etiology and antimicrobial resistance of community-acquired pneumonia in adult patients in china

8/18/2019 Etiology and Antimicrobial Resistance of Community-Acquired Pneumonia in Adult Patients in China

1/7

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/230762148

Etiology and antimicrobial resistance of community-acquired pneumonia in adult

patients in China

ARTICLE in CHINESE MEDICAL JOURNAL · SEPTEMBER 2012

Impact Factor: 1.05 · DOI: 10.3760/cma.j.issn.0366-6999.2012.17.002 · Source: PubMed

CITATIONS

10

READS

134

10 AUTHORS, INCLUDING:

Tao Lili

University of Texas Southwestern Medical …

21 PUBLICATIONS 161 CITATIONS

SEE PROFILE

Available from: Tao Lili

Retrieved on: 04 April 2016

https://www.researchgate.net/?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_1https://www.researchgate.net/profile/Tao_Lili?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_7https://www.researchgate.net/institution/University_of_Texas_Southwestern_Medical_Center?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_6https://www.researchgate.net/profile/Tao_Lili?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_5https://www.researchgate.net/profile/Tao_Lili?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_4https://www.researchgate.net/?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_1https://www.researchgate.net/publication/230762148_Etiology_and_antimicrobial_resistance_of_community-acquired_pneumonia_in_adult_patients_in_China?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_3https://www.researchgate.net/publication/230762148_Etiology_and_antimicrobial_resistance_of_community-acquired_pneumonia_in_adult_patients_in_China?enrichId=rgreq-3e3b8b5f-6bbf-4a4a-9ab8-2462a10fad35&enrichSource=Y292ZXJQYWdlOzIzMDc2MjE0ODtBUzoyMDgzNTk1NTU4OTkzOTJAMTQyNjY4ODE5NzE4OQ%3D%3D&el=1_x_2


2/7

Chinese Medical Journal 2012;125(17):2967-2972 2967

Original article

Etiology and antimicrobial resistance of community-acquired

pneumonia in adult patients in ChinaTAO Li-li, HU Bi-jie, HE Li-xian, WEI Li, XIE Hong-mei, WANG Bao-qing, LI Hua-ying, CHEN Xue-hua,ZHOU Chun-mei and DENG Wei-wu

Keywords: community-acquired infection; pneumonia; etiology; antimicrobial drug resistance; epidemiology

Background Appropriate antimicrobial therapy of community-acquired pneumonia (CAP) is mainly based on the

distribution of etiology and antimicrobial resistance of major pathogens. We performed a prospective observational study

of adult with CAP in 36 hospitals in China.

Methods

Etiological pathogens were isolated in each of the centers, and all of the isolated pathogens were sent to

Zhongshan Hospital for antimicrobial susceptibility tests using agar dilution.

Results A total of 593 patients were enrolled in this study, and 242 strains of bacteria were isolated from 225 patients.Streptococcus pneumoniae (79/242, 32.6%) was the most frequently isolated pathogen, followed by Haemophilus

influenzae (55/242, 22.7%) and Klebsiella pneumoniae (25/242, 10.3%). Totally 527 patients underwent serological tests

for atypical pathogens; Mycoplasma pneumoniae and Chlamydia pneumoniae infections were identified in 205 (38.9%)

and 60 (11.4%) patients respectively. Legionella pneumophila infections were identified in 4.0% (13/324) of patients. The

non-susceptibility rate of isolated Streptococcus pneumoniae to erythromycin and penicillin was 63.2% and 19.1%

respectively. Six patients died from the disease, the 30-day mortality rate was 1.1% (6/533).

Conclusions The top three bacteria responsible for CAP in Chinese adults were Streptococcus pneumonia,

Haemophilus influenza and Klebsiella pneumonia. There was also a high prevalence of atypical pathogens and mixed

pathogens. The resistance rates of the major isolated pathogens were relatively low except for the high prevalence of

macrolide resistance in Streptococcus pneumoniae.

Chin Med J 2012;125(17):2967-2972

ommunity-acquired pneumonia (CAP) remains acommon disease associated with significant

morbidity and mortality. In adults, the incidence variesamong countries from 1.6 to 11 per 1000 adults, and40%–60% of the patients need hospitalization.1 CAP has

been described as a leading cause of death frominfectious diseases.2 Mortality varied from


3/7

Chin Med J 2012;125(17):2967-2972 2968

(Guangzhou, Shenzhen), Liaoning (Shenyang), Shandong(Jinan, Qingdao), Jiangsu (Nanjing, Suzhou, Wuxi),Zhejiang (Hangzhou, Ningbo, Jiaxing), Anhui (Hefei),Jiangxi (Nanchang), Shanxi (Xi’an), Henan (Zhengzhou),Hubei (Wuhan), Hunan (Changsha), Sichuan (Chengdu),and Yunnan (Kunming). Zhongshan Hospital, Fudan

University was responsible for this study. The study wasapproved by ethics committee of each center, andinformed consent was acquired from all the patients.

Study populationAccording to guidelines of the American ThoracicSociety and Society of Respiratory Disease, ChineseMedical Association, CAP was defined as a new or

progressive pulmonary infiltration with/without pleuraleffusion on a chest radiograph and at least one of thefollowing signs or symptoms: (1) new or increasedcough, (2) purulent sputum or a change in sputumcharacteristics, (3) fever or a history of fever (defined asan oral temperature >38°C), (4) auscultatory findings on

pulmonary examination of rales and/or evidence of pulmonary consolidation, (5) peripheral white blood cell(WBC) count ≥10×109/L or immature neutrophils >15%or leukopenia with a total WBC count 25 WBCs and


4/7


Table 1. Summary of characteristics of enrolled patientsCharacteristics Patient number (n (%))*

Symptoms and signsFever 312/523 (59.7)Cough 513/593 (86.5)Purulent sputum 255/532 (42.3)

Leukocytosis >10×109/L 203/532 (38.2)

Mental alteration 10/529 (1.9)Radiological findings

Bilateral infiltration 111/593 (18.7)Cavity 5/593 (0.8)Pleural effusion 41/593 (6.9)

Risk factors

Immune compromised 5/531 (0.9)Long-term smoking 163/533 (30.6)Alcoholism 28/530 (5.3)Residence in nursing home 1/531 (0.2)Recent hospitalization 38/528 (7.2)

Antibiotic therapy within past 3 months 81/531 (15.3)Underlying disease

COPD 88/528 (16.7)

Bronchiectasis 18/532 (3.4)

Heart failure 12/532 (2.3)Chronic kidney disease 1/533 (0.2)Diabetes 14/533 (2.6)

* Parts of the patients do not have an integrated medical history.

Table 2. Etiological distribution of community-acquired pneumonia among 593 adult patients

Pathogens Patient number (n (%))

Mono-infection Mycoplasma pneumoniae 124 (31.1)Streptococcus pneumoniae 48 (12.0) Haemophilus influenzae 31 (7.8)

Chlamydophila pneumoniae 25 (6.3) Klebsiella pneumoniae 13 (3.2)Staphylococcus aureus 10 (2.5)

Pseudomonas aeruginosa 9 (2.3) Legionella pneumophila 5 (1.2) Moraxella catarrhalis

Other bacteria4 (1.0)

23 (5.8)

Mixed infectionTwo pathogens

S. pneumoniae + M. pneumoniae

M. pneumoniae+C. pneumoniae

M. pneumoniae+H. influenzae

Other combination

15 (3.8)13 (3.2)13 (3.2)

51 (12.8)Three pathogens 15 (3.8)

Total 399

Infections with some pathogens were found to relate withthe age of the patient. M. pneumoniae infections weremuch more frequent in young patients than in the elderly(defined as ≥65 years), whereas K. pneumoniae and C. pneumoniae infections were more prevalent in the elderly.In our study, we failed to discover any relationship

between S. pneumoniae infections and the age of the patients (Table 3).

Antimicrobial susceptibility

The results of antimicrobial susceptibility testing for themajor pathogens are summarized in Table 4. Of the 79 S. pneumoniae isolates, 55 (80.9%) were susceptible to penicillin, 7 (10.3%) were intermediate and 6 (8.8%)

were resistant to penicillin. Resistance rate toerythromycin was as high as 63.2% (43/79). In our study,no S. pneumoniae isolate was found to be resistant toamoxicillin or moxifloxacin.

Table 3. The relationship between age and pathogen infections(n (%))

Pathogens Old patients Young patients

Mycoplasma pneumoniae 42/172 (24.4) 163/357 (45.7) †

Streptococcus pneumoniae 31/186 (16.7) 48/407 (11.8)

Haemophilus influenzae 21/186 (11.3) 34/407 (8.4)

Chlamydophila pneumoniae 27/172 (15.7) † 33/357 (9.2)

Klebsiella pneumoniae 13/186 (7.0) * 12/407 (2.9)Staphylococcus aureus 7/186 (3.8) 10/407 (2.5)

Pseudomonas aeruginosa 5/186 (2.7) 9/407 (2.2)

Legionella pneumophila 7/118 (5.9) 6/206(2.9)

Moraxella catarrhalis 6/186 (3.2)* 3/407 (0.7)

The incidence of infection was significantly higher than that in the other age

group, * P


5/7

Chin Med J 2012;125(17):2967-2972 2970

resulted in their death. The other three patients were previously healthy, and they died of respiratory failuredue to the severe infection.

DISCUSSION

This study is the largest, multicenter, prospectiveepidemiological study in China. The results of the studyhighlight several characteristics of CAP in China.

High prevalence of S. pneumoniae as an etiology of

CAP in China

In our study, etiological pathogens were identified in70.9% of cases based on cultures and serological tests.Among identified bacteria, S. pneumoniae was the major

pathogen, as previously reported from other regions.9-11

Prior use of antimicrobial agents can influence theisolation of pathogens and antimicrobial susceptibility.

Lim et al

12

have reported that usage of antimicrobialdrugs before sampling would reduce the isolation of S. pneumoniae significantly. Our study enrolled patientswho had not received any antimicrobial agents for oneweek prior to presentation in order to increase theisolation of bacteria, especially for fastidiousmicroorganisms.

The relatively high incidence of K. pneumoniae pneumonia was observed in our study compared to thefindings of US and European countries, but the result wascoincident with the former studies conducted in Shanghaiand Taiwan.8,13 The selective pressure of antibiotics may

be partly responsible for such a phenomenon.

High prevalence of atypical pathogens and mixed

infections

Many previous studies have reported the high prevalenceof atypical pathogens in CAP, sometimes even higherthan bacterial infections. In our study, serological tests foratypical pathogens had been done for 527 patients.Approximately 38.9% of them were confirmed with M. pneumonia infection, 11.4% with C. pneumonia infection,and 4.0% with L. pneumophila infection. These resultswere comparable with those from other regions.11,14-16

Another meaningful finding from our study was therelatively high incidence of mixed infection by bacteriaand atypical pathogens. Overall, 107 cases of mixedinfections were detected, and 35.6% of cases of M. pneumoniae infection were combined with bacterialinfection. The importance of mixed pathogens in CAP has

been demonstrated by many studies, although theincidence differs from 10% to 38%.12,17,18 Previousstudies have shown that C. pneumoniae inducedciliostasis can influence the normal function of the

bronchial mucosa, and M. pneumoniae can deliver toxinsto ciliated epithelial cells.19 These mechanisms promotemixed infection with bacteria. This epidemiologicalfinding is important in clinical practice because this typeof mixed infection requires combined therapy with

β-lactam agents and macrolides, or monotherapy offluoroquinolones.

Low resistance of antimicrobial agents to major

pathogens of CAP

The spread of penicillin resistant S. pneumoniae (PRSP)

is a big concern worldwide. In America, as much as30%–40% cases of S. pneumonia infection were caused

by penicillin non-susceptible S. pneumonia (PNSSP), and10%–20% were highly resistant to penicillin.20 Asian-Pacific countries have resistance rates as high as60%. In our study, the prevalence of PNSSP was 19.1%,much lower than many international reports, andcomparable to other results reported from China.21

However the prevalence of PRSP (8.8%) was higher thanreported by Sun et al,22 who found an extremely low rateof penicillin resistance (0.5%). The relative low resistantrate in our study might be the result of the exclusion

criteria. We had excluded patients younger than 18 years,and patients who used antimicrobial agents one week prior to presentation. The criteria helped us to improvethe sensitivity of the sputum culture, but might also haveinfluenced the results of drug resistance. Despite lowresistant rate to penicillin, the strains were highlyresistant to macrolides, more than 60% were resistant toerythromycin, clarothromycin and azithromycin.According to the Infectious Diseases Society of America(IDSA)/American Thoracic Society (ATS) guidelines,macrolides are recommended as a monotherapy optionfor treating outpatients with CAP without risk factors.23

However, this may not be an appropriate option in China.

Multi-drug resistance was common in PNSSP isolates,most PNSSP were resistant to macrolides (11/13), and69.2% were resistant to cefaclor. It was a big challenge tochoose antimicrobial agents for isolates which weremulti-drug resistant. The relationship between clinicaloutcome and drug resistance is controversial; the increaseof the drug resistance did not significantly affect thereported mortality in S. pneumoniae infection.24 Severalstudies reported a complex relationship between

penicillin susceptibility and virulence in mice but do notentirely separate these characteristics from the role of the

capsular type. It is probably because penicillin resistanceis related to a loss of virulence.25

All isolated strains of H. influenzae were highlysusceptible to most of antimicrobial agents; few of themwere resistant to amoxicillin and clarithromycin (8.8%and 11.8%). K. penumoniae still had a high susceptibilityto β-lactams, the susceptible rates to ceftriaxone andceftazidime being 91.7% and 95.8% respectively, and allof the isolates were susceptible to ertapenem.

The resistance patterns of atypical pathogens were notcarried out in our study due to the diagnostic methods.Recent studies of atypical pathogens suggested that these

pathogens are highly resistant to macrolides, especially M. pneumoniae.26,27 The molecular mechanisms of such


6/7


resistance mainly involved the modification of the targetsites on the 23S rRNA by methylation or mutation, aswell as on the efflux pump.28,29

Relatively low overall mortality of CAP

The overall mortality rate in our study was 1.1%, while

studies from other countries showed a mortality rate ofabout 4% in outpatients,3 4%–10% in hospitalized

patients,12 and ANSORP reported an overall mortalityrate of 7.3%,9 much higher than our study. The lowmortality rate may involve the exclusion criteria. Weexcluded patients who received antimicrobial agents inthe previous week, so the enrolled patients were inrelatively good condition, concomitant with lessunderlying disease and had lower PORT classifications.

The prognosis of CAP was influenced by many factors.The British Thoracic Society has proposed the CURB-65

criteria to evaluate the prognosis of pneumonia.

30

Jinks etal31 considers liver function as a predictive factor of the prognosis. He found that patients with hypoalbuminemiaand elevated ALT correlated with a higher mortality rate.

Trend of etiology in CAP

The etiology of CAP is different between countries andchanges over time. The application of nucleic acidamplification technology for epidemiological studies hasled to a new understanding of etiology in CAP.32,33 Viruses should be considered as the pathogen causingCAP due to its high prevalence. Our study focused on the

bacteria pathogens of CAP, so it was the limitation that

viruses were not tested. Increasingly reported numbers ofinfections by S. aureus, especially methicillin resistant S.aureus (MRSA), is also a major concern.34 The highvirulence of the bacteria and lack of effectiveantimicrobial agents result in a high mortality rate ofMRSA pneumonia, yet in our study, the prevalence of S.aureus was low, and did not lead to any death.

In conclusion, our study provides a better understandingof etiology, clinical and laboratory characteristics,antimicrobial susceptibility, along with outcome of CAPin China. These results may benefit clinicians to choose

antimicrobial agents and determine the prognosis of CAP.

Acknowledgements: We are grateful to the following people and

hospitals for their participation in the study: Beijing Union Hospital

(CAI Bai-qiang, CAO Bing, XU Ying-chun, XIE Xiu-li), Beijing

Hospital (SUN Tie-ying, ZHANG Xiu-zheng, PU Chun, HU

Yun-jian), Peking University Third Hospital (YAO Wan-zhen,

WANG Xiao-hong, HAO Zhen-ting), Shanghai Ruijin Hospital

(DENG Wei-wu, LI Min, SUN Jing-yong), Shanghai Renji

Hospital (LI Yan-qin, XIONG Li-fan), Shanghai Changhai Hospital

(HUANG Yi, WANG Jin), Sixth Hospital of Shanghai (SHEN Ce,

JIANG Yan-qun), Tianjin Medical University General Hospital

(WU Qi, HU Zhi-dong, ZHAO Li-hong), Guangzhou Institute of

Respiratory Diseases (CHEN Rong-chang, ZHONG Su-qin, YUAN

Jin-ping, LI De-rong), Third Affiliated Hospital of Sun Yat-sen

University (ZHANG Tian-tuo, ZHU Jia-xing), Guangzhou First

Municipal People’s Hospital (ZENG Jun, YE Hui-fen, ZHONG

Wei-nong), Shenzhen People’s Hospital (CHEN Sheng-wen, FU

Ying-yun, WU Wei-yuan), First Hospital of China Medical

University (LI Yan-ling, LI Zhen-hua, LI Meng), Second Hospital

of China Medical University (LI Sheng-qi, LIU Yong, ZHANG

Zhe-jie), Qilu Hospital of Shandong University (WU Da-wei, YU

Xiu-jian), Affiliated Hospital of Qingdao University (CHENGZhao-zhong, LIU Peng-peng), Nanjing General Hospital of

Nanjing Military Command (SI Yi, SHAO Hai-feng, XIAO

Yong-ying), Jiangsu Province Hospital (YIN Kai-sheng, HUANG

Mao, ZHAO Wang-sheng), First Affiliated Hospital of Soochow

University (HUANG Jian-an, ZHANG Xian-feng, JIANG

Jun-hong), Wuxi No. 2 People’s Hospital (LI Xian-cun, YAN

Zi-he), First Affiliated Hospital of Zhejiang University School of

Medicine (WANG Xue-feng, KONG Hai-shen), Second Affiliated

Hospital of Zhejiang University School of Medicine (WANG

Xuan-ding, YUAN Shuang-jin), Zhejiang Provincial People’s

Hospital (YAN Jian-ping, LÜ Huo-yang), Ningbo No. 2 Hospital

(ZHAO Wei-he, MA Jian-bo, CHEN Lin, XU Xiao-min), FirstHospital of Jiaxing (ZHUANG Yan-bing, SONG Xiu-lan), First

Affiliated Hospital of Anhui Medical University (SUN Geng-yun,

XU Yuan-hong, HE Jie-gui), First Affiliated Hospital of Nanchang

University (WEN Gui-lan, MIU Wan-zheng, LIU Qin), Xijing

Hospital (LI Zhi-kui XU Xiu-li, YANG Pei-hong), First Affiliated

Hospital of Zhengzhou University (WANG Jing, FENG Xian-ju),

Union Hospital, Huazhong University of Science and Technology

(XIN Jian-bo, ZHOU Xian-qin, DAI Li-ren, LIU Ying, XIONG

Yan), Tongji Hospital, Huazhong University of Science and

Technology (XIONG Sheng-dao, SUN Zi-yong), Xiangya Hospital

of Central South University (HU Cheng-ping, LI Xian, PAN

Pin-hua), Second Xiangya Hospital of Central South University

(CHEN Ping, CAO Wei, CHEN Yan, LI Wen-pu), West ChinaCenter of Medical Sciences (LÜ Xiao-ju, LIANG Zong-an, FAN

Hong, CHEN Zhi-xing), First Affiliated Hospital of Kunming

Medical College (HAO Qing-lin, SHEN Bing, LIU Ling).

REFERENCES

1. Polverino E, Torres Marti A. Community-acquired

pneumonia. Minerva anestesiologica 2011; 77: 196-211.

2. Apisarnthanarak A, Mundy LM. Etiology of

community-acquired pneumonia. Clin Chest Med 2005; 26:

47-55.

3. Welte T, Torres A, Nathwani D. Clinical and economic burden of community-acquired pneumonia among adults in

Europe. Thorax 2012; 67: 71-79.

4. Niederman MS, McCombs JS, Unger AN, Kumar A,

Popovian R. The cost of treating community-acquired

pneumonia. Clin Ther 1998; 20: 820-837.

5. Monte SV, Paolini NM, Slazak EM, Schentag JJ, Paladino

JA. Costs of treating lower respiratory tract infections. Am J

Manag Care 2008; 14: 190-196.

6. Carbonara S, Monno L, Longo B, Angarano G.

Community-acquired pneumonia. Curr Opin Pulm Med 2009;

15: 261-273.

7. Liu Y, Chen M, Zhao T, Wang H, Wang R, Cai B, et al.

Causative agent distribution and antibiotic therapy

assessment among adult patients with community acquired

pneumonia in Chinese urban population. BMC Infect Dis


7/7

Chin Med J 2012;125(17):2967-2972 2972

2009; 9: 31.

8. Huang HH, Zhang YY, Xiu QY, Zhou X, Huang SG, Lu Q, et

al. Community-acquired pneumonia in Shanghai, China:

microbial etiology and implications for empirical therapy in a

prospective study of 389 patients. Eur J Clin Microbiol Infect

Dis 2006; 25: 369-374.

9. Song JH, Oh WS, Kang CI, Chung DR, Peck KR, Ko KS, etal. Epidemiology and clinical outcomes of

community-acquired pneumonia in adult patients in Asian

countries: a prospective study by the Asian network for

surveillance of resistant pathogens. Int J Antimicrob Agents

2008; 31: 107-114.

10. Köksal I, Ozlü T, Bayraktar O, Yılmaz G, Bülbül Y, Oztuna F,

et al. Etiological agents of community-acquired pneumonia in

adult patients in Turkey; a multicentric, cross-sectional study.

Tuberk Toraks 2010; 58: 119-127.

11. Cillóniz C, Ewig S, Polverino E, Marcos MA, Esquinas C,

Gabarrús A, et al. Microbial aetiology of

community-acquired pneumonia and its relation to severity.Thorax 2011; 66: 340-346.

12. Lim WS, Macfarlane JT, Boswell TC, Harrison TG, Rose D,

Leinonen M, et al. Study of community acquired pneumonia

aetiology (SCAPA) in adults admitted to hospital:

implications for management guidelines. Thorax 2001; 56:

296-301.

13. Lin YT, Jeng YY, Chen TL, Fung CP. Bacteremic

community-acquired pneumonia due to Klebsiella

pneumoniae: clinical and microbiological characteristics in

Taiwan, 2001–2008. BMC Infect Dis 2010; 10: 307.

14. Wattanathum A, Chaoprasong C, Nunthapisud P,

Chantaratchada S, Limpairojn N, Jatakanon A, et al.

Community-acquired pneumonia in southeast Asia: themicrobial differences between ambulatory and hospitalized

patients. Chest 2003; 123: 1512-1519.

15. Thibodeau KP, Viera AJ. Atypical pathogens and challenges

in community-acquired pneumonia. Am Fam Physician 2004;

69: 1699-1706.

16. Woodhead M. Community-acquired pneumonia in Europe:

causative pathogens and resistance patterns. Eur Respir J

Suppl 2002; 36: 20s-27s.

17. Kauppinen MT, Herva E, Kujala P, Leinonen M, Saikku P,

Syrjälä H. The etiology of community-acquired pneumonia

among hospitalized patients during a Chlamydia pneumoniae

epidemic in Finland. J Infect Dis 1995; 172: 1330-1335.18. De Roux A, Ewig S, García E, Marcos MA, Mensa J, Lode

H, et al. Mixed community-acquired pneumonia in

hospitalised patients. Eur Respir J 2006; 27: 795-800.

19. Shemer-Avni Y, Lieberman D. Chlamydia

pneumoniae-induced ciliostasis in ciliated bronchial epithelial

cells. J Infect Dis 1995; 171: 1274-1278.

20. Hoban DJ, Biedenbach DJ, Mutnick AH, Jones RN. Pathogen

of occurrence and susceptibility patterns associated with

pneumonia in hospitalized patients in North America: results

of the SENTRY Antimicrobial Surveillance Study (2000).

Diagn Microbiol Infect Dis 2003; 45: 279-285.

21. Yang F, Xu XG, Yang MJ, Zhang YY, Klugman KP, McGee

L. Antimicrobial susceptibility and molecular epidemiology

of Streptococcus pneumoniae isolated from Shanghai, China.

Int J Antimicrob Agents 2008; 32: 386-391.

22. Sun HL, Wang H, Chen MJ, Liu YM, Hu ZD, Liao K, et al.

An antimicrobial resistance surveillance of gram-positive

cocci isolated from 12 teaching hospitals in China in 2009.

Chin J Intern Med (Chin) 2010; 49: 735-740.

23. Mandell LA, Wunderink RG, Anzueto A, Bartlett JG,

Campbell GD, Dean NC, et al. Infectious Diseases Society ofAmerica/American Thoracic Society consensus guidelines on

the management of community-acquired pneumonia in

adults. Clin Infect Dis 2007; 44 Suppl 2: S27-S72.

24. Lynch JP, Zhanel GG. Streptococcus pneumoniae: does

antimicrobial resistance matter? Semin Respir Crit Care Med

2009; 30: 210-238.

25. Azoulay-Dupuis E, Rieux V, Muffat-Joly M, Bédos JP, Vallée

E, Rivier C, et al. Relationship between capsular type,

penicillin susceptibility, and virulence of human

Streptococcus pneumoniae isolates in mice. Antimicrob

Agents Chemother 2000; 44: 1575-1577.

26. Cao B, Zhao CJ, Yin YD, Zhao F, Song SF, Bai L, et al. High prevalence of macrolide resistance in Mycoplasma

pneumoniae isolates from adult and adolescent patients with

respiratory tract infection in China. Clin Infect Dis 2010; 51:

189-194.

27. Miyashita N, Oka M, Group AP, Kawai Y, Yamaguchi T,

Ouchi K. Macrolide-resistant Mycoplasma pneumoniae in

adults with community-acquired pneumonia. Int J Antimicrob

Agents 2010; 36: 384-385.

28. Morozumi M, Takahashi T, Ubukata K. Macrolide-resistant

Mycoplasma pneumoniae: characteristics of isolates and

clinical aspects of community-acquired pneumonia. J Infect

Chemother 2010; 16: 78-86.

29. Xin D, Mi Z, Han X, Qin L, Li J, Wei T, et al. Molecularmechanisms of macrolide resistance in clinical isolates of

Mycoplasma pneumoniae from China. Antimicrob Agents

Chemother 2009; 53: 2158-2159.

30. British Thoracic Society Standards of Care Committee. BTS

Guidelines for the Management of Community Acquired

Pneumonia in Adults. Thorax 2001; 56 Suppl 4: IV1-IV64.

31. Jinks MF, Kelly CA. The pattern and significance of

abnormal liver function tests in community-acquired

pneumonia. Eur J Intern Med 2004; 15: 436-440.

32. Lieberman D, Shimoni A, Shemer-Avni Y, Keren-Naos A,

Shtainberg R, Lieberman D. Respiratory viruses in adults

with community-acquired pneumonia. Chest 2010; 138:811-816.

33. Cao B, Ren LL, Zhao F, Gonzalez R, Song SF, Bai L, et al.

Viral and Mycoplasma pneumoniae community-acquired

pneumonia and novel clinical outcome evaluation in

ambulatory adult patients in China. Eur J Clin Microbiol

Infect Dis 2010; 29: 1443-1448.

34. Dean N. Methicillin-resistant Staphylococcus aureus in

community-acquired and health care-associated pneumonia:

incidence, diagnosis, and treatment options. Hosp Pract

(Minneap) 2010; 38: 7-15.

(Received December 21, 2011) Edited by WANG Mou-yue and LIU Huan

etiology and antimicrobial resistance of community-acquired pneumonia in adult patients in china

Documents