alexa Epidemiology of Respiratory Syncytial Virus Lower Respiratory Tract Infection (Rsv-Lrti) In Children in Developing Countries | Open Access Journals
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Epidemiology of Respiratory Syncytial Virus Lower Respiratory Tract Infection (Rsv-Lrti) In Children in Developing Countries

Sirintip Sricharoenchai1,2*, Emanuela Palla3, Franco Laghi Pasini4 and Melvin Sanicas1,5

1Faculty of Medicine and Surgery, Università di Siena, Italy

2Pediatric Infectious Diseases Unit, Siriraj, Mahidol University, Thailand

3Novartis Vaccines & Diagnostics, Siena, Italy

4Department of Medicine, Surgery and Neuroscience, Università di Siena, Italy

5Global Health, Bill and Melinda Gates Foundation, Seattle, WA, USA

*Corresponding Author:
Dr Sirintip Sricharoenchai
Pediatric Infectious Diseases Unit Department of Pediatrics
Siriraj Hospital Mahidol University
2 Prannok Road, Bangkok 10700, Thailand
Tel: 66-2-866-0944
E-mail: sirintipsri@gmail.com

Received Date: February 16, 2016; Accepted Date: April 09, 2016; Published Date: April 16, 2016

Citation: Sricharoenchai S, Palla E, Pasini FL, Sanicas M (2016) Epidemiology of Respiratory Syncytial Virus Lower Respiratory Tract Infection (Rsv-Lrti) In Children in Developing Countries. J Trop Dis 4:212. doi:10.4172/2329-891X.1000212

Copyright: © 2016 Sricharoenchai S, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Abstract

The global estimate in 2005 indicate that at least 33.8 million episodes of respiratory syncytial virus (RSV) associated acute lower respiratory infection (ALRI) occurred worldwide in children younger than 5 years and most of these deaths occurred in developing countries. The review aimed to analyze published epidemiological data on RSV lower respiratory tract infection in young children in developing countries to ascertain the burden of the disease for evidence-based public health priorities. Articles in English published between 2002 and 2014 were identified through literature searches in PubMed, Web of knowledge, and Embase. The incidence of RSV-LRTI in Asian.

Keywords

Respiratory syncytial virus; RSV; Lower respiratory tract infection; Children; Developing countries

Introduction

Lower respiratory tract infection (LRTI) is the leading global cause of death in children between 1 month and 5 years of age. Nearly 70% of LRTI deaths under five years old are among children in developing countries [1-4]. Clinical characteristics of RSV infection include upper respiratory infection with rhinorrhea and nasal congestion lasting between 7 and 12 days. Re-infection rates vary between 6% and 83% each year, showing that initial infection does not confer immunity to succeeding infection [5]. By the age of 2 years, nearly all children have had RSV infection [6]. More serious disease involving the lower respiratory tract may develop in older children especially in immunocompromised and cardiopulmonary disease patients [7,8]. The review aimed to systematically aggregate and analyze published epidemiological data on RSV lower respiratory tract infection in young children in developing countries, in order to ascertain the burden of the disease for evidence-based public health priorities and to summarize the currently available data and identify the gaps and scope for further epidemiological study of RSV lower respiratory tract infection in developing countries.

Literature Reviewed

Potentially relevant published articles were identified through literature searches of the following bibliographic database: Pubmed database, Web of knowledge, and Embase. To access publications from developing countries that might not be included in those databases, searches in Scielo, Indian Medlars Centre, Bioline International, and African Journals online were also performed. The following combination of MesH terms (Medical Subject Heading term) and individual search terms were used: (Respiratory Syncytial Viruses OR pneumonia OR bronchiolitis OR respiratory tract infections) AND (developing country OR each individual country of developing countries) for the epidemiological review, and (Respiratory Syncytial Viruses AND vaccine) for the review of vaccine development updates. The searches were restricted to studies of human subjects that were published in English between 2002 and 2014. For the purpose of this review, the developing countries were defined as the ones designated as such by either World Bank (low, lower middle and upper middleincome countries) or World Health Organization. For the results of epidemiological review, data extracted from original articles describing incidence, prevalence, and demographic distribution, comorbidities, complications and outcomes, and case fatality rates of RSV infection were tabulated and presented in descriptive form.

Results and Discussion

Pneumonia is one of the leading causes of childhood mortality. Of the 6.3 million children who died before age 5 years in 2013, infectious diseases caused 51.8% (3.257 million) of them, with the largest percentage due to pneumonia 935,000 deaths (817,000-1,057,000; 14.9% of total deaths, 13.0-16.8%), followed by diarrhea 578,000 deaths (448,000-750,000; 9.2%, 7.1- 11.9) [9] (Figure 1). The global estimate in 2005 indicate that at least 33.8 million episodes of respiratory syncytial virus (RSV) associated acute lower respiratory infection (ALRI) occurred worldwide in children younger than five years. This estimate represents approximately 22% of all episodes of ALRI in young children, and 96% of them were in developing countries (where 90% of the world’s population aged younger than 5 years reside).The global estimates also have shown that 3.4 million young children worldwide developed RSVassociated severe ALRI necessitating hospital admission, of which 91% occurred in developing countries. And 66,000-199,000 children younger than 5 years died from RSV associated ALRI, with 99% of these occur in developing countries [10]. Ninety-three studies were included in the review, 20 were community-based studies and 52 were hospital-based studies. The other studies discussed complications and outcomes of RSV-LRTI. The main outcome of 52 of the studies included was to identify the viral etiology of LRTI while the main outcome of the other studies was to identify the incidence of RSV-associated LRTI. PCR was the diagnostic method used by over 60% of the studies. Other diagnostic methods included ELISA, immunofluorescence and viral isolation. Countries included in the study and the corresponding number of studies for each are as follows:

tropical-diseases-causes-child-deaths

Figure 1: Global causes of child deaths [9].

Countries included in the study

Countries included in the study and the corresponding number of studies for each are as follows:

Africa: Madagascar (1), Kenya (13), Egypt (3), South Africa (4), Nigeria (2), Mozambique (3), Ghana (2), The Gambia (1), Tunisia (1).

Asia: Bangladesh (4), Nepal (5), Vietnam (4), China (5), India (6), Iran (1), Turkey (3), Thailand (10), Myanmar (1), Philippines (1), Indonesia (4), Malaysia (1), Jordan (1), Yemen (1), Russia (1) (borders European and Asian countries as well as the Pacific and Arctic oceans but for the purpose of this review is included here).

Latin America: Brazil (13), Argentina (1), Mexico (1), Guatemala (2).

A review of the community-based studies revealed that 39.7% to 84% of LRTI were positive for viral etiology and 11.8% to 80.8% of total viral LRTI were confirmed as RSV infection using PCR or ELISA (Table 1).

Country Age Sample size Disease studied Study period Mode of sampling Diagnostic method % Viral LRI of enrolled subjects % RSV of viral LRI
Madagascar [11] 2 to 59 mos 295 ARI Feb 10  to Feb 11 NP swab PCR 74.60% 11.80%
Kenya [12] < 5 yo 2,973 SARI Mar 07 to Feb 10 NP / OP swab PCR 84% 22%
Kenya [13] < 5 yo 1,815 (ILI) 4,449 (SARI) ILI, SARI Sept 07 to Aug 10 NP / OP swab PCR 49.80% 12.50%
Kenya [14] >1; <13 yo 451 LRI 2009 to 2010 NP aspirate PCR N / A 38%
Kenya [15] < 5 yo 4,012 (R) 2,744 (U) ILI, SARI Mar 07 to Feb 11 NP / OP swab PCR N / A 12.5% 11.7%
Bangladesh [16] ≤ 2 252 LRI 1993 to 1996 NP aspirate ELISA 44.80% 80.80%
Bangladesh [17] < 2 515 pneumonia Apr 09 to Mar 11 NP wash PCR 77.50% 29.00%
Nepal [18] 2mos to <3 yo 1,909 pneumonia Jul 04 to Jun 07 NP aspirate PCR 40.00% 37.70%
Nepal [19] 2 to 35 mos 2,230 pneumonia severe pneumonia Jun 04 to Jun 07 NP aspirate PCR 39.7% 44.3% 14.3% 27.5%
Vietnam [20] < 24 mos 4,800 ARI 2006 to 2007 NP aspirate PCR 64% 20.10%
China [21] < 5 yo 511 SARI 2010 to 2011 NP aspirate PCR 51.40% 33.10%

Table 1: Viral etiology of LRTI in community-based studies.

For hospital-based studies (Table 2), 11.2% to 94.3% of LRTI were positive for viral etiology and RSV accounted for 8% to 91% of total viral LRTI cases. The majority of hospital-based studies and all of community-based studies have shown that RSV was the most frequently detected virus in children with bronchiolitis, LRTI, pneumonia and severe pneumonia, suggesting that RSV was one of the major contributors of respiratory illnesses regardless of geographic location, disease studied, severity and setting of study. Only in one study from Iran and in two studies from Brazil and Mozambique, RSV is reported as being the second (Iran) and the third (Brazil and Mozambique) more frequently detected virus in locally conducted studies.

Country Age Sample size Disease studied Study period Mode of sampling Diagnostic method % Viral of enrolled subject %RSV out of viral LRI
Egypt [22] < 5 yo 450 LRI Nov 06 to Dec 07 NP aspirate DFA, PCR, virus isolation 59.90% 23.80%
Egypt [23] < 5 yo 427 LRI Dec 06 to Nov 07 NP aspirate IFA 21% 77%
South Africa [24] 3 mos to 2 yo 114 bronchiolitis Jun 99 to May 00 NP aspirate IF, viral isolation 48.30% 74.60%
South Africa [25] < 5 yo 4,293 LRI Jan 10 to Dec 11 NP aspirate PCR n/a 27%
Nigeria [26] < 5 yo 122 pneumonia N / A NP aspirate IFA 50.00% 45.90%
Mozambique [27] < 5 yo 807 severe pneumonia Sep 06 to Sep 07 NP aspirate PCR 48.80% 12.70%
Ghana [28] < 5 yo 128 severe pneumonia Jan 08 to Dec 08 NP swab PCR 25.80% 54.50%
Ghana [28] < 5 yo 128 LRI Jan 08 to Dec 08 NP aspirate / swab PCR 25.90% 14.10%
Kenya [29] 1 mo to <5 yo 810 severe pneumonia Jan 10 to Dec 10 NP swab PCR 60.40% 43.80%
Kenya [29,30] < 5 yo 2,143 ARI May 02 to  Apr 04 NP swab IF N / A 8.00%
Kenya [31] 1 mo to 59 mos 805 pneumonia Jan 10 to Dec 10 NP swab, OP swab, IS PCR 60.80% 12.50%
Brazil [32] 6mos to < 5 yo 472 pneumonia Jun 94 to Jun 95 NP swab DFA 11.20% 45.00%
Brazil [33] < 5 yo 336 LRI Jan 03 to Dec 03 nasal wash PCR 55.60% 43.30%
Brazil [34] < 5 yo 184 pneumonia Sep 03 to May 05 NP aspirate and paired serum IF, ELISA serology 66.30% 25.30%
Brazil [35] < 5 yo 455 LRI Feb 05 to Sep 06 NP aspirate IFA 30.20% 73.00%
Brazil [36] < 2 yo 77 bronchiolitis Mar 06 to Jul 07 NP aspirate PCR 93.50% 68.00%
Brazil [37] 0 to 3 yo 1,050 pneumonia Nov 06 to Oct 07 NP aspirate IFA, PCR n/a 23.10%
Brazil [38] 0 to 12 yo 12,160 RTI 2007 to 2010 NP aspirate IFA n/a 81.5% (07), 61% (08), 37.7% (09), 53.5% (10)
Argentina [39] < 5 yo 18561 LRI Jan 98 to Dec 02 NP aspirate IFA 32.80% 78.80%
Mexico [40] 0 to 18 yo 2,797 RTI Jan 04 to Dec 08 Nasal secretion, bronchial aspirate IFA 12.70% 74.70%
India [41] 1 mo to 1 yo 245 bronchiolitis Jan 07 to Dec 07 NP aspirate, NP swab, throat swab viral isolation, ELISA, PCR 46.10% 63.70%
China [42] ≤3 (a) 29183 LRI Jan 01 to Dec 06 NP aspirate IFA 36.30% 74.80%
China [43] <5 (c) 688 pneumonia Oct 04 to Oct 05 NP aspirate and paired serum DFA, ELISA serology 44.20% 43.40%
China [44] < 6 yo 370 SARI May 08 to Mar 10 NP aspirate or blood or IS Virus spin kit 94.30% 51.08%
China [45] < 14 yo 720 LRI, URTI Jul 09 to Jun 10 NP aspirate, NP swab, BAL PCR 55.80% 9.91%
Iran [46] 1 mo to 5 yo 202 LRI Oct 01 to May 02 NP secretion IFA 54.00% 23.80%
Turkey [47] 1mo to 5 yo 147 LRI Oct 06 to Mar 07 NP swab DFA 36.70% 55.60%
Turkey [48] < 2 yo 671 LRI N / A NP swab Respi-Strip n/a 38%
India [49] 1mo to ≤ 5 yo 301 LRI Apr 05 to Mar 07 NP aspirate PCR 35.20% 57.60%
India [50] 0 to 14 yo 188 LRI Jun 11 to May 12 NP aspirate PCR 45.70% 21.30%
India [51] < 2 yo 77 ALRI Sept 08 to Mar 09 NP aspirate DFA 22.10% 22.10%
Nepal [52] 2 mos to < 3 yo 627 severe pneumonia Jan 06 to Jun 08 NP aspirate PCR 30.00% 46.80%
Nepal [53] < 5 yo 772 pneumonia Jul 08 to Aug 11 NP aspirate Culture, viral isolation N / A 12.60%
Bangladesh# [54] < 2 yo 29 bronchiolitis Jul-10 NP swab, throat swab PCR 91% 91%
Vietnam [55] ≤ 5 yo (c) 295 LRI Nov 04 to Jan 08 NP aspirate, NP swab, throat swab PCR 72.50% 33.60%
Vietnam [56] 0 to 12 yo 1,082 ARI Apr 10 to May 11 NP swab PCR 63.80% 23.80%
Thailand [57] < 5 yo 467 LRI Nov 98 to Feb 01 NP aspirate IFA 36.00% 71.80%
Thailand [58] < 5 yo (d) 1325 pneumonia Sep 03 to Dec 05 NP swab ELISA, PCR 74.80% 50.20%
Thailand [59] 1 to 12 mos 354 LRI Dec 07 to Aug 09 NP swab PCR 36.70% 29.40%
Thailand – Myanmar [60] < 5 yo 708 pneumonia Apr 09 to Sept 11 NP aspirate PCR 53.70% 24.90%
Philippines [61] < 13 yo 819 severe pneumonia May 08 to May 09 NP swab PCR 61.20% 20.10%

Table 2: Viral etiology of LRTI in hospital-based studies.

a) Study recruited children aged 1 month to 13 years, but identified viral etiology in children aged ≤ 3 years.

b) Study recruited children, adults and elderly up to 76 years old, but identified viral etiology in children aged ≤ 5 years.

c) Study recruited children aged 2 months to 13 years, but identified viral etiology in children aged ≤ 5 years.

d) Study recruited children and adults up to 50 years old, but identified viral etiology in children aged <5 years.

e) Study recruited children aged 2 months to 14 years, but identified viral etiology in children aged <5 years.

Among community-based studies, a Nepalese study reported the lowest percentage of RSV among LRTI cases (14.3%) This might be due to age of study populations, as the study excluded young infants <2 months of age, who are considered to be the population at higher incidence. Frequency of viral detection depends on a variety of factors including the characteristics of study like study site, case definition, disease severity, duration of the study, season of the year, age range for study inclusion, patients selection criteria, health care and hospitalization setting or laboratory and specimen management like sampling method (nasopharyngeal aspiration/wash and nasal wash vs. nasal swab, nasopharyngeal swab or throat swab technique), quality of specimen samples, transport and storage condition of the samples, time of collection in relation to onset of illness, methodology applied to establish the diagnosis (e.g. RT-PCR, immunofluorescence, serology, culture), quality of reagents, laboratory technician experience, interand intra-laboratory standardization.

Besides the aforementioned factors, the proportion of viral LRI cases among enrolled subjects and the proportion of RSV cases among viral LRTI depend also on the number of etiologic agents in diagnostic panels. More virus types included in diagnostic panel can contribute to higher proportion of viral LRTI cases, thus to lower proportion of RSV cases among the viral LRTI cases identified. Viral LRTI cases tend to be detected more in studies using PCR method and diagnostic panel including various types of viruses. On the contrary, studies using diagnostic panel with less viral types (e.g. excluding rhinovirus, one of the common respiratory pathogen and human metapneumovirus) identified RSV in > 70%of viral LRTI cases. However, this is not necessarily the case, as inconsistent findings were demonstrated in some studies with fewer etiologic agents in the diagnostic panel but modest percentage of RSV in viral LRTI cases.

Incidence of RSV-associated LRTI in young children aged ≤ 5 years

Incidence rates were available mainly from two regions, Africa and Asia with one study from Latin America. The RSV-associated LRTI incidences reported by community-based studies in children aged <1 year ranged from 86.9-154/1000 child-years (Africa) and 333-125/1000 child-years (Asia). The incidence rates of RSV-associated LRTI in children aged <5 years reported were 90-94/1000 child-years (Africa) and 34-95/1000 child years in Asia (Table 3).

Country Study Period Study denominator Diagnostic method RSV-LRTI (per 1,000 child-years of observation) RSV severe LRTI (per 1,000 child-years of observation)
        <1 yo <5 yo <1 yo <5 yo
Nigeria [62] Jun 99 to May 01 Defined population based ELISA 116 94 n/a n/a
Kenya [63] Jan 02 to Jan 03 Defined population based DFA 154 n/a 104 n/a
Kenya [64] 2002 to 2005 Defined population based DFA 104 90 (b) 66 43 (b)
Kenya [15] Mar 07 to Feb 11 Defined population based DFA 86.9 (R) 62.8 (U) n/a n/a n/a
Indonesia [65] Feb 99 to Jan 01 Defined population based ELISA 41 34 16 1000%
Indonesia [66] Feb 99 to May 01 Defined population based ELISA and PCR n/a 95 n/a n/a
Bangladesh [17] Apr 09 to Mar 11 Defined population based PCR 125 (a) n/a n/a n/a
India [67] Oct 01 to Mar 05 Defined population based DFA, viral isolation 33 39 (c) 14 9(c)
Guatemala [68] Nov 07 to Dec 12 Feb 09 to Dec 12 Nov 09 to Apr 11 Defined population based PCR 58 n/a n/a n/a

Table 3: Incidence of RSV-associated LRTI and severe LRTI in community-based studies.

a) Study recruited children aged 1 month to 13 years, but identified viral etiology in children aged ≤ 3 years.

b) Study recruited children, adults and elderly up to 76 years old, but identified viral etiology in children aged ≤ 5 years.

c) Study recruited children aged 2 months to 13 years, but identified viral etiology in children aged ≤ 5 years.

In general, hospital-based studies reported lower incidence of both RSV-LRTI and RSV-severe LRTI than community-based studies. Although RSV-severe LRTI cases are expected to be hospitalized, different studies from the same district in Kenya reported hospitalbased estimates 5-6 times lower than community-based estimates (Table 4).

Country Study period Study denominator Diagnostic method RSV-LRTI (per 1,000 child-years of observation) RSV severe LRTI (per 1,000 child-years of observation)
        <1yr <5yr <1yr <5yr
Gambia [69] Oct 93 to Dec 97 Defined population base IF N/A N/A 8.7-17.7 (d) n/a
Kenya [70] Jan 02 to Dec 07 Defined population base DFA N/A N/A 11.1 290.00%
Kenya [71] Jan 07 to Dec 07 Defined population base PCR N/A N/A 20.4 540.00%
Mozambique [72] Feb 99 to Jan 00 Defined population base ELISA 30 N/A 15 500.00%
South Africa  [72] Apr 00 to Mar 01 Defined population base ELISA N/A N/A 15 900.00%
Indonesia [59] Jan 00 to Dec 01 Defined population base ELISA N/A N/A 25 n/a
Thailand [73] Nov 98 to Feb 01 Defined population base IF N/A 5.8-12.6 (e) N/A N/A
Thailand [74] Sep 03 to Dec 07 Census derived estimate PCR, ELISA serology 10.9 8.8 N/A N/A
Thailand [75] Sep 03 to Dec 05 Census derived estimate PCR, viral isolation, ELISA serology n/a 8.2 N/A N/A
Thailand [76] Jan 08 to Dec 11 Census derived estimate PCR 15.43 9.8 N/A N/A
India [77] Aug 09 to Jul 11 Census derived estimate PCR 346 N/A N/A N/A
Guatemala [78] Nov 07 to Jul 10 Defined population based PCR 5.9 2 45.9 1370.00%

Table 4: Incidence of RSV-associated LRTI and severe LRTI in hospital-based studies.

a) Incidence of RSV-LRTI in children aged <2 years

b) Incidence of RSV LRTI/severe LRTI in children aged <2.5 years

c) Incidence of RSV LRTI/severe LRTI in children aged <3 years

d) Incidence of RSV severe LRTI in urban (8.7) and rural (17.7) settings

e) Incidence of RSV LRTI during the first (12.6) and second studied year (5.8)

Few epidemiological studies reported RSV incidence stratified by comparable age groups. The highest incidence rates were found in young infants aged < 6 months in 2 studies and even younger aged <3 months in 1 study [68]. Interestingly, studies from Indonesia found the lowest incidence in infants younger than 6 months of age [64] and lack of RSV-LRTI in infants aged less than 3 months [63,64]. In another study from the same country (Indonesia), the presence of RSV-LRTI in infants younger than 3 months old was reported but the incidence was not found to be the highest rate [70]. Incidence studies were mainly from Africa and Southeast Asia, which are the world regions with the highest incidence of pneumonia. It should be noted, however, that those studies are largely from only some countries such as Nigeria, Kenya, Mozambique, South Africa, Gambia, Indonesia, Bangladesh, India. Other countries with highest estimated absolute number of new cases of pneumonia such as China, Pakistan, Ethiopia, Democratic Republic of Congo, Vietnam, Philippines, Sudan, Afghanistan, United Republic of Tanzania, Myanmar, and Brazil are not proportionally represented in this review. It is crucial to generate data from countries where child pneumonia incidence is highest. No incidence studies were identified from the Eastern Mediterranean, the Western Pacific, Latin Americas, and developing European Regions. This may be due to the use of English language as one of the inclusion criteria. Fourteen studies reported underlying conditions known to be risk factors for serious RSV infection among young children with RSV-LRTI. History of premature birth was found in 4.6% to 27.0% of children with RSVLRTI. 1.0% to 17.7% of cases had congenital heart disease and chronic lung disease was found in 1.0% of the cases.

Rates of hospitalized LRTI were similar in magnitude across all studies. But in the South African study, there was a documented drop in clinic attendance rates during the study period due to a shortage of medications. Thus, the findings represent minimum estimates of the burden of severe LRI. The Indonesian study stated that most acute respiratory illness deaths in the study villages occurred at home, thus the hospitalization incidences reported here should be considered a fraction of the true incidence of RSV cases that resulted in hospitalizations.

Co-morbidities of RSV-LRTI cases

Malaria: Four studies from Africa reported malaria parasitemia in children with RSV-LRTI. Malaria co-occurred in 2.0% to 28.4% of children with RSV-LRTI. A prospective population-based surveillance study from Kenya reported that concurrent malaria parasitemia were significantly less common among RSV-positive children than RSVnegative children (Relative Risk, RR=0.36; 95%CI 0.26-0.49). Similarly, a study from Mozambique reported the association of malaria with a lower prevalence of RSV infection (Odd Ratio, OR=0.5; 95%CI 0.20-0.90). Two African studies reported a negative association between malaria and RSV. Suppression of malaria parasitemia has been observed with another on-going viral infection (measles and influenza). However, a study from Mozambique found that the prevalence of malaria parasitemia among RSV-positive patients is similar to that seen in community surveys (30%), therefore suggesting that this negative association may be an artifact resulting from the high prevalence of malaria parasitemia among other admitted children.

HIV infection: Two studies from Africa found that 10.0% to 13.6% of RSV-LRTI children were HIV-positive. A study from South Africa reported higher rates of concomitant bacteremia in HIV-positive children with RSV LRTI than HIV-negative children. (HIV vs. non-HIV; 6.9% vs. 1.4%). Case fatality rate of HIV-infected children was higher than for HIV-uninfected children (7.4% vs. 0.6%, respectively). Of note, this study could not exclude that concurrent PCP (Pneumocystis carinii pneumonia) might have contributed to a higher mortality rate in HIV-infected children as the investigation for Pneumocystis carinii pneumonia was not done in every HIV-infected children who died.

Malnutrition: Five studies reported a proportion of malnourished condition in children with RSV-LRTI by using various definition of malnutrition. Overall, 6.6% to 24.8% of children with RSV-LRTI had malnutrition. A study from Kenya reported that severe malnutrition was significantly less common among RSV-positive children (RR=0.47; 95%CI 0.36-0.61). A study from Mozambique reported that mild or moderate and severe malnutrition were associated with a lower risk for RSV infections, (OR=0.50; 95%CI 0.30-0.80 and 0.20; 95%CI 0.10-0.60), respectively). Malnutrition is a well-known cause of immunodeficiency and has been shown to be associated with increased incidence and mortality of respiratory illness, but this risk is not common to all acute respiratory and seems to be low for RSV. The negative association found between malnutrition and RSV infection is in agreement with other previous studies in Nigeria and the Gambia, where RSV was found less frequently in malnourished children with pneumonia.

Malaria may result in fever and raised respiratory rate, therefore, it could be another confounding infection mimicking LRTI in countries where malaria is endemic [76,77]. Moreover, the common practice of treating children with respiratory symptoms with antimalarial drugs causes delays in care seeking for children with pneumonia. Most children who died from pneumonia were reportedly first treated at home with antimalarial drugs [78]. Hence, malaria endemicity affects the estimation of RSV prevalence/incidence among LRTI cases and case fatality rate of RSV-LRTI. Increasing awareness is important for healthcare workers who should provide adequate diagnosis and treatment of both pneumonia and malaria. The contribution of RSVLRTI differs between HIV-infected and HIV-uninfected children. HIV-infected children have greater evidence of bacterial co-infection and greater mortality than HIV-uninfected children, as previously described [79,80]. In a lot of the health facilities in developing countries, a moderate degree of malnutrition is so common that it is frequently not recorded as an admission diagnosis, and the increased risk of death is not appreciated. Moreover, the clinical signs such as fast breathing and retractions have poor predictive values in malnourished children [81]. Thus, the difference and consequences of malnutrition should not be neglected.

Limitations of the current literature review

Despite various literature databases utilized to make this review as exhaustive as possible, some limitations exist. Only English literature was searched. This likely biased the findings by excluding some studies from certain regions such as China, and some countries in Latin America, Russia, and the Middle East where there may be substantial information in local language publications. The comparability of various findings from the reviewed literature included is problematic for a number of reasons including dissimilar case finding procedures, variable study year, and non-uniform classification schemes for age. Studies that were published before 2002 have been excluded, and this may have led to an underestimation of some results. However, it does ensure that the most current epidemiological data was focused and previous studies, in which conventional virological diagnostic techniques were used, have most likely underestimated rates of RSV infection. The possibility of excluding relevant studies because the published studies were screened by abstract review and were excluded if the abstract did not indicate that the paper contained information on RSV epidemiology. Some papers may have contained relevant information, even if this was not apparent from the abstract.

Conclusions

Despite the increasing number of epidemiological studies of RSV-LRTI published over the past 13 years in developing countries, there are still clearly many areas that merit further study. There is still a need to establish further RSV surveillance studies to improve the incidence estimates and to explore the extent to which national and regional variation in RSV infection rates exist in countries where there is a high burden and high mortality attributable to LRTI but lack of understanding of local RSV epidemiology. Studies of RSV disease burden should ideally be prospective, community-based, with a known population denominator, with standardized case definition, with specimens collected by nasopharyngeal aspirate or nasal wash and tested by sensitive viral detection method (preferably using PCR assay), and with active surveillance by dedicated research staffs who can obtain specimens at the household level. To strengthen the available body of evidence for RSV epidemiology, future incidence studies should be conducted in compliance with the existing WHO protocol to be standardized and facilitate international comparisons. Specifically, in areas of disease severity in various age groups, reinfection and agespecific incidence which have implications for vaccine development and immunization strategies, have been incompletely reported. Reporting of information on underlying illnesses, prematurity, complications and therapy administered to RSV-LRTI cases should be encouraged and harmonized to permit a valid comparison of RSVLRTI epidemiology across studies. Furthermore, these data would supplement the basis of a cost-effectiveness quantification to justify the cost and effort of introducing a vaccine and of sustainability when a vaccine becomes available. Given the importance of HIV and malaria on RSV epidemiology, their impact on RSV should be further explored in HIV and malaria endemic countries.

A number of important challenges remain including: (1) in community-based studies, case ascertainment would be difficult in communities where a variety of different sources of medical care are utilized, for example, use of private practitioners, over-the-counter drugs, or household remedies; (2) morbidity and mortality is likely to be under-recognized due to delayed healthcare seeking behavior and limited healthcare access; (3) diagnosis of bacterial pneumonia secondary to RSV infection in young children with communityacquired pneumonia is difficult to establish, (4) funding and resources are needed to enable studies with adequate study design and adequate study methodologies to be conducted. The high burden of RSV-LRTI in developing countries justifies the investment of resources for widescale epidemiologic studies, and investments to fund such studies should be considered by international organizations. At a national level, governments must give high priority to the fight against RSVLRTI and should identify centers to be equipped with laboratory facilities. Investigations of epidemiology as recommended above and systematic data collection will help decision-makers in understanding RSV epidemiology, thereby avoiding delays in vaccine deployment in developing nations with tremendous need. Good quality data from countries and regions will facilitate precise global estimation of RSVLRTI burden. Such estimates are useful to motivate international efforts such as vaccine development or financing.

Author Contributions

SS, EP, FLP contributed to the design and interpretation of data for this manuscript. SS, MS were responsible for drafting the work and revising it critically for intellectual content. All authors agree to be fully accountable for ensuring the integrity and accuracy of the work and read and approved the final manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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