Investigation of the factors that cause respiratory tract infection during the COVID-19 pandemic in Afyonkarahisar, Turkey  (2020-2021).

Investigation of the factors that cause respiratory tract infection during the COVID-19 pandemic in Afyonkarahisar, Turkey (2020-2021). | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Investigation of the factors that cause respiratory tract infection during the COVID-19 pandemic in Afyonkarahisar, Turkey (2020-2021). Ramazan Köklu, Emek TÜRKEKUL ŞEN, Berrin ESEN, Petek ŞARLAK KONYA, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5787720/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Background Respiratory tract infections are a significant cause of morbidity and mortality worldwide. In particular, closely monitoring pathogens with pandemic potential is essential for early diagnosis and control of possible pandemics. In this study, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and viruses that most commonly cause respiratory tract infections in patients with similar clinical symptoms during the COVID-19 pandemic were examined; Influenza A/Influenza B; influenza A H1/H3/H5/H7; Human MetapneumoVirus (HMPV), Human respiratory syncytial virus (HRSV) A/B, Human rhinovirus (HRV); human bocavirus (HBoV); The simultaneous presence of Human enterovirus (HEV), Human parechvirus (HPeV), Human adenovirus (AV), Human coronavirus (HCoV) HKU/NL63/OC43/229E and Parainfluenza (PIV) 1/2/3/4 viruses were investigated. Methods Nasopharyngeal swab samples taken from 100 patients were analyzed using the multiplex single-step reverse transcription polymerase chain reaction (Multiplex RT qPCR) method. Results SARS-CoV-2 was detected in two (1%) of 50 samples taken from pediatric patients, and Human coronavirus (HCoV) OC43 was positive in one. While 14 samples (28%) were found to be positive for SARS-CoV-2 in the adult patient group, other respiratory tract viruses were not detected. Conclusions Although the study was carried out during the high season of influenza and other respiratory viral pathogens, they were found to be at low numbers and ratios. The reason for the low detection rate of SARS-CoV-2 virus and other respiratory tract viruses was interpreted as taking personal precautions and quarantine measures during the COVID-19 pandemic. It was thought that SARS-CoV-2 activity and its effect on seasonal influenza and other respiratory tract virus activities should be followed closely in the coming years. SARS CoV-2 pandemic Respiratory tract infections Multiplex RT qPCR Figures Figure 1 Figure 2 Introduction Acute respiratory diseases are one of the leading causes of morbidity and mortality worldwide. Bacteria, viruses, and parasites can cause respiratory tract infections (RTIs). Viruses have been reported to be the causative agents in approximately 20–60% of these infections [ 1 ]. Most respiratory viruses are transmitted by droplet and can cause clinical conditions ranging from uncomplicated upper respiratory tract infections to more severe disease states such as bronchiolitis, pneumonia and chronic lung disease [ 2 , 3 ]. The most common viruses causing respiratory tract infections are influenza, human respiratory syncytial virus (HRSV), human rhinovirus (HRV), parainfluenza (PIV), human metapneumovirus (HMPV), human bocavirus (HBoV), human enterovirus (HEV), human parechovirus (HPeV), human adenovirus (AV), human coronavirus (HCoV). While acute respiratory infectious agents can be detected throughout the year, their incidence varies seasonally. Seasonal flu viruses are most common in the fall and winter. The exact timing and duration of flu seasons can vary. However, flu activity usually increases in the northern hemisphere in October, often peaking between December and February, although activity can continue into May. In the southern hemisphere, it occurs between May and October. It usually peaks in August [ 4 – 7 ]. Since the sixteenth century, influenza viruses have caused varying severity and impact pandemics at intervals ranging from 10–50 years. The devastating influenza pandemic of 1918 had a lasting impact on the population, and the importance of global influenza surveillance was soon recognized. Global influenza surveillance is carried out as Influenza Like Illness "ILI" and Severe Acute Respiratory Illness "SARI" syndromic surveillance, which allows for the monitoring of similar diseases with a standard case definition globally since influenza cannot be easily distinguished clinically from other respiratory infections and is a virus with pandemic potential [ 4 , 7 , 8 ]. As part of ILI and SARI surveillance, in December 2019, a new coronavirus was detected in a group of patients in Wuhan, China, and the virus was named Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). The World Health Organization (WHO) named the disease caused by this new virus Coronavirus disease-19 (COVID-19) on 11 February 2020. WHO declared the disease, which is spreading rapidly in all countries, a pandemic on March 11, 2020 [ 9 ]. From the first case to 25.04.2021, 147,127,354 people worldwide have been infected with COVID-19, reaching 4,591,41 in our country. The disease, for which there is no definitive cure yet, is still important worldwide, and the pandemic continues [ 10 ]. With the identification of COVID-19 infection, routine ILI and SARI surveillance continued while monitoring the spread of the pandemic virus. Due to the seasonal nature of the diseases, assessments of the impact of COVID-19 on routine ILI/SARI surveillance, conducted with COVID-19 surveillance, were first initiated in the southern hemisphere in 2020 and then continued in the northern hemisphere during the 2020-21 influenza season [ 9 , 11 ]. Molecular diagnostic methods, which enable the precise and accurate identification of pathogenic viruses, especially during epidemic periods, contributed to the timely taking of quarantine and isolation measures and the rapid initiation of treatment during the SARS-CoV-2 pandemic. With the increase in cases due to the COVID-19 pandemic and the onset of the influenza season, the need for multiplex methods to test large numbers of samples for multiple viruses has increased. The multiplex real-time PCR technique helps us to understand better the seasonality, geographical distribution, and risk groups of viruses and, therefore, the epidemiology of respiratory tract infections. The multiplex real-time PCR method has reduced the spread of nosocomial infections in high-risk patients, limited the unnecessary use of antibiotics, and facilitated the clinical evaluation of the disease. In this study, we aimed to investigate the simultaneous presence of SARS CoV-2 and the viruses that most commonly cause respiratory tract infections in patients with similar clinical symptoms during the COVID-19 pandemic using the multiplex single-step reverse transcription polymerase chain reaction method [ 12 ]. Materials and Methods Ethic: This study received approval from the Ethics Committee of Afyonkarahisar Health Sciences University, Faculty of Medicine (Approval No: 2020/533, Date: 04.12.2020). Patient selection and sample collection were conducted accordingly. A total of 100 patients, including 50 patients aged 0-18 years and 50 patients aged 18-90 years, who were admitted to Afyonkarahisar Health Sciences University Faculty of Medicine Hospital between December 2020 and April 2021were included in the study. Patients with a pre-diagnosis of respiratory tract infection who met the COVID-19 probable case definition were included in the study. The patient's swab sample was placed in a Biospeedy vNAT® transfer tube. According to the manufacturer's instructions, patient samples were stored at -20°C under appropriate conditions until the day of the study. Used test kits In our study, respiratory viruses SARS-CoV-2, InfA/B; Inf A H1/H3/H5/H5/H7; HMPV, RSV A/B, HRV; HBoV, HEV, HPeV, AV, HCoV; HKU/NL63/OC43/229E, and PIV 1/2/3/4 were investigated by multiplex RT qPZR method using Biospeedy® "Respiratory Viruses Multiplex Real-Time PCR Screening Kit" (Bioeksen, Turkey). Bio-Rad CFX96/384 Touch Rt-PCR (Bio-Rad, USA) was used for multiplex RT qPCR. Viral genome extraction After the samples were taken from -20˚C, they were thawed at room temperature and vortexed for PCR. According to the manufacturer's recommendations, the nucleic acid extraction process was carried out in viral nucleic acid extraction buffer (vNAT). Multiplex RT- PCR The reaction mixture for amplification was prepared according to the manufacturer's recommended procedure. During the procedure, oligo mixes containing 6 separate components were pipetted into 6 different wells for each patient. The process was completed by adding a negative control for each 96-well plate. Patient samples (5 µl) were added to the reaction mixture, completing a total reaction volume of 20 µL. Plates were placed on the Rt-PCR device. In the study, amplification of the RdRp gene region; 5 min at 52 °C (cDNA formation), 10 s pre-denaturation at 95 °C, and 40 cycles of 95 °C 2 s denaturation, 55 °C 1 s primer coupling, and selecting FAM/HEX/ROX/Cy5 channels were performed. Two negative and positive controls, each provided by the manufacturer, were used in each PCR run. Interpretation of results According to the manufacturer's recommendations, the 'threshold' level was set to 200 RFU (relative fluorescence units). The shape of the proliferation curves obtained in FAM/HEX/ROX/Cy5 (Green/Yellow/Orange/Red) channels was examined. Non-sigmoidal curves were recorded as negative. The threshold cycle number (Cq) was calculated. The threshold cycle number (Cq) was calculated. If a sample was not assigned a Cq value by the device or was assigned a Cq value but the curve was not sigmoidal, the result was recorded as negative. If Cq <38 and a sigmoidal curve was formed, the results were recorded as positive, and the analysis result was interpreted according to the evaluation criteria included in the kit content of the manufacturer. Statistical analysis Statistical analysis was performed using the “IBM SPSS Statistics 20” program. Analysis of the results was done using the "Fisher's exact test" and "Chi-square" method, and p values <0.05 were considered statistically significant. Ethical approval Approval for this study was obtained from the Afyonkarahisar Health Sciences University Faculty of Medicine Clinical Research Ethics Committee (date 04.12.2020 and number 2020/533). Results Fifty samples were taken from pediatric patients, 30 were from outpatient clinics, and 20 were from patients hospitalized in various services. All 50 samples taken from adult patients consisted of outpatient clinic patients. While 22 (44%) of the pediatric patients were female and 28 (56%) were male, 27 (54%) of the adult patients were female and 23 (46%) were male. While the age range in pediatric patients was 1-18 years and the average age was 9.6, the age range in adult patients was 19-90 years, and the average age was calculated as 41.18. When the symptoms and clinical findings of the patients in the study group were evaluated, The most common symptom in the pediatric patient group was fever. The most common symptom in the adult patient group was malaise, followed by sore throat, cough, and headache. Clinical symptoms of cough, respiratory distress, and fever were detected at a statistically significantly higher rate in adults than pediatric patients ( p <0.05). Two (4%) of 50 samples taken from pediatric patients were SARS-CoV-2 positive. HCoV OC43 was detected as positive in one of the pediatric patients (Figure 1). This patient's symptoms were reported as a history of fever and cough. Since SARS-CoV-2 was positive in two pediatric patients, the relationship between positivity, symptoms, and epidemiological features could not be evaluated statistically. Influenza A/B; Influenza A H1/H3/H5/H7; HMPV, RSV A/B, HRV; HBoV, HEV, HPeV, AV, HCoV and HKU/NL63/229E, PIV 1/2/3/4 viruses were not detected in pediatric patients included in the study. In the adult patient group, 14 (28%) samples were detected as SARS-CoV-2 positive. Other respiratory viruses other than SARS-CoV-2 have not been detected in adult patients. The RT-PCR result of positive samples is shown in Figure 2. When symptoms are evaluated in adult patients, Cough symptom was detected at a statistically significantly higher rate in SARS-CoV-2 positive patients compared to negative patients ( p <0.05). Table 1: Evaluation of the results according to some variables in adult patients with SARS-CoV-2 positive and negative results. Variable Presence of symptoms Positive Negative P value (<0,05) n/ % n/ % Cough Yes No 1/ 2 13/ 26 10/ 20 39/ 78 0.249 Respiratory distress Yes No 10/ 20 4/ 8 14 / 28 22/ 44 0.038* Sore Throat Yes No 4/ 8 10/ 20 8/ 16 28/ 56 0.636 Resentment Yes No 10/ 20 4/ 8 17/ 34 19/ 38 0.123 Headache Yes No 10/ 20 4/ 8 18/ 36 18/ 36 0.170 Vomiting Yes No 4/ 8 10/ 20 13/ 26 23/ 46 0.613 Diarrhea Yes No 1/ 2 13/ 26 1/ 2 35/ 70 0.479 Myalgia Yes No 2/ 4 12/ 24 3/ 6 33/ 66 0.528 Abdominal Pain Yes No 5/ 10 9/ 18 7/ 14 29/ 58 0.226 * p <0.05 according to Fisher's test Discussion Viral respiratory tract infections constitute an important public health problem all over the world due to their widespread prevalence, easy transmission between people, high morbidity and mortality. Although deaths due to respiratory viral infections are rare in developed countries, more than five million children under five years of age are reported to die each year in developing countries due to these infections [13]. Influenza virus, AV, HMPV, RSV, HRV, PIV, HBoV, and HCoV are the primary viruses infecting the respiratory tract. It is reported that influenza, PIV, MPV, and RSV cause epidemic infections, while AV, HCoV, and HRV cause endemic infections. It is important to monitor epidemic viruses at national and international levels due to their potential to cause pandemics. Syndromes called ILI and SARI are reported weekly, seasonally, by national and international surveillance systems [13-15]. In the SARS-CoV-2 pandemic, as in the SARS-CoV and MERS-CoV pandemics, unusual cases and clusters of cases were detected by the global ILI and SARI surveillance systems. On December 31, 2019, the WHO Country Office of China made the first notification following a cluster of pneumonia cases of unknown cause in Wuhan, China in December 2019 [14] [13]. In the study conducted by Kong WH et al. in Wuhan between October 2019 and January 2020, SARS-CoV-2 RNA was found positive in nine patient samples from 640 patients with ILI syndrome. They reported that the number of ILI cases across all age groups increased dramatically from early December and reached a peak in early 2020. Especially in the 5-14 age group, the rate of ILI increased more than 24-fold during this period. When evaluated according to years, it was reported that the ILI data for the winter of 2019-2020 was significantly higher than previous years. It was also noted that cases need to be confirmed as the clinical presentation of ILI overlaps with the described mild/moderate COVID-19 [16]. Although the symptoms of COVID-19 in patients with a prediagnosis of respiratory tract infection are non-specific, COVID-19 infection can be asymptomatic and has a broad clinical spectrum ranging from mild respiratory tract infection to pneumonia, severe acute respiratory tract infection, and even death. In the study conducted by Chaolin et al. in Wuhan between December 2019 and January 2020, 49% of 41 SARS-CoV-2 positive patients were aged 25-49 years and 34% were aged 50-64 years. The most common symptoms were fever (98%), cough (76%), myalgia or fatigue (44%), excrete sputum (28%), headache (8%), hemoptysis (5%) and diarrhea (3%) [17]. In another study by NanShan Zhong et al. with 1099 SARS-CoV-2 positive patients, 87.9% of patients had a fever, 67.7% had a cough, 3.7% had diarrhea, and 5% had vomiting [18] [17]. It has been reported that the infection can be asymptomatic in children, while fever, dry cough, fatigue, and headache are observed in symptomatic cases [19]. In our study, fever was the most common symptom in the pediatric patient group. The most common symptom in the adult patient group was malaise, followed by sore throat, cough, and headache. Clinical symptoms of cough, respiratory distress, and fever were statistically significantly higher in adults compared to children. Among other respiratory viral agents, a pediatric patient with HCoV OC43 positive was found to have a history of fever and cough, among clinical symptoms. In the later stages of the pandemic, ILI and SARI surveillance continued during the diagnosis and treatment processes of SARS-CoV-2, and the associations of COVID-19 infection with similar clinical symptoms and ILI and SARI syndromes were investigated. The association of the SARS-CoV-2 virus with other viruses monitored in influenza-like disease surveillance and whether it interacts with these viruses were investigated. Various studies were reported from the northern hemisphere after the southern hemisphere in the spring and summer of 2020, when the global flu season started early. In the Liang En Wee L. E. et al. study, which included 3807 patients in Singapore between February and April 2020, 11.3% were positive for SARS-CoV-2 and 8.2% for other common respiratory viruses. SARS-CoV-2 co-infection (three rhinovirus, two parainfluenza, and one other coronavirus) was detected in six patients [20]. Different studies have reported that the rate of respiratory viruses coinfected with SARS-CoV-2 is between 0-3% [8, 21, 22]. Influenza activity has been reported to be at interseasonal levels in the temperate region of the Southern Hemisphere. No cases of influenza have been reported in the Caribbean and Central American countries. While no detection of influenza has been reported in tropical South America, other respiratory viruses have been reported to be detected at low levels in some countries. Influenza activity was observed in the last weeks of the 2021 influenza season in some reporting countries in West and East Africa [23]. In the study conducted by Sulliva S.G et al. in Australia in March-September 2020, only one influenza and three respiratory syncytial viruses were detected in samples from 587 patients who met the ILI case definition. When the influenza activity was compared with the previous year, it was determined that the influenza activity in 2020 was well below [24]. Huang S. S. et al. published a study in New Zealand in 2021, reporting that during and after the implementation of non-pharmaceutical interventions, such as quarantine and closure of the country's borders to the world, the influenza virus outbreak was eradicated and there was a significant reduction in other respiratory viral infections. When influenza data during the COVID-19 period is compared with data from 2015-2019, dramatic decreases of 67.7% during quarantine and 99.9% after quarantine were observed. Compared to 2015-2019 data, other respiratory viruses showed significant decreases after quarantine. Accordingly, a 98% reduction in RSV, 92.2% in HMPV, 82.2% in HEV, 81.4% in AV, 80.1% in PIV, and 74.6% in HRV were detected. When the period from May 2020 to September 2020 was analyzed, it was observed that influenza-associated SARI was not detected at all [25]. When we look at the studies conducted in our country before COVID-19, Kuşkucu MA et al. published in 2020, investigated the frequency and seasonal distribution of respiratory viruses in adult patients over approximately 8 years by examining the data of 788 patients. In the study, at least one viral agent was detected in 51.78% of the samples, while multiple agents were detected in 7.23%. However, no causative agent was detected in 48.22% of the samples. Influenza A/B in 16.88% of the samples (Influenza A = 11.42%, Influenza B = 5.46%), HRV in 14.85%, HCoV (C229 = 3.3%, C-OC43 = 3.05%, C-NL63) in 8.63%. =1.65%, HKU=0.63%), RSVA/B in 6.98%, HMPV in 4.06%, AV in 3.93%, PIV in 3.55% (PIV-1 =0.63%, PIV-2 =0.51%, PIV-3 = 1.90%, PIV-4 = 0.51%), EV was found in 0.51% and HBOV was found in 0.38%. HPeV was not detected in any sample [26]. In a study involving a total of 997 patients between 2016 and 2017 in Konya, Turkey, one or more respiratory viruses were detected in 761 (76.3%) of the samples and no virus was detected in 236 (22.8%) of the patients. In this study, the distribution of respiratory viruses was as follows: Adenovirus (2.76%), Bocavirus (4.20%), Coronavirus 229E (0.92%), Coronavirus OC43 (6.96%), Enterovirus (6.04%), Metapneumovirus A (4.60%), Metapneumovirus B (4.47%), Parainfluenza 1 (0.13%), Parainfluenza 2 (1.18%), Parainfluenza 3 (8.80%), Parainfluenza 4 (1.12%), Parainfluenza 4 (1.12%), Parainfluenza 1 (0.13%). 13%), Parainfluenza 2 (1.18%), Parainfluenza 3 (8.80%), Parainfluenza 4 (1.12%), Parainfluenza 4a (0.13%), Parainfluenza 4b (0. 13%), Rhinovirus (48.75%), Respiratory syncytial virus A/B (37.84%), Influenza B (3.02%), Parechovirus (6.57%). When the seasonal distribution of the agents was examined, it was determined that the most common agent was RSV in winter and rhinovirus in spring, summer and autumn [27]. When the data on respiratory viruses during the COVID-19 pandemic period in Turkey are examined; there are studies in which SARS-CoV-2 and respiratory viral panel tests were examined together from cases showing symptoms of respiratory tract infection. There are two important reasons why the two tests are ordered together. The first is to investigate other pathogens in cases that meet the COVID-19 case definition but have a negative SARS-CoV-2 RT-PCR test. The second is to investigate the presence of co-infection. Özdemir A. et al. investigated respiratory viral agents in 12,355 patients at Hacettepe University Hospital between April and November 2020. Among the 2,398 patients who were positive for SARS-CoV-2 PCR, 131 samples were positive for both SARS-CoV-2 and other respiratory pathogens. Two different pathogens [(Adenovirus, Bocavirus), (influenza A, influenza B)] were detected in the same sample in 2 out of 131 patients co-infected with SARS-CoV-2. The distribution of viral pathogens in patients with co-infection was Rhinovirus (85 patients), Influenza A (15 patients), Influenza B (12 patients), Respiratory syncytial virus A (one patient), Respiratory syncytial virus B (10 patients), Bocavirus (5 patients), Adenovirus (one patient), Parainfluenza 4 (one patient), Coronavirus 229E (one patient) [28]. Yiğit S. et al. analyzed 756 respiratory tract samples of patients aged 0-94 years with respiratory tract infection symptoms during the pandemic period. Of the 756 samples included in this study, 97 (12.8%) were positive for SARS-CoV-2 and 145 (19%) were positive for other respiratory viral agents. It was determined that 14 (14.4%) of the samples found to be positive for SARS-CoV-2 were positive with at least one of the other respiratory viral agents. In three of these samples, more than one viral agent was detected at the same time. Rhinovirus was detected in eight (57.1%) and Adenovirus in four (28.5%) of the samples that were positive for SARS-CoV-2 and at least one other viral agent [29]. Our study found HCoV OC43 positivity in only one pediatric patient. No respiratory viruses other than SARS-CoV-2 were detected in adult patients. In addition, the association of SARS CoV2 and other respiratory viruses was not detected in our study. Influenza activity in our country has followed an inter-seasonal level (summer season) as in the world. A >99% reduction in influenza infections detected was observed. The main reasons for this dramatic decrease in influenza infections are; These can be listed as decreasing the circulation of influenza, RSV, and other respiratory viruses with quarantine measures, the influenza virus having a lower transmission coefficient compared to SARS-CoV-2, and the measures having a much stronger effect on influenza circulation. The fact that we could not detect influenza virus in any patient in our study is parallel to the low influenza activity in our country. When we look at the studies' results in terms of human orientation, the functioning of hospitals, the working conditions of laboratories, and the human labour force in the COVID-19 pandemic, it suggests that influenza surveillance in countries is also affected depending on the behaviour of people applying to health institutions and testing policies. Conclusion The strict measures taken to control the COVID-19 pandemic around the world have led to a slowdown in the activity of influenza and other respiratory viruses. A similar situation was observed in our country. Although our study was conducted when influenza activity was expected to be high, the COVID-19 pandemic accelerated in our country during this period, and strict control measures had to be taken. It is thought that the fact that influenza and other respiratory viruses were not detected at the expected numbers and rates in our study may be due to the strict quarantine measures taken during the study period. Declarations Ethical approval Approval for this study was obtained from the Afyonkarahisar Health Sciences University Faculty of Medicine Clinical Research Ethics Committee (date 04.12.2020 and number 2020/533). Funding: This research was supported financially by Bioeksen ARGE Technology A.Ş., and we acknowledge their contribution, which made this study possible. Author Contribution RA: DNA extraction, Real-time PCR, writing paper, EM: Real-time PCR, writing paper, BE: writing paper, PK, DK, AB, ET: Sample collection . Acknowledgement The authors thank the academic and administrative staff for their support throughout the research process. Thanks to my colleagues for their valuable insights and assistance during the study. 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Köklu","email":"data:image/png;base64,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","orcid":"","institution":"Nigde Omer Halisdemir Training and Research Hospital","correspondingAuthor":true,"prefix":"","firstName":"Ramazan","middleName":"","lastName":"Köklu","suffix":""},{"id":399983933,"identity":"0644a4e5-5215-4cba-8a36-e06e238e9bd1","order_by":1,"name":"Emek TÜRKEKUL ŞEN","email":"","orcid":"","institution":"Ankara Education and Research Hospital Medical Microbiology Clinic","correspondingAuthor":false,"prefix":"","firstName":"Emek","middleName":"TÜRKEKUL","lastName":"ŞEN","suffix":""},{"id":399983934,"identity":"b8a27974-4539-463a-9f83-1a943a2eb935","order_by":2,"name":"Berrin ESEN","email":"","orcid":"","institution":"Afyonkarahisar Health Sciences University Medical Faculty Hospital","correspondingAuthor":false,"prefix":"","firstName":"Berrin","middleName":"","lastName":"ESEN","suffix":""},{"id":399983935,"identity":"9e4a2538-40ae-43ff-ad3c-651a46318853","order_by":3,"name":"Petek ŞARLAK KONYA","email":"","orcid":"","institution":"Afyonkarahisar Health Sciences University Medical Faculty Hospital","correspondingAuthor":false,"prefix":"","firstName":"Petek","middleName":"ŞARLAK","lastName":"KONYA","suffix":""},{"id":399983936,"identity":"bfabb89a-ecf1-439f-951f-2e3d66607f57","order_by":4,"name":"Derya KORKMAZ","email":"","orcid":"","institution":"Afyonkarahisar Health Sciences University Medical Faculty Hospital","correspondingAuthor":false,"prefix":"","firstName":"Derya","middleName":"","lastName":"KORKMAZ","suffix":""},{"id":399983937,"identity":"3b797647-2238-4654-a4b3-f8fcf0e8d3c8","order_by":5,"name":"Ayşegül BÜKÜLMEZ","email":"","orcid":"","institution":"Afyonkarahisar Health Sciences University Medical Faculty Hospital","correspondingAuthor":false,"prefix":"","firstName":"Ayşegül","middleName":"","lastName":"BÜKÜLMEZ","suffix":""},{"id":399983938,"identity":"4a4a86c0-ada3-497c-8fee-29dcec2f9105","order_by":6,"name":"Evrim Gürhan Tahta","email":"","orcid":"","institution":"Afyonkarahisar Health Sciences University Medical Faculty Hospital","correspondingAuthor":false,"prefix":"","firstName":"Evrim","middleName":"Gürhan","lastName":"Tahta","suffix":""}],"badges":[],"createdAt":"2025-01-08 09:38:26","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5787720/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5787720/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":73781743,"identity":"1315384e-1547-4b0d-b963-32747999c10a","added_by":"auto","created_at":"2025-01-14 15:27:08","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":54038,"visible":true,"origin":"","legend":"\u003cp\u003eRT-PCR image of the Human Coronavirus (HCoV) OC43 sample.\u003c/p\u003e","description":"","filename":"Fig1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5787720/v1/692f2f922981a813b0f8c08a.jpg"},{"id":73781744,"identity":"a267f4dc-8955-4c63-b923-30fa9377601a","added_by":"auto","created_at":"2025-01-14 15:27:08","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":56051,"visible":true,"origin":"","legend":"\u003cp\u003eRT-PCR images of SARS-CoV-2 samples.\u003c/p\u003e","description":"","filename":"Fig2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5787720/v1/df37b19766994c99eed22033.jpg"},{"id":73783346,"identity":"bc66965f-5a25-4f71-8112-10dfd81b25db","added_by":"auto","created_at":"2025-01-14 15:43:10","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":591198,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5787720/v1/50aa389a-df30-4318-ad1d-8c9421bb81a2.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Investigation of the factors that cause respiratory tract infection during the COVID-19 pandemic in Afyonkarahisar, Turkey (2020-2021).","fulltext":[{"header":"Introduction","content":"\u003cp\u003eAcute respiratory diseases are one of the leading causes of morbidity and mortality worldwide. Bacteria, viruses, and parasites can cause respiratory tract infections (RTIs). Viruses have been reported to be the causative agents in approximately 20\u0026ndash;60% of these infections [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eMost respiratory viruses are transmitted by droplet and can cause clinical conditions ranging from uncomplicated upper respiratory tract infections to more severe disease states such as bronchiolitis, pneumonia and chronic lung disease [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eThe most common viruses causing respiratory tract infections are influenza, human respiratory syncytial virus (HRSV), human rhinovirus (HRV), parainfluenza (PIV), human metapneumovirus (HMPV), human bocavirus (HBoV), human enterovirus (HEV), human parechovirus (HPeV), human adenovirus (AV), human coronavirus (HCoV). While acute respiratory infectious agents can be detected throughout the year, their incidence varies seasonally. Seasonal flu viruses are most common in the fall and winter. The exact timing and duration of flu seasons can vary. However, flu activity usually increases in the northern hemisphere in October, often peaking between December and February, although activity can continue into May. In the southern hemisphere, it occurs between May and October. It usually peaks in August [\u003cspan additionalcitationids=\"CR5 CR6\" citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eSince the sixteenth century, influenza viruses have caused varying severity and impact pandemics at intervals ranging from 10\u0026ndash;50 years. The devastating influenza pandemic of 1918 had a lasting impact on the population, and the importance of global influenza surveillance was soon recognized. Global influenza surveillance is carried out as Influenza Like Illness \"ILI\" and Severe Acute Respiratory Illness \"SARI\" syndromic surveillance, which allows for the monitoring of similar diseases with a standard case definition globally since influenza cannot be easily distinguished clinically from other respiratory infections and is a virus with pandemic potential [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eAs part of ILI and SARI surveillance, in December 2019, a new coronavirus was detected in a group of patients in Wuhan, China, and the virus was named Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). The World Health Organization (WHO) named the disease caused by this new virus Coronavirus disease-19 (COVID-19) on 11 February 2020. WHO declared the disease, which is spreading rapidly in all countries, a pandemic on March 11, 2020 [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eFrom the first case to 25.04.2021, 147,127,354 people worldwide have been infected with COVID-19, reaching 4,591,41 in our country. The disease, for which there is no definitive cure yet, is still important worldwide, and the pandemic continues [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eWith the identification of COVID-19 infection, routine ILI and SARI surveillance continued while monitoring the spread of the pandemic virus. Due to the seasonal nature of the diseases, assessments of the impact of COVID-19 on routine ILI/SARI surveillance, conducted with COVID-19 surveillance, were first initiated in the southern hemisphere in 2020 and then continued in the northern hemisphere during the 2020-21 influenza season [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eMolecular diagnostic methods, which enable the precise and accurate identification of pathogenic viruses, especially during epidemic periods, contributed to the timely taking of quarantine and isolation measures and the rapid initiation of treatment during the SARS-CoV-2 pandemic. With the increase in cases due to the COVID-19 pandemic and the onset of the influenza season, the need for multiplex methods to test large numbers of samples for multiple viruses has increased. The multiplex real-time PCR technique helps us to understand better the seasonality, geographical distribution, and risk groups of viruses and, therefore, the epidemiology of respiratory tract infections. The multiplex real-time PCR method has reduced the spread of nosocomial infections in high-risk patients, limited the unnecessary use of antibiotics, and facilitated the clinical evaluation of the disease.\u003c/p\u003e \u003cp\u003eIn this study, we aimed to investigate the simultaneous presence of SARS CoV-2 and the viruses that most commonly cause respiratory tract infections in patients with similar clinical symptoms during the COVID-19 pandemic using the multiplex single-step reverse transcription polymerase chain reaction method [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e].\u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003cp\u003e\u003cstrong\u003eEthic:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study received approval from the Ethics Committee of Afyonkarahisar Health Sciences University, Faculty of Medicine (Approval No: 2020/533, Date: 04.12.2020). Patient selection and sample collection were conducted accordingly.\u003c/p\u003e\n\u003cp\u003eA total of 100 patients, including 50 patients aged 0-18 years and 50 patients aged 18-90 years, who were admitted to Afyonkarahisar Health Sciences University Faculty of Medicine Hospital between December 2020 and April 2021were included in the study. Patients with a pre-diagnosis of respiratory tract infection who met the COVID-19 probable case definition were included in the study.\u003c/p\u003e\n\u003cp\u003eThe patient\u0026apos;s swab sample was placed in a Biospeedy vNAT\u0026reg; transfer tube. According to the manufacturer\u0026apos;s instructions, patient samples were stored at -20\u0026deg;C under appropriate conditions until the day of the study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eUsed test kits\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eIn our study, respiratory viruses SARS-CoV-2, InfA/B; Inf A H1/H3/H5/H5/H7; HMPV, RSV A/B, HRV; HBoV, HEV, HPeV, AV, HCoV; HKU/NL63/OC43/229E, and PIV 1/2/3/4 were investigated by multiplex RT qPZR method using Biospeedy\u0026reg; \u0026quot;Respiratory Viruses Multiplex Real-Time PCR Screening Kit\u0026quot; (Bioeksen, Turkey). Bio-Rad CFX96/384 Touch Rt-PCR (Bio-Rad, USA) was used for multiplex RT qPCR.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eViral genome extraction\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAfter the samples were taken from -20˚C, they were thawed at room temperature and vortexed for PCR. According to the manufacturer\u0026apos;s recommendations, the nucleic acid extraction process was carried out in viral nucleic acid extraction buffer (vNAT).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMultiplex RT- PCR\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe reaction mixture for amplification was prepared according to the manufacturer\u0026apos;s recommended procedure. During the procedure, oligo mixes containing 6 separate components were pipetted into 6 different wells for each patient. The process was completed by adding a negative control for each 96-well plate. Patient samples (5 \u0026micro;l) were added to the reaction mixture, completing a total reaction volume of 20 \u0026micro;L. Plates were placed on the Rt-PCR device.\u003c/p\u003e\n\u003cp\u003eIn the study, amplification of the RdRp gene region; 5 min at 52 \u0026deg;C (cDNA formation), 10 s pre-denaturation at 95 \u0026deg;C, and 40 cycles of 95 \u0026deg;C 2 s denaturation, 55 \u0026deg;C 1 s primer coupling, and selecting FAM/HEX/ROX/Cy5 channels were performed. Two negative and positive controls, each provided by the manufacturer, were used in each PCR run.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eInterpretation of results\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAccording to the manufacturer\u0026apos;s recommendations, the \u0026apos;threshold\u0026apos; level was set to 200 RFU (relative fluorescence units). The shape of the proliferation curves obtained in FAM/HEX/ROX/Cy5 (Green/Yellow/Orange/Red) channels was examined. Non-sigmoidal curves were recorded as negative. The threshold cycle number (Cq) was calculated. The threshold cycle number (Cq) was calculated. If a sample was not assigned a Cq value by the device or was assigned a Cq value but the curve was not sigmoidal, the result was recorded as negative. If Cq \u0026lt;38 and a sigmoidal curve was formed, the results were recorded as positive, and the analysis result was interpreted according to the evaluation criteria included in the kit content of the manufacturer.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eStatistical analysis\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eStatistical analysis was performed using the \u0026ldquo;IBM SPSS Statistics 20\u0026rdquo; program. Analysis of the results was done using the \u0026quot;Fisher\u0026apos;s exact test\u0026quot; and \u0026quot;Chi-square\u0026quot; method, and p values \u0026lt;0.05 were considered statistically significant.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthical approval\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eApproval for this study was obtained from the Afyonkarahisar Health Sciences University Faculty of Medicine Clinical Research Ethics Committee (date 04.12.2020 and number 2020/533).\u003c/p\u003e"},{"header":"Results ","content":"\u003cp\u003eFifty samples were taken from pediatric patients, 30 were from outpatient clinics, and 20 were from patients hospitalized in various services. All 50 samples taken from adult patients consisted of outpatient clinic patients. While 22 (44%) of the pediatric patients were female and 28 (56%) were male, 27 (54%) of the adult patients were female and 23 (46%) were male. While the age range in pediatric patients was 1-18 years and the average age was 9.6, the age range in adult patients was 19-90 years, and the average age was calculated as 41.18.\u003c/p\u003e\n\u003cp\u003eWhen the symptoms and clinical findings of the patients in the study group were evaluated, The most common symptom in the pediatric patient group was fever. The most common symptom in the adult patient group was malaise, followed by sore throat, cough, and headache. Clinical symptoms of cough, respiratory distress, and fever were detected at a statistically significantly higher rate in adults than pediatric patients (\u003cem\u003ep\u003c/em\u003e\u0026lt;0.05).\u003c/p\u003e\n\u003cp\u003eTwo (4%) of 50 samples taken from pediatric patients were SARS-CoV-2 positive. HCoV OC43 was detected as positive in one of the pediatric patients (Figure 1). This patient\u0026apos;s symptoms were reported as a history of fever and cough. Since SARS-CoV-2 was positive in two pediatric patients, the relationship between positivity, symptoms, and epidemiological features could not be evaluated statistically.\u003c/p\u003e\n\u003cp\u003eInfluenza A/B; Influenza A H1/H3/H5/H7; HMPV, RSV A/B, HRV; HBoV, HEV, HPeV, AV, HCoV and HKU/NL63/229E, PIV 1/2/3/4 viruses were not detected in pediatric patients included in the study.\u003c/p\u003e\n\u003cp\u003eIn the adult patient group, 14 (28%) samples were detected as SARS-CoV-2 positive. Other respiratory viruses other than SARS-CoV-2 have not been detected in adult patients. The RT-PCR result of positive samples is shown in Figure 2.\u003c/p\u003e\n\u003cp\u003eWhen symptoms are evaluated in adult patients, Cough symptom was detected at a statistically significantly higher rate in SARS-CoV-2 positive patients compared to negative patients (\u003cem\u003ep\u003c/em\u003e\u0026lt;0.05).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eTable 1:\u003c/strong\u003e Evaluation of the results according to some variables in adult patients with SARS-CoV-2 positive and negative results.\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd rowspan=\"2\" valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eVariable\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd rowspan=\"2\" valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003ePresence of symptoms\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 96px;\"\u003e\n \u003cp\u003ePositive\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 105px;\"\u003e\n \u003cp\u003eNegative\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd rowspan=\"2\" valign=\"top\" style=\"width: 95px;\"\u003e\n \u003cp\u003e\u003cem\u003eP\u003c/em\u003e value (\u0026lt;0,05)\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 96px;\"\u003e\n \u003cp\u003e\u003cstrong\u003en/ %\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 105px;\"\u003e\n \u003cp\u003e\u003cstrong\u003en/ %\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eCough\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e1/ 2\u003c/p\u003e\n \u003cp\u003e13/ 26\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e10/ 20\u003c/p\u003e\n \u003cp\u003e39/ 78\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.249\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eRespiratory distress\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e10/ 20\u003c/p\u003e\n \u003cp\u003e4/ 8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e14 / 28\u003c/p\u003e\n \u003cp\u003e22/ 44\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.038*\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eSore Throat\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e4/ 8\u003c/p\u003e\n \u003cp\u003e10/ 20\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e8/ 16\u003c/p\u003e\n \u003cp\u003e28/ 56\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.636\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eResentment\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e10/ 20\u003c/p\u003e\n \u003cp\u003e4/ 8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e17/ 34\u003c/p\u003e\n \u003cp\u003e19/ 38\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.123\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eHeadache\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e10/ 20\u003c/p\u003e\n \u003cp\u003e4/ 8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e18/ 36\u003c/p\u003e\n \u003cp\u003e18/ 36\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.170\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eVomiting\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e4/ 8\u003c/p\u003e\n \u003cp\u003e10/ 20\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e13/ 26\u003c/p\u003e\n \u003cp\u003e23/ 46\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.613\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eDiarrhea\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e1/ 2\u003c/p\u003e\n \u003cp\u003e13/ 26\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e1/ 2\u003c/p\u003e\n \u003cp\u003e35/ 70\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.479\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eMyalgia\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e2/ 4\u003c/p\u003e\n \u003cp\u003e12/ 24\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e3/ 6\u003c/p\u003e\n \u003cp\u003e33/ 66\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.528\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 192px;\"\u003e\n \u003cp\u003eAbdominal Pain\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 124px;\"\u003e\n \u003cp\u003eYes\u0026nbsp;\u003c/p\u003e\n \u003cp\u003eNo\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 96px;\"\u003e\n \u003cp\u003e5/ 10\u003c/p\u003e\n \u003cp\u003e9/ 18\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 105px;\"\u003e\n \u003cp\u003e7/ 14\u003c/p\u003e\n \u003cp\u003e29/ 58\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 95px;\"\u003e\n \u003cp\u003e0.226\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u003cstrong\u003e*\u003c/strong\u003e\u003cem\u003e\u0026nbsp;p\u003c/em\u003e\u0026lt;0.05 according to Fisher\u0026apos;s test\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eViral respiratory tract infections constitute an important public health problem all over the world due to their widespread prevalence, easy transmission between people, high morbidity and mortality. Although deaths due to respiratory viral infections are rare in developed countries, more than five million children under five years of age are reported to die each year in developing countries due to these infections [13].\u003c/p\u003e\n\u003cp\u003eInfluenza virus, AV, HMPV, RSV, HRV, PIV, HBoV, and HCoV are the primary viruses infecting the respiratory tract. It is reported that influenza, PIV, MPV, and RSV cause epidemic infections, while AV, HCoV, and HRV cause endemic infections. It is important to monitor epidemic viruses at national and international levels due to their potential to cause pandemics. Syndromes called ILI and SARI are reported weekly, seasonally, by national and international surveillance systems [13-15]. In the SARS-CoV-2 pandemic, as in the SARS-CoV and MERS-CoV pandemics, unusual cases and clusters of cases were detected by the global ILI and SARI surveillance systems. On December 31, 2019, the WHO Country Office of China made the first notification following a cluster of pneumonia cases of unknown cause in Wuhan, China in December 2019 [14] [13]. In the study conducted by Kong WH et al. in Wuhan between October 2019 and January 2020, SARS-CoV-2 RNA was found positive in nine patient samples from 640 patients with ILI syndrome. They reported that the number of ILI cases across all age groups increased dramatically from early December and reached a peak in early 2020. Especially in the 5-14 age group, the rate of ILI increased more than 24-fold during this period. When evaluated according to years, it was reported that the ILI data for the winter of 2019-2020 was significantly higher than previous years. It was also noted that cases need to be confirmed as the clinical presentation of ILI overlaps with the described mild/moderate COVID-19 [16]. \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eAlthough the symptoms of COVID-19 in patients with a prediagnosis of respiratory tract infection are non-specific, COVID-19 infection can be asymptomatic and has a broad clinical spectrum ranging from mild respiratory tract infection to pneumonia, severe acute respiratory tract infection, and even death.\u003c/p\u003e\n\u003cp\u003eIn the study conducted by Chaolin et al. in Wuhan between December 2019 and January 2020, 49% of 41 SARS-CoV-2 positive patients were aged 25-49 years and 34% were aged 50-64 years. The most common symptoms were fever (98%), cough (76%), myalgia or fatigue (44%), \u003cem\u003eexcrete sputum\u003c/em\u003e (28%), headache (8%), hemoptysis (5%) and diarrhea (3%) [17]. In another study by NanShan Zhong et al. with 1099 SARS-CoV-2 positive patients, 87.9% of patients had a fever, 67.7% had a cough, 3.7% had diarrhea, and 5% had vomiting [18] [17]. It has been reported that the infection can be asymptomatic in children, while fever, dry cough, fatigue, and headache are observed in symptomatic cases [19].\u003c/p\u003e\n\u003cp\u003eIn our study, fever was the most common symptom in the pediatric patient group. The most common symptom in the adult patient group was malaise, followed by sore throat, cough, and headache. Clinical symptoms of cough, respiratory distress, and fever were statistically significantly higher in adults compared to children. Among other respiratory viral agents, a pediatric patient with HCoV OC43 positive was found to have a history of fever and cough, among clinical symptoms.\u003c/p\u003e\n\u003cp\u003eIn the later stages of the pandemic, ILI and SARI surveillance continued during the diagnosis and treatment processes of SARS-CoV-2, and the associations of COVID-19 infection with similar clinical symptoms and ILI and SARI syndromes were investigated. The association of the SARS-CoV-2 virus with other viruses monitored in influenza-like disease surveillance and whether it interacts with these viruses were investigated. Various studies were reported from the northern hemisphere after the southern hemisphere in the spring and summer of 2020, when the global flu season started early.\u003c/p\u003e\n\u003cp\u003eIn the Liang En Wee L. E. et al. study, which included 3807 patients in Singapore between February and April 2020, 11.3% were positive for SARS-CoV-2 and 8.2% for other common respiratory viruses. SARS-CoV-2 co-infection (three rhinovirus, two parainfluenza, and one other coronavirus) was detected in six patients [20]. Different studies have reported that the rate of respiratory viruses coinfected with SARS-CoV-2 is between 0-3% [8, 21, 22].\u003c/p\u003e\n\u003cp\u003eInfluenza activity has been reported to be at interseasonal levels in the temperate region of the Southern Hemisphere. No cases of influenza have been reported in the Caribbean and Central American countries. While no detection of influenza has been reported in tropical South America, other respiratory viruses have been reported to be detected at low levels in some countries. Influenza activity was observed in the last weeks of the 2021 influenza season in some reporting countries in West and East Africa [23].\u003c/p\u003e\n\u003cp\u003eIn the study conducted by Sulliva S.G et al. in Australia in March-September 2020, only one influenza and three respiratory syncytial viruses were detected in samples from 587 patients who met the ILI case definition. When the influenza activity was compared with the previous year, it was determined that the influenza activity in 2020 was well below [24].\u003c/p\u003e\n\u003cp\u003eHuang S. S. et al. published a study in New Zealand in 2021, reporting that during and after the implementation of non-pharmaceutical interventions, such as quarantine and closure of the country\u0026apos;s borders to the world, the influenza virus outbreak was eradicated and there was a significant reduction in other respiratory viral infections. When influenza data during the COVID-19 period is compared with data from 2015-2019, dramatic decreases of 67.7% during quarantine and 99.9% after quarantine were observed. Compared to 2015-2019 data, other respiratory viruses showed significant decreases after quarantine. Accordingly, a 98% reduction in RSV, 92.2% in HMPV, 82.2% in HEV, 81.4% in AV, 80.1% in PIV, and 74.6% in HRV were detected. When the period from May 2020 to September 2020 was analyzed, it was observed that influenza-associated SARI was not detected at all [25].\u003c/p\u003e\n\u003cp\u003eWhen we look at the studies conducted in our country before COVID-19, Kuşkucu MA et al. published in 2020, investigated the frequency and seasonal distribution of respiratory viruses in adult patients over approximately 8 years by examining the data of 788 patients. In the study, at least one viral agent was detected in 51.78% of the samples, while multiple agents were detected in 7.23%. However, no causative agent was detected in 48.22% of the samples. Influenza A/B in 16.88% of the samples (Influenza A = 11.42%, Influenza B = 5.46%), HRV in 14.85%, HCoV (C229 = 3.3%, C-OC43 = 3.05%, C-NL63) in 8.63%. =1.65%, HKU=0.63%), RSVA/B in 6.98%, HMPV in 4.06%, AV in 3.93%, PIV in 3.55% (PIV-1 =0.63%, PIV-2 =0.51%, PIV-3 = 1.90%, PIV-4 = 0.51%), EV was found in 0.51% and HBOV was found in 0.38%. HPeV was not detected in any sample [26].\u003c/p\u003e\n\u003cp\u003eIn a study involving a total of 997 patients between 2016 and 2017 in Konya, Turkey, one or more respiratory viruses were detected in 761 (76.3%) of the samples and no virus was detected in 236 (22.8%) of the patients. In this study, the distribution of respiratory viruses was as follows: Adenovirus (2.76%), Bocavirus (4.20%), Coronavirus 229E (0.92%), Coronavirus OC43 (6.96%), Enterovirus (6.04%), Metapneumovirus A (4.60%), Metapneumovirus B (4.47%), Parainfluenza 1 (0.13%), Parainfluenza 2 (1.18%), Parainfluenza 3 (8.80%), Parainfluenza 4 (1.12%), Parainfluenza 4 (1.12%), Parainfluenza 1 (0.13%). 13%), Parainfluenza 2 (1.18%), Parainfluenza 3 (8.80%), Parainfluenza 4 (1.12%), Parainfluenza 4a (0.13%), Parainfluenza 4b (0. 13%), Rhinovirus (48.75%), Respiratory syncytial virus A/B (37.84%), Influenza B (3.02%), Parechovirus (6.57%). When the seasonal distribution of the agents was examined, it was determined that the most common agent was RSV in winter and rhinovirus in spring, summer and autumn [27].\u003c/p\u003e\n\u003cp\u003eWhen the data on respiratory viruses during the COVID-19 pandemic period in Turkey are examined; there are studies in which SARS-CoV-2 and respiratory viral panel tests were examined together from cases showing symptoms of respiratory tract infection. There are two important reasons why the two tests are ordered together. The first is to investigate other pathogens in cases that meet the COVID-19 case definition but have a negative SARS-CoV-2 RT-PCR test. The second is to investigate the presence of co-infection.\u003c/p\u003e\n\u003cp\u003e\u0026Ouml;zdemir A. et al. investigated respiratory viral agents in 12,355 patients at Hacettepe University Hospital between April and November 2020. Among the 2,398 patients who were positive for SARS-CoV-2 PCR, 131 samples were positive for both SARS-CoV-2 and other respiratory pathogens. Two different pathogens [(Adenovirus, Bocavirus), (influenza A, influenza B)] were detected in the same sample in 2 out of 131 patients co-infected with SARS-CoV-2. The distribution of viral pathogens in patients with co-infection was Rhinovirus (85 patients), Influenza A (15 patients), Influenza B (12 patients), Respiratory syncytial virus A (one patient), Respiratory syncytial virus B (10 patients), Bocavirus (5 patients), Adenovirus (one patient), Parainfluenza 4 (one patient), Coronavirus 229E (one patient) [28].\u003c/p\u003e\n\u003cp\u003eYiğit S. et al. analyzed 756 respiratory tract samples of patients aged 0-94 years with respiratory tract infection symptoms during the pandemic period. Of the 756 samples included in this study, 97 (12.8%) were positive for SARS-CoV-2 and 145 (19%) were positive for other respiratory viral agents. It was determined that 14 (14.4%) of the samples found to be positive for SARS-CoV-2 were positive with at least one of the other respiratory viral agents. In three of these samples, more than one viral agent was detected at the same time. Rhinovirus was detected in eight (57.1%) and Adenovirus in four (28.5%) of the samples that were positive for SARS-CoV-2 and at least one other viral agent [29].\u003c/p\u003e\n\u003cp\u003eOur study found HCoV OC43 positivity in only one pediatric patient. No respiratory viruses other than SARS-CoV-2 were detected in adult patients. In addition, the association of SARS CoV2 and other respiratory viruses was not detected in our study.\u003c/p\u003e\n\u003cp\u003eInfluenza activity in our country has followed an inter-seasonal level (summer season) as in the world. A \u0026gt;99% reduction in influenza infections detected was observed. The main reasons for this dramatic decrease in influenza infections are; These can be listed as decreasing the circulation of influenza, RSV, and other respiratory viruses with quarantine measures, the influenza virus having a lower transmission coefficient compared to SARS-CoV-2, and the measures having a much stronger effect on influenza circulation. The fact that we could not detect influenza virus in any patient in our study is parallel to the low influenza activity in our country.\u003c/p\u003e\n\u003cp\u003eWhen we look at the studies\u0026apos; results in terms of human orientation, the functioning of hospitals, the working conditions of laboratories, and the human labour force in the COVID-19 pandemic, it suggests that influenza surveillance in countries is also affected depending on the behaviour of people applying to health institutions and testing policies.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eThe strict measures taken to control the COVID-19 pandemic around the world have led to a slowdown in the activity of influenza and other respiratory viruses. A similar situation was observed in our country. Although our study was conducted when influenza activity was expected to be high, the COVID-19 pandemic accelerated in our country during this period, and strict control measures had to be taken. It is thought that the fact that influenza and other respiratory viruses were not detected at the expected numbers and rates in our study may be due to the strict quarantine measures taken during the study period.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eEthical approval\u003c/h2\u003e\n\u003cp\u003eApproval for this study was obtained from the Afyonkarahisar Health Sciences University Faculty of Medicine Clinical Research Ethics Committee (date 04.12.2020 and number 2020/533).\u003c/p\u003e\n\u003ch2\u003eFunding:\u003c/h2\u003e\n\u003cp\u003eThis research was supported financially by Bioeksen ARGE Technology A.Ş., and we acknowledge their contribution, which made this study possible.\u003c/p\u003e\n\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\n\u003cp\u003eRA: DNA extraction, Real-time PCR, writing paper, EM: Real-time PCR, writing paper, BE: writing paper, PK, DK, AB, ET: Sample collection .\u003c/p\u003e\n\u003ch2\u003eAcknowledgement\u003c/h2\u003e\n\u003cp\u003eThe authors thank the academic and administrative staff for their support throughout the research process. Thanks to my colleagues for their valuable insights and assistance during the study. Additionally, appreciation is given to the participants for their contributions, which made this research possible. Finally, the authors acknowledge the funding sources that facilitated this work.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003e\u0026Ccedil;i\u0026ccedil;ek C, Arslan A, Karakuş HS et al (2015) Akut solunum yolu enfeksiyonu olan hastalarda solunum viruslarının prevalansı ve mevsimsel dağılımı, 2002-2014. Mikrobiyol Bul 49, 188-200\u003c/li\u003e\n\u003cli\u003eSubbarao K and Mahanty S (2020) Respiratory virus infections: understanding COVID-19. Immunity 52, 905-909\u003c/li\u003e\n\u003cli\u003eKutter JS, Spronken MI, Fraaij PL, Fouchier RA and Herfst S (2018) Transmission routes of respiratory viruses among humans. 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The impact of COVID-19 on the circulation of influenza and other respiratory viruses, Australia, March to September 2020. Eurosurveillance 25, 2001847\u003c/li\u003e\n\u003cli\u003eHuang QS, Wood T, Jelley L et al (2021) Impact of the COVID-19 nonpharmaceutical interventions on influenza and other respiratory viral infections in New Zealand. Nature communications 12, 1-7\u003c/li\u003e\n\u003cli\u003eKuşkucu MA, Mete B, Tabak F and Midilli K (2020) Yetişkinlerde solunum yolu viral etkenlerinin 2010-2018 yılları arasındaki prevalansı ve mevsimsel dağılımı. Turk Mikrobiyol Cem Derg 50, 21-26\u003c/li\u003e\n\u003cli\u003eTokak S, G\u0026uuml;lseren YD and \u0026Ouml;zdemir M (2019) Solunum Yolu Enfeksiyonlu \u0026Ccedil;ocuklarda Saptanan Viral Etkenlerin Epidemiyolojisi ve Mevsim Dağılımının Belirlenmesi. Journal of Pediatric Infection/\u0026Ccedil;ocuk Enfeksiyon Dergisi 13\u003c/li\u003e\n\u003cli\u003e\u0026Ouml;zdemir A, Alp, A. and Pınar, A. . (2020) Retrospective investigation of coinfection rates of SARS-CoV-2 and other respiratory pathogens.\u003c/li\u003e\n\u003cli\u003eYiğit S, Sarzhanova, S., Dizbay, M., \u0026Ccedil;ağlar, K. and Bozdayı, G. (2020) Evaluation of the coexistence of SARS-CoV-2 and other respiratory viral agents during the pandemic period.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"SARS CoV-2 pandemic, Respiratory tract infections, Multiplex RT qPCR","lastPublishedDoi":"10.21203/rs.3.rs-5787720/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5787720/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eRespiratory tract infections are a significant cause of morbidity and mortality worldwide. In particular, closely monitoring pathogens with pandemic potential is essential for early diagnosis and control of possible pandemics. In this study, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and viruses that most commonly cause respiratory tract infections in patients with similar clinical symptoms during the COVID-19 pandemic were examined; Influenza A/Influenza B; influenza A H1/H3/H5/H7; Human MetapneumoVirus (HMPV), Human respiratory syncytial virus (HRSV) A/B, Human rhinovirus (HRV); human bocavirus (HBoV); The simultaneous presence of Human enterovirus (HEV), Human parechvirus (HPeV), Human adenovirus (AV), Human coronavirus (HCoV) HKU/NL63/OC43/229E and Parainfluenza (PIV) 1/2/3/4 viruses were investigated.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eNasopharyngeal swab samples taken from 100 patients were analyzed using the multiplex single-step reverse transcription polymerase chain reaction (Multiplex RT qPCR) method.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eSARS-CoV-2 was detected in two (1%) of 50 samples taken from pediatric patients, and Human coronavirus (HCoV) OC43 was positive in one. While 14 samples (28%) were found to be positive for SARS-CoV-2 in the adult patient group, other respiratory tract viruses were not detected.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eAlthough the study was carried out during the high season of influenza and other respiratory viral pathogens, they were found to be at low numbers and ratios. The reason for the low detection rate of SARS-CoV-2 virus and other respiratory tract viruses was interpreted as taking personal precautions and quarantine measures during the COVID-19 pandemic. It was thought that SARS-CoV-2 activity and its effect on seasonal influenza and other respiratory tract virus activities should be followed closely in the coming years.\u003c/p\u003e","manuscriptTitle":"Investigation of the factors that cause respiratory tract infection during the COVID-19 pandemic in Afyonkarahisar, Turkey (2020-2021).","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-01-14 15:27:03","doi":"10.21203/rs.3.rs-5787720/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"40dd0fb6-9d8e-419e-9df3-f46b1f775bb3","owner":[],"postedDate":"January 14th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2025-01-14T15:27:06+00:00","versionOfRecord":[],"versionCreatedAt":"2025-01-14 15:27:03","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5787720","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5787720","identity":"rs-5787720","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}