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1.  Improving pandemic influenza risk assessment 
eLife  2014;3:e03883.
Assessing the pandemic risk posed by specific non-human influenza A viruses is an important goal in public health research. As influenza virus genome sequencing becomes cheaper, faster, and more readily available, the ability to predict pandemic potential from sequence data could transform pandemic influenza risk assessment capabilities. However, the complexities of the relationships between virus genotype and phenotype make such predictions extremely difficult. The integration of experimental work, computational tool development, and analysis of evolutionary pathways, together with refinements to influenza surveillance, has the potential to transform our ability to assess the risks posed to humans by non-human influenza viruses and lead to improved pandemic preparedness and response.
PMCID: PMC4199076  PMID: 25321142
influenza; pandemic; emergence; human; viruses
2.  Enhanced Surveillance of Norovirus Outbreaks of Gastroenteritis in Georgia 
Public Health Reports  2011;126(2):251-258.
The role of noroviruses in both foodborne and person-to-person outbreaks of acute gastroenteritis (AGE) has been difficult to determine in the U.S. because of lack of routine norovirus testing and of national reporting of person-to-person outbreaks. We conducted a prospective study in one state in which enhanced testing for noroviruses was performed to better understand the relative contribution of all gastroenteric pathogens.
During the two-year period, 2000–2001, we took all fecal specimens from AGE outbreaks reported in Georgia that were negative for bacteria and tested these for norovirus.
We investigated 78 AGE outbreaks, from which suitable fecal samples were collected from 57 of them. Norovirus was identified in 25 (44%) outbreaks, bacteria in 20 (35%) outbreaks, and parasites in one (2%) outbreak. Forty-three (75%) of the outbreaks tested were foodborne, of which 17 (40%) were attributable to norovirus and 18 (42%) were attributable to bacteria. Adjusting for incomplete testing, we estimated that 53% of all AGE outbreaks were attributable to norovirus. A total of 2,674 people were reported ill in the 57 outbreaks, and norovirus infections accounted for 1,735 (65%) of these cases. Norovirus outbreaks tended to be larger than bacterial outbreaks, with a median number of 30 vs. 16 cases per outbreak, respectively (p=0.057).
This study provides further evidence that noroviruses are, overall, the most common cause of AGE outbreaks in the U.S. Improved specimen collection, reporting person-to-person outbreaks, and access to molecular assays are needed to further understand the role of these viruses and methods for their prevention.
PMCID: PMC3056038  PMID: 21387955
3.  Are Noroviruses Emerging? 
Emerging Infectious Diseases  2005;11(5):95-102.
PMCID: PMC3320389  PMID: 15898170
Epidemiology; Norovirus; Communicable Diseases; Emerging
4.  Norovirus and Foodborne Disease, United States, 1991–2000 
Emerging Infectious Diseases  2005;11(1):95-102.
Analysis of foodborne outbreaks shows how advances in viral diagnostics are clarifying the causes of foodborne outbreaks and determining the high impact of norovirus infections.
Efforts to prevent foodborne illness target bacterial pathogens, yet noroviruses (NoV) are suspected to be the most common cause of gastroenteritis. New molecular assays allow for better estimation of the role of NoV in foodborne illness. We analyzed 8,271 foodborne outbreaks reported to the Centers for Disease Control and Prevention from 1991 to 2000 and additional data from 6 states. The proportion of NoV-confirmed outbreaks increased from 1% in 1991 to 12% in 2000. However, from 1998 to 2000, 76% of NoV outbreaks were reported by only 11 states. In 2000, an estimated 50% of foodborne outbreaks in 6 states were attributable to NoV. NoV outbreaks were larger than bacterial outbreaks (median persons affected: 25 versus 15), and 10% of affected persons sought medical care; 1% were hospitalized. More widespread use of molecular assays will permit better estimates of the role of NoV illness and help direct efforts to control foodborne illness.
PMCID: PMC3294339  PMID: 15705329
research; food; norovirus; disease outbreaks; burden of illness
5.  Norovirus Transmission on Cruise Ship 
Emerging Infectious Diseases  2005;11(1):154-157.
We documented transmission by food and person-to-person contact; persistence of virus despite sanitization onboard, including introductions of new strains; and seeding of an outbreak on land.
We describe an investigation of a norovirus gastroenteritis outbreak aboard a cruise ship affecting 6 consecutive cruises and the use of sequence analysis to determine modes of virus transmission. Noroviruses (NoV), are the most common cause of infectious acute gastroenteritis and are transmitted feco-orally through food and water, directly from person to person and by environmental contamination (1). These viruses are often responsible for protracted outbreaks in closed settings, such as cruise ships, nursing homes, and hospitals (2,3).
PMCID: PMC3294347  PMID: 15705344
viral gastroenteritis; outbreak; Norwalk; cruise ship; dispatch
6.  Automated, Laboratory-based System Using the Internet for Disease Outbreak Detection, the Netherlands 
Emerging Infectious Diseases  2003;9(9):1046-1052.
Rapid detection of outbreaks is recognized as crucial for effective control measures and has particular relevance with the recently increased concern about bioterrorism. Automated analysis of electronically collected laboratory data can result in rapid detection of widespread outbreaks or outbreaks of pathogens with common signs and symptoms. In the Netherlands, an automated outbreak detection system for all types of pathogens has been developed within an existing electronic laboratory-based surveillance system called ISIS. Features include the use of a flexible algorithm for daily analysis of data and presentation of signals on the Internet for interpretation by health professionals. By 2006, the outbreak detection system will analyze laboratory-reported data on all pathogens and will cover 35% of the Dutch population.
PMCID: PMC3016793  PMID: 14519238
Disease outbreaks; algorithms; Internet; laboratories; data collection
7.  Timing of Influenza A(H5N1) in Poultry and Humans and Seasonal Influenza Activity Worldwide, 2004–2013 
Emerging Infectious Diseases  2015;21(2):202-208.
Co-circulation of H5N1 in poultry and humans during seasonal influenza epidemic periods signals the need for enhanced surveillance and biosafety measures.
Co-circulation of influenza A(H5N1) and seasonal influenza viruses among humans and animals could lead to co-infections, reassortment, and emergence of novel viruses with pandemic potential. We assessed the timing of subtype H5N1 outbreaks among poultry, human H5N1 cases, and human seasonal influenza in 8 countries that reported 97% of all human H5N1 cases and 90% of all poultry H5N1 outbreaks. In these countries, most outbreaks among poultry (7,001/11,331, 62%) and half of human cases (313/625, 50%) occurred during January–March. Human H5N1 cases occurred in 167 (45%) of 372 months during which outbreaks among poultry occurred, compared with 59 (10%) of 574 months that had no outbreaks among poultry. Human H5N1 cases also occurred in 59 (22%) of 267 months during seasonal influenza periods. To reduce risk for co-infection, surveillance and control of H5N1 should be enhanced during January–March, when H5N1 outbreaks typically occur and overlap with seasonal influenza virus circulation.
PMCID: PMC4313643  PMID: 25625302
H5N1; poultry; human; seasonal influenza; global; influenza; viruses; outbreaks; surveillance; biosafety
8.  The Burden of Influenza and RSV among Inpatients and Outpatients in Rural Western Kenya, 2009–2012 
PLoS ONE  2014;9(8):e105543.
In Kenya, detailed data on the age-specific burden of influenza and RSV are essential to inform use of limited vaccination and treatment resources.
We analyzed surveillance data from August 2009 to July 2012 for hospitalized severe acute respiratory illness (SARI) and outpatient influenza-like illness (ILI) at two health facilities in western Kenya to estimate the burden of influenza and respiratory syncytial virus (RSV). Incidence rates were estimated by dividing the number of cases with laboratory-confirmed virus infections by the mid-year population. Rates were adjusted for healthcare-seeking behavior, and to account for patients who met the SARI/ILI case definitions but were not tested.
The average annual incidence of influenza-associated SARI hospitalization per 1,000 persons was 2.7 (95% CI 1.8–3.9) among children <5 years and 0.3 (95% CI 0.2–0.4) among persons ≥5 years; for RSV-associated SARI hospitalization, it was 5.2 (95% CI 4.0–6.8) among children <5 years and 0.1 (95% CI 0.0–0.2) among persons ≥5 years. The incidence of influenza-associated medically-attended ILI per 1,000 was 24.0 (95% CI 16.6–34.7) among children <5 years and 3.8 (95% CI 2.6–5.7) among persons ≥5 years. The incidence of RSV-associated medically-attended ILI was 24.6 (95% CI 17.0–35.4) among children <5 years and 0.8 (95% CI 0.3–1.9) among persons ≥5 years.
Influenza and RSV both exact an important burden in children. This highlights the possible value of influenza vaccines, and future RSV vaccines, for Kenyan children.
PMCID: PMC4136876  PMID: 25133576
9.  Economic burden of influenza-associated hospitalizations and outpatient visits in Bangladesh during 2010 
Understanding the costs of influenza-associated illness in Bangladesh may help health authorities assess the cost-effectiveness of influenza prevention programs. We estimated the annual economic burden of influenza-associated hospitalizations and outpatient visits in Bangladesh.
From May through October 2010, investigators identified both outpatients and inpatients at four tertiary hospitals with laboratory-confirmed influenza infection through rRT-PCR. Research assistants visited case-patients' homes within 30 days of hospital visit/discharge and administered a structured questionnaire to capture direct medical costs (physician consultation, hospital bed, medicines and diagnostic tests), direct non-medical costs (food, lodging and travel) and indirect costs (case-patients' and caregivers' lost income). We used WHO-Choice estimates for routine healthcare service costs. We added direct, indirect and healthcare service costs to calculate cost-per-episode. We used median cost-per-episode, published influenza-associated outpatient and hospitalization rates and Bangladesh census data to estimate the annual economic burden of influenza-associated illnesses in 2010.
We interviewed 132 outpatients and 41 hospitalized patients. The median cost of an influenza-associated outpatient visit was US$4.80 (IQR = 2.93–8.11) and an influenza-associated hospitalization was US$82.20 (IQR = 59.96–121.56). We estimated that influenza-associated outpatient visits resulted in US$108 million (95% CI: 76–147) in direct costs and US$59 million (95% CI: 37–91) in indirect costs; influenza-associated hospitalizations resulted in US$1.4 million (95% CI: 0.4–2.6) in direct costs and US$0.4 million (95% CI: 0.1–0.8) in indirect costs in 2010.
In Bangladesh, influenza-associated illnesses caused an estimated US$169 million in economic loss in 2010, largely driven by frequent but low-cost outpatient visits.
PMCID: PMC4181799  PMID: 24750586
Bangladesh; cost; hospitalization; influenza; outpatient
10.  The Role of Temperature and Humidity on Seasonal Influenza in Tropical Areas: Guatemala, El Salvador and Panama, 2008–2013 
PLoS ONE  2014;9(6):e100659.
The role of meteorological factors on influenza transmission in the tropics is less defined than in the temperate regions. We assessed the association between influenza activity and temperature, specific humidity and rainfall in 6 study areas that included 11 departments or provinces within 3 tropical Central American countries: Guatemala, El Salvador and Panama.
Logistic regression was used to model the weekly proportion of laboratory-confirmed influenza positive samples during 2008 to 2013 (excluding pandemic year 2009). Meteorological data was obtained from the Tropical Rainfall Measuring Mission satellite and the Global Land Data Assimilation System. We found that specific humidity was positively associated with influenza activity in El Salvador (Odds Ratio (OR) and 95% Confidence Interval of 1.18 (1.07–1.31) and 1.32 (1.08–1.63)) and Panama (OR = 1.44 (1.08–1.93) and 1.97 (1.34–2.93)), but negatively associated with influenza activity in Guatemala (OR = 0.72 (0.6–0.86) and 0.79 (0.69–0.91)). Temperature was negatively associated with influenza in El Salvador's west-central departments (OR = 0.80 (0.7–0.91)) whilst rainfall was positively associated with influenza in Guatemala's central departments (OR = 1.05 (1.01–1.09)) and Panama province (OR = 1.10 (1.05–1.14)). In 4 out of the 6 locations, specific humidity had the highest contribution to the model as compared to temperature and rainfall. The model performed best in estimating 2013 influenza activity in Panama and west-central El Salvador departments (correlation coefficients: 0.5–0.9).
The findings highlighted the association between influenza activity and specific humidity in these 3 tropical countries. Positive association with humidity was found in El Salvador and Panama. Negative association was found in the more subtropical Guatemala, similar to temperate regions. Of all the study locations, Guatemala had annual mean temperature and specific humidity that were lower than the others.
PMCID: PMC4067338  PMID: 24956184
11.  Implementing hospital-based surveillance for severe acute respiratory infections caused by influenza and other respiratory pathogens in New Zealand 
Recent experience with pandemic influenza A(H1N1)pdm09 highlighted the importance of global surveillance for severe respiratory disease to support pandemic preparedness and seasonal influenza control. Improved surveillance in the southern hemisphere is needed to provide critical data on influenza epidemiology, disease burden, circulating strains and effectiveness of influenza prevention and control measures. Hospital-based surveillance for severe acute respiratory infection (SARI) cases was established in New Zealand on 30 April 2012. The aims were to measure incidence, prevalence, risk factors, clinical spectrum and outcomes for SARI and associated influenza and other respiratory pathogen cases as well as to understand influenza contribution to patients not meeting SARI case definition.
All inpatients with suspected respiratory infections who were admitted overnight to the study hospitals were screened daily. If a patient met the World Health Organization’s SARI case definition, a respiratory specimen was tested for influenza and other respiratory pathogens. A case report form captured demographics, history of presenting illness, co-morbidities, disease course and outcome and risk factors. These data were supplemented from electronic clinical records and other linked data sources.
Hospital-based SARI surveillance has been implemented and is fully functioning in New Zealand. Active, prospective, continuous, hospital-based SARI surveillance is useful in supporting pandemic preparedness for emerging influenza A(H7N9) virus infections and seasonal influenza prevention and control.
PMCID: PMC4113656  PMID: 25077034
12.  Improvements in pandemic preparedness in 8 Central American countries, 2008 - 2012 
In view of ongoing pandemic threats such as the recent human cases of novel avian influenza A(H7N9) in China, it is important that all countries continue their preparedness efforts. Since 2006, Central American countries have received donor funding and technical assistance from the U.S. Centers for Disease Control and Prevention (CDC) to build and improve their capacity for influenza surveillance and pandemic preparedness. Our objective was to measure changes in pandemic preparedness in this region, and explore factors associated with these changes, using evaluations conducted between 2008 and 2012.
Eight Central American countries scored their pandemic preparedness across 12 capabilities in 2008, 2010 and 2012, using a standardized tool developed by CDC. Scores were calculated by country and capability and compared between evaluation years using the Student’s t-test and Wilcoxon Rank Sum test, respectively. Virological data reported to WHO were used to assess changes in testing capacity between evaluation years. Linear regression was used to examine associations between scores, donor funding, technical assistance and WHO reporting.
All countries improved their pandemic preparedness between 2008 and 2012 and seven made statistically significant gains (p < 0.05). Increases in median scores were observed for all 12 capabilities over the same period and were statistically significant for eight of these (p < 0.05): country planning, communications, routine influenza surveillance, national respiratory disease surveillance, outbreak response, resources for containment, community interventions and health sector response. We found a positive association between preparedness scores and cumulative funding between 2006 and 2011 (R2 = 0.5, p < 0.01). The number of specimens reported to WHO from participating countries increased significantly from 5,551 (2008) to 18,172 (2012) (p < 0.01).
Central America has made significant improvements in influenza pandemic preparedness between 2008 and 2012. U.S. donor funding and technical assistance provided to the region is likely to have contributed to the improvements we observed, although information on other sources of funding and support was unavailable to study. Gains are also likely the result of countries’ response to the 2009 influenza pandemic. Further research is required to determine the degree to which pandemic improvements are sustainable.
PMCID: PMC4022548  PMID: 24886275
Pandemic; Influenza; Preparedness; IHR; Central America; Capacity-building; Technical assistance
13.  Influenza-associated Hospitalizations and Deaths, Costa Rica, 2009–2012 
Emerging Infectious Diseases  2014;20(5):878-881.
Data needed to guide influenza vaccine policies are lacking in tropical countries. We multiplied the number of severe acute respiratory infections by the proportion testing positive for influenza. There were ≈6,699 influenza hospitalizations and 803 deaths in Costa Rica during 2009–2012, supporting continuation of a national influenza vaccine program.
PMCID: PMC4012819  PMID: 24750897
influenza; hospitalization rate; mortality rate; severe acute respiratory infections; viruses; Costa Rica; tropical; Americas
14.  Population-Based Incidence of Severe Acute Respiratory Virus Infections among Children Aged <5 Years in Rural Bangladesh, June–October 2010 
PLoS ONE  2014;9(2):e89978.
Better understanding the etiology-specific incidence of severe acute respiratory infections (SARIs) in resource-poor, rural settings will help further develop and prioritize prevention strategies. To address this gap in knowledge, we conducted a longitudinal study to estimate the incidence of SARIs among children in rural Bangladesh.
During June through October 2010, we followed children aged <5 years in 67 villages to identify those with cough, difficulty breathing, age-specific tachypnea and/or danger signs in the community or admitted to the local hospital. A study physician collected clinical information and obtained nasopharyngeal swabs from all SARI cases and blood for bacterial culture from those hospitalized. We tested swabs for respiratory syncytial virus (RSV), influenza viruses, human metapneumoviruses, adenoviruses and human parainfluenza viruses 1–3 (HPIV) by real-time reverse transcription polymerase chain reaction. We calculated virus-specific SARI incidence by dividing the number of new illnesses by the person-time each child contributed to the study.
We followed 12,850 children for 279,029 person-weeks (pw) and identified 141 SARI cases; 76 (54%) at their homes and 65 (46%) at the hospital. RSV was associated with 7.9 SARI hospitalizations per 100,000 pw, HPIV3 2.2 hospitalizations/100,000 pw, and influenza 1.1 hospitalizations/100,000 pw. Among non-hospitalized SARI cases, RSV was associated with 10.8 illnesses/100,000 pw, HPIV3 1.8/100,000 pw, influenza 1.4/100,000 pw, and adenoviruses 0.4/100,000 pw.
Respiratory viruses, particularly RSV, were commonly associated with SARI among children. It may be useful to explore the value of investing in prevention strategies, such as handwashing and respiratory hygiene, to reduce respiratory infections among young children in such settings.
PMCID: PMC3934972  PMID: 24587163
15.  Risk factors associated with fatal influenza, Romania, October 2009 – May 2011 
Limited data are available from Central and Eastern Europe on risk factors for severe complications of influenza. Such data are essential to prioritize prevention and treatment resources and to adapt influenza vaccination recommendations.
To use sentinel surveillance data to identify risk factors for fatal outcomes among hospitalized patients with severe acute respiratory infections (SARI) and among hospitalized patients with laboratory-confirmed influenza.
Retrospective analysis of case-based surveillance data collected from sentinel hospitals in Romania during the 2009/2010 and 2010/2011 winter influenza seasons was performed to evaluate risk factors for fatal outcomes using multivariate logistic regression.
During 2009/2010 and 2010/2011, sentinel hospitals reported 661 SARI patients of which 230 (35%) tested positive for influenza. In the multivariate analyses, infection with influenza A(H1N1)pdm09 was the strongest risk factor for death among hospitalized SARI patients (OR: 6·6; 95% CI: 3·3–13·1). Among patients positive for influenza A(H1N1)pdm09 virus infection (n = 148), being pregnant (OR: 7·1; 95% CI: 1·6–31·2), clinically obese (OR: 2·9;95% CI: 1·6–31·2), and having an immunocompromising condition (OR: 3·7;95% CI: 1·1–13·4) were significantly associated with fatal outcomes.
These findings are consistent with several other investigations of risk factors associated with influenza A(H1N1)pdm09 virus infections. They also support the more recent 2012 recommendations by the WHO Strategic Advisory Group of Experts on Immunization (SAGE) that pregnant women are an important risk group for influenza vaccination. Ongoing sentinel surveillance can be useful tool to monitor risk factors for complications of influenza virus infections during each influenza season, and pandemics as well.
PMCID: PMC4177790  PMID: 24251915
Influenza; risk factors; Romania; severe acute respiratory illness; surveillance
16.  Clinical differences between influenza A (H1N1) pdm09 & influenza B infections identified through active community surveillance in north India 
Background & objectives:
Most studies on the clinical presentation with influenza viruses have been conducted in outpatient or inpatient medical facilities with only a few studies in community settings. Clinical differences between influenza A (H1N1) pdm 09 and influenza B virus infections have importance for community-based public health surveillance. An active community surveillance at the time of emergence of pandemic influenza provided us with an opportunity to compare the clinical features among patients infected with influenza A (H1N1) pdm09 virus and those with influenza B virus co-circulating in an active community-based weekly surveillance in three villages in Faridabad, Haryana, north India.
Active surveillance for febrile acute respiratory infection (FARI) was carried out in a rural community (n=16,182) in the context of an inactivated trivalent influenza vaccine trial (among children <11 yr). Individuals with FARI were assessed clinically by nurses and respiratory samples collected and tested for influenza viruses by real time RT-PCR from November 2009 to August 2010. Clinical symptoms of patients with influenza A (H1N1) pdm 09 and influenza B infection were compared.
Of the 4796 samples tested, 822 (17%) were positive for influenza virus. Of these, 443 (54%) were influenza A (H1N1) pdm09, 373 (45%) were influenza B and six were other subtypes/mixed infections. The mean age was lower for patients with influenza B (16.4 yr) than influenza A (H1N1) pdm09 infection (18.7 yr; P=0.04). Among children aged 5-18 yr, chills/rigours (OR 4.0; CI 2.2, 7.4), sore throat (OR 6.8; CI 2.3, 27.3) and headache (OR2.0; CI 1.3, 3.3) were more common in influenza A (H1N1) pdm09 infection than in influenza B cases. Chills/rigours (OR 2.4; CI 1.4, 4.0) and headache (OR 1.7; CI 1.0, 2.7) were associated with influenza A (H1N1) pdm09 infection in those >18 yr. No significant differences were seen in children <5 yr.
Our findings show that the differences in the clinical presentation of influenza A(H1N1)pdm09 and influenza B infections are not likely to be of clinical or public health significance.
PMCID: PMC3978989  PMID: 24521643
Diagnosis; influenza A; influenza B; H1N1 subtype; respiratory tract infections; signs and symptoms
17.  Use of National Pneumonia Surveillance to Describe Influenza A(H7N9) Virus Epidemiology, China, 2004–2013 
Emerging Infectious Diseases  2013;19(11):1784-1790.
In mainland China, most avian influenza A(H7N9) cases in the spring of 2013 were reported through the pneumonia of unknown etiology (PUE) surveillance system. To understand the role of possible underreporting and surveillance bias in assessing the epidemiology of subtype H7N9 cases and the effect of live-poultry market closures, we examined all PUE cases reported from 2004 through May 3, 2013. Historically, the PUE system was underused, reporting was inconsistent, and PUE reporting was biased toward A(H7N9)-affected provinces, with sparse data from unaffected provinces; however, we found no evidence that the older ages of persons with A(H7N9) resulted from surveillance bias. The absolute number and the proportion of PUE cases confirmed to be A(H7N9) declined after live-poultry market closures (p<0.001), indicating that market closures might have positively affected outbreak control. In China, PUE surveillance needs to be improved.
PMCID: PMC3837642  PMID: 24206646
pneumonia surveillance; influenza A(H7N9) virus; influenza virus; viruses; influenza; epidemiology; China
18.  Protection by Face Masks against Influenza A(H1N1)pdm09 Virus on Trans-Pacific Passenger Aircraft, 2009 
Emerging Infectious Diseases  2013;19(9):1403-1410.
In response to several influenza A(H1N1)pdm09 infections that developed in passengers after they traveled on the same 2 flights from New York, New York, USA, to Hong Kong, China, to Fuzhou, China, we assessed transmission of influenza A(H1N1)pdm09 virus on these flights. We defined a case of infection as onset of fever and respiratory symptoms and detection of virus by PCR in a passenger or crew member of either flight. Illness developed only in passengers who traveled on the New York to Hong Kong flight. We compared exposures of 9 case-passengers with those of 32 asymptomatic control-passengers. None of the 9 case-passengers, compared with 47% (15/32) of control-passengers, wore a face mask for the entire flight (odds ratio 0, 95% CI 0–0.71). The source case-passenger was not identified. Wearing a face mask was a protective factor against influenza infection. We recommend a more comprehensive intervention study to accurately estimate this effect.
PMCID: PMC3810906  PMID: 23968983
influenza; influenza A virus; influenza A(H1N1)pdm09 virus; viruses; aircraft; trans-pacific passenger aircraft; disease outbreak; face masks; China; Hong Kong; United States; outbreak; air travel; travel
19.  Monitoring Avian Influenza A(H7N9) Virus through National Influenza-like Illness Surveillance, China 
Emerging Infectious Diseases  2013;19(8):1289-1292.
In China during March 4–April 28, 2013, avian influenza A(H7N9) virus testing was performed on 20,739 specimens from patients with influenza-like illness in 10 provinces with confirmed human cases: 6 (0.03%) were positive, and increased numbers of unsubtypeable influenza-positive specimens were not seen. Careful monitoring and rapid characterization of influenza A(H7N9) and other influenza viruses remain critical.
PMCID: PMC3739526  PMID: 23879887
influenza; avian influenza; avian influenza A(H7N9) virus; H7N9; subtype H7N9; China; influenza-like illness; surveillance; viruses
20.  Effect of Winter School Breaks on Influenza-like Illness, Argentina, 2005–2008 
Emerging Infectious Diseases  2013;19(6):938-944.
School closures are used to reduce seasonal and pandemic influenza transmission, yet evidence of their effectiveness is sparse. In Argentina, annual winter school breaks occur during the influenza season, providing an opportunity to study this intervention. We used 2005–2008 national weekly surveillance data of visits to a health care provider for influenza-like illness (ILI) from all provinces. Using Serfling-specified Poisson regressions and population-based census denominators, we developed incidence rate ratios (IRRs) for the 3 weeks before, 2 weeks during, and 3 weeks after the break. For persons 5–64 years of age, IRRs were <1 for at least 1 week after the break. Observed rates returned to expected by the third week after the break; overall decrease among persons of all ages was 14%. The largest decrease was among children 5–14 years of age during the week after the break (37% lower IRR). Among adults, effects were weaker and delayed. Two-week winter school breaks significantly decreased visits to a health care provider for ILI among school-aged children and nonelderly adults.
PMCID: PMC3713818  PMID: 23735682
Influenza; school closure; community mitigation; social isolation; Argentina; winter; viruses; respiratory infections
21.  Estimation of the National Disease Burden of Influenza-Associated Severe Acute Respiratory Illness in Kenya and Guatemala: A Novel Methodology 
PLoS ONE  2013;8(2):e56882.
Knowing the national disease burden of severe influenza in low-income countries can inform policy decisions around influenza treatment and prevention. We present a novel methodology using locally generated data for estimating this burden.
Methods and Findings
This method begins with calculating the hospitalized severe acute respiratory illness (SARI) incidence for children <5 years old and persons ≥5 years old from population-based surveillance in one province. This base rate of SARI is then adjusted for each province based on the prevalence of risk factors and healthcare-seeking behavior. The percentage of SARI with influenza virus detected is determined from provincial-level sentinel surveillance and applied to the adjusted provincial rates of hospitalized SARI. Healthcare-seeking data from healthcare utilization surveys is used to estimate non-hospitalized influenza-associated SARI. Rates of hospitalized and non-hospitalized influenza-associated SARI are applied to census data to calculate the national number of cases. The method was field-tested in Kenya, and validated in Guatemala, using data from August 2009–July 2011. In Kenya (2009 population 38.6 million persons), the annual number of hospitalized influenza-associated SARI cases ranged from 17,129–27,659 for children <5 years old (2.9–4.7 per 1,000 persons) and 6,882–7,836 for persons ≥5 years old (0.21–0.24 per 1,000 persons), depending on year and base rate used. In Guatemala (2011 population 14.7 million persons), the annual number of hospitalized cases of influenza-associated pneumonia ranged from 1,065–2,259 (0.5–1.0 per 1,000 persons) among children <5 years old and 779–2,252 cases (0.1–0.2 per 1,000 persons) for persons ≥5 years old, depending on year and base rate used. In both countries, the number of non-hospitalized influenza-associated cases was several-fold higher than the hospitalized cases.
Influenza virus was associated with a substantial amount of severe disease in Kenya and Guatemala. This method can be performed in most low and lower-middle income countries.
PMCID: PMC3584100  PMID: 23573177
22.  Characteristics of Hospitalized Cases with Influenza A (H1N1)pdm09 Infection during First Winter Season of Post-Pandemic in China 
PLoS ONE  2013;8(2):e55016.
Influenza A (H1N1)pdm09 (2009 H1N1) re-circulated as the predominant virus from January through February 2011 in China. National surveillance of 2009 H1N1 as a notifiable disease was maintained to monitor potential changes in disease severity from the previous season.
Methodology/Principal Findings
To describe the characteristics of hospitalized cases with 2009 H1N1 infection and analyze risk factors for severe illness during the 2010–2011winter season in China, we obtained surveillance data from hospitalized cases with 2009 H1N1 infection from November 2010 through May 2011, and reviewed medical records from 701 hospitalized cases. Age-standardized risk ratios were used to compare the age distribution of patients that were hospitalized and died due to 2009 H1N1 between the 2010–2011winter season to those during the 2009–2010 pandemic period. During the 2010–2011 winter season, children less than 5 years of age had the highest relative risk of hospitalization and death, followed by adults aged 65 years or older. Additionally, the relative risk of hospitalized cases aged 5–14 and 15–24 years was lower compared to children less than 5 years of age. During the winter season of 2010–2011, the proportions of adults aged 25 years or older for hospitalization and death were significantly higher than those during the 2009–2010 pandemic period. Being male, having a chronic medical condition, delayed hospital admission (≥3 days from onset) or delayed initiation of antiviral treatment (≥5 days from onset) were associated with severe illness among non-pregnant patients ≥2 years of age.
We observed a change in high risk groups for hospitalization for 2009 H1N1 during the winter months immediately following the pandemic period compared to the high risk groups identified during the pandemic period. Our nationally notifiable disease surveillance system enabled us to understand the evolving epidemiology of 2009 H1N1 infection after the pandemic period.
PMCID: PMC3564919  PMID: 23393563
23.  Mortality, Severe Acute Respiratory Infection, and Influenza-Like Illness Associated with Influenza A(H1N1)pdm09 in Argentina, 2009 
PLoS ONE  2012;7(10):e47540.
While there is much information about the burden of influenza A(H1N1)pdm09 in North America, little data exist on its burden in South America.
During April to December 2009, we actively searched for persons with severe acute respiratory infection and influenza-like illness (ILI) in three sentinel cities. A proportion of case-patients provided swabs for influenza testing. We estimated the number of case-patients that would have tested positive for influenza by multiplying the number of untested case-patients by the proportion who tested positive. We estimated rates by dividing the estimated number of case-patients by the census population after adjusting for the proportion of case-patients with missing illness onset information and ILI case-patients who visited physicians multiple times for one illness event.
We estimated that the influenza A(H1N1)pdm09 mortality rate per 100,000 person-years (py) ranged from 1.5 among persons aged 5–44 years to 5.6 among persons aged ≥65 years. A(H1N1)pdm09 hospitalization rates per 100,000 py ranged between 26.9 among children aged <5 years to 41.8 among persons aged ≥65 years. Influenza A(H1N1)pdm09 ILI rates per 100 py ranged between 1.6 among children aged <5 to 17.1 among persons aged 45–64 years. While 9 (53%) of 17 influenza A(H1N1)pdm09 decedents with available data had obesity and 7 (17%) of 40 had diabetes, less than 4% of surviving influenza A(H1N1)pdm09 case-patients had these pre-existing conditions (p≤0.001).
Influenza A(H1N1)pdm09 caused a similar burden of disease in Argentina as in other countries. Such disease burden suggests the potential value of timely influenza vaccinations.
PMCID: PMC3485247  PMID: 23118877
24.  Demographic Shift of Influenza A(H1N1)pdm09 during and after Pandemic, Rural India 
Emerging Infectious Diseases  2012;18(9):1472-1475.
Population-based active surveillance in India showed higher incidence rates for influenza A(H1N1)pdm09 among children during pandemic versus postpandemic periods (345 vs. 199/1,000 person-years), whereas adults had higher rates during postpandemic versus pandemic periods (131 vs. 69/1,000 person-years). Demographic shifts as pandemics evolve should be considered in public health response planning.
PMCID: PMC3437708  PMID: 22932477
influenza; seasonal influenza; influenza A(H1N1)pdm09; India; pandemic; viruses; H1N1; pH1N1
25.  Risk Factors for Death among Children Less than 5 Years Old Hospitalized with Diarrhea in Rural Western Kenya, 2005–2007: A Cohort Study 
PLoS Medicine  2012;9(7):e1001256.
A hospital-based surveillance study conducted by Ciara O'Reilly and colleagues describes the risk factors for death amongst children who have been hospitalized with diarrhea in rural Kenya.
Diarrhea is a leading cause of childhood morbidity and mortality in sub-Saharan Africa. Data on risk factors for mortality are limited. We conducted hospital-based surveillance to characterize the etiology of diarrhea and identify risk factors for death among children hospitalized with diarrhea in rural western Kenya.
Methods and Findings
We enrolled all children <5 years old, hospitalized with diarrhea (≥3 loose stools in 24 hours) at two district hospitals in Nyanza Province, western Kenya. Clinical and demographic information was collected. Stool specimens were tested for bacterial and viral pathogens. Bivariate and multivariable logistic regression analyses were carried out to identify risk factors for death. From May 23, 2005 to May 22, 2007, 1,146 children <5 years old were enrolled; 107 (9%) children died during hospitalization. Nontyphoidal Salmonella were identified in 10% (118), Campylobacter in 5% (57), and Shigella in 4% (42) of 1,137 stool samples; rotavirus was detected in 19% (196) of 1,021 stool samples. Among stools from children who died, nontyphoidal Salmonella were detected in 22%, Shigella in 11%, rotavirus in 9%, Campylobacter in 5%, and S. Typhi in <1%. In multivariable analysis, infants who died were more likely to have nontyphoidal Salmonella (adjusted odds ratio [aOR] = 6·8; 95% CI 3·1–14·9), and children <5 years to have Shigella (aOR = 5·5; 95% CI 2·2–14·0) identified than children who survived. Children who died were less likely to be infected with rotavirus (OR = 0·4; 95% CI 0·2–0·8). Further risk factors for death included being malnourished (aOR = 4·2; 95% CI 2·1–8·7); having oral thrush on physical exam (aOR = 2·3; 95% CI 1·4–3·8); having previously sought care at a hospital for the illness (aOR = 2·2; 95% CI 1·2–3·8); and being dehydrated as diagnosed at discharge/death (aOR = 2·5; 95% CI 1·5–4·1). A clinical diagnosis of malaria, and malaria parasites seen on blood smear, were not associated with increased risk of death. This study only captured in-hospital childhood deaths, and likely missed a substantial number of additional deaths that occurred at home.
Nontyphoidal Salmonella and Shigella are associated with mortality among rural Kenyan children with diarrhea who access a hospital. Improved prevention and treatment of diarrheal disease is necessary. Enhanced surveillance and simplified laboratory diagnostics in Africa may assist clinicians in appropriately treating potentially fatal diarrheal illness.
Please see later in the article for the Editors' Summary
Editors' Summary
Diarrhea—passing three or more loose or liquid stools per day—kills about 1.5 million young children every year, mainly in low- and middle-income countries. Globally, it is the second leading cause of death in under-5-year olds, causing nearly one in five child deaths. Diarrhea, which can lead to life-threatening dehydration, is a common symptom of gastrointestinal infections. The pathogens (viruses, bacteria, and parasites) that cause diarrhea spread through contaminated food or drinking water, and from person to person through poor hygiene and inadequate sanitation (unsafe disposal of human excreta). Interventions that prevent diarrhea include improvements in water supplies, sanitation and hygiene, the promotion of breast feeding, and vaccination against rotavirus (a major viral cause of diarrhea). Treatments for diarrhea include oral rehydration salts, which prevent and treat dehydration, zinc supplementation, which decreases the severity and duration of diarrhea, and the use of appropriate antibiotics when indicated for severe bacterial diarrhea.
Why Was This Study Done?
Nearly half of deaths from diarrhea among young children occur in Africa where diarrhea is the single largest cause of death among under 5-year-olds and a major cause of childhood illness. Unfortunately, although some of the risk factors for death from diarrhea in children in sub-Saharan Africa have been identified (for example, having other illnesses, poor nutrition, and not being breastfed), little is known about the relative contributions of different diarrhea-causing pathogens to diarrheal deaths. Clinicians need to know which of these pathogens are most likely to cause death in children so that they can manage their patients appropriately. In this cohort study, the researchers characterize the causes and risk factors associated with death among young children hospitalized for diarrhea in Nyanza Province, western Kenya, an area where most households have no access to safe drinking water and a quarter lack latrines. In a cohort study, a group of people with a specific condition is observed to identify which factors lead to different outcomes.
What Did the Researchers Do and Find?
The researchers enrolled all the children under 5 years old who were hospitalized over a two-year period for diarrhea at two district hospitals in Nyanza Province, tested their stool samples for diarrhea-causing viral and bacterial pathogens, and recorded which patients died in-hospital. They then used multivariable regression analysis (a statistical method) to determine which risk factors and diarrheal pathogens were associated with death among the children. During the study, 1,146 children were hospitalized, 107 of whom died in the hospital. 10% of all the stool samples contained nontyphoidal Salmonella, 4% contained Shigella (two types of diarrhea-causing bacteria), and 19% contained rotavirus. By contrast, 22% of the samples taken from children who died contained nontyphoidal Salmonella, 11% contained Shigella, 9% contained rotavirus, and 5% contained Campylobacter (another bacterial pathogen that causes diarrhea). Compared to survivors, infants (children under 1 year of age) who died were nearly seven times more likely to have nontyphoidal Salmonella in their stools and children under 5 years old who died were five and half times more likely to have Shigella in their stools but less likely to have rotavirus in their stools. Other factors associated with death included being malnourished, having oral thrush (a fungal infection of the mouth), having previously sought hospital care for diarrhea, and being dehydrated.
What Do These Findings Mean?
These findings indicate that, among young children admitted to the hospital in western Kenya with diarrhea, infections with nontyphoidal Salmonella and with Shigella (but not with rotavirus) were associated with an increased risk of death. Because this study only captured deaths in hospital and most diarrheal deaths in developing countries occur at home, these results may not accurately reflect the pathogens associated with overall childhood diarrheal deaths. In addition, they may not be generalizable to other geographical regions. Nevertheless, given that that there are currently no vaccines available for most bacterial diarrheal diseases, these findings highlight the importance of Kenya and other developing countries implementing effective strategies for the prevention and management of diarrheal diseases in children such as increasing access to improved water, sanitation, and hygiene, and community-level promotion of the use of oral rehydration solution and zinc supplements. They also suggest that enhanced surveillance and simplified laboratory diagnostics for diarrheal pathogens could help clinicians identify those children presenting to hospital with diarrhea who are at high risk of death and prioritize their treatment.
Additional Information
Please access these Web sites via the online version of this summary at
The World Health Organization provides information on diarrhea (in several languages); its 2009 report with UNICEF Diarrhea: why children are still dying and what can be done, which includes the WHO/UNICEF recommendations for the treatment and prevention of diarrhea in children, can be downloaded from the Internet
The children's charity UNICEF, which protects the rights of children and young people around the world, provides information on diarrhea (in several languages)
PMCID: PMC3389023  PMID: 22802736

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