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Increase in Fitness of Streptococcus pneumoniae Is Associated With the Severity of Necrotizing Pneumonia

Hsieh, Yu-Chia MD, PhD*; Chi, Hsin MD, PhD; Chang, Kuang-Yi MD, PhD‡§; Lai, Shen-Hao MD*; Mu, Jung-Jung PhD; Wong, Kin-Sun MD*; Liu, Ching-Chuan MD; Huang, Yi-Chuan MD**; Lin, Hsiao-Chuan MD††; Chang, Luan-Yin MD, PhD‡‡; Huang, Yhu-Chering MD, PhD*; Huang, Li-Min MD, PhD‡‡for The Taiwan Pediatric Infectious Diseases Alliance

The Pediatric Infectious Disease Journal: May 2015 - Volume 34 - Issue 5 - p 499–505
doi: 10.1097/INF.0000000000000631
Original Studies
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Background: The incidence of necrotizing pneumococcal pneumonia has increased during the past 2 decades. We hypothesized that increased pneumococcal load or augmented inflammatory cytokine production might lead to destructive pneumococcal lung disease.

Methods: This study enrolled prospectively 0- to 18-year-old children with a diagnosis of community-acquired pneumonia with pleural effusion admitted to 6 medical centers from March 2010 to April 2012. Children were diagnosed with pneumococcal empyema if the pleural fluid tested positive for quantitative pneumococcal (lytA) detection by real-time polymerase chain reaction. Pneumococcal empyema cases were further divided into 4 groups according to necrosis severity: (0) nonnecrosis, (1) mild necrosis, (2) cavitation and (3) bronchopleural fistula. Nasopharyngeal and pleural pneumococcal load, as well as levels of proinflammatory cytokines (TNF-α, IL-1β, IL-6, IL-8), Th1-(IL-2, IFN-γ), Th2-(IL-4, IL-10) and Th17-cytokines (IL-17), in the pleural fluid was measured.

Results: Serotypes 19A and 3 accounted for 69.4% and 12.5%, respectively, of 72 cases of pneumococcal empyema. Pleural pneumococcal load was significantly higher in serotypes 19A and 3 infection than in the other strains causing infection (P = 0.006). There was a correlation between nasopharyngeal and pleural pneumococcal load (ρ = 0.35; P = 0.05). In multivariate ordinal logistic regression analysis, pleural pneumococcal load (adjusted odds ratio: 1.79; 95% confidence interval: 1.03–3.06) and IL-8 (adjusted odds ratio: 2.64; 95% confidence interval: 1.21–5.75) were independent factors associated with the severity of lung necrosis.

Conclusions: Evolution of Streptococcus pneumoniae toward increased fitness in their interaction with host and exaggerated IL-8 expression may be responsible for the increase of necrotizing pneumococcal pneumonia.

From the *Department of Pediatrics, Chang Gung Children’s Hospital, Chang Gung Memorial Hospital, College of Medicine, Chang Gung University, Taoyuan, Taiwan; Department of Pediatrics, Mackay Memorial Hospital, Taipei, Taiwan; Division of Biostatistics, Graduate Institute of Epidemiology and Preventive Medicine, National Taiwan University, Taipei, Taiwan; §Department of Anesthesiology, Taipei Veterans General Hospital and National Yang-Ming University School of Medicine, Taipei, Taiwan; Bacterial Enteric and Emerging Diseases Laboratory, Center for Research, Diagnostics and Vaccine Development, Centers for Disease Control, Taipei, Taiwan; Department of Pediatrics, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan; **Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan; ††Department of Pediatrics, China Medical University Hospital, Taichung, Taiwan; and ‡‡Department of Pediatrics, National Taiwan University Hospital, Taipei, Taiwan.

Accepted for publication November 20, 2014.

This work was supported by a grant from the National Science Council, Taiwan, and 2 grants (grant CMRPG4A0091 and CMRPG480023 to Y.C.H.) from the Chang Gung Memorial Hospital.

Y.-C. Huang and L.-M. Huang contributed equally to this article.

Address for correspondence: Yhu-Chering Huang, MD, PhD, Division of Pediatric Infectious Diseases, Department of Pediatrics, Chang Gung children’s Hospital, 5 Fu-Hsin Street, Kwei-Shan Hsiang, Taoyuan County, Taiwan. E-mail: ychuang@adm.cgmh.org.tw; Li-Min Huang, MD, PhD, Department of Pediatrics, National Taiwan University Hospital, 8 Chung-Shan South Road, Taipei 100, Taiwan. E-mail: lmhuang@ntu.edu.tw.

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