Human metapneumovirus and respiratory syncytial virus disease in children, Yemen.Factors increasing the severity of respiratory infections in developing countries are poorly described. We report factors associated with severe acute respiratory illness Noun 1. respiratory illness - a disease affecting the respiratory system respiratory disease, respiratory disorder adult respiratory distress syndrome, ARDS, wet lung, white lung - acute lung injury characterized by coughing and rales; inflammation of the in Yemeni children (266 infected with respiratory syncytial virus respiratory syncytial virus (sĭnsĭsh`əl): see cold, common. and 66 with human metapneumovirus). Age, indoor air pollution, and incomplete vaccinations were risk factors and differed from those in industrialized in·dus·tri·al·ize v. in·dus·tri·al·ized, in·dus·tri·al·iz·ing, in·dus·tri·al·iz·es v.tr. 1. To develop industry in (a country or society, for example). 2. countries. ********** A cute respiratory infections (ARIs) are the main cause of childhood death worldwide (1). Respiratory syncytial virus (RSV RSV respiratory syncytial virus; Rous sarcoma virus. RSV abbr. respiratory syncytial virus RSV 1 Respiratory syncytial virus, see there 2 Rous sarcoma virus, see there ) is most frequently implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. in childhood illness (2). Although factors predisposing to severe ARI ARI Acute respiratory infection, see there caused by RSV are well known in industrialized countries, little information exists for developing countries. Infection with human metapneumovirus (HMPV) has clinical symptoms similar to those for RSV (3). Despite its frequency, little information exists on factors that predispose pre·dis·pose v. To make susceptible, as to a disease. children to severe ARI caused by HMPV. We describe factors associated with severe ARI caused by RSV or HMPV in Yemeni children. The Study Children [less than or equal to] 2 years of age with ARI attending Al-Sabeen Hospital, a reference hospital in Sana'a, Yemen, were enrolled in a study from October 2002 to May 2003. All children attending emergency and outpatient services outpatient services Hospital-based services Managed care Medical and other services provided, to a nonadmitted Pt, by a hospital or other qualified facility–eg, mental health clinic, rural health clinic, mobile X-ray unit, free-standing dialysis unit Examples between 8:00 a.m. and 1:00 a.m. with signs and symptoms of ARI were recruited independent of disease severity. Diagnosis was based on clinical signs, as suggested by the World Health Organization protocol for research on ARI (4). A total of 62% of the patients were hospitalized. Patients admitted at night were recruited the next morning. Oxygen pressure (p[O.sub.2]) was measured by using pulse oximetry pulse oximetry Oxygen saturation measurement, SaO Critical care A method used to determine the O2 saturation–SaO2 and desaturation of blood in a continuous noninvasive fashion, through the noninvasive assessment of arterial Hb-bound (Nonin Medical, Inc., Plymouth, MN, USA), and children were classified as having no or moderate (p[O.sub.2] [greater than or equal to] 88%) or severe (P[O.sub.2] <88%) hypoxia hypoxia Condition in which tissues are starved of oxygen. The extreme is anoxia (absence of oxygen). There are four types: hypoxemic, from low blood oxygen content (e.g., in altitude sickness); anemic, from low blood oxygen-carrying capacity (e.g. , as suggested for high altitudes (5), since Sana'a is 2,200 m above sea level. Nasopharyngeal nasopharyngeal pertaining to the nasal and pharyngeal cavities. nasopharyngeal meatus see nasopharyngeal meatus. nasopharyngeal spasm see reverse sneeze. aspirates were tested by using reverse transcription reverse transcription n. The process by which DNA is synthesized from an RNA template. PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) , as previously reported (6). Children with severe hypoxia caused by RSV were compared with children with RSV and no or moderate hypoxia. The same comparisons were used for children infected with HMPV. The [chi square chi square (kī), n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies. ] and Student t tests were used, and values with p values <0.20 were entered into backward logistic regressions. Ethical approval was obtained from the ethics committees of the Liverpool School of Tropical Medicine The Liverpool School of Tropical Medicine (LSTM), England, was founded on 12 November 1898, by a donation from Sir Alfred Lewis Jones, a Liverpool Shipowner. The donation of £350 created the first school of its kind. and Al-Sabeen Hospital. Parents were interviewed after informed consent was obtained. A total of 325 (54%) children were recruited from the emergency service, 235 (39%) from outpatient clinics and 41 (7%) from wards. RSV was identified in 266 (44%) and HMPV in 66 (11%) children, including 25 (4%) coinfected with RSV and HMPV. Two hundred thirty-two (87%) children with RSV, 46 (70%) with HMPV (p<0.01), and 22 (88%) coinfected with both viruses had severe hypoxia (Table). Among RSV-positive specimens, 171 (82%) of 208 were group A and 37 (18%) of 208 were group B. No association was seen between groups or genotypes and hypoxia. Children [less than or equal to] 3 months of age were more likely to have severe hypoxia if they were infected with both viruses (Figure). Children with severe RSV hypoxia were more likely to have relatives with ARI, and this factor plus a history of recurrent respiratory infections were risk factors for HMPV hypoxia. Personal or family histories of atopy atopy /at·o·py/ (at´ah-pe) a genetic predisposition toward the development of immediate hypersensitivity reactions against common environmental antigens (atopic allergy), most commonly manifested as allergic rhinitis but also as , prematurity, or chronic lung or congenital heart diseases congenital heart disease, any defect in the heart present at birth. There is evidence that some congenital heart defects are inherited, but the cause of most cases is unknown. were not associated with ARI severity caused by RSV or HMPV. [FIGURE OMITTED] Among household characteristics, the presence of animals (cows and donkeys), a person in the house smoking, using private water sources, and cooking with fuels other than gas were more frequent for children with severe RSV hypoxia. Only the presence of cows, private water, and cooking fuels other than gas were associated with severe HMPV hypoxia. Multivariate analysis multivariate analysis, n a statistical approach used to evaluate multiple variables. multivariate analysis, n a set of techniques used when variation in several variables has to be studied simultaneously. showed that age [less than or equal to] 3 months and using cooking fuels other than gas were risk factors for severe RSV hypoxia (adjusted odds ratio [AOR AOR The ISO 4217 currency code for Angolan Reajustado Kwanza. ] 3.4, 95% confidence interval confidence interval, n a statistical device used to determine the range within which an acceptable datum would fall. Confidence intervals are usually expressed in percentages, typically 95% or 99%. [CI] 1.3-8.7 and AOR 10.3, 95% CI 2.2-48) and HMPV hypoxia (AOR 14.2, 95% CI 3.1-65 and AOR 13.1, 95% CI 2.2-78), while incomplete vaccinations (AOR 4.5, 95% CI 1.7-12) and smoking (AOR 3.8, 95% CI 1.5-9.8) were associated with severe RSV hypoxia but not HMPV hypoxia. Conversely, a history of recurrent ARI (AOR 13, 95% CI 2.0-84) was associated with severe HMPV hypoxia but not with RSV hypoxia. Conclusions Identification of factors that increase the severity of ARI may affect health policies. However, little information is available about such factors in developing countries. Young children are especially susceptible to severe ARI, and our findings confirm that in a hospital setting age is a factor for both severe RSV and severe HMPV ARI. Prematurity and congenital heart and chronic lung diseases, which have been associated with increased risk for hospitalization for RSV and HMPV infections, were not risk factors. Since most Yemeni children are born at home, with limited access to health services health services Managed care The benefits covered under a health contract , these children are underrepresented un·der·rep·re·sent·ed adj. Insufficiently or inadequately represented: the underrepresented minority groups, ignored by the government. in our sample. We did not identify malnutrition as a risk factor for RSV or HMPV infection. Infection with RSV was more frequent and severe in well-nourished children in Nigeria, The Gambia, and Chile (7), but this finding was not confirmed by other investigators (8), and it is still contentious. We found no association of the 2 viral infections with atopy. Although no information exists about their role in infection with HMPV, increased levels of common allergens within households had no effect on RSV infection severity in the United States (9). However, Gambian mothers of children hospitalized with RSV infections reported asthma more frequently in their children than mothers of nonhospitalized children (10). The role of atopy in development of severe RSV or HMPV infections in developing countries needs further elucidation. Several reports have suggested that coinfections with RSV and HMPV increase disease severity, but we did not find such an interaction. Although we cannot exclude coinfection with bacterial or other viral agents, for which RSV or HMPV may increase disease severity, our findings are similar to reports from the Mediterranean region (11,12). This finding suggests that HMPV strains vary with location and time, and certain strains increase disease severity. Children with severe hypoxia were less likely to be vaccinated, which is a likely indicator of poverty because poor parents in Yemen only use health services if their children are ill and are less likely to have their children vaccinated. In industrialized countries, poverty is associated with a higher incidence of RSV, and risk factors for infection with RSV are more likely to occur simultaneously (13). We also observed that other household characteristics, such as cooking fuel and water, proximity to animals and relatives with ARI, or smoking increased the risk for hypoxia. Although we did not quantify air pollution within households, traditional mud stoves are built at ground level, use wood or dung, and generate large amounts of fumes fumes odorous gases and other volatile materials; inhalation of irritating fumes causes coughing and, if sufficiently severe, irreversible pulmonary edema. , which blacken black·en v. black·ened, black·en·ing, black·ens v.tr. 1. To make black. 2. To sully or defame: a scandal that blackened the mayor's name. 3. adjacent walls. Exposure to this pollution is associated with severe ARI. Parental and maternal smoking during pregnancy, indoor pollution, and presence of pets are also risk factors in industrialized countries (14,15). However, in The Gambia the relationship between severe RSV infection and frequency of cooking was inverse (10), which may reflect the lower socioeconomic status socioeconomic status, n the position of an individual on a socio-economic scale that measures such factors as education, income, type of occupation, place of residence, and in some populations, ethnicity and religion. of mothers who cook frequently; this finding needs to be explored further. Finally, as a hospital-based study, our study had a selection bias toward children with severe ARI, and community-based studies might find different risk factors than those reported here. In conclusion, age [less than or equal to] 3 months, incomplete vaccinations, persons smoking in the house, and using cooking fuels other than gas were associated with an increased risk for severe RSV hypoxia. Similarly, age [less than or equal to] 3 months, using cooking fuels other than gas, and recurrent ARI were associated with severe HMPV hypoxia. Interventions to eliminate air pollution in households may reduce the severity of RSV and HMPV infections in developing countries, and further studies should be encouraged. This work was supported in part by the Islamic Development Bank Islamic Development Bank (also known as IDB), is a multilateral development financing institution. located in Jeddah, Saudi Arabia. It was founded by the first conference of Finance Ministers of the Organization of the Islamic Conference (OIC), convened 18 December 1973. . References (1.) Vardas E, Blaauw D, McAnemey J. The epidemiology of respiratory syncytial virus (RSV) infections in South African children. S Afr Med J. 1999;89:1079-84. (2.) Shay shay n. Informal A chaise. [Back-formation from chaise (taken as pl. )] Noun 1. DK, Holman RC, Newman RD, Liu LL, Stout JW, Anderson LJ, Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA JAMA abbr. Journal of the American Medical Association . 1999;282:1440-6. (3.) van den Hoogen BG, de Jong JC, Groen J, Kuiken T, de Groot R, Fouchier RA, et al. A newly discovered human pneumovirus isolated from young children with respiratory tract respiratory tract n. The air passages from the nose to the pulmonary alveoli, including the pharynx, larynx, trachea, and bronchi. Respiratory tract disease. Nat Med. 2001;7:719-24. (4.) World Health Organization. Technical bases for the WHO recommendations on the management of pneumonia in children at first-level health facilities. WHO/ARI/91.20. Geneva Geneva, canton and city, Switzerland Geneva (jənē`və), Fr. Genève, canton (1990 pop. 373,019), 109 sq mi (282 sq km), SW Switzerland, surrounding the southwest tip of the Lake of Geneva. : The Organization; 1993. (5.) Duke T, Blaschke AJ, Sialis S, Bonkowsky JL. Hypoxaemia in acute respiratory and non-respiratory illnesses in neonates and children in a developing country. Arch Dis Child. 2002;86:108-12. (6.) Al-Sonboli N, Hart CA, Al-Aeryani A, Banajeh SM, Al-Aghbari N, Dove W, et al. Respiratory syncytial virus and human metapneumovirus in children with acute respiratory infections in Yemen. Pediatr Infect Dis J. 2005;24:734-6. (7.) Weber MW, Mulholland EK, Greenwood BM. Respiratory syncytial virus infection Respiratory Syncytial Virus Infection Definition Respiratory syncytial virus (RSV) is a virus that can cause severe lower respiratory infections in children under the age of two, and milder upper respiratory infections in older children and adults. in tropical and developing countries. Trop Med Int Health. 1998;3:268-80. (8.) Hussey GD, Apolles P, Arendse Z, Yeates J, Robertson A, Swingler G, et al. Respiratory syncytial virus infection in children hospitalised with acute lower respiratory tract infection While often used as a synonym for pneumonia, the rubric of lower respiratory tract infection can also be applied to other types of infection including lung abscess, acute bronchitis, and emphysema. . S Afr Med J. 2000;90:509-12. (9.) Bradley JP, Bacharier LB, Bonfiglio J, Schechtman KB, Strunk R, Storch G, et al. Severity of respiratory syncytial virus bronchiolitis Bronchiolitis Definition Bronchiolitis is an acute viral infection of the small air passages of the lungs called the bronchioles. Description Bronchiolitis is extremely common. is affected by cigarette smoke exposure and atopy. Pediatrics. 2005;115:e7-14. (10.) Weber MW, Milligan P, Hilton S, Lahai G, Whittle H, Mulholland EK, et al. Risk factors for severe respiratory syncytial virus infection leading to hospital admission in children in the Western Region of The Gambia. Int J Epidemiol. 1999;28:157-62. (11.) Maggi F, Pifferi M, Vatteroni M, Fornai C, Tempestini E, Anzilotti S, et al. Human metapneumovirus associated with respiratory tract infections in a 3-year study of nasal swabs from infants in Italy. J Clin Microbiol. 2003;41:2987-91. (12.) Xepapadaki P, Psarras S, Bossios A, Tsolia M, Gourgiotis D, Liapi-Adamidou G, et al. Human metapneumovirus as a causative agent of acute bronchiolitis in infants. J Clin Virol. 2004;30:267-70. (13.) Jansson L, Nilsson P, Olsson M. Socioeconomic environmental factors and hospitalization for acute bronchiolitis during infancy. Acta Paediatr. 2002;91:335-8. (14.) McConnochie KM, Hall CB, Barker WH. Lower respiratory tract Noun 1. lower respiratory tract - the bronchi and lungs lung - either of two saclike respiratory organs in the chest of vertebrates; serves to remove carbon dioxide and provide oxygen to the blood illness in the first two years of life: epidemiologic patterns and costs in a suburban pediatric pediatric /pe·di·at·ric/ (pe?de-at´rik) pertaining to the health of children. pe·di·at·ric adj. Of or relating to pediatrics. practice. Am J Public Health. 1988;78:34-9. (15.) Lanari M, Giovannini M, Giuffre L, Marini A, Rondini G, Rossi GA, et al. Prevalence of respiratory syncytial virus infection in Italian infants hospitalized for acute lower respiratory tract infections, and association between respiratory syncytial virus infection risk factors and disease severity. Pediatr Pulmonol. 2002;33:458-65. Najla Al-Sonboli, * ([dagger]) Charles A. Hart, ([double dagger]) Nasher Al-Aghbari, * ([dagger]) Ahmed Al-Ansi, ([dagger]) Omar Ashoor, ([section]) and Luis E. Cuevas * * Liverpool School of Tropical Medicine, Liverpool, United Kingdom; ([dagger]) Sana'a University, Sana'a, Yemen; ([double dagger]) University of Liverpool The University of Liverpool is a university in the city of Liverpool, England. History The University was established in 1881 as University College Liverpool, admitting its first students in 1882. , Liverpool, United Kingdom; and ([section]) Al-Sabeen Hospital for Women and Children, Sana'a, Yemen Dr Al-Sonboli is a pediatrician and lecturer at Sana'a University. Her main research interests are acute respiratory infections and diarrhea in children. Address for correspondence: Luis E. Cuevas, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK; email: lcuevas@liv.ac.uk
Table. Characteristics of children with mild and severe hypoxia
caused by infection with RSV and HMPV *
RSV hypoxia
Mild Severe
Characteristic (n = 34) (n = 232) p value
Male 22 (65) 154 (68) 0.4
Mean (SD) age, mo. 7.9 (5.6) 4.2 (4.8) <0.001
Preterm 1 (3) 11 (5) 0.5
Height-for-age Z scores
[less than or equal to] 2 13 (38) 73 (32) 0.2
Not exclusively breastfed 12 (35) 138 (59) 0.01
Incomplete vaccinations 7 (21) 178 (77) <0.001
Recurrent ARI 6 (18) 40 (17) 0.4
Recurrent wheeze 1 (3) 12 (5) 0.4
Eczema 1 (3) 11 (5) 0.5
Asthma 1 (3) 1 (0.4) 0.2
CHD 0 2 (1) 0.7
Family member with ARI 18 (53) 165 (71) 0.02
Family member with allergies 3 (9) 29 (13) 0.3
Family member with asthma 5 (15) 24 (10) 0.2
Family member with eczema 3 (9) 11 (5) 0.2
Smoker at home 9 (27) 120 (52) 0.002
Indoor animals 9 (27) 97 (42) 0.04
Cows 1 (3) 52 (22) 0.003
Goats 6 (18) 69 (30) 0.07
Chicken 3 (9) 39 (17) 0.1
Cats 3 (9) 26 (11) 0.4
Dogs 0 8 (3) 0.3
Donkeys 0 32 (10) 0.03
Outdoor animals 2 (6) 88 (38) <0.001
Private source of water 11 (32) 138 (60) 0.002
Cooking fuel other than gas 2 (6) 128 (55) <0.001
HMPV hypoxia
Mild Severe
Characteristic (n = 20) (n = 46) p value
Male 17 (85) 30 (65) 0.08
Mean (SD) age, mo. 9.1 (5.9) 5.7 (5.4) 0.02
Preterm 1 (5) 3 (7) 0.6
Height-for-age Z scores
[less than or equal to] 2 12 (60) 19 (41.3) 0.08
Not exclusively breastfed 15 (75) 23 (50) 0.1
Incomplete vaccinations 4 (20) 30 (65) <0.001
Recurrent ARI 2 (10) 15 (33) 0.04
Recurrent wheeze 0 (0) 5 (11) 0.1
Eczema 1 (5) 1 (2) 0.5
Asthma 0 3 (7) 0.3
CHD 0 0 0.3
Family member with ARI 7 (35) 28 (61) 0.03
Family member with allergies 4 (20) 4 (9) 0.1
Family member with asthma 1 (5) 5 (11) 0.4
Family member with eczema 1 (5) 5 (11) 0.4
Smoker at home 10 (50) 28 (61) 0.2
Indoor animals 4 (20) 15 (33) 0.2
Cows 0 (0) 9 (20) 0.02
Goats 1 (5) 7 (15) 0.2
Chicken 2 (10) 7 (15) 0.4
Cats 3 (15) 7 (15) 0.6
Dogs 0 0 0.2
Donkeys 0 4 (9) 0.2
Outdoor animals 1 (5) 14 (30) 0.01
Private source of water 5 (25) 22 (47) 0.04
Cooking fuel other than gas 2 (10) 23 (50) 0.001
* Values are no. (%) unless otherwise indicated. RSV, respiratory
syncytial virus; HMPV, human melapneumovirus; SD, standard deviation;
ARI, acute respiratory illness; CHD, congenital heart disease.
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