Factors associated with Severe Acute Respiratory Syndrome in a Brazilian central region

Kamilla Lelis Rodrigues de Araujo Érika Carvalho de Aquino Lara Lívia Santos da Silva Yves Mauro Fernandes Ternes About the authors

Abstract

Severe Acute Respiratory Infection (SARI) is a notifiable syndrome that must be investigated. This study aimed to analyze the epidemiological profile and factors associated with SARI-related hospitalization and deaths reported in Goiás. Retrospective cohort study, with data from the investigation files of the Notifiable Diseases Information System’s Influenza Web. Multivariate analysis methods were employed to verify the association between exposure variables with the outcomes of ICU admission and death. A total of 4,832 SARI cases were reported in Goiás from 2013 to 2018. The primary etiological diagnosis was Influenza A (22.3%) with the predominant subtype A (H1N1pdm09), followed by the Respiratory Syncytial Virus. A total of 34.6% of the patients required ICU admission, and 19% died. A longer time to start treatment with antivirals was associated with a higher likelihood to have an ICU admission, while a previous non-vaccination against Influenza, longer time to start treatment, and older age were associated with a higher likelihood to suffer death. The study showed a high frequency of respiratory diseases caused by the Influenza virus in Goiás and that the severity of the syndrome, characterized by ICU admission and deaths, is associated with the start of antiviral treatment vaccine status, and patient’s age.

Key words
Human Influenza; Surveillance; Epidemiology; Severe Acute Respiratory Infection

Introduction

Severe Acute Respiratory Infection (SARI) is an infectious viral respiratory syndrome caused by influenza viruses and other etiological agents, such as the respiratory syncytial virus (RSV), parainfluenza, and adenovirus, which infect the upper respiratory tract11 Ribeiro SA, Brasileiro GS, Soleiman LNC, Silva CC, Kavaguti CS. Severe acute respiratory syndrome caused by the influenza A (H1N1) virus. Jornal Bras Pneumol 2010; 36:386-389.. Patients have a flu-like condition associated with dyspnea or tachypnea (respiratory rate equal to or above 20 incursions per minute) or hypoxemia, with oxygen saturation (SpO22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018.) < 95% in room air22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018..

It is a disease of epidemiological relevance that must be notified and investigated. The epidemiological monitoring of SARI in Brazil occurs through the epidemiological surveillance of the disease by completing notification forms through the Notifiable Diseases Information System (SINAN), and the operation of sentinel units. These units monitor SARI-related hospitalized cases and deaths to identify circulating respiratory viruses22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018.,33 Goiás. Sevretaria de Estado da Saúde. Nota Técnica SUVISA/SES-GO. Recomendações referentes à prevenção, vigilância epidemiológica e tratamento da síndrome gripal (SG) e síndrome respiratória aguda grave (SRAG). Goinânia: Superintendência de Vigilância em Saúde; 2018.. Thus, all suspected SARI cases are hospitalized, notified, and investigated for the disease11 Ribeiro SA, Brasileiro GS, Soleiman LNC, Silva CC, Kavaguti CS. Severe acute respiratory syndrome caused by the influenza A (H1N1) virus. Jornal Bras Pneumol 2010; 36:386-389..

Epidemiological surveillance of SARI allows preventing and monitoring severe cases of the syndrome, identifying circulating viral types and subtypes, performing antigenic and genetic analysis of viruses, identifying new viral subtypes, monitoring resistance to antivirals and demand for care by disease, and controlling possible outbreaks, aiming at public health decision-making for its prevention and control44 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Guia para a Rede Laboratorial de Vigilância de Influenza no Brasil. Brasília: MS; 2016..

Globally, the circulation of influenza viruses remains high, and seasonal A virus is the most prevalent55 Centers for Diseases Control and Prevention (CDC). Centros de Controle e Prevenção de Doenças, Centro Nacional de Imunização e Doenças Respiratórias (NCIRD) [Internet]. 2020. Disponível em: https://www.cdc.gov/flu/index.htm
https://www.cdc.gov/flu/index.htm...
. According to the epidemiological bulletin of the Ministry of Health66 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde.. Influenza: Monitoramento até a Semana Epidemiológica 49 de 2019. Boletim Epidemiológico 2019; 50:1-43., Brazil has the same circulation profile, with the highest prevalence of the Influenza A H1N1 pandemic virus 2009 (H1N1pdm09). This scenario has recently changed with the new coronavirus pandemic, which started in late 2019 in China, with first Brazilian cases in early 202077 Brasil. Ministério da Saúde (MS). Boletim Epidemiológico Especial 14. COE-COVID19 [Internet]. 2020 [acessado 2020 Jun 16]. Disponível em: https://portalarquivos.saude.gov.br/images/pdf/2020/April/27/2020-04-27-18-05h-BEE14-Boletim-do-COE.pdf
https://portalarquivos.saude.gov.br/imag...
.

SARI can progress to complications, which lead to an increased risk of ICU admissions, mechanical ventilation, and even death88 Coleman BL, Fadel SA, Fitzpatrick T, Tomas SM. Risk factors for serious outcomes associated with influenza illness in high-versus low-and middle-income countries: Systematic literature review and meta-analysisle. Influenza Other Respiratory Viruses 2018; 12(1):22-29.. Some factors are associated with a worse prognosis, such as the presence of chronic diseases, age extremes, viral strain, no previous vaccination, and use of antivirals 72 hours after the onset of symptoms, characteristics that should be investigated99 Ribeiro AF, Pellini ACG, Kitagawa BY, Marques D, Madalosso G, Figueira GCN, Fred J, Albernaz RKM, Carvalhanas TRMP, Zanetta DMT. Risk Factors for Death from Influenza A (H1N1) pdm09, State of São Paulo, Brazil. Public Library od Sci 2015; 1-14.,1010 Ren Y, Yin Y, Li W, Lin Y, Liu T, Wang S, Zhang SY, Li Z, Wang XJ, Bi ZQ. Risk factors associated with severe manifestations of 2009 pandemic influenza A (H1N1) infection in China: a case-control study. Virology J 2013; 1-7..

Thus, this study aimed to analyze the epidemiological profile and the factors associated with hospitalization and deaths from SARI in a central Brazilian region from 2013 to 2018.

Methods

This is a retrospective cohort study with data analysis regarding notified SARI cases and their progress during hospitalization in Goiás. Goiás is located in the Midwest region, with an area of 340,125,715 km², and is the seventh-largest Brazilian state in territorial extension. Its HDI ranks eighth in the country, at 0.7351111 Brasil. Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados Brasileiros [Internet]. 2019 [acessado 2020 Jun 16]. Disponível em: https://www.ibge.gov.br/cidades-e-estados/go.html.
https://www.ibge.gov.br/cidades-e-estado...
.

According to the definition of the Ministry of Health22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018., all reported SARI cases in SINAN’s Influenza Web, residing in the state of Goiás, regardless of age, were considered eligible for the study. The Ministry of Health defines SARI as the individual of any age with a flu-like syndrome (fever, cough, or sore throat, and at least one of the following symptoms: headache, myalgia, or arthralgia) associated with dyspnea or oxygen saturation SpO22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018. < 95%22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018..

Data was collected on April 10, 2019. In 2012, a change was implemented in the notification form, and epidemiological surveillance directed the monitoring of Influenza by a new pandemic subtype for SARI. We decided to use 2012 data to ensure the performance of analyses with the same variables homogeneously. Thus, the data reported between 2013 and 2018 were collected.

This project was approved by the Research Ethics Committee linked directly to the “Leide das Neves Ferreira” Center for Excellence in Education, Research and Projects (GCEEPP-LNF) and the Research Ethics Committee linked to the Hospital das Clínicas of the Federal University of Goiás (UFG), and met the conditions established by Resolution MS/CNS 466/2012.

Data statistical analysis

Absolute and relative frequencies were obtained in the descriptive analysis according to each category under analysis (sociodemographic characteristics and data on the prevention, treatment, and development of the disease). Multivariate data analysis methods were used to verify the association between exposure variables and outcomes (deaths and ICU admission), and previous vaccination, use of antivirals, presence of the Influenza A/B virus, RSV, other respiratory viruses, treatment time in days, and age group, were considered variables of exposure.

Initially, a bivariate analysis was performed, testing the association of exposure variables with outcomes by calculating Odds Ratio (OR) and p-value. The variables whose association with the outcome was p ≤ 0.20 were included in the multivariate logistic regression model. This model was progressively saturated with each variable’s addition, observing its effects on the precision of the final model on the adjustment of the other variables for inclusion in the definitive model. The variables associated with the outcome finally showed a p-value < 0.05. IBM SPSS Statistics software version 25.0 was used for statistical data analysis.

Results

A total of 4,832 SARI cases were reported in Goiás from 2013 to 2018. The highest percentage of notifications occurred in females (53.4%) and the 20-59 years’ age group (45.8%). Other sociodemographic data are shown in Table 1.

Table 1
Sociodemographic characteristics of patients with SARI notified in Goiás and characteristics related to the prevention, treatment, and development of the disease, 2013-2018 (n=4.832).

Regarding the prevention, treatment, and development of the syndrome, only 20.7% of patients were previously vaccinated against Influenza, and 70.7% of them used antivirals. ICU admission was found in 34.6% of the cases, while 19% died (Table 1).

A predominance of Influenza A virus was observed throughout the study, followed by RSV. Influenza A virus (H1N1pdm09) was the predominant virus subtype. As for cases without etiology, defined as unspecified SARI, we observed 2,796 patients, which corresponds to approximately 58% of notifications, with an increase in notifications in 2016 and 2018. These same years recorded a significant increase in cases compared to other seasonal factors and, consequently, increased ICU admissions and deaths (Figure 1).

Figure 1
Temporal evolution of deaths and hospitalizations in ICU due to SARI in Goiás and the number of cases according to etiological diagnosis, 2013-2018.

RSV = Respiratory Syncytial Virus; ICU = Intensive Care Unit.

Table 2 shows the results of the bivariate and multivariate analyses between the exposure variables with the death outcome. In the bivariate analysis, a higher likelihood of death was observed in individuals who did not use antivirals, whose SARI was caused by Influenza A or B virus, with a higher number of days to start treatment, and older age. In the multivariate analysis, in turn, the variables use of antivirals, Influenza A or B infection, and RSV, lost association with the outcome, keeping the association between the time of onset of treatment and age group. A higher likelihood of death was also observed in the multivariate analysis in individuals who had not previously been vaccinated against Influenza.

Table 2
Factors associated with death by SARI cases notified in Goiás, 2013 to 2018.

For the outcome of ICU admission, in the bivariate analysis, the non-use of antivirals, infection by Influenza A or B, RSV, and other respiratory viruses reduced the likelihood of ICU admission. At the same time, the longer time to start treatment increased the likelihood of this complication. In the multivariate analysis, the variables infection by Influenza A or B and RSV continued to be negatively associated with the outcome, while the time to start treatment remained positively associated with the outcome (Table 3).

Table 3
Factors associated with the ICU admission for SARI cases notified in Goiás, 2013 to 2018.

Discussion

This study allowed observing SARI notifications in the state of Goiás for six years. Analyzing the confirmed cases’ sociodemographic characteristics, we observed no significant difference regarding gender, unlike studies carried out in New Zealand, the U.S., and France, in which females were predominant1212 Delgado-Sanz C, Mazagatos-Ateca C, Oliva J, Gherasim A, Larrauri A. Illness Severity in Hospitalized Influenza Patients by Virus Type and Subtype, Spain, 2010-2017. CDC-Centre for Disease Prevention and Control Emerging Infectious Diseases. CDC 2020; 26(2):2010-2017.

13 Reacher M, Warne B , Reeve L, Verlander NQ, Jones NK, Ranellou K, Cristou S, Wrigth C, Choudhry S, Zambon M, Sander C, Zhang H, Jalal H. Influenza-associated mortality in hospital care: a retrospective cohort study of risk factors and impact of oseltamivir in an English teaching hospital, 2016 to 2017. Revista da Europa sobre vigilância de doenças infecciosas, epidemiologia, prevenção e controle. Euro Surveill 2019; 1-12.

14 Guerrisi C, Ecollan H, Southy C, Rossignol G, Turbelin C, Debin H, Goronflot T, Boelle PY, Hanslik T, Colizza V, Blanchon T. Factors associated with influenza-like-illnes: a crowdsourced cohort study from 2012/13 to 2017/18. BMC Public Health 2019; 879:1-9.

15 Huang QS, Bandaranayake D, Madeira T, Newbern EC, Sements R, Ralston J, Waite B, Bissielo A, Prasad N, Todd A, Jelley L, Gunn W, McNicholas A, Metz T, Lawrence S, Collis E, Retter U, Wong SS, Webby R, Bocacao J, Haubrock J, Mackereth L, Turner N, McArdle B, Cameron J, Reynolds EG, Baker MG, Grant CC, McArthur C, Roberts S, Trenholme A, Wong C, Taylor S, Thomas P, Duque J, Gross D, Thompson MG, Widdowson MA. Risk Factors and Attack Rates of Seasonal Influenza Infection: Results of the Southern Hemisphere Influenza and Vaccine Effectiveness Research and Surveillance (SHIVERS) Seroepidemiologic Cohort Study. J Infect Dis 2019; 219:347-357.
-1616 Ferdinands JM, Gaglani M, Martin ET, Middleton D, Monto AS, Murthy K, Silveira FP, Talbot HK, Zimmerman R, Alyanak E, Strickland C, Spencer S, Fry AM. Prevention of Influenza Hospitalization Among Adults in the United States, 2015-2016: Results From the US Hospitalized Adult Influenza Vaccine Effectiveness Network (HAIVEN). J Infect Dis Vaccination Against Influenza Hospitalization 2019; 220:2015-2016.. Regarding the age group, the largest number of people affected was aged between 20 and 59 years, a group that is not part of the indication for vaccination against Influenza by the Brazilian Ministry of Health. A high frequency of cases was also observed in groups considered to be at higher risk, children under five years old (28.6%) and older adults above 60 years (15.0%), as seen in other studies1212 Delgado-Sanz C, Mazagatos-Ateca C, Oliva J, Gherasim A, Larrauri A. Illness Severity in Hospitalized Influenza Patients by Virus Type and Subtype, Spain, 2010-2017. CDC-Centre for Disease Prevention and Control Emerging Infectious Diseases. CDC 2020; 26(2):2010-2017.,1717 Rabarison JH, Tempia S, Harimanana A, Guillebaud J, Razanajatovo NH, Ratsitorahina M, Heraud JM. Burden and epidemiology of influenza-and respiratory associated severe acute respiratory illness hospitalization in Madagascar, 2011-2016. Influenza Other Respir Viruses 2019; 13(2):138-147.,1818 Código SH, Bakken IJ, Blasio BF Haberg SE. Burden of medically attended influenza in Norway 2008-2017. Influenza Other Respir Viruses 2019; 13(3):240-247.. In the literature, individuals at extreme ages are at higher risk for respiratory conditions, such as Influenza and pneumonia1919 Brent SE, Pullenayegum E, Russell ML, Loeb M. Effect of seasonal influenza vaccination on influenza symptom severity among children in Hutterite communities: Follow up study of a randomized trial. Influenza Other Respir Viruses 2020; 14(1):28-36.,2020 Lopes NR, Rodrigues BB, Tiago DC, Alvarenga LCR, Medeiros LMM, Ribeiro FAC, Rabahi MF. Factors associated with anti-influenza and anti-pneumococcal vaccination in elderly. Braz J Development 2019; 5(9):15451-15462..

Brazil has one of the most extensive immunization programs globally, with a considerable volume of doses administered against various diseases, and is provided free of charge2121 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Programa Nacional de Imunizações (PNI): 40 anos. Brasília: MS; 2013.. Among these vaccines is the one against Influenza, incorporated in the National Vaccination Program (PNI) in 19992222 Brasil. Ministério da Saúde (MS). Informe Técnico 21a Campanha Nacional de Vacinação contra a Influenza. Brasília: MS; 2019., which is made available free of charge to risk groups nationwide, among them: children aged six months to under six years of age, pregnant women, puerperae, and patients with NCDs. In this study, we observed that 59.1% of the SARI individuals had not received previous vaccination against Influenza. It is worth mentioning that the largest number of cases in our study is in the age group not covered by vaccination provided by the PNI. While not provided to the entire population through the SUS, influenza vaccination is available in the private health network. It is essential to highlight that influenza vaccination, as a public health measure, reduces hospitalizations, especially in people at risk (children under five, older adults, and pregnant women)2323 Andrew MK, Shinde V, Ye L, Hatchette T, Haguinet F, Dos Santos L, McE-lhaney JE, Ambrose U, Boivin G, Bowie W, Chit Um, Elsherif H, Verde K, Halperin S, Ibarguchi B, Johnstone J, Katz K, Langley J, Leblanc J, Loeb M, MacKinnon-D C, McCarthy U, McGeer U, Powis J, Richardson D, Semret M, Stiver G, Trottier S, Valiquette L, Webster D, McNeil SA. The Importance of Frailty in the Assessment of Influenza Vaccine Effectiveness Against Influenza-Related Hospitalization in Elderly People. J Infect Dis 2017; 216:405-414.. However, several factors influence the vaccine’s effectiveness, such as the compatibility of the circulating strains with the vaccine strains, the individual’s immune response, and previous vaccination by the same strain of the current vaccine2424 Chow EJ, Davis CT, Elal AIA, Alabi N, Azziz-Baumgartner E, Barnes J, Blanton L, Brammer L, Budd AP, Burns E, Davis WW, Dugan VG, Fry AM, Garten R, Grohskopf LA, Gubareva L, Jang Y, Jones J, Kniss K, Lindstrom S, Mustaquim D, Porter R, Rolfes M, Sessions W, Taylor C, Wentworth DE, Xu X, Zanders N, Katz J, Jernigan D. Update?: Influenza Activity-United States and Worldwide, May 20-October 13, 2018. CDC 2018; 67(42):1178-1185.,2525 Flannery B, Chung JR, Belongia EA, Mclean HQ, Gaglani M, Murthy K, Zimermmam RK, Nowalk MP, Jackson ML, Jackson LA, Monto AS, Martin ET, Foust A, Sessões W, Berman L, Barnes JR, Spencer S, Fry AM. Interim Estimates of 2017-18 Seasonal Influenza Vaccine Effectiveness-United States, February 2018. CDC 2018; 67(6):180-185..

With a suspected disease, all patients should start antiviral treatment as early as possible, even without the etiological identification22 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018.. Antiviral administration can reduce the duration of symptoms, viral load, and the transmission capacity2626 Cheng HY, Chen WC, Chou YJ, Huang AS, Huang WT. Containing influenza outbreaks with antiviral use in long-term care facilities in Taiwan, 2008-2014. Influenza Other Respir Viruses 2018; 12(2):287-292.. Failure to use antivirals or inappropriate use (more than 48 hours after the onset of symptoms) is associated with virus infection complications, such as aggravation followed by ICU admission and progression to death88 Coleman BL, Fadel SA, Fitzpatrick T, Tomas SM. Risk factors for serious outcomes associated with influenza illness in high-versus low-and middle-income countries: Systematic literature review and meta-analysisle. Influenza Other Respiratory Viruses 2018; 12(1):22-29.. The non-use of the medication was observed in 24.9% of patients in this study. Thus, it is necessary to strengthen actions for the proper management of patients with SARI as a strategy to reduce severe cases of this disease.

We observed that the influenza virus is the most prevalent etiological agent, followed by RSV. A higher frequency of virus A (H1N1pdm09) was noted among the influenza viruses, followed by A (H3N2) and the influenza B virus. Year-to-year variations were observed for both pathogens, which may be due to different strains and circulation patterns of viruses at every season2727 Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Cohen C, Gran JM. Schanzer D, Cowling BJ, Wu P, Kyncl J, Ang LW, Park M, Redlberger-Fritz M, Yu H, Espenhain L, Krishnan A, Emukule G, VanAsten L, Silva PS, Aungkulanon S, Buchholz U, Widdowson MA, Bresse JS. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 2019; 391(10127):1285-1300., and highlights the importance of estimating the disease burden associated with virus infection and strengthening surveillance actions in the epidemiological investigation of the syndrome, which corroborates public health measures44 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Guia para a Rede Laboratorial de Vigilância de Influenza no Brasil. Brasília: MS; 2016.,2828 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Coordenação-Geral de Desenvolvimento da Epidemiologia em Serviços. Guia de Vigilância em Saúde: volume único. Brasilia: MS; 2017.. This same viral circulation pattern is observed in other studies, where A viruses (H1N1pdm09) represent the majority of identified viruses2929 Chow EJ, Davis CT, Elal AIA, Alabi N, Azziz-Baumgartne Er, Barnes J, Blanton L, Brammer L, Budd AP, Burns E, Davis WW, Dugan VG, Fry AM, Garten R, Grohskopf LA, Gubareva L, Jang Y, Jones J, Kniss K, Lindstrom S, Mustaquim D, Porter R, Rolfes M, Sessions W, Taylor C, Wentworth DE, Xu X, Zanders N, Katz J, Jernigan D. Update: Influenza Activity-United States and Worldwide, May 20-October 13, 2018. US Department of Health and Human Services/Centers for Disease Control and Prevention. CDC 2019; 67(42):2-9.

30 Epperson S, Davis CT, Lynnette B, Elal AIA, Ajayi N, Barnes J, Budd AP, Burns E, Daly P, Dugan VG, Fry AM, Jang Y, Johnson SJ, Kniss K, Kondor R, Grohskopf LA, Gubareva L, Merced-Morales A, Sessions W, Stevens J, Wentworth DE, Xu X, Jernigan D. Update: Influenza Activity-United States and Worldwide , May 19-September 28, 2019, and Composition of the 2020 Southern Hemisphere Influenza Vaccine. US Department of Health and Human Services/Centers for Disease Control and Prevention. CDC 2019; 68.
-3131 Xu X, Blanton L, Elal AIA, Alabi N, Barnes J, Biggerrstaff M, Brammer L, Budd AP, Burns E, Cummings CN, Garg S, Kondor R, Gubareva L, Kniss K, Nyanseor S, O'Halloran A, Rolfes M, Wendy S, Dugan VD, Fry AM, Wentworth DE, Stevens J, Jernigan D. Update: Influenza Activity in the United States During the 2018-19 Season and Composition of the 2019-20 Influenza Vaccine. US Department of Health and Human Services/Centers for Disease Control and Prevention. CDC 2019; 68(24):544-551..

It is interesting to note a significant increase in SARI cases in the state of Goiás in 2016 and 2018, which may be because vaccination coverage for some specific groups, such as patients with comorbidities, was below the 90% target in previous years (2015 and 2017), favoring higher viral circulation in the following seasons.

Identifying the influenza virus in symptomatic patients is associated with an increased risk of respiratory complications, represented by deaths and ICU admission, besides other contributing factors, such as the patient’s age, viral strain, vaccine status, and antiviral use2727 Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Cohen C, Gran JM. Schanzer D, Cowling BJ, Wu P, Kyncl J, Ang LW, Park M, Redlberger-Fritz M, Yu H, Espenhain L, Krishnan A, Emukule G, VanAsten L, Silva PS, Aungkulanon S, Buchholz U, Widdowson MA, Bresse JS. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 2019; 391(10127):1285-1300.. Our study observed that 19% of patients died, and 34.6% were admitted to the ICU, as seen in other studies88 Coleman BL, Fadel SA, Fitzpatrick T, Tomas SM. Risk factors for serious outcomes associated with influenza illness in high-versus low-and middle-income countries: Systematic literature review and meta-analysisle. Influenza Other Respiratory Viruses 2018; 12(1):22-29.,3232 Pivette M, Nicolay N, Lauzun V, Hubert B. Characteristics of hospitalizations with an influenza diagnosis, France, 2012-2013 to 2016-2017 influenza seasons. Influenza Other Respir Viruses 2020; 14(3):1-9.. Also, we observed that the likelihood of having a severe outcome (death and ICU admission) was higher in young adults or older adults than children, in those who had not previously been vaccinated against Influenza and with a higher number of days to start antiviral treatment. According to Naudion et al.3333 Naudion P, Lepiller Q, Boullier K. Risk factors and clinical characteristics of patients with nosocomial influenza A infection. J Med Virol 2020; 92(8):1047-1052., this virus is the most associated with the complications of the syndrome and, likewise, the non-use of antivirals and the absence of immunization are related to the complications3333 Naudion P, Lepiller Q, Boullier K. Risk factors and clinical characteristics of patients with nosocomial influenza A infection. J Med Virol 2020; 92(8):1047-1052.. Other studies indicate that patients who used antivirals and had previous vaccination for Influenza had a significant reduction in the risk of complications1919 Brent SE, Pullenayegum E, Russell ML, Loeb M. Effect of seasonal influenza vaccination on influenza symptom severity among children in Hutterite communities: Follow up study of a randomized trial. Influenza Other Respir Viruses 2020; 14(1):28-36.,2222 Brasil. Ministério da Saúde (MS). Informe Técnico 21a Campanha Nacional de Vacinação contra a Influenza. Brasília: MS; 2019.. Regarding the age group, studies in the literature have also shown a higher likelihood of complications at older ages88 Coleman BL, Fadel SA, Fitzpatrick T, Tomas SM. Risk factors for serious outcomes associated with influenza illness in high-versus low-and middle-income countries: Systematic literature review and meta-analysisle. Influenza Other Respiratory Viruses 2018; 12(1):22-29.,3333 Naudion P, Lepiller Q, Boullier K. Risk factors and clinical characteristics of patients with nosocomial influenza A infection. J Med Virol 2020; 92(8):1047-1052..

As a limitation of the study, we can highlight that the frequency of cases and deaths due to SARI can be underestimated due to their passive notification and the sensitivity of health professionals in identifying suspected cases. Underreporting of cases in the SINAN should not occur, as SARI is mandatory for health surveillance3434 Rosetto EV, Luna EJA. Database linkage for surveillance of the influenza A (H1N1) pdm09 pandemic in Brazil, 2009-2010. Cad Saúde Pública 2016; 32(7):e00014115.. The number of unidentified cases, but capable of transmitting the disease, is a critical epidemiological characteristic that modulates the potential for the spread of the virus3535 Nogueira AL, Nogueira CL, Zibetti AW, Roqueiro N, Bruna-Romero O, Carciofi BAM. Estimativa da Subnotificação de Casos da COVID-19 no Estado de Santa Catarina. Joinville: Universidade Federal de Santa Catarina; 2020.. Another downside is the use of secondary data, which can sometimes be incomplete and with limitations on variables. Thus, local surveillance levels should be trained and make extensive use of data from information systems to identify weaknesses and inconsistencies in the data, improve the quality of the systems, and make them effective3434 Rosetto EV, Luna EJA. Database linkage for surveillance of the influenza A (H1N1) pdm09 pandemic in Brazil, 2009-2010. Cad Saúde Pública 2016; 32(7):e00014115..

SINAN and other Health Information Systems of the Brazilian Ministry of Health are a valuable source of health information that assists in planning health policies and programs, collaborating in the decision-making process, besides allowing assessment of the impact of interventions. Thus, even in the face of limitations, they are essential tools for public health and, especially, for disease epidemiological surveillance. Also, with the new coronavirus pandemic in the country in 2020, the SARI surveillance system is being strengthened and is an essential step for public health concerning the epidemiological and laboratory surveillance of respiratory agents.

Conclusion

Several cases of respiratory diseases caused by the Influenza virus and other etiological agents occur in the state of Goiás, and we observed that the severity of the syndrome, characterized by ICU admission and deaths, is associated with the patient’s age, start time to treatment with antivirals, and vaccination status.

References

  • 1
    Ribeiro SA, Brasileiro GS, Soleiman LNC, Silva CC, Kavaguti CS. Severe acute respiratory syndrome caused by the influenza A (H1N1) virus. Jornal Bras Pneumol 2010; 36:386-389.
  • 2
    Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de tratamento de Influenza: 2018. Brasília: MS; 2018.
  • 3
    Goiás. Sevretaria de Estado da Saúde. Nota Técnica SUVISA/SES-GO. Recomendações referentes à prevenção, vigilância epidemiológica e tratamento da síndrome gripal (SG) e síndrome respiratória aguda grave (SRAG). Goinânia: Superintendência de Vigilância em Saúde; 2018.
  • 4
    Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Guia para a Rede Laboratorial de Vigilância de Influenza no Brasil Brasília: MS; 2016.
  • 5
    Centers for Diseases Control and Prevention (CDC). Centros de Controle e Prevenção de Doenças, Centro Nacional de Imunização e Doenças Respiratórias (NCIRD) [Internet]. 2020. Disponível em: https://www.cdc.gov/flu/index.htm
    » https://www.cdc.gov/flu/index.htm
  • 6
    Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde.. Influenza: Monitoramento até a Semana Epidemiológica 49 de 2019. Boletim Epidemiológico 2019; 50:1-43.
  • 7
    Brasil. Ministério da Saúde (MS). Boletim Epidemiológico Especial 14. COE-COVID19 [Internet]. 2020 [acessado 2020 Jun 16]. Disponível em: https://portalarquivos.saude.gov.br/images/pdf/2020/April/27/2020-04-27-18-05h-BEE14-Boletim-do-COE.pdf
    » https://portalarquivos.saude.gov.br/images/pdf/2020/April/27/2020-04-27-18-05h-BEE14-Boletim-do-COE.pdf
  • 8
    Coleman BL, Fadel SA, Fitzpatrick T, Tomas SM. Risk factors for serious outcomes associated with influenza illness in high-versus low-and middle-income countries: Systematic literature review and meta-analysisle. Influenza Other Respiratory Viruses 2018; 12(1):22-29.
  • 9
    Ribeiro AF, Pellini ACG, Kitagawa BY, Marques D, Madalosso G, Figueira GCN, Fred J, Albernaz RKM, Carvalhanas TRMP, Zanetta DMT. Risk Factors for Death from Influenza A (H1N1) pdm09, State of São Paulo, Brazil. Public Library od Sci 2015; 1-14.
  • 10
    Ren Y, Yin Y, Li W, Lin Y, Liu T, Wang S, Zhang SY, Li Z, Wang XJ, Bi ZQ. Risk factors associated with severe manifestations of 2009 pandemic influenza A (H1N1) infection in China: a case-control study. Virology J 2013; 1-7.
  • 11
    Brasil. Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados Brasileiros [Internet]. 2019 [acessado 2020 Jun 16]. Disponível em: https://www.ibge.gov.br/cidades-e-estados/go.html
    » https://www.ibge.gov.br/cidades-e-estados/go.html
  • 12
    Delgado-Sanz C, Mazagatos-Ateca C, Oliva J, Gherasim A, Larrauri A. Illness Severity in Hospitalized Influenza Patients by Virus Type and Subtype, Spain, 2010-2017. CDC-Centre for Disease Prevention and Control Emerging Infectious Diseases. CDC 2020; 26(2):2010-2017.
  • 13
    Reacher M, Warne B , Reeve L, Verlander NQ, Jones NK, Ranellou K, Cristou S, Wrigth C, Choudhry S, Zambon M, Sander C, Zhang H, Jalal H. Influenza-associated mortality in hospital care: a retrospective cohort study of risk factors and impact of oseltamivir in an English teaching hospital, 2016 to 2017. Revista da Europa sobre vigilância de doenças infecciosas, epidemiologia, prevenção e controle. Euro Surveill 2019; 1-12.
  • 14
    Guerrisi C, Ecollan H, Southy C, Rossignol G, Turbelin C, Debin H, Goronflot T, Boelle PY, Hanslik T, Colizza V, Blanchon T. Factors associated with influenza-like-illnes: a crowdsourced cohort study from 2012/13 to 2017/18. BMC Public Health 2019; 879:1-9.
  • 15
    Huang QS, Bandaranayake D, Madeira T, Newbern EC, Sements R, Ralston J, Waite B, Bissielo A, Prasad N, Todd A, Jelley L, Gunn W, McNicholas A, Metz T, Lawrence S, Collis E, Retter U, Wong SS, Webby R, Bocacao J, Haubrock J, Mackereth L, Turner N, McArdle B, Cameron J, Reynolds EG, Baker MG, Grant CC, McArthur C, Roberts S, Trenholme A, Wong C, Taylor S, Thomas P, Duque J, Gross D, Thompson MG, Widdowson MA. Risk Factors and Attack Rates of Seasonal Influenza Infection: Results of the Southern Hemisphere Influenza and Vaccine Effectiveness Research and Surveillance (SHIVERS) Seroepidemiologic Cohort Study. J Infect Dis 2019; 219:347-357.
  • 16
    Ferdinands JM, Gaglani M, Martin ET, Middleton D, Monto AS, Murthy K, Silveira FP, Talbot HK, Zimmerman R, Alyanak E, Strickland C, Spencer S, Fry AM. Prevention of Influenza Hospitalization Among Adults in the United States, 2015-2016: Results From the US Hospitalized Adult Influenza Vaccine Effectiveness Network (HAIVEN). J Infect Dis Vaccination Against Influenza Hospitalization 2019; 220:2015-2016.
  • 17
    Rabarison JH, Tempia S, Harimanana A, Guillebaud J, Razanajatovo NH, Ratsitorahina M, Heraud JM. Burden and epidemiology of influenza-and respiratory associated severe acute respiratory illness hospitalization in Madagascar, 2011-2016. Influenza Other Respir Viruses 2019; 13(2):138-147.
  • 18
    Código SH, Bakken IJ, Blasio BF Haberg SE. Burden of medically attended influenza in Norway 2008-2017. Influenza Other Respir Viruses 2019; 13(3):240-247.
  • 19
    Brent SE, Pullenayegum E, Russell ML, Loeb M. Effect of seasonal influenza vaccination on influenza symptom severity among children in Hutterite communities: Follow up study of a randomized trial. Influenza Other Respir Viruses 2020; 14(1):28-36.
  • 20
    Lopes NR, Rodrigues BB, Tiago DC, Alvarenga LCR, Medeiros LMM, Ribeiro FAC, Rabahi MF. Factors associated with anti-influenza and anti-pneumococcal vaccination in elderly. Braz J Development 2019; 5(9):15451-15462.
  • 21
    Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Programa Nacional de Imunizações (PNI): 40 anos. Brasília: MS; 2013.
  • 22
    Brasil. Ministério da Saúde (MS). Informe Técnico 21a Campanha Nacional de Vacinação contra a Influenza Brasília: MS; 2019.
  • 23
    Andrew MK, Shinde V, Ye L, Hatchette T, Haguinet F, Dos Santos L, McE-lhaney JE, Ambrose U, Boivin G, Bowie W, Chit Um, Elsherif H, Verde K, Halperin S, Ibarguchi B, Johnstone J, Katz K, Langley J, Leblanc J, Loeb M, MacKinnon-D C, McCarthy U, McGeer U, Powis J, Richardson D, Semret M, Stiver G, Trottier S, Valiquette L, Webster D, McNeil SA. The Importance of Frailty in the Assessment of Influenza Vaccine Effectiveness Against Influenza-Related Hospitalization in Elderly People. J Infect Dis 2017; 216:405-414.
  • 24
    Chow EJ, Davis CT, Elal AIA, Alabi N, Azziz-Baumgartner E, Barnes J, Blanton L, Brammer L, Budd AP, Burns E, Davis WW, Dugan VG, Fry AM, Garten R, Grohskopf LA, Gubareva L, Jang Y, Jones J, Kniss K, Lindstrom S, Mustaquim D, Porter R, Rolfes M, Sessions W, Taylor C, Wentworth DE, Xu X, Zanders N, Katz J, Jernigan D. Update?: Influenza Activity-United States and Worldwide, May 20-October 13, 2018. CDC 2018; 67(42):1178-1185.
  • 25
    Flannery B, Chung JR, Belongia EA, Mclean HQ, Gaglani M, Murthy K, Zimermmam RK, Nowalk MP, Jackson ML, Jackson LA, Monto AS, Martin ET, Foust A, Sessões W, Berman L, Barnes JR, Spencer S, Fry AM. Interim Estimates of 2017-18 Seasonal Influenza Vaccine Effectiveness-United States, February 2018. CDC 2018; 67(6):180-185.
  • 26
    Cheng HY, Chen WC, Chou YJ, Huang AS, Huang WT. Containing influenza outbreaks with antiviral use in long-term care facilities in Taiwan, 2008-2014. Influenza Other Respir Viruses 2018; 12(2):287-292.
  • 27
    Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Cohen C, Gran JM. Schanzer D, Cowling BJ, Wu P, Kyncl J, Ang LW, Park M, Redlberger-Fritz M, Yu H, Espenhain L, Krishnan A, Emukule G, VanAsten L, Silva PS, Aungkulanon S, Buchholz U, Widdowson MA, Bresse JS. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 2019; 391(10127):1285-1300.
  • 28
    Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Coordenação-Geral de Desenvolvimento da Epidemiologia em Serviços. Guia de Vigilância em Saúde: volume único Brasilia: MS; 2017.
  • 29
    Chow EJ, Davis CT, Elal AIA, Alabi N, Azziz-Baumgartne Er, Barnes J, Blanton L, Brammer L, Budd AP, Burns E, Davis WW, Dugan VG, Fry AM, Garten R, Grohskopf LA, Gubareva L, Jang Y, Jones J, Kniss K, Lindstrom S, Mustaquim D, Porter R, Rolfes M, Sessions W, Taylor C, Wentworth DE, Xu X, Zanders N, Katz J, Jernigan D. Update: Influenza Activity-United States and Worldwide, May 20-October 13, 2018. US Department of Health and Human Services/Centers for Disease Control and Prevention. CDC 2019; 67(42):2-9.
  • 30
    Epperson S, Davis CT, Lynnette B, Elal AIA, Ajayi N, Barnes J, Budd AP, Burns E, Daly P, Dugan VG, Fry AM, Jang Y, Johnson SJ, Kniss K, Kondor R, Grohskopf LA, Gubareva L, Merced-Morales A, Sessions W, Stevens J, Wentworth DE, Xu X, Jernigan D. Update: Influenza Activity-United States and Worldwide , May 19-September 28, 2019, and Composition of the 2020 Southern Hemisphere Influenza Vaccine. US Department of Health and Human Services/Centers for Disease Control and Prevention. CDC 2019; 68.
  • 31
    Xu X, Blanton L, Elal AIA, Alabi N, Barnes J, Biggerrstaff M, Brammer L, Budd AP, Burns E, Cummings CN, Garg S, Kondor R, Gubareva L, Kniss K, Nyanseor S, O'Halloran A, Rolfes M, Wendy S, Dugan VD, Fry AM, Wentworth DE, Stevens J, Jernigan D. Update: Influenza Activity in the United States During the 2018-19 Season and Composition of the 2019-20 Influenza Vaccine. US Department of Health and Human Services/Centers for Disease Control and Prevention. CDC 2019; 68(24):544-551.
  • 32
    Pivette M, Nicolay N, Lauzun V, Hubert B. Characteristics of hospitalizations with an influenza diagnosis, France, 2012-2013 to 2016-2017 influenza seasons. Influenza Other Respir Viruses 2020; 14(3):1-9.
  • 33
    Naudion P, Lepiller Q, Boullier K. Risk factors and clinical characteristics of patients with nosocomial influenza A infection. J Med Virol 2020; 92(8):1047-1052.
  • 34
    Rosetto EV, Luna EJA. Database linkage for surveillance of the influenza A (H1N1) pdm09 pandemic in Brazil, 2009-2010. Cad Saúde Pública 2016; 32(7):e00014115.
  • 35
    Nogueira AL, Nogueira CL, Zibetti AW, Roqueiro N, Bruna-Romero O, Carciofi BAM. Estimativa da Subnotificação de Casos da COVID-19 no Estado de Santa Catarina Joinville: Universidade Federal de Santa Catarina; 2020.

Publication Dates

  • Publication in this collection
    30 Sept 2020
  • Date of issue
    Oct 2020

History

  • Received
    19 Apr 2020
  • Accepted
    10 Aug 2020
  • Published
    12 Aug 2020
ABRASCO - Associação Brasileira de Saúde Coletiva Rio de Janeiro - RJ - Brazil
E-mail: revscol@fiocruz.br