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## Surveillance for respiratory infectious diseases caused by 6 common viruses in a recruit training site in the Northern region of China

Background

Due to their high incidence, ease of spread and the difficult nature of prevention and treatment, acute respiratory diseases (ARDs) are major threats to armies worldwide. Therefore, ARDs have become an important part of military medical study. Recruit training is a necessary step and effective way for improving the quality of troops and guaranteeing their combat capacity. During the training period, intensive physical training and changes in lifestyle, living environment and social support expose the recruits to different types of injuries, including physical injuries and ARDs [2, 3]. Furthermore, due to dramatic weather changes, the incidence of ARDs is higher in autumn and winter when recruitment in China usually occurs, and recruits are sensitive to respiratory infections. In recent years, a number of massive ARDs epidemics associated with adenovirus infection have occurred at recruit training sites [4–8], causing significant damage to soldiers’ health and imposing a huge burden of health protection and disease prevention in the troops.

Monitoring respiratory symptoms and the causal pathogens is an effective way to understand infectious pathogens, monitor the epidemic dynamics of infectious diseases, and prevent the occurrence of respiratory tract infectious diseases during the recruit training period. From the early 1970s to the late 1990s, the United States (US) military had implemented the ARDs surveillance program. This program helped track and monitor all hospitalized recruits with ARDs. Over the past decade (2000–2014), the US military insisted on this program and has monitored patients with uncomplicated febrile ARDs (such as non-hospitalized patients). This program has been implemented for nearly 50 years, and it has been immensely valuable in identifying clusters of respiratory diseases among U.S. Army trainees. Surveillance of febrile respiratory diseases was introduced in 2013 in China, when the ARDs pathogens surveillance network laboratories and surveillance sites were established.

To prevent respiratory infection outbreaks and investigate the causal pathogens for infections that occur in recruits, we monitored respiratory symptoms and performed respiratory infection surveillance in 800 recruits enlisted in autumn 2015 at a Chinese recruit training site.

Study design and subject selection

This study was an assigned mission. All 800 recruits at a recruit training site in the Hebei province of China enlisted in autumn 2015 were enrolled in this study. The background survey was conducted within 24 h of settlement at the training site in a cross-sectional manner. The period of ARDs surveillance was from September to December 2015 (the same as the training duration). An individual was considered a pathogen carrier if the nasopharyngeal swabs were positive for at least one pathogen without overt symptoms.

Collection of background information of recruits

A questionnaire was prepared in a unified form to collect background information from the recruits within 3 days after arrival at the training site (the questionnaire included birth place; place of recruitment; history of infectious diseases; vaccination history; nutrition condition; mental state; and whether suffering from fever, cough, runny nose, sore throat or other respiratory symptoms within 3 days). The questionnaire survey was conducted in the dormitory of the recruits. The interviewers gave every recruit the questionnaire and explained every term that the recruits did not understand. The duration of this questionnaire survey was not limited allowing everyone sufficient time to fill out the form. All recruits could freely ask questions of the interviewers, but discussion among the recruits was not allowed. The interviewers were well trained health technicians.

Collection of blood samples and swabs

Within 3 days of recruit settlement at the training site, 10 ml of fasting venous blood was collected in the morning by professional nurses, and serum was separated and stored at −20 °C to detect adenovirus IgG. Nasopharyngeal swabs were collected following appropriate procedures, and they were placed in universal transport medium. These samples were sent to the laboratory immediately for testing or storage at −80 °C.

The adenovirus IgG in serum was detected using semi-quantitative ELISA kits (catalog number: 20160301) provided by Beijing Beier Biological Engineering Co. Ltd. (Beijing, China), according to the manufacturer’s instructions. The cut-off absorption value for this kit was defined as the mean value of negative controls plus 0.1. A positive sample was defined as having an absorption value higher than the cut-off value.

Surveillance of febrile respiratory symptoms

During the training period, the body temperature of the recruits was monitored, and individuals with a temperature ≥38 °C and other respiratory symptoms (cough, sputum, nasal congestion, runny nose, sore throat, headache, and fatigue) were isolated at a separate ward. Nasal swabs of these recruits were collected within 4 h of symptoms onset. Case report forms (including body temperature, cough, runny nose, sore throat and other symptoms, as well as the respiratory rate, pulse, blood pressure, etc.) were completed and sent to the central laboratory of the Institute of Disease Control and Prevention, Academy of Military Medical Sciences (Beijing, China). Nasal swabs were sub-packaged promptly and stored in a refrigerator at −80 °C; they were then sent to the network laboratory at 302 Hospital of PLA (Beijing, China) for further testing.

Pathogen detection

The various pathogens were detected by real-time quantitative PCR from the collected nasopharyngeal swabs. Pathogenic genomes were extracted from the nasopharyngeal swabs using a Viral Genomic DNA/RNA Extraction Kit (Catalog No. DP315, Tiangen Biotech, Beijing, China), and they were assessed by Influenza A/B Viral RNA Detection Kit (Catalog No. P0101C-24, MOKOGENE, Nanjing, China) and Respiratory Syncytial Virus (RSV)/Adenovirus/Human Metapneumovirus/Human Bocavirus Nucleic Acid Detection Kit (Catalog No. P0304-24, MOKOGENE, Nanjing, China). Adenovirus positive samples were re-tested using the One Step PrimeScript RT-PCR Kit (Catalog No. RR064A, Takara, Shiga, Japan) with common adenovirus primers to confirm the results. Samples positive for influenza virus A, influenza virus B or adenovirus were further tested with the genotyping primers shown in Table 1. All reactions were performed on an ABI 7500 PCR System (Applied Biosystems, Foster City, CA, USA). Two segments of the hexon gene of HAdV were amplified by PCR using 2 pairs of specific primers (Table 2), and the resulting products were sequenced by Beijing AuGCT Biotechnology Co., Ltd. (Beijing, China). Then, a sequence homology search was performed to identify the subgroup of adenovirus via the BLAST program at NCBI (http://blast.ncbi.nlm.nih.gov/Blast.cgi, 2015).

Data analysis

All data were entered into a database, and logical errors were detected and corrected using the Excel program (Microsoft Office EXCEL 2003, WA, USA). The corresponding frequency, constituent ratio, or incidence was calculated. Measurement data consistent with a normal distribution (tested by the Kolmogorov-Smirnov test) and expressed as \documentclass[12pt]{minimal}

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Background information of recruits

Background information was collected from the 800 recruits. There were 722 males and 78 females, who were aged 18.9 ± 1.69 years. Most recruits came from Hebei (199, 24.9%), Shandong (102, 12.8%), Jiangsu (196, 24.5%), Shanxi (99, 12.4%) and Hunan (204, 25.5%). The ratio of recruits from urban areas to those from rural areas was 1:1.12 (378:422). Basic information, lifestyle, and medical history of the assessed recruits are summarized in Table 3.

Pathogen identification

None of the recruits had fever or respiratory symptoms when nasopharyngeal swabs were collected for the background survey. A total of 795 samples of nasopharyngeal swabs were tested, and 2 cases were adenovirus-positive as assessed by real-time PCR. None of the samples was positive for influenza virus A, influenza virus B, RSV, human metapneumovirus or human bocavirus. After genotyping and sequencing, the 2 adenovirus-positive cases were identified as group C type 1 adenovirus. The labels of 5 samples were missing or could not be recognized clearly; these samples were not tested.

Monitoring of cases with febrile respiratory symptoms

During the three months of training, 39 recruits had febrile respiratory infection symptoms (incidence rate of 4.9%) with an average temperature of 38.7 °C (38.0–40.2 °C). The main symptoms included cough (34, 87.2%), expectoration (15, 38.4%), sore throat (27, 74.3%), headache (27, 69.2%), fatigue (29, 74.3%), runny nose (19, 48.0%), muscle pain (8, 20.0%) and diarrhea (3, 7.7%). No chest distress, chest pain or suffocation was observed. All cases had fever abatement within 3 days after supportive treatment. The disease course was 2–7 days.

Pathogen detection in cases with febrile respiratory symptoms

Five of 39 nasopharyngeal swabs were adenovirus-positive (positive rate of 12.8%). Further adenovirus genotyping showed that there were 3 cases with group B adenovirus type 4 and 2 with adenovirus type 3. No type 7, 14 or 55 adenovirus was detected. Influenza virus was not detected in any cases with febrile respiratory symptoms.

Investigation of serum adenovirus immunoglobulin G (IgG) of recruits

Because of missing or blurred label or an inadequate sample volume, 70 samples were not tested. Adenovirus IgG (Adv-IgG) in 730 serum samples was tested, and 352 samples were Adv-IgG positive (positive rate of 48.2%). Further analysis of the Adv-IgG of 39 cases with febrile respiratory symptoms showed that among the 5 adenovirus-positive cases, 4 were Adv-IgG positive (positive rate of 80%). Among the 34 adenovirus-negative patients, 13 cases were Adv-IgG positive (positive rate of 38.2%, Table 4).

Discussion

We performed a general survey on pathogens responsible for respiratory infectious diseases at a recruit training site for the first time. To improve the data quality, we selected commercial kits for preliminary screening. The results showed that the pathogen carrier rate in recruits without respiratory symptoms was very low, and among 795 nasopharyngeal swab samples, only two were adenovirus-positive; they were identified as group C type 1 adenovirus with low virulence.

During the 3 months of training, 5 cases of adenovirus were detected among 39 recruits with fever and respiratory symptoms, indicating that adenovirus is the major causal pathogen for respiratory infectious disease at recruit training sites. According to retrospective studies on respiratory infections in troops during the past 25 years in the USA, the most common ARDs pathogens in troops are adenovirus, influenza (parainfluenza) viruses, respiratory syncytial virus, metapneumovirus, rhinovirus, human coronavirus, mycoplasma pneumonia and Chlamydia pneumonia. As early as the World War I, “Spanish flu” occurred in U.S. troops (1917–1918), and studies exploring the prevention and control of ARDs were initiated and have continued i.e., for approximately 100 years. In China, such surveillance only started 3 years ago. There is still a lack of comprehensive information regarding the spectrum of febrile respiratory diseases. During the Vietnam War period (1965–1970), RSV infection ranked second among the febrile respiratory diseases affecting US troops, surpassed only by adenovirus infection (21.0%). According to a survey, RSV accounts for 0.73% of pathogens of upper respiratory tract infections in Chinese troops, less than the infection rates of mycoplasma pneumonia and Legionella. However, we did not detect RSV positive cases in this investigation, nor did we find metapneumovirus or bocavirus. These viruses are common in upper respiratory tract infections that affected children, but they are less common in Chinese adults [13, 14], which suggests that these pathogens will not be detected in future background investigations and pathogen surveillances.