Abstract
As a cause of vulvovaginitis in prepubertal girls, Streptococcus pyogenes (S. pyogenes) is commonly isolated from vaginal introitus swabs. Studies have identified several risk factors, but have not focused on the correlation between ambient air pollutants and S. pyogenes-induced vulvovaginitis in prepubertal girls. This study was conducted to determine whether ambient air pollutants were associated with S. pyogenes-induced vulvovaginitis in prepubertal girls. Daily data about S. pyogenes-induced vulvovaginitis in prepubertal girls from the outpatient department of Children’s Hospital at the Zhejiang University School of Medicine in Hangzhou City between January 1, 2015, and December 31, 2018, were retrospectively reviewed. Ambient air pollutants in Hangzhou were measured daily. A generalized additive model (GAM) was utilized to assess the associations between daily air pollutants and S. pyogenes isolates obtained from vaginal introitus swabs of prepubertal girls. The mean daily concentration of nitrogen dioxide (NO2) in Hangzhou City during the study period was 44.6 μg/m3 (25th–75th percentiles, 32.0–56.0 μg/m3). The GAM showed that the largest estimate effects in S. pyogenes-induced vulvovaginitis in prepubertal girls were found in NO2 with a moving (accumulative) average on day 3. The excess risk of NO2 in terms of the daily number of S. pyogenes isolates obtained from the vaginal introitus swabs was 14.91% (95% confidence interval [CI]: 4.85–25.94%) in the single-pollutant model. The multipollutant model revealed that an increase of 10 μg/m3 in NO2 exposure was associated with an 18.33% increased risk for acquiring S. pyogenes-induced vulvovaginitis in prepubertal girls (95% CI: 1.21–38.35%; P < 0.05). In conclusion, short-term NO2 exposure was strongly associated with the spread of S. pyogenes-induced vulvovaginitis in prepubertal girls.
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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Brugha R, Grigg J (2014) Urban air pollution and respiratory infections. Paediatr Respir Rev 15:194–199. https://doi.org/10.1016/j.prrv.2014.03.001
Bumbuliene Z, Venclaviciute K, Ramasauskaite D, Arlauskiene A, Bumbul E, Drasutiene G (2014) Microbiological findings of vulvovaginitis in prepubertal girls. Postgrad Med J 90:8–12. https://doi.org/10.1136/postgradmedj-2013-131959
Carugno M, Dentali F, Mathieu G, Fontanella A, Mariani J, Bordini L, Milani GP, Consonni D, Bonzini M, Bollati V, Pesatori AC (2018) PM10 exposure is associated with increased hospitalizations for respiratory syncytial virus bronchiolitis among infants in Lombardy, Italy. Environ Res 166:452–457. https://doi.org/10.1016/j.envres.2018.06.016
Chauhan AJ, Inskip HM, Linaker CH, Smith S, Schreiber J, Johnston SL, Holgate ST (2003) Personal exposure to nitrogen dioxide (NO2) and the severity of virus-induced asthma in children. Lancet 361:1939–1944. https://doi.org/10.1016/s0140-6736(03)13582-9
Chen Y, Zang L, du W, Xu D, Shen G, Zhang Q, Zou Q, Chen J, Zhao M, Yao D (2018) Ambient air pollution of particles and gas pollutants, and the predicted health risks from long-term exposure to PM2.5 in Zhejiang province, China. Environ Sci Pollut Res 25:23833–23844. https://doi.org/10.1007/s11356-018-2420-5
Ciencewicki J, Jaspers I (2007) Air pollution and respiratory viral infection. Inhal Toxicol 19:1135–1146. https://doi.org/10.1080/08958370701665434
Feng W, Li H, Wang S, van Halm-Lutterodt N, An J, Liu Y, Liu M, Wang X, Guo X (2019) Short-term PM10 and emergency department admissions for selective cardiovascular and respiratory diseases in Beijing, China. Sci Total Environ 657:213–221. https://doi.org/10.1016/j.scitotenv.2018.12.066
Gasparrini A (2011) Distributed lag linear and non-linear models in: The package. J Stat Soft 43:1–20. http://www.jstatsoft.org/v43/i08/
Gu S, Yang J, Woodward A, Li M, He T, Wang A, Lu B, Liu X, Xu G, Liu Q (2017) The short-term effects of visibility and haze on mortality in a coastal city of China: a time-series study. Int J Environ Res Public Health 14:1419. https://doi.org/10.3390/ijerph14111419
Hashemzadeh B, Idani E, Goudarzi G, Ankali KA, Sakhvidi MJZ, Akbar Babaei A, Hashemzadeh H, Vosoughi M, Mohammadi MJ, Neisi A (2019) Effects of PM2.5 and NO2 on the 8-isoprostane and lung function indices of FVC and FEV1 in students of Ahvaz city, Iran. Saudi J Biol Sci 26:473–480. https://doi.org/10.1016/j.sjbs.2016.11.008
Hassan A, Latif MT, Soo CI, Faisal AH, Roslina AM, Andrea YLB, Hassan T (2017) Short communication: diagnosis of lung cancer increases during the annual southeast Asian haze periods. Lung Cancer 113:1–3. https://doi.org/10.1016/j.lungcan.2017.08.025
Kowalska M, Skrzypek M, Kowalski M, Cyrys J (2020) Effect of NOx and NO2 concentration increase in ambient air to daily bronchitis and asthma exacerbation, Silesian Voivodeship in Poland. Int J Environ Res Public Health 17. https://doi.org/10.3390/ijerph17030754
Mei L, Guan P, Kong Z (2017) Remote sensing of atmospheric NO2 by employing the continuous-wave differential absorption lidar technique. Opt Express 25:A953–A962. https://doi.org/10.1364/OE.25.00A953
Muller WJ, Schmitt BD (2004) Group A beta-hemolytic streptococcal vulvovaginitis: diagnosis by rapid antigen testing. Clin Pediatr 43:179–183. https://doi.org/10.1177/000992280404300208
Nenna R et al (2017) Respiratory syncytial virus bronchiolitis, weather conditions and air pollution in an Italian urban area: an observational study. Environ Res 158:188–193. https://doi.org/10.1016/j.envres.2017.06.014
Randelovic G et al (2012) Microbiological aspects of vulvovaginitis in prepubertal girls. Eur J Pediatr 171:1203–1208. https://doi.org/10.1007/s00431-012-1705-9
Stricker T, Navratil F, Sennhauser FH (2003) Vulvovaginitis in prepubertal girls. Arch Dis Child 88:324–326. https://doi.org/10.1136/adc.88.4.324
Tao Y, Mi S, Zhou S, Wang S, Xie X (2014) Air pollution and hospital admissions for respiratory diseases in Lanzhou, China. Environ Pollut 185:196–201. https://doi.org/10.1016/j.envpol.2013.10.035
Verstraelen H, Verhelst R, Vaneechoutte M, Temmerman M (2011) Group A streptococcal vaginitis: an unrecognized cause of vaginal symptoms in adult women. Arch Gynecol Obstet 284:95–98. https://doi.org/10.1007/s00404-011-1861-6
Xu H, Bechle MJ, Wang M, Szpiro AA, Vedal S, Bai Y, Marshall JD (2019) National PM2.5 and NO2 exposure models for China based on land use regression, satellite measurements, and universal kriging. Sci Total Environ 655:423–433. https://doi.org/10.1016/j.scitotenv.2018.11.125
Yang B-Y et al (2018a) Ambient air pollution in relation to diabetes and glucose-homoeostasis markers in China: a cross-sectional study with findings from the 33 Communities Chinese Health Study. Lancet Planet Health 2:e64–e73. https://doi.org/10.1016/s2542-5196(18)30001-9
Yang B et al (2018b) On-road chemical transformation as an important mechanism of NO2 formation. Environ Sci Technol 52:4574–4582. https://doi.org/10.1021/acs.est.7b05648
Zeng W et al (2020) Association between NO2 cumulative exposure and influenza prevalence in mountainous regions: a case study from southwest China. Environ Res 189:109926. https://doi.org/10.1016/j.envres.2020.109926
Zhan Y, Luo Y, Deng X, Zhang K, Zhang M, Grieneisen ML, Di B (2018) Satellite-based estimates of daily NO2 exposure in China using hybrid random forest and spatiotemporal kriging model. Environ Sci Technol 52:4180–4189. https://doi.org/10.1021/acs.est.7b05669
Zheng PW, Wang JB, Zhang ZY, Shen P, Chai PF, Li D, Jin MJ, Tang ML, Lu HC, Lin HB, Chen K (2017) Air pollution and hospital visits for acute upper and lower respiratory infections among children in Ningbo, China: a time-series analysis. Environ Sci Pollut Res Int 24:18860–18869. https://doi.org/10.1007/s11356-017-9279-8
Zhu Y, Zhan Y, Wang B, Li Z, Qin Y, Zhang K (2019) Spatiotemporally mapping of the relationship between NO2 pollution and urbanization for a megacity in Southwest China during 2005-2016. Chemosphere 220:155–162. https://doi.org/10.1016/j.chemosphere.2018.12.095
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CF takes responsibility for conception and writing the manuscript. ZZ takes responsibility for analysis of data. MZ contributed to acquisition and interpretation of data. JL and XC take responsibility for reviewing and editing the manuscript. All authors read and approved the final manuscript.
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This work was approved by the ethics committee of the Children’s Hospital, Zhejiang University School of Medicine, China (2019-IRB-074). The requirement of informed consent was waived, because anonymized and de-identified data collected from medical and laboratory records were used.
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Fang, C., Zhou, Z., Li, J. et al. Short-term nitrogen dioxide exposure is associated with the spread of S. pyogenes-induced vulvovaginitis in prepubertal girls in Hangzhou, China. Environ Sci Pollut Res 28, 35790–35797 (2021). https://doi.org/10.1007/s11356-021-13268-z
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DOI: https://doi.org/10.1007/s11356-021-13268-z