported that urban children had a higher rate of hospitalization for respiratory episodes than rural children, which is thought to be related to the distance to hospital facility, leading to more diagnoses in urban children . This is in contrast to Awadalla et al.  who reported that nearly three-quarters (74.2%) of recorded cases with acute respiratory illness came from rural inhabitants. This could be explained by the fact that in rural areas of developing countries, there is increased burning biomass, principally wood and crop residues, which are an important source of exposure to a variety of toxins.
Additionally, this study showed that 62.2% of the studied children with pneumonia had been exposed to second-hand smoking. This comes in agreement with Azad et al.  who reported that among the children with ARTIs, 50.5% were exposed to second-hand smoking. Second-hand smoking is the most common and dangerous indoor environmental pollutant, to which children are exposed. The effect of tobacco smoke exposure was found to be more prominent in infants . Passive smoking in children is associated with a higher rate of respiratory problems like asthma, bronchitis, pneumonia, bronchiolitis as well as otitis media and sudden infant death . Passive smoking paralyzes cilia, allowing mucus accumulation, and promotes goblet cell growth, resulting in an increase in mucus .
In the current study, there was significant difference between pneumonia group and nonpneumonia group in neutrophil percentage, as the mean neutrophil percentage in pneumonia group was higher at 61 ± 9.51. In addition, CRP was significantly high in pneumonia group (91.9% sensitivity) than nonpneumonia group (46.7% sensitivity). Similarly, Williams et al.  mentioned that increasing CRP was associated with increased fever duration and increased length of hospital stay for children with pneumonia. Ning et al.  demonstrated that the white blood cell count, neutrophil count, neutrophil percentage, and erythrocyte sedimentation rate in the CAP group were significantly higher than those of control group. There is some scientific evidence that a high CRP level indicates a severe respiratory tract infection such as pneumonia and that the general practitioner can use the CRP test if unsure of infection severity .
In our study, CXR showed that consolidation was diagnosed in 88.9% and effusion in 15.6% of pneumonia cases, whereas patients without pneumonia had consolidation in 13.3%, with no pleural effusion detected. LUS was diagnostic in 95.6% of pneumonia cases. Moreover, LUS could detect more obvious findings in pneumonia cases compared with nonpneumonia cases, with evidence of 95.6% of patients with consolidation, 86.7% with air bronchogram, but multiple b-lines in 48.9%, along with fluid bronchogram in 31.1%, pleural effusion in 24.4%, but pleural line abnormalities in 17.8%. This is similar to Copetti and Cattarossi  who reported that ultrasound was positive for the diagnosis of pneumonia in 100% of patients, whereas CXR was positive in 88.3%. In the seven patients with negative CXR and positive ultrasound findings, pneumonia was confirmed by chest computed tomography scans. Moreover, Ho et al.  reported that CXR could detect pneumonia in 93.3% of patients, whereas LUS detected pneumonia in 97.5%. In LUS, the following findings were observed: the positive rates of the multiple b-lines, air bronchograms, vascular pattern within the consolidation, and pleural effusion were 50.9, 93.7, 20.1, and 28.9%, respectively. Reali et al.  reported that 81 of 107 children were diagnosed with CAP. LUS and CXR were performed in all patients. Ultrasound had a sensitivity of 94% and specificity of 96%, whereas CXR showed a sensitivity of 82% and specificity of 94%. Cortellaro et al.  reported that the sensitivity of CXR for diagnosing pneumonia was 69%, whereas that of bedside ultrasonography was significantly higher at 96%.
In our study, LUS was superior to CXR in identifying parapneumonic effusion in one case with free chest x-ray. Moreover, LUS was superior to CXR in identifying consolidation pneumonia in five negative CXR cases. LUS could be used in the follow-up of patient through measurement the volume of the consolidating lesion and determining the presence of complication or resolving of the pathology, which did happen in two cases that showed decrease in the volume of the consolidating patch regarding clinical improvement, whereas the CXR showed no difference in the consolidating patch. Similarly, Sartori and Tombesi  reported more than one lung consolidation in their sonographic finding in 26/89 patients' versus CXR, which detected in 6/89 cases. Moreover, Caiulo et al.  demonstrated that follow-up through sonographic findings for more than 14 days in 76/83 patients with consolidations showed a decrease in size or disappearance of hypoechoic areas, which is always associated with clinical improvement.
In the current study, LUS is superior to CXR for identifying pleurapulmonary abnormalities in children with suspected pneumonia, with sensitivity of 95.6%, specificity of 93.3% and diagnostic accuracy of 94.4%, whereas CXR showed sensitivity of 88.9%, specificity of 86.6% and diagnostic accuracy of 86.7%. Similarly, Corradi et al.  showed that quantitative ultrasonography had higher sensitivity of 93%, specificity of 95%, and diagnostic accuracy of 94% than CXR, with sensitivity of 64%, specificity of 80%, and diagnostic accuracy of 69%.
| Conclusion|| |
In view of our study, it can be concluded that chest ultrasonography offers an important contribution to the diagnostic procedures of pleuropulmonary disorders in children, such as pneumonia and pleural effusion, with higher sensitivity, specificity, and positive predictive index compared with CXR. LUS is a simple, safe, more sensitive, and more specific tool than CXR in diagnosis of childhood CAP.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Zar HJ, Ferkol TW. The global burden of respiratory disease impact on child health. Pediatr Pulmonol 2014; 49
Harris M, Clark J, Coote N, Fletcher P, Harnden A, McKean M, et al
. British Thoracic Society guidelines for the management of community acquired pneumonia in children: update 2011. Thorax 2011; 66
United Nations International Children's Emergency Fund (UNICEF). UNICEF Data, despite steady progress, pneumonia remains one of the single largest killer of young children worldwide. Available at: https://data.unicef.org/topic/child-health/pneumonia/
[Last accessed on 2015 Nov 26].
Blaivas M. Lung ultrasound in evaluation of pneumonia. J Ultrasound Med 2012; 31
Bradley JS, Byington CL, Shah SS, Alverson B, Carter ER, Harrison C, et al
. The management of community-acquired pneumonia in infants and children older than 3 months of age: clinical practice guidelines by the Pediatric Infectious Diseases Society and the Infectious Diseases Society of America. CID 2011; 53
Ayalon I, Glatstein MM, Zaidenberg-Israeli G, Scolnik D, Ben-Tov A, Ben-Sira L, et al
. The role of physical examination in establishing the diagnosis of pneumonia. Pediatr Emerg Care 2013; 29
Little MP. Risks associated with ionizing radiation: environmental pollution and health. Br Med Bull 2003; 68
Weinberg B, Diakoumakis EE, Kass EG, Seife B, Zvi ZB. The air bronchogram: sonographic demonstration. Am J Roentgenol 1986; 147
Smargiassi A, Inchingolo R, Soldati G, Copetti R, Marchetti G, Zanforlin A, et al
. The role of chest ultrasonography in the management of respiratory diseases. Multidiscip Respir Med 2013; 8
Lichtenstein D, Meziere G, Seitz J. The dynamic air bronchogram. An ultrasound sign of alveolar consolidation ruling out atelectasis. Chest 2009; 135
Al-khayat KF, Alam-Eldeen MH. Value of chest ultrasound in diagnosis of community acquired pneumonia. Egypt J Chest Dis Tuberc 2014; 63
Volpicelli G. Sonographic diagnosis of pneumothorax. Intensive Care Med 2011; 37
Kurian SM, Le-Niculescu H, Patel SD, Bertram D, Davis J, Dike C, et al
. Identification of blood biomarkers for psychosis using convergent functional genomics. Mol Psychiatry 2011; 16
Duncan H, Hutchinson J, Parshuram CS. The pediatric early warning system score: a severity of illness scores to predict urgent medical need in hospitalized children. J Crit Care 2006; 21
Coley BD. Chest sonography in children: current indications, techniques and imaging finding. Radiol Clin N
Am 2011; 49
Siziya S, Muula AS, Rudatsikira E. Diarrhoea and acute respiratory infections prevalence and risk factors among under-five children in Iraq in 2000. Ital J Pediatr 2009; 35
Falagas ME, Mourtzoukou EG, Vardakas KZ. Sex differences in the incidence and severity of respiratory tract infections. Respir Med 2007; 101
Montasser N, Helal R, Rezq R. Assessment and classification of acute respiratory tract infections among Egyptian rural children. Br J Med Med Res 2012; 2
Bigogo G, Audi A, Aura B, Aol G, Breiman RF, Feikin DR. Health-seeking patterns among participants of population-based morbidity surveillance in rural western Kenya: implications for calculating disease rates. Int J Infect Dis 2010; 14
Awadalla HI, El-kholy NF, Barkat AB. Trends of influenza infection in Egypt during two consecutive seasons. J Public Health 2009; 17
Azad SMY, Bahauddin KM, Uddin MH, Perveen S. Indoor air pollution and prevalence of acute respiratory infection among children in rural area of Bangladesh. Journal of Biology, Agriculture and Healthcare, 2014; 3
Peat JK, Keena V, Harakeh Z, Marks G. Parental smoking and respiratory tract infections in children. Paediatr Respir Rev 2001; 2
Srtitippayawan S, Prapphal N, Wong P, Tosukhowong P, Samransamruajkit R, Deerojanawong J. Environmental tobacco smoke exposure and respiratory syncytial virus infection in young children hospitalized with acute lower respiratory tract infection. J Med Assoc Thai 2006; 89
Savitha MR, Nandeeshwara SB, Pradeep Kumar MJ, Ul-Haque F, Raju CK. Modifiable risk factors for acute lower respiratory tract infections. Indian J Pediatr 2007; 74
Williams DJ, Hall M, Auger KA, Tieder JS, Jerardi KE, Queen MA, et al
. Association of white blood cell count and C-reactive protein with outcomes in children hospitalized for community-acquired pneumonia. Pediatr Infect Dis J 2015; 34
Ning J, Shao X, Ma Y, Lv D. Valuable hematological indicators for the diagnosis and severity assessment of Chinese children with community-acquired pneumonia. Medicine 2016; 95
Watkins RR, Lemonovich TL. Diagnosis and management of community-acquired pneumonia in adults. Am Fam Physician 2011; 83
Copetti R, Cattarossi L. Ultrasound diagnosis of pneumonia in children. Radiol Med 2008; 113
Ho MC, Ker CR, Hsu JH, Wu JR, Dai ZK, Chen IC. Usefulness of lung ultrasound in the diagnosis of community-acquired pneumonia in children. Pediatr Neonatol 2015; 56
Reali F, Sferrazza Papa GF, Carlucci P, Fracasso P, Di Marco F, Mandelli M, et al
. Can lung ultrasound replace chest radiography for the diagnosis of pneumonia in hospitalized children? Respiration 2014; 88
Cortellaro F, Colombo S, Coen D, Duca PG. Lung ultrasound is an accurate diagnostic tool for the diagnosis of pneumonia in the Emergency Department. Emerg Med J 2012; 29
Sartori S, Tombesi P. Emerging roles for transthoracic ultrasonography in pulmonary diseases. World J Radiol 2010; 2
Caiulo VA, Gargani L, Caiulo S, Fisicaro A, Moramarco F, Latini G, et al
. Lung ultrasound characteristics of community-acquired pneumonia in hospitalized children. Pediatr Pulmonol 2013; 48
Corradi F, Brusasco C, Garlaschi A, Paparo F, Ball L. Quantitative analysis of lung ultrasonography for the detection of community acquired pneumokna. A pilot study. Biomed Res Int 2015; 8
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]