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ORIGINAL ARTICLE  
Year : 2014  |  Volume : 57  |  Issue : 3  |  Page : 413-417
Comparison of severe pneumonia caused by Human metapneumovirus and respiratory syncytial virus in hospitalized children


1 Department of Respiratory Medicine, Children's Hospital Affiliated to Soochow University, Suzhou 215003, China
2 Department of Clinical Laboratory, Children's Hospital Affiliated to Soochow University, Suzhou 215003, China

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Date of Web Publication14-Aug-2014
 

   Abstract 

Objectives: The objective of this study is to compare the incidence and clinical characteristics of severe pneumonia caused by Human metapneumovirus (hMPV) to respiratory syncytial virus (RSV) infection in children. Patients and Methods: A total of 151 children hospitalized with severe pneumonia, were tested for hMPV using reverse-transcription polymerase chain reaction. At the same time, samples were tested for RSV and other common respiratory viruses. Medical records, including clinical, laboratory data, and chest radiography findings, were reviewed for all children. Results: Of the 151 samples, 88 (58.3%) were positive for respiratory viruses. Of the 88 positive, there were 6 (4.0%) with hMPV, 66 (43.7%) with RSV, 13 (8.6%) with influenza A, 2 (1.3%) with parainfluenza virus III, 1 (0.7%) with parainfluenza virus I, 1 (0.7%) with adenovirus and 1 (0.7%) with influenza B. hMPV-infected patients were significantly older than RSV-infected patients (P < 0.001). Children with hMPV pneumonia had fever more frequently (P = 0.03). Two hMPV-positive patients (33.3%) required admission to an intensive care unit, and two patients (33.3%) required mechanical ventilation. The duration of illness was 18.33 ± 7.09 days. These characteristics of hMPV infections were similar to patients with RSV infections. Conclusion: Human metapneumovirus is an infrequent viral pathogen causing severe pneumonia in children. Children with hMPV were older than those with RSV. The disease caused by hMPV was similar in presentation and severity to RSV, with a minority of children requiring additional respiratory support.

Keywords: Child, Human metapneumovirus, respiratory syncytial virus, severe pneumonia

How to cite this article:
Wang Y, Ji W, Chen Z, Yan YD, Shao X, Xu J. Comparison of severe pneumonia caused by Human metapneumovirus and respiratory syncytial virus in hospitalized children. Indian J Pathol Microbiol 2014;57:413-7

How to cite this URL:
Wang Y, Ji W, Chen Z, Yan YD, Shao X, Xu J. Comparison of severe pneumonia caused by Human metapneumovirus and respiratory syncytial virus in hospitalized children. Indian J Pathol Microbiol [serial online] 2014 [cited 2021 Nov 28];57:413-7. Available from: https://www.ijpmonline.org/text.asp?2014/57/3/413/138735



   Introduction Top


0Human metapneumovirus (hMPV) was first identified as a novel respiratory virus in 2001, in The Netherlands, and later in other European countries, North America, Asia, and Africa. [1],[2],[3],[4],[5] hMPV belongs to the order Mononegavirales, and is a new member of the metapneumovirus genus. hMPV, which is closely related to avian metapneumovirus, is the first disease-causing pathogen identified in the metapneumovirus genus that can infect human beings. [1] hMPV is a major cause of upper and lower respiratory illness in all age groups. Infants, immunocompromised individuals and the elderly are most susceptible to this infection. [6],[7],[8],[9],[10] hMPV infection in children causes a similar range of clinical presentations to the human respiratory syncytial virus (RSV), including slight upper respiratory tract discomfort accompanied by high fever, flu-like symptoms, laryngotracheobronchitis, bronchitis and pneumonia. Some studies indicate that the clinical severity of hMPV infections is slightly lower than that of RSV infections. [11],[12],[13] An Australian study demonstrated that hMPV is an important cause of severe respiratory illness in infants and young children, and disease severity is similar to those admitted with RSV. [14] Pelletier et al. observed fatal secondary lower respiratory tract infection by hMPV in an immune transplant patient. [15] Varman et al. have reported severe hMPV pneumonia in a child with chronic illness. [16] In high-risk adult patients, this virus causes severe life-threatening infections. [17],[18] However, information on severe hMPV infections in children is rather limited. The main objective of this study was to investigate the role of hMPV in children with severe pneumonia and to compare the illness with RSV infection.


   Patients and methods Top


Patients

Retrospective data were collected, using a standardized form, from a total of 151 children with severe pneumonia that were identified from the Department of Respiration Medicine and intensive care unit (ICU) at the children's hospital affiliated with Soochow University between January 2007 and December 2012. This hospital has 400 beds with an average yearly admission of about 10,000 children in the age group of 0-14 years. This hospital is also a pediatric referral center for the Greater Suzhou Area and the surrounding region. There are 5.26 million people in Suzhou itself with a pediatric population (0-14 years) of 0.9 million.

Diagnosis of severe pneumonia was made with reference to British Thoracic Society Guidelines for the Management of Community Acquired Pneumonia in Childhood. [19] The guidelines for infants included temperature >38.5°C, >70 breaths/min, moderate to the severe recession, nasal flaring, cyanosis, intermittent apnea, grunting respiration, and not feeding. For older children guidelines included temperature >38.5°C, >50 breaths/min, severe difficulty in breathing, nasal flaring, cyanosis, and grunting respiration. Indications for admission to the ICU included the patient failing to maintain a SaO 2 of >92% in FiO 2 of >0.6, the patient in shock, rising respiratory and pulse rates with clinical evidence of severe respiratory distress and exhaustion with or without a raised arterial carbon dioxide tension (PaCO 2 ), and recurrent apnea or slow irregular breathing. Prematurely born children, those with heart diseases, chronic pulmonary diseases, congenital airway malformations, known immunodeficiencies and children with missing data were excluded from the study. Ethics Committee of Soochow University approved the study and the parents of all children gave informed consent.

Sample collection

Nasal aspirate samples were obtained from each patient within 24 h of admission using a sterile plastic catheter that was introduced into the lower part of the pharynx via the nasal cavity. The samples were then divided into two aliquots for the detection and culture of seven common viruses and hMPV.

Detection of seven common viruses by direct immunofluorescence assay

The nasal aspirate suspension was centrifuged at 300-500 rpm for 10 min. Pelleted cells were then collected for cell smear. Next, a direct immunofluorescence assay was performed to detect seven common respiratory viruses (i.e., RSV, adenovirus [ADV], influenza A and B viruses, and parainfluenza virus Types I, II, and III). Antigen detection was carried out according to the manufacturer's instructions (Chemicon, USA). Slides were examined under a fluorescence microscope (Leica 020-518.500, Germany).

Detection of the Human metapneumovirus gene by reverse-transcription polymerase chain reaction (RT-PCR)

Primer design

Using information from whole genome sequences of multiple hMPV virus strains and the N gene sequence available from the Gen-Bank database, we designed a primer pair to specifically amplify a fragment of 213 bp (562-774) in the N gene. Primers were synthesized by Shanghai Sangon using the sequences as follows: Sense, 5-AACCGTGTACTAAGTGATGCACTC-3; antisense, 5-CATTGTTTGACCGGCCCCATAA-3.

Reverse-transcription polymerase chain reaction of Human metapneumovirus RNA

Viral RNA was extracted with Trizol reagent (Invitrogen). Reverse-transcription was performed with the use of random hexamer primers. Next, PCR assays were performed in an automatic PCR cycler (Perkin Elmer, USA). PCR techniques included 45 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 30 s and extension at 68°C for 30 s. The final extension was carried out at 68°C for 7 min. Hexamer random primers provided by Shanghai Sangon were used. Reverse transcriptase Moloney murine leukemia virus and Taq DNA polymerase were purchased from Promega. The PCR products were separated by 1.5% agarose gel electrophoresis and visualized by ethidium bromide staining. Positive results were indicated by the appearance of a 213-bp band under ultraviolet detection. A primer pair - 5-AACCGTGTACTAAGTGATGCACT-C-3 (sense) and 5-CATTGTTTGACCGGCCCCATAA-3 (antisense) - was used for sequencing analysis. Ten positive PCR products were randomly selected and recovered from agarose gels, followed by nucleotide sequence determination. These sequences were then compared with a hMPV sequence available from Gen-Bank using Chromas software.

Statistical analysis

Fisher's exact test was applied for the comparison of demographic and clinical differences between groups if each cell number was <5. The Chi-square test was used to compare the variances in positive rates in all groups. SAS version 8.0 software (Statistical Analysis System Institute Inc.) was used in the data analysis. P < 0.05 was considered as significant.


   Results Top


Baseline characteristics of the study population

A total of 151 children with severe pneumonia were screened in this study. The proportion of male: Female subjects was 2.15:1, with 103 male (68.2%) and 48 female cases (31.8%). The youngest was 1-month-old, while the oldest was 13-year-old. Stratified by age groups: 97 (64.2%) were aged <6 months, 21 (13.9%) were aged 6-12 months, 22 (14.6%) were aged 1-3 years, 4 (2.6%) were aged 3-5 years, and 7 (4.6%) were ≥5-year-old.

Detection rates of respiratory viruses

Of 151 samples, 88 (58.3%) were positive for respiratory viruses, 33 (21.9%) were positive for bacterial infection and 5 (3.3%) were positive for bacterial-viral co-infections. Among the 88 virus cases, were 6 (4.0%) positive for hMPV, 66 (43.7%) positive for RSV, 13 (8.6%) positive for influenza A, 2 (1.3%) positive for parainfluenza viruses III, 1 (0.7%) positive for parainfluenza virus I, 1 (0.7%) positive for ADV, and 1 (0.7%) positive for influenza B. Viral co-infection was observed in three cases; two patients were co-infected with RSV and influenza A virus and one patient was co-infected with RSV and parainfluenza virus I. Of the 33 bacterial infection cases, there were 17 (11.3%) with Streptococcus pneumoniae, 5 (3.3%) with methicillin-susceptible Staphylococcus aureus, 5 (3.3%) with Haemophilus influenzae, 4 (2.6%) with Escherichia coli, and 2 (1.3%) with Klebsiella pneumoniae.

Age distribution of respiratory viruses infected children

All six hMPV positive children were below the age of 3 years. The highest hMPV infection rate was observed in those aged between 6 months and 1 year (χ2 = 23.54, P < 0.0001). Among RSV positive samples, 80.3% were aged <6 months, 15.2% were aged from 6 to 12 months while the greatest proportion among the influenza virus A (IVA) positive patients aged older than 5 years and children <6 months of age [Table 1].
Table 1: Age distribution of children with a respiratory virus pneumonia (n [%])

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Clinical features of severe pneumonia with Human metapneumovirus infection

None of the six hMPV-infected children were co-infected with other respiratory viruses. The mean age of patients with severe hMPV infection was 11 ± 5.3 months, and all were <3 years of age. There were four boys and two girls. Of the six cases with hMPV infection, 4 (66.7%) showed varying degrees of fever. Three cases were complicated with heart failure and respiratory failures and one with deranged liver function. The average leukocyte count in peripheral blood was 10.71 ± 5.43 × 109/l. The mean C-reactive protein value was 15.83 ± 22 mg/l. Chest radiographs revealed blurred bilateral lung markings and patchy shadows in 4 (66.7%) cases, left upper massive infiltration in one case (13.6%), and right upper lobe atelectasis in one case (13.6%). Mechanical ventilation was required for the duration of 2 days in one case and for 7 days in another. All six patients recovered from their illness and the average illness time was 18.33 ± 7.09 days (median, 18.3 days) [Table 2].
Table 2: Clinical features of patients with severe hMPV pneumonia

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Comparison of clinical features between patients with Human metapneumovirus infection and patients with respiratory syncytial virus infection

There were more boys than girls in both groups, but the difference was not statistically significant (P = 0.32). The mean age of hMPV-infected children was 11 months - significantly older than children infected with RSV (3.9 months) (P < 0.001). Fever was more common in children with hMPV infection (66.7% vs. 20.9%, P = 0.03); however, wheezing, pH <7.35, and PCO 2 >45 mmHg with hMPV infections were not significantly different from those with RSV infections. There were no significant differences in need for ICU admission, length of ICU stay, the need for mechanical ventilation, or the length of illness between children who were infected with hMPV and those infected with RSV [Table 3].
Table 3: Demographic and clinical features in patients with hMPV and RSV infections

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   Discussion Top


Pneumonia is one of the leading causes of illness and death in children younger than 5 years of age worldwide. There is little information on the viral etiology of severe pneumonia in the developing countries, where the disease burden is particularly high. This study demonstrated that viral infections are a leading cause for severe pneumonia in children. We believe that this is the first study in Southeast China to examine the role of hMPV in children with severe pneumonia. The finding that 4.6% of cases were positive for hMPV suggests that this virus is an infrequent pathogen causing severe pneumonia in children in Suzhou, China. RSV was the predominant respiratory viral pathogen and IVA was the second most common pathogen. The observed infection rate was consistent with other studies that showed that hMPV was not a frequent agent of lung disease in children with or without underlying diseases, but the virus can elicit severe illness. [24],[25] We found that children with hMPV infections were significantly older than those admitted with RSV infections. This finding was similar to earlier studies. [14],[26] Previously, studies have reported different disease severity for hMPV and RSV infections; a few studies found differences in disease severity during infection in healthy infants while most studies found similar presentations. [1],[8],[9],[11],[12] Children with hMPV infections are likely to present with pneumonia and less likely to present with bronchiolitis, [14] but the disease was less severe with hMPV than RSV infection. [1],[3],[7],[8] Paget reported that children with hMPV are likely to be older than those with RSV, and children admitted to the paediatricpediatric intensive care unit (PICU) with hMPV have a similar disease presentation and severity as children admitted with RSV, including some with extremely severe disease who require additional ventilatory or cardiovascular support. [14] Beneri et al. found a significantly higher proportion of hospitalization and admission to the PICU in hMPV-infected children compared with RSV. [27] In our study, there were more children with RSV than with hMPV that required ICU admissions and that needed mechanical ventilation, but these differences did not reach statistical significance. However, there were no significant differences in length of ICU stay and the average duration of illness between children who were infected with hMPV and those infected with RSV. This suggests similar severity of illness caused by hMPV and RSV. The differences in the pathogenesis of both infections remain poorly understood. Laham et al. [28] have reported that levels of inflammatory cytokines in respiratory secretions of hMPV-infected infants were 2- to 6-fold lower than those in infants infected with RSV. hMPV did not stimulate a strong inflammatory response, but elicited identical symptoms. These findings suggest that hMPV and RSV either cause disease through different mechanisms or share a common mechanism that is distinct from innate immune activation. A systematic study of the role of hMPV in populations at risk for severe lung disease had not been conducted to date.

Recently, a report described severe infection with hMPV and requirement of extracorporeal membrane oxygenation in an infant with chronic lung disease. [20] Mόller et al. [17] found that some hMPV-infected children had a history of premature birth, chronic lung disease, or complicated congenital heart disease. [21] An outbreak of hMPV was also reported in which one-half of infected children had an underlying chronic illness. [22] Compared with RSV, hMPV infection was more common in children with congenital abnormalities, cardiopulmonary diseases, and in those who required ventilatory support. [23] Some studies [29],[30] have found high rates of co-infection with hMPV and RSV in those requiring ventilator support, and have suggested that co-infection is a risk factor for severe disease. However, Williams et al. [11] took the opposite view that the single infection with hMPV does not show appreciable differences with co-infection with hMPV and other viruses and thought that children with other viral infections in combination with hMPV did not aggravate the disease severity. We found no co-infection of hMPV with RSV in our study. Defining the length of viral shedding and asymptomatic infection rates will further help to explain the role of hMPV in co-infection with other respiratory viruses.

The present study has certain limitations. The hMPV gene was detected using RT-PCR, but the other common viruses were detected using direct fluorescent-antigen (DFA). DFA is a rapid and simple test, has high specificity and is more cost-effective for patients, [31] but its sensitivity is definitely lower than PCR. Due to this lower sensitivity, the role of other viruses in causing severe pneumonia would have been underestimated. In addition, the number of hMPV viruses was small.

In summary, our study suggests that hMPV is an infrequent viral pathogen causing severe pneumonia in children. The disease caused by hMPV is mostly similar in presentation and severity to RSV, with a minority of children requiring additional respiratory support. This study is limited by a sample size of six hMPV patients. Further studies, with a greater number of hMPV cases would improve the characterization of this disease.


   Acknowledgments Top


This work was supported by Youth Fund, Science and Technology and Education Projects of Suzhou (Grant No. SWKQ1021). Registration number of clinical trials: SDFEY200701.

 
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Correspondence Address:
Wei Ji
Department of Respiratory Medicine, Children's Hospital Affiliated to Soochow University, No. 303, Jing De Road, Suzhou 215003
China
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Source of Support: This work was supported by Youth Fund, Science and Technology and Education Projects of Suzhou (Grant No. SWKQ1021)., Conflict of Interest: None


DOI: 10.4103/0377-4929.138735

Clinical trial registration SDFEY200701

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    Tables

  [Table 1], [Table 2], [Table 3]

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