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1.  Trends in the Susceptibility of Clinically Important Resistant Bacteria to Tigecycline: Results from the Tigecycline In Vitro Surveillance in Taiwan Study, 2006 to 2010 
The Tigecycline In Vitro Surveillance in Taiwan (TIST) study, a nationwide, prospective surveillance during 2006 to 2010, collected a total of 7,793 clinical isolates, including methicillin-resistant Staphylococcus aureus (MRSA) (n = 1,834), penicillin-resistant Streptococcus pneumoniae (PRSP) (n = 423), vancomycin-resistant enterococci (VRE) (n = 219), extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (n = 1,141), ESBL-producing Klebsiella pneumoniae (n = 1,330), Acinetobacter baumannii (n = 1,645), and Stenotrophomonas maltophilia (n = 903), from different specimens from 20 different hospitals in Taiwan. MICs of tigecycline were determined following the criteria of the U.S. Food and Drug Administration (FDA) and the European Committee on Antimicrobial Susceptibility Testing (EUCAST-2011). Among drug-resistant Gram-positive pathogens, all of the PRSP isolates were susceptible to tigecycline (MIC90, 0.03 μg/ml), and only one MRSA isolate (MIC90, 0.5 μg/ml) and three VRE isolates (MIC90, 0.125 μg/ml) were nonsusceptible to tigecycline. Among the Gram-negative bacteria, the tigecycline susceptibility rates were 99.65% for ESBL-producing E. coli (MIC90, 0.5 μg/ml) and 96.32% for ESBL-producing K. pneumoniae (MIC90, 2 μg/ml) when interpreted by FDA criteria but were 98.7% and 85.8%, respectively, when interpreted by EUCAST-2011 criteria. The susceptibility rate for A. baumannii (MIC90, 4 μg/ml) decreased from 80.9% in 2006 to 55.3% in 2009 but increased to 73.4% in 2010. A bimodal MIC distribution was found among carbapenem-susceptible A. baumannii isolates, and a unimodal MIC distribution was found among carbapenem-nonsusceptible A. baumannii isolates. In Taiwan, tigecycline continues to have excellent in vitro activity against several major clinically important drug-resistant bacteria, with the exception of A. baumannii.
PMCID: PMC3294947  PMID: 22203598
2.  Agreement Assessment of Tigecycline Susceptibilities Determined by the Disk Diffusion and Broth Microdilution Methods among Commonly Encountered Resistant Bacterial Isolates: Results from the Tigecycline In Vitro Surveillance in Taiwan (TIST) Study, 2008 to 2010 
The Tigecycline In Vitro Surveillance in Taiwan (TIST) study, initiated in 2006, is a nationwide surveillance program designed to longitudinally monitor the in vitro activity of tigecycline against commonly encountered drug-resistant bacteria. This study compared the in vitro activity of tigecycline against 3,014 isolates of clinically important drug-resistant bacteria using the standard broth microdilution and disk diffusion methods. Species studied included methicillin-resistant Staphylococcus aureus (MRSA; n = 759), vancomycin-resistant Enterococcus faecium (VRE; n = 191), extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (n = 602), ESBL-producing Klebsiella pneumoniae (n = 736), and Acinetobacter baumannii (n = 726) that had been collected from patients treated between 2008 and 2010 at 20 hospitals in Taiwan. MICs and inhibition zone diameters were interpreted according to the currently recommended U.S. Food and Drug Administration (FDA) criteria and the European Committee on Antimicrobial Susceptibility Testing (EUCAST) criteria. The MIC90 values of tigecycline against MRSA, VRE, ESBL-producing E. coli, ESBL-producing K. pneumoniae, and A. baumannii were 0.5, 0.125, 0.5, 2, and 8 μg/ml, respectively. The total error rates between the two methods using the FDA criteria were high: 38.4% for ESBL-producing K. pneumoniae and 33.8% for A. baumannii. Using the EUCAST criteria, the total error rate was also high (54.6%) for A. baumannii isolates. The total error rates between these two methods were <5% for MRSA, VRE, and ESBL-producing E. coli. For routine susceptibility testing of ESBL-producing K. pneumoniae and A. baumannii against tigecycline, the broth microdilution method should be used because of the poor correlation of results between these two methods.
PMCID: PMC3294924  PMID: 22155819
3.  Increase of Carbapenem-Resistant Acinetobacter baumannii Infection in Acute Care Hospitals in Taiwan: Association with Hospital Antimicrobial Usage 
PLoS ONE  2012;7(5):e37788.
Carbapenem-resistant Acinetobacter baumannii (CRAB) has emerged as an important pathogen causing healthcare-associated infections (HAIs) in Taiwan. The present study is aimed to investigate the epidemiology of HAIs caused by CRAB and the association of CRAB infection and hospital usage of different antimicrobials.
Two nationwide databases in the period 2003 to 2008, the Taiwan Nosocomial Infection Surveillance System and National Health Insurance claim data, were used for analysis. A total of 13,811 healthcare-associated A. baumannii infections and antimicrobial usage data from 121 hospitals were analyzed.
There was a significant increase in the proportion of number of HAIs caused by CRAB over that by all A. baumannii (CRABpAB), from 14% in 2003 to 46% in 2008 (P<0.0001). The greatest increase was in central Taiwan, from 4% in 2003 to 62% in 2008 (P<0.0001). Use of anti-pseudomonal carbapenems, but not other classes of antibiotics, was significantly correlated with the increase of CRABpAB (r = 0.86, P<0.0001).
We suggested that dedicated use of anti-pseudomonal carbapenems would be an important intervention to control the increase of CRABpAB.
PMCID: PMC3357347  PMID: 22629456
4.  Dissemination of imipenem-resistant Acinetobacter baumannii with new plasmid-borne blaOXA-72 in Taiwan 
BMC Infectious Diseases  2013;13:319.
The systemic surveillance of imipenem-resistant Acinetobacter baumannii (IRAB) from multicenters in Taiwan revealed the emergence of isolates with blaOXA-72. This study described their genetic makeup, mechanism of spread, and contribution to carbapenem resistance.
Two hundred and ninety-one non-repetitive isolates of A. baumannii were collected from 10 teaching hospitals from different geographical regions in Taiwan from June 2007 to September 2007. Minimal inhibitory concentrations (MICs) were determined by agar dilution. Clonality was determined by pulsed-field gel electrophoresis. Plasmid was extracted and digested by restriction enzymes, and subsequently analyzed by electrophoresis and Southern blot for blaOXA-72. The flanking regions of blaOXA-72 were determined by inverse PCR. The contribution of blaOXA-72 to imipenem MIC was determined by transforming plasmids carrying blaOXA-72 into imipenem-susceptible A. baumannii.
Among 142 IRAB in Taiwan, 27 harbored blaOXA-72; 22 originated from Southern Taiwan, 5 from Central Taiwan, and none from Northern Taiwan. There were two major clones. The blaOXA-72 was identified in the plasmids of all isolates. Two genetic structures flanking plasmid-borne blaOXA-72 were identified and shared identical sequences in certain regions; the one described in previous literature was present in only one isolate, and the new one was present in the remaining isolates. Introduction of blaOXA-72 resulted in an increase of imipenem MIC in the transformants. The overexpression of blaOXA-72 mRNA in response to imipenem further supported the contribution of blaOXA-72.
In conclusion, isolates with new plasmid-borne blaOXA-72 were found to be disseminated successfully in Southern Taiwan. The spread of the resistance gene depended on clonal spread and dissemination of a new plasmid. BlaOXA-72 in these isolates directly led to their imipenem-resistance.
PMCID: PMC3728158  PMID: 23849336
Imipenem-resistant; Acinetobacter baumannii; Carbapenemase; BlaOXA-72
5.  Significant Reduction of Antibiotic Use in the Community after a Nationwide Campaign in France, 2002–2007 
PLoS Medicine  2009;6(6):e1000084.
Didier Guillemot and colleagues describe the evaluation of a nationwide programme in France aimed at decreasing unnecessary outpatient prescriptions for antibiotics. The campaign was successful, particularly in reducing prescriptions for children.
Overuse of antibiotics is the main force driving the emergence and dissemination of bacterial resistance in the community. France consumes more antibiotics and has the highest rate of beta-lactam resistance in Streptococcus pneumoniae than any other European country. In 2001, the government initiated “Keep Antibiotics Working”; the program's main component was a campaign entitled “Les antibiotiques c'est pas automatique” (“Antibiotics are not automatic”) launched in 2002. We report the evaluation of this campaign by analyzing the evolution of outpatient antibiotic use in France 2000–2007, according to therapeutic class and geographic and age-group patterns.
Methods and Findings
This evaluation is based on 2000–2007 data, including 453,407,458 individual reimbursement data records and incidence of flu-like syndromes (FLSs). Data were obtained from the computerized French National Health Insurance database and provided by the French Sentinel Network. As compared to the preintervention period (2000–2002), the total number of antibiotic prescriptions per 100 inhabitants, adjusted for FLS frequency during the winter season, changed by −26.5% (95% confidence interval [CI] −33.5% to −19.6%) over 5 years. The decline occurred in all 22 regions of France and affected all antibiotic therapeutic classes except quinolones. The greatest decrease, −35.8% (95% CI −48.3% to −23.2%), was observed among young children aged 6–15 years. A significant change of −45% in the relationship between the incidence of flu-like syndromes and antibiotic prescriptions was observed.
The French national campaign was associated with a marked reduction of unnecessary antibiotic prescriptions, particularly in children. This study provides a useful method for assessing public-health strategies designed to reduce antibiotic use.
Editors' Summary
In 1928, Alexander Fleming discovered penicillin, the first antibiotic (a drug that kills bacteria). By the early 1940s, large amounts of penicillin could be made and, in the following decades, several other classes of powerful antibiotics were discovered. For a time, it looked like bacteria and the diseases that they cause had been defeated. But bacteria rapidly became resistant to these wonder drugs and nowadays, antibiotic resistance is a pressing public-health concern. Almost every type of disease-causing bacteria has developed resistance to one or more antibiotic in clinical use, and multidrug-resistant bacteria are causing outbreaks of potentially fatal diseases in hospitals and in the community. For example, multidrug-resistant Streptococcus pneumoniae (multidrug-resistant pneumococci or MRP) is now very common. S. pneumoniae colonize the nose and throat (the upper respiratory tract) and can cause diseases that range from mild ear infections to life-threatening pneumonia, particularly in young children and elderly people.
Why Was This Study Done?
For years, doctors have been prescribing (and patients have been demanding) antibiotics for viral respiratory infections (VRIs) such as colds and flu even though antibiotics do not cure viral infections. This overuse of antibiotics has been the main driving force in the spread of MRP. Thus, the highest rate of S. pneumoniae antibiotic resistance in Europe occurs in France, which has one of the highest rates of antibiotic consumption in the world. In 2001 France initiated “le plan national pour préserver l'efficacité des antibiotiques” to reduce the inappropriate use of antibiotics, particularly for the treatment of VRIs among children. The main component of the program was the “Antibiotiques c'est pas automatique” (“Antibiotics are not automatic”) campaign, which ran from 2002 to 2007 during the winter months when VRIs mainly occur. The campaign included an educational campaign for health care workers, the promotion of rapid tests for diagnosis of streptococcal infections, and a public information campaign about VRIs and about antibiotic resistance. In this study, the researchers evaluate the campaign by analyzing outpatient antibiotic use throughout France from 2000 to 2007.
What Did the Researchers Do and Find?
The researchers obtained information about antibiotic prescriptions and about the occurrence of flu-like illnesses during the study period from the French National Health Insurance database and national disease surveillance system, respectively. After adjusting for variations in the frequency of flu-like illnesses, compared to the preintervention period (2000–2002), the number of antibiotic prescriptions per 100 inhabitants decreased by a quarter over the five winters of the “Antibiotics are not automatic” campaign. The use of all major antibiotic classes except quinolones decreased in all 22 regions of France. Thus, whereas in 2000, more than 70 prescriptions per 100 inhabitants were issued during the winter in 15 regions, by 2006/7, no regions exceeded this prescription rate. The greatest decrease in prescription rate (a decrease of more than a third by 2006/7) was among children aged 6–15 years. Finally, although the rates of antibiotic prescriptions reflected the rates of flu-like illness throughout the campaign, by 2006/7 this relationship was much weaker, which suggests that fewer antibiotics were being prescribed for VRIs.
What Do These Findings Mean?
These findings indicate that the “Antibiotics are not automatic” campaign was associated with a reduction in antibiotic prescriptions, particularly in children. Because the whole French population was exposed to the campaign, these findings do not prove that the campaign actually caused the reduction in antibiotic prescriptions. The observed decrease might have been caused by other initiatives in France or elsewhere or by the introduction of a S. pneumoniae vaccine during the study period, for example. However, an independent survey indicated that fewer members of the public expected an antibiotic prescription for a VRI at the end of the campaign than at the start, that more people knew that antibiotics only kill bacteria, and that doctors were more confident about not prescribing antibiotics for VRIs. Thus, campaigns like “Antibiotics are not automatic” may be a promising way to reduce the overuse of antibiotics and to slow the spread of antibiotic resistance until new classes of effective antibiotics are developed.
Additional Information
Please access these Web sites via the online version of this summary at
This study is further discussed in a PLoS Medicine Perspective by Stephen Harbarth and Benedikt Huttner
The Bugs and Drugs Web site from the UK National electronic Library of Infection provides information about antibiotic resistance and links to other resources
The US National Institute of Allergy and Infectious Diseases provides information on antimicrobial drug resistance and on pneumococcal pneumonia
The US Centers for Disease Control and Prevention also have information on antibiotic resistance (in English and Spanish)
The European Surveillance of Antimicrobial Consumption Web site provides information on antibiotic consumption in European countries
Les antibiotiques c'est pas automatique provides information about the “Antibiotics are not automatic” campaign (in French)
Information on the Plan National pour Pérserver l'efficacité des antibiotiques is also available (in French)
PMCID: PMC2683932  PMID: 19492093
6.  Changes in HIV Incidence among People Who Inject Drugs in Taiwan following Introduction of a Harm Reduction Program: A Study of Two Cohorts 
PLoS Medicine  2014;11(4):e1001625.
Kenrad Nelson and colleagues report on the association between HIV incidence and exposure to a national harm-reduction program among people who inject drugs in Taiwan.
Please see later in the article for the Editors' Summary
Harm reduction strategies for combating HIV epidemics among people who inject drugs (PWID) have been implemented in several countries. However, large-scale studies using sensitive measurements of HIV incidence and intervention exposures in defined cohorts are rare. The aim of this study was to determine the association between harm reduction programs and HIV incidence among PWID.
Methods and Findings
The study included two populations. For 3,851 PWID who entered prison between 2004 and 2010 and tested HIV positive upon incarceration, we tested their sera using a BED HIV-1 capture enzyme immunoassay to estimate HIV incidence. Also, we enrolled in a prospective study a cohort of 4,357 individuals who were released from prison via an amnesty on July 16, 2007. We followed them with interviews at intervals of 6–12 mo and by linking several databases. A total of 2,473 participants who were HIV negative in January 2006 had interviews between then and 2010 to evaluate the association between use of harm reduction programs and HIV incidence. We used survival methods with attendance at methadone clinics as a time-varying covariate to measure the association with HIV incidence. We used a Poisson regression model and calculated the HIV incidence rate to evaluate the association between needle/syringe program use and HIV incidence. Among the population of PWID who were imprisoned, the implementation of comprehensive harm reduction programs and a lower mean community HIV viral load were associated with a reduced HIV incidence among PWID. The HIV incidence in this population of PWID decreased from 18.2% in 2005 to 0.3% in 2010. In an individual-level analysis of the amnesty cohort, attendance at methadone clinics was associated with a significantly lower HIV incidence (adjusted hazard ratio: 0.20, 95% CI: 0.06–0.67), and frequent users of needle/syringe program services had lower HIV incidence (0% in high NSP users, 0.5% in non NSP users). In addition, no HIV seroconversions were detected among prison inmates.
Although our data are affected by participation bias, they strongly suggest that comprehensive harm- reduction services and free treatment were associated with reversal of a rapidly emerging epidemic of HIV among PWID.
Please see later in the article for the Editors' Summary
Editors' Summary
About 35 million people worldwide are currently infected with HIV, the virus that causes AIDS, and about 2.3 million people become newly infected every year. HIV is mainly transmitted through unprotected sex with an infected partner. However, people who inject drugs (PWID) have a particularly high risk of HIV infection because blood transfer through needle and syringe sharing can transmit the virus. It is estimated that 5%–10% of all people living with HIV are PWID. Indeed, in some regions of the world the primary route of HIV transmission is through shared drug injection equipment and the prevalence (the proportion of a population that has a specific disease) of HIV infection among PWID is very high. In Asia, for example, more than a quarter of PWID are HIV positive. Because the high prevalence of HIV among PWID poses a global health challenge, bodies such as the Joint United Nations Programme on HIV/AIDS endorse harm reduction strategies to prevent risky injection behaviors among PWID. These strategies include the provision of clean needles and syringes, opioid substitution therapy such as methadone maintenance treatment, and antiretroviral treatment for HIV-positive PWID.
Why Was This Study Done?
Although harm reduction strategies for combating HIV epidemics among PWID have been implemented in several countries, few large-scale studies have examined the association between HIV incidence (the proportion of new cases of HIV in a population per year) and exposure to harm reduction programs among PWID. In this cohort study (an investigation that determines the characteristics of a group of people and then follows them over time), the researchers determine the association between harm reduction programs and HIV incidence among PWID in Taiwan. HIV infections used to be rare among the 60,000 PWID living in Taiwan, but after the introduction of a new HIV strain into the country in 2003, an HIV epidemic spread rapidly. In response, the Taiwanese government introduced a pilot program of harm reduction that included the provision of clean needles and syringes and health education in July 2005. The program was expanded to include methadone maintenance treatment in early 2006 and implemented nationwide in June 2006.
What Did the Researchers Do and Find?
The researchers enrolled two study populations. The first cohort comprised 3,851 PWID who were incarcerated for illicit drug use between 2004 and 2010 and who tested positive for HIV upon admission into prison. By using the BED assay, which indicates whether an HIV infection is recent, the researchers were able to determine the HIV incidence among the prisoners. In 2004, the estimated HIV incidence among prisoners with a history of drug injection was 6.44%. The incidence peaked in 2005 at 18.2%, but fell to 0.3% in 2010.
The second study population comprised 2,473 individuals who were HIV negative on January 1, 2006, and who had been incarcerated for drug use crimes but were released on July 16, 2007, during an amnesty. The researchers regularly interviewed these participants between their release and 2010 about their use of harm reduction interventions, and obtained other data about them (for example, diagnosis of HIV infection) from official databases. Analysis of all these data indicated that, in this cohort, attendance at methadone maintenance treatment clinics and frequent use of needle and syringe services were both associated with a significantly lower HIV incidence.
What Do These Findings Mean?
These findings suggest that the introduction of a comprehensive harm reduction program in Taiwan was associated with a significant reduction in the HIV incidence rate among PWID. These findings must be interpreted with caution, however. First, because the participants in the study were selected from PWID with histories of incarceration, the findings may not be representative of all PWID in Taiwan or of PWID in other countries. Second, PWID who chose to use needle and syringe services or methadone maintenance treatment clinics might have shared other unknown characteristics that affected their risk of HIV infection. Finally, some of the reduction in HIV incidence seen during the study is likely to be associated with the availability of free treatment, which has been offered to all HIV-positive individuals in Taiwan since 1997. Despite these limitations, these findings suggest that countries with a high prevalence and incidence of HIV among PWID should provide comprehensive harm reduction services to their populations to reduce risky drug injection behaviors.
Additional Information
Please access these websites via the online version of this summary at
Information is available from the US National Institute of Allergy and Infectious diseases on HIV infection and AIDS
NAM/aidsmap provides basic information about HIV/AIDS, and summaries of recent research findings on HIV care and treatment
Information is available from Avert, an international AIDS charity, on many aspects of HIV/AIDS, including information on injecting drug users and HIV/AIDS and on harm reduction and HIV prevention (in English and Spanish)
The US National Institute on Drug Abuse also provides information about drug abuse and HIV/AIDS (in English and Spanish)
The 2013 UNAIDS World AIDS Day report provides up-to-date information about the AIDS epidemic and efforts to halt it
Personal stories about living with HIV/AIDS are available through Avert, Nam/aidsmap, and Healthtalkonline
PMCID: PMC3979649  PMID: 24714449
7.  Regional Changes in Charcoal-Burning Suicide Rates in East/Southeast Asia from 1995 to 2011: A Time Trend Analysis 
PLoS Medicine  2014;11(4):e1001622.
Using a time trend analysis, Ying-Yeh Chen and colleagues examine the evidence for regional increases in charcoal-burning suicide rates in East and Southeast Asia from 1995 to 2011.
Please see later in the article for the Editors' Summary
Suicides by carbon monoxide poisoning resulting from burning barbecue charcoal reached epidemic levels in Hong Kong and Taiwan within 5 y of the first reported cases in the early 2000s. The objectives of this analysis were to investigate (i) time trends and regional patterns of charcoal-burning suicide throughout East/Southeast Asia during the time period 1995–2011 and (ii) whether any rises in use of this method were associated with increases in overall suicide rates. Sex- and age-specific trends over time were also examined to identify the demographic groups showing the greatest increases in charcoal-burning suicide rates across different countries.
Methods and Findings
We used data on suicides by gases other than domestic gas for Hong Kong, Japan, the Republic of Korea, Taiwan, and Singapore in the years 1995/1996–2011. Similar data for Malaysia, the Philippines, and Thailand were also extracted but were incomplete. Graphical and joinpoint regression analyses were used to examine time trends in suicide, and negative binomial regression analysis to study sex- and age-specific patterns. In 1995/1996, charcoal-burning suicides accounted for <1% of all suicides in all study countries, except in Japan (5%), but they increased to account for 13%, 24%, 10%, 7%, and 5% of all suicides in Hong Kong, Taiwan, Japan, the Republic of Korea, and Singapore, respectively, in 2011. Rises were first seen in Hong Kong after 1998 (95% CI 1997–1999), followed by Singapore in 1999 (95% CI 1998–2001), Taiwan in 2000 (95% CI 1999–2001), Japan in 2002 (95% CI 1999–2003), and the Republic of Korea in 2007 (95% CI 2006–2008). No marked increases were seen in Malaysia, the Philippines, or Thailand. There was some evidence that charcoal-burning suicides were associated with an increase in overall suicide rates in Hong Kong, Taiwan, and Japan (for females), but not in Japan (for males), the Republic of Korea, and Singapore. Rates of change in charcoal-burning suicide rate did not differ by sex/age group in Taiwan and Hong Kong but appeared to be greatest in people aged 15–24 y in Japan and people aged 25–64 y in the Republic of Korea. The lack of specific codes for charcoal-burning suicide in the International Classification of Diseases and variations in coding practice in different countries are potential limitations of this study.
Charcoal-burning suicides increased markedly in some East/Southeast Asian countries (Hong Kong, Taiwan, Japan, the Republic of Korea, and Singapore) in the first decade of the 21st century, but such rises were not experienced by all countries in the region. In countries with a rise in charcoal-burning suicide rates, the timing, scale, and sex/age pattern of increases varied by country. Factors underlying these variations require further investigation, but may include differences in culture or in media portrayals of the method.
Please see later in the article for the Editors' Summary
Editors' Summary
Every year, almost one million people die by suicide globally; suicide is the fifth leading cause of death in women aged 15–49 and the sixth leading cause of death in men in the same age group. Most people who take their own life are mentally ill. For others, stressful events (the loss of a partner, for example) have made life seem worthless or too painful to bear. Strategies to reduce suicide rates include better treatment of mental illness and programs that help people at high risk of suicide deal with stress. Suicide rates can also be reduced by limiting access to common suicide methods. These methods vary from place to place. Hanging is the predominant suicide method in many countries, but in Hong Kong, for example, jumping from a high building is the most common method. Suicide methods also vary over time. For example, after a woman in Hong Kong took her life in 1998 by burning barbecue charcoal in a sealed room (a process that produces the toxic gas carbon monoxide), charcoal burning rapidly went from being a rare method of killing oneself in Hong Kong to the second most common suicide method.
Why Was This Study Done?
Cases of charcoal-burning suicide have also been reported in several East and Southeast Asian countries, but there has been no systematic investigation of time trends and regional patterns of this form of suicide. A better understanding of regional changes in the number of charcoal-burning suicides might help to inform efforts to prevent the emergence of other new suicide methods. Here, the researchers investigate the time trends and regional patterns of charcoal-burning suicide in several countries in East and Southeast Asia between 1995 and 2011 and ask whether any rises in the use of this method are associated with increases in overall suicide rates. The researchers also investigate sex- and age-specific time trends in charcoal-burning suicides to identify which groups of people show the greatest increases in this form of suicide across different countries.
What Did the Researchers Do and Find?
The researchers analyzed method-specific data on suicide deaths for Hong Kong, Japan, the Republic of Korea, Taiwan, and Singapore between 1995/1996 and 2011 obtained from the World Health Organization Mortality Database and from national death registers. In 1995/1996, charcoal-burning suicides accounted for less than 1% of all suicides in all these countries except Japan (4.9%). By 2011, charcoal-burning suicides accounted for between 5% (Singapore) and 24% (Taiwan) of all suicides. Rises in the rate of charcoal-burning suicide were first seen in Hong Kong in 1999, in Singapore in 2000, in Taiwan in 2001, in Japan in 2003, and in the Republic of Korea in 2008. By contrast, incomplete data from Malaysia, the Philippines, and Thailand showed no evidence of a marked increase in charcoal-burning suicide in these countries over the same period. Charcoal-burning suicides were associated with an increase in overall suicide rates in Hong Kong in 1998–2003, in Taiwan in 2000–2006, and in Japanese women after 2003. Finally, the annual rate of change in charcoal-burning suicide rate did not differ by sex/age group in Taiwan and Hong Kong, whereas in Japan people aged 15–24 and in the Republic of Korea people aged 25–64 tended to have the greatest rates of increase.
What Do These Findings Mean?
These findings show that charcoal-burning suicides increased markedly in several but not all East and Southeast Asian countries during the first decade of the 21st century. Moreover, in countries where there was an increase, the timing, scale, and sex/age pattern of the increase varied by country. The accuracy of these findings is likely to be limited by several aspects of the study. For example, because of the way that method-specific suicides are recorded in the World Health Organization Mortality Database and national death registries, the researchers may have slightly overestimated the number of charcoal-burning suicides. Further studies are now needed to identify the factors that underlie the variations between countries in charcoal-burning suicide rates and time trends reported here. However, the current findings highlight the need to undertake surveillance to identify the emergence of new suicide methods and the importance of policy makers, the media, and internet service providers working together to restrict graphic and detailed descriptions of new suicide methods.
Additional Information
Please access these websites via the online version of this summary at
A PLOS Medicine research article by Shu-Sen Chang and colleagues investigates time trends and regional patterns of charcoal-burning suicide in Taiwan
The World Health Organization provides information on the global burden of suicide and on suicide prevention (in several languages); it also has an article on international patterns in methods of suicide
The US National Institute of Mental Health provides information on suicide and suicide prevention
The UK National Health Service Choices website has detailed information about suicide and its prevention
MedlinePlus provides links to further resources about suicide (in English and Spanish)
The International Association for Suicide Prevention provides links to crisis centers in Asia
The charity Healthtalkonline has personal stories about dealing with suicide
PMCID: PMC3972087  PMID: 24691071
8.  Molecular Characterization and Antimicrobial Susceptibility of Streptococcus pneumoniae Isolated from Children Hospitalized with Respiratory Infections in Suzhou, China 
PLoS ONE  2014;9(4):e93752.
Dissemination of antibiotic resistant clones is recognized as an important factor in the emergence and prevalence of resistance in pneumococcus. This study was undertaken to survey the antimicrobial susceptibility and serotypes distribution of pneumococci and to explore the circulating clones in hospitalized children in Suzhou, China.
The pneumococci were isolated from the nasopharyngeal aspirates of children less than 5 years of age admitted to Soochow-University-Affiliated-Children's-Hospital with respiratory infections. The capsular serotypes were identified by multiplex polymerase chain reaction (PCR). Antimicrobial susceptibility was tested by E-test. The presence of ermB, mefA/E genes were detected by PCR and the genotypes were explored by Multilocus sequence typing (MLST).
From July 2012 to July 2013, a total of 175 pneumococcal isolates were collected and all strains were resistant to erythromycin and clindamycin, about 39.4% strains were non-susceptible to penicillin G. Overall, 174 (99.4%) isolates were resistant to ≥3 types of antibiotics. Serotypes 19F (28.1%), 6B (19.7%), 19A (18.0%), and 23F (17.4%) were the most common serotypes in all identified strains. The serotypes coverage of PCV7 and PCV13 were 71.9% and 89.9%, respectively. Four international antibiotic-resistant clones, including Taiwan19F-14 (n = 79), Spain23F-1(n = 25), Taiwan23F-15(n = 7) and Spain6B-2(n = 7), were identified. The Taiwan19F-14 clones have a higher non-susceptibility rate in β-lactams than other clones and non-clone isolates (p<0.001). In addition, 98.7% Taiwan19F-14 clones were positive of both ermB and mefA/E genes, compare to 33.3% in other clones and non-clone strains.
The spread of international antibiotic-resistant clones, especially Taiwan19F-14 clones, played a predominant role in the dissemination of antimicrobial resistant isolates in Suzhou, China. Considering the high prevalence of PCV7 serotypes and serotype 19A, the introduction of PCV13 may be a promising preventive strategy to control the increasing trend of clonal spread in China.
PMCID: PMC3977860  PMID: 24710108
9.  The Evolution of the Epidemic of Charcoal-Burning Suicide in Taiwan: A Spatial and Temporal Analysis 
PLoS Medicine  2010;7(1):e1000212.
Shu-Sen Chang and colleagues describe the epidemiology of an epidemic of suicide by charcoal burning in Taiwan and discuss possible reasons for its spread.
An epidemic of carbon monoxide poisoning suicide by burning barbecue charcoal has occurred in East Asia in the last decade. We investigated the spatial and temporal evolution of the epidemic to assess its impact on the epidemiology of suicide in Taiwan.
Methods and Findings
Age-standardised rates of suicide and undetermined death by charcoal burning were mapped across townships (median population aged 15 y or over = 27,000) in Taiwan for the periods 1999–2001, 2002–2004, and 2005–2007. Smoothed standardised mortality ratios of charcoal-burning and non-charcoal-burning suicide and undetermined death across townships were estimated using Bayesian hierarchical models. Trends in overall and method-specific rates were compared between urban and rural areas for the period 1991–2007. The epidemic of charcoal-burning suicide in Taiwan emerged more prominently in urban than rural areas, without a single point of origin, and rates of charcoal-burning suicide remained highest in the metropolitan regions throughout the epidemic. The rural excess in overall suicide rates prior to 1998 diminished as rates of charcoal-burning suicide increased to a greater extent in urban than rural areas.
The charcoal-burning epidemic has altered the geography of suicide in Taiwan. The observed pattern and its changes in the past decade suggest that widespread media coverage of this suicide method and easy access to barbecue charcoal may have contributed to the epidemic. Prevention strategies targeted at these factors, such as introducing and enforcing guidelines on media reporting and restricting access to charcoal, may help tackle the increase of charcoal-burning suicides.
Please see later in the article for the Editors' Summary
Editors' Summary
Every year, about a million people take their own lives. Most people who die by suicide are mentally ill but some people take their lives because stressful events (the loss of a partner, for example) have made life seem worthless or too painful to bear. Strategies to reduce suicide rates include better treatment of mental illness and programs that help people at high risk of suicide deal with stress. Suicide rates can also be reduced by limiting access to common suicide methods. These methods differ from place to place. Hanging is the predominant suicide method in many countries but, in Hong Kong, for example, jumping from a high building is the commonest method. Suicide methods also vary over time. In 1998, a woman in Hong Kong took her life by burning barbecue charcoal in a sealed room (a process that produces high levels of the toxic gas carbon monoxide). This method was unheard of before and was extensively reported by the mass media; by the end of 2004, charcoal-burning suicide became the second most common form of suicide in Hong Kong.
Why Was This Study Done?
The epidemic of charcoal-burning suicide that started in Hong Kong has rapidly spread to other countries in East Asia, including Taiwan, where it is also now the second most common method of suicide. It would be useful to identify the factors that have contributed to the spread of this particular form of suicide because such knowledge might help to improve strategies for preventing charcoal-burning suicide. One way to identify these factors is to examine the space–time clustering of charcoal-burning suicides. Clustering of specific types of suicides in both time and space usually occurs in settings such as institutions where the individuals who die by suicide have been in social contact. By contrast, clustering of specific types of suicide in time more than place is often associated with media coverage of events such as celebrity suicides, which can lead to imitative suicides. In this study, therefore, the researchers investigate the evolution of the epidemic of charcoal-burning suicide over time and across areas in Taiwan.
What Did the Researchers Do and Find?
The researchers obtained data on suicides and undetermined deaths (most “missed” suicides are recorded as undetermined deaths) from 1999 to 2007 from the Taiwan Department of Health. They then used statistical methods to estimate the standardized mortality rates (the ratio of the observed to the expected numbers of deaths) of charcoal-burning and non-charcoal-burning suicides and undetermined deaths in different areas of Taiwan. The proportion of suicides that were charcoal-burning suicides rose from 0.1% in 1991 to 26.6% in 2007, they report, and the epidemic of charcoal-burning suicide was more marked in urban than in rural areas. However, there was no single point of origin of the epidemic. Finally, they report, rates of charcoal-burning suicide were consistently higher in urban than in rural areas throughout the study period, a result that means that, although overall suicide rates were higher in rural than in urban regions of Taiwan prior to the epidemic of charcoal-burning suicide, the difference has now almost disappeared.
What Do These Findings Mean?
These findings suggest that the epidemic of charcoal-burning suicide may underlie recent changes in the geography of suicide in Taiwan. However, the study's findings may not be numerically accurate because of some of the assumptions made by the researchers. For example, there is no specific code for charcoal-burning suicides in official records so the researchers assumed that suicides classified as “poisoning using nondomestic gas” were all charcoal-burning suicides, although other studies have shown that nearly 90% of deaths in the category were indeed charcoal-burning suicides. Nevertheless, the observed geographical pattern of charcoal-burning suicides and the changes in this pattern over time suggest that widespread media coverage and easy access to barbecue coal in supermarkets and convenience stores may have contributed to the epidemic of charcoal-burning suicide and to the increase in overall suicide rate in Taiwan and elsewhere in East Asia. Thus, guidelines that encourage responsible media reporting of charcoal-burning suicide (that is, reporting that does not contain detailed descriptions of the method or suggest that this type of suicide is easy and painless) and strategies that restrict access to barbecue charcoal may help to halt the epidemic of charcoal-burning suicide in East Asia.
Additional Information
Please access these Web sites via the online version of this summary at
Another PLoS Medicine research article by David Studdert and colleagues investigates the relationship between changes in vehicle emissions laws and the incidence of suicide by motor vehicle exhaust gas in Australia
The World Health Organization provides information on the global burden of suicide and on suicide prevention (in several languages); see also the article Methods of Suicide: International Suicide Patterns Derived from the WHO Mortality Database
The US National Institute of Mental Health provides information on suicide and suicide prevention
The UK National Health Service Choices website has detailed information about suicide and its prevention
MedlinePlus provides links to further resources about suicide (in English and Spanish)
The Taiwan Suicide Prevention Center provides information on suicide and its prevention in Taiwan (in Chinese)
The Centre for Suicide Research and Prevention, the University of Hong Kong, provides information on suicide and its prevention in Hong Kong (in Chinese and English)
PMCID: PMC2794367  PMID: 20052273
10.  Telithromycin and Quinupristin-Dalfopristin Resistance in Clinical Isolates of Streptococcus pyogenes: SMART Program 2001 Data 
This study evaluated the current status of antimicrobial resistance in clinical isolates of Streptococcus pyogenes in Taiwan as part of the SMART (Surveillance from Multicenter Antimicrobial Resistance in Taiwan) program. In 2001, 419 different isolates of S. pyogenes, including 275 from respiratory secretions, 87 from wound pus, and 31 from blood, were collected from nine hospitals in different parts of Taiwan. MICs of 23 antimicrobial agents were determined at a central location by the agar dilution method. All of the isolates were susceptible to penicillin (MIC at which 90% of the isolates were inhibited [MIC90], ≤0.03 μg/ml), cefotaxime (MIC90, ≤0.03 μg/ml), cefepime (MIC90, 0.06 μg/ml), meropenem (MIC90, ≤0.03 μg/ml), moxifloxacin (MIC90, 0.25 μg/ml), vancomycin (MIC90, 0.5 μg/ml), and linezolid (MIC90, 1 μg/ml). Overall, 78% of isolates were not susceptible to erythromycin (54% were intermediate, and 24% were resistant), and 5% were not susceptible to clindamycin. Of the 101 erythromycin-resistant isolates, 80.2% exhibited the M phenotype (mefA gene positive), 18.9% exhibited the cMLS (constitutive resistance to macrolides-lincosamides-streptogramin B [MLS]) phenotype (ermB gene positive), and 1% exhibited the iMLS (inducible resistance to MLS) phenotype (ermB gene positive). Fluoroquinolones (sitafloxacin > moxifloxacin > ciprofloxacin = levofloxacin = gatifloxacin > gemifloxacin) demonstrated potent activity against nearly all of the isolates of S. pyogenes tested. Thirty-two isolates (8%) were not susceptible to quinupristin-dalfopristin. Seventeen percent of isolates had telithromycin MICs of ≥1 μg/ml, and all of these isolates exhibited erythromycin MICs of ≥32 μg/ml. The high prevalence of resistance to telithromycin (which is not available in Taiwan) limits its potential use in the treatment of S. pyogenes infections, particularly in areas with high rates of macrolide resistance.
PMCID: PMC161833  PMID: 12821461
11.  Establishing a nationwide emergency department-based syndromic surveillance system for better public health responses in Taiwan 
BMC Public Health  2008;8:18.
With international concern over emerging infectious diseases (EID) and bioterrorist attacks, public health is being required to have early outbreak detection systems. A disease surveillance team was organized to establish a hospital emergency department-based syndromic surveillance system (ED-SSS) capable of automatically transmitting patient data electronically from the hospitals responsible for emergency care throughout the country to the Centers for Disease Control in Taiwan (Taiwan-CDC) starting March, 2004. This report describes the challenges and steps involved in developing ED-SSS and the timely information it provides to improve in public health decision-making.
Between June 2003 and March 2004, after comparing various surveillance systems used around the world and consulting with ED physicians, pediatricians and internal medicine physicians involved in infectious disease control, the Syndromic Surveillance Research Team in Taiwan worked with the Real-time Outbreak and Disease Surveillance (RODS) Laboratory at the University of Pittsburgh to create Taiwan's ED-SSS. The system was evaluated by analyzing daily electronic ED data received in real-time from the 189 hospitals participating in this system between April 1, 2004 and March 31, 2005.
Taiwan's ED-SSS identified winter and summer spikes in two syndrome groups: influenza-like illnesses and respiratory syndrome illnesses, while total numbers of ED visits were significantly higher on weekends, national holidays and the days of Chinese lunar new year than weekdays (p < 0.001). It also identified increases in the upper, lower, and total gastrointestinal (GI) syndrome groups starting in November 2004 and two clear spikes in enterovirus-like infections coinciding with the two school semesters. Using ED-SSS for surveillance of influenza-like illnesses and enteroviruses-related infections has improved Taiwan's pandemic flu preparedness and disease control capabilities.
Taiwan's ED-SSS represents the first nationwide real-time syndromic surveillance system ever established in Asia. The experiences reported herein can encourage other countries to develop their own surveillance systems. The system can be adapted to other cultural and language environments for better global surveillance of infectious diseases and international collaboration.
PMCID: PMC2249581  PMID: 18201388
12.  Current Status of Antimicrobial Resistance in Taiwan 
Emerging Infectious Diseases  2002;8(2):132-137.
While some trends in antimicrobial resistance rates are universal, others appear to be unique for specific regions. In Taiwan, the strikingly high prevalence of resistance to macrolides and streptogramin in clinical isolates of gram-positive bacteria correlates with the widespread use of these agents in the medical and farming communities, respectively. The relatively low rate of enterococci that are resistant to glycopeptide does not parallel the high use of glycopeptides and extended-spectrum beta-lactams in hospitals. The evolving problem of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates is substantial, and some unique enzymes have been found. Recently, some gram-negative bacteria (e.g., Pseudomonas aeruginosa and Acinetobacter baumannii) that are resistant to all available antimicrobial agents including carbapenems have emerged.
PMCID: PMC3369580  PMID: 11897063
antimicrobial resistance; Taiwan
13.  Telithromycin- and Fluoroquinolone-Resistant Streptococcus pneumoniae in Taiwan with High Prevalence of Resistance to Macrolides and β-Lactams: SMART Program 2001 Data 
There is a high prevalence of β-lactam- and macrolide-resistant Streptococcus pneumoniae in Taiwan. To understand the in vitro susceptibilities of recent isolates of S. pneumoniae to fluoroquinolones and telithromycin (which is not available in Taiwan), the MICs of 23 antimicrobial agents for 936 clinical isolates of S. pneumoniae isolated from different parts of Taiwan from 2000 to 2001 were determined by the agar dilution method. Overall, 72% of isolates were not susceptible to penicillin (with 61% being intermediate and 11% being resistant) and 92% were resistant to erythromycin. Telithromycin MICs were ≥1 μg/ml for 16% of the isolates, and for 99% of these isolates the MICs of all macrolides tested were ≥256 μg/ml; all of these isolates had the constitutive macrolide-lincosamide-streptogramin B phenotype. Eighty-eight percent of the isolates were resistant to three or more classes of drugs. The ciprofloxacin MICs were ≥4 μg/ml for six (0.6%) isolates from five patients collected in 2000 and 2001, and the levofloxacin MICs were ≥8 μg/ml for five of these isolates. Seven isolates for which ciprofloxacin MICs were ≥4 μg/ml, including one isolate recovered in 1999, belonged to three serotypes (serotype 19F, five isolates; serotype 23A, one isolate; and serotype 23B, one isolate). The isolates from the six patients for which ciprofloxacin MICs were ≥4 μg/ml had different pulsed-field gel electrophoresis profiles and random amplified polymorphic DNA patterns, indicating that no clonal dissemination occurred over this time period. Despite the increased rate of fluoroquinolone use, the proportion of pneumococcal isolates for which ciprofloxacin MICs were elevated (≥4 μg/ml) remained low. However, the occurrence of telithromycin resistance is impressive and raises concerns for the future.
PMCID: PMC161856  PMID: 12821460
14.  Molecular Epidemiology of Integron-Associated Antimicrobial Gene Cassettes in the Clinical Isolates of Acinetobacter baumannii from Northern Taiwan 
Annals of Laboratory Medicine  2013;33(4):242-247.
The aims of this study were to understand the molecular epidemiology of integron-associated gene cassettes in Acinetobacter baumannii across four hospitals in northern Taiwan and to clarify the relationship between the presence of integrons and antibiotic-resistant phenotypes.
Sixty-five A. baumannii isolates, collected from the patients of four regional hospitals in northern Taiwan in 2009, were tested for the presence of integrons and their associated gene cassettes. The susceptibility difference between integron-positive and integron-negative A. baumannii strains was analyzed. Antibiotic-resistant phenotypes among A. baumannii with different types of gene cassette array combinations were also compared.
Around 72% of the A. baumannii isolates carried class 1 integrase genes. Despite this, only three gene cassette arrays were found in the integrons. Integron-positive strains were significantly more resistant to all the tested antibiotics than the integrase-negative strains. All the four types of A. baumannii with different gene cassette array combinations were multidrug-resistant in nature. Gene cassette array aacA4-catB8-aadA1 existed in all the integron-positive A. baumannii isolates. Repetitive-sequence-based PCR (rep-PCR) results revealed the prevalence of one major cluster of imipenem-resistant A. baumannii strains (84%) in the four regional hospitals.
The presence of integrons with associated antimicrobial resistance gene cassettes can be used as a representative marker of multidrug resistance in A. baumannii. Some prevalent gene cassette arrays may exist among epidemiologically unrelated A. baumannii strains.
PMCID: PMC3698301  PMID: 23826559
Acinetobacter baumannii; Integron; Antimicrobial
15.  Complete Genome Analysis of Three Acinetobacter baumannii Clinical Isolates in China for Insight into the Diversification of Drug Resistance Elements 
PLoS ONE  2013;8(6):e66584.
The emergence and rapid spreading of multidrug-resistant Acinetobacter baumannii strains has become a major health threat worldwide. To better understand the genetic recombination related with the acquisition of drug-resistant elements during bacterial infection, we performed complete genome analysis on three newly isolated multidrug-resistant A. baumannii strains from Beijing using next-generation sequencing technology.
Methodologies/Principal Findings
Whole genome comparison revealed that all 3 strains share some common drug resistant elements including carbapenem-resistant blaOXA-23 and tetracycline (tet) resistance islands, but the genome structures are diversified among strains. Various genomic islands intersperse on the genome with transposons and insertions, reflecting the recombination flexibility during the acquisition of the resistant elements. The blood-isolated BJAB07104 and ascites-isolated BJAB0868 exhibit high similarity on their genome structure with most of the global clone II strains, suggesting these two strains belong to the dominant outbreak strains prevalent worldwide. A large resistance island (RI) of about 121-kb, carrying a cluster of resistance-related genes, was inserted into the ATPase gene on BJAB07104 and BJAB0868 genomes. A 78-kb insertion element carrying tra-locus and blaOXA-23 island, can be either inserted into one of the tniB gene in the 121-kb RI on the chromosome, or transformed to conjugative plasmid in the two BJAB strains. The third strains of this study, BJAB0715, which was isolated from spinal fluid, exhibit much more divergence compared with above two strains. It harbors multiple drug-resistance elements including a truncated AbaR-22-like RI on its genome. One of the unique features of this strain is that it carries both blaOXA-23 and blaOXA-58 genes on its genome. Besides, an Acinetobacter lwoffii adeABC efflux element was found inserted into the ATPase position in BJAB0715.
Our comparative analysis on currently completed Acinetobacter baumannii genomes revealed extensive and dynamic genome organizations, which may facilitate the bacteria to acquire drug-resistance elements into their genomes.
PMCID: PMC3691203  PMID: 23826102
16.  The trend of susceptibilities to amphotericin B and fluconazole of Candida species from 1999 to 2002 in Taiwan 
Candida species have various degrees of susceptibility to common antifungal drugs. The extent of resistance to amphotericin B and fluconazole of Candida glabrata isolates causing candidemia has been reported. Active surveillance may help us to monitor the trend of susceptibility to antifungal drugs and to determine if there is an emerging co-resistance to both drugs of Candida species, specifically, of C. glabrata in Taiwan.
The susceptibilities to amphotericin B and fluconazole of Candida species collected in 1999 and 2002 of the Taiwan Surveillance of Antimicrobial Resistance of Yeasts (TSARY) were determined by the microdilution method.
The antifungal susceptibilities of 342 and 456 isolates collected from 11 hospitals participating in both TSARY 1999 and TSARY 2002, respectively, have been determined. The resistance rate to amphotericin B has increased from 0.3% in the TSARY1999 to 2.2% in the TSARY 2002. In contrast, the resistance rate to fluconazole has decreased from 8.8% to 2.2%. Nevertheless, significantly more C. glabrata isolates were not susceptible to fluconazole in the TSARY 2002 (47.4%) than that in the TSARY 1999 (20.8%). There were 9.8% and 11% of C. glabrata isolates having susceptible-dose dependent and resistant phenotype to fluconazole in the TSARY 1999, verse 45.3% and 2.1% in the TSARY 2002.
There was an increase of resistance rate to amphotericin B in C. glabrata. On the other hand, although the resistance rate to fluconazole has decreased, almost half of C. glabrata isolates were not susceptible to this drug. Hence, continuous monitoring the emerging of co-resistance to both amphotericin B and fluconazole of Candida species, specifically, of C. glabrata, will be an important early-warning system.
PMCID: PMC1298299  PMID: 16266438
17.  Comparison of Genospecies and Antimicrobial Resistance Profiles of Isolates in the Acinetobacter calcoaceticus-Acinetobacter baumannii Complex from Various Clinical Specimens 
Antimicrobial Agents and Chemotherapy  2012;56(12):6267-6271.
This study was conducted to compare the prevalences of antimicrobial resistance profiles of clinical isolates in the Acinetobacter calcoaceticus-Acinetobacter baumannii complex from sterile and nonsterile sites and to further study the relationship of antimicrobial resistance profiles and genospecies by amplified rRNA gene restriction analysis (ARDRA). A total of 1,381 isolates were tested with 12 different antibiotics to show their antimicrobial susceptibility profiles. A total of 205 clinical isolates were further analyzed by ARDRA of the intergenic spacer (ITS) region of the 16S-23S rRNA gene. It was found that the overall percentage of isolates from nonsterile sites (urine, sputum, pus, or catheter tip) that were resistant to the 12 antibiotics tested was significantly higher than that of isolates from sterile sites (cerebrospinal fluid [CSF], ascites fluid, and bloodstream) (46% versus 22%; P < 0.05). After ARDRA, it was found that 97% of the 62 isolates resistant to all antibiotics tested were the A. baumannii genospecies, which was identified in only 31% of the isolates susceptible to all antibiotics tested. More genospecies diversity was identified in the isolates susceptible to all antibiotics tested, including genospecies of 13TU (34%), genotype 3 (29%), and A. calcoaceticus (5%). Furthermore, as 91% (10/11) of the isolates from CSF were susceptible to all antibiotics tested, the A. calcoaceticus-A. baumannii complex isolates with multidrug resistance could be less invasive than the more susceptible isolates. This study also indicated current emergence of carbapenem-, fluoroquinolone-, aminoglycoside-, and cephalosporin-resistant A. calcoaceticus-A. baumannii complex isolates in Taiwan.
PMCID: PMC3497195  PMID: 23006758
18.  National Surveillance of Antimicrobial Resistance in Pseudomonas aeruginosa Isolates Obtained from Intensive Care Unit Patients from 1993 to 2002 
Antimicrobial Agents and Chemotherapy  2004;48(12):4606-4610.
Nosocomial infections caused by Pseudomonas aeruginosa in critically ill patients are often difficult to treat due to resistance to multiple antimicrobials. The purpose of this study was to evaluate antimicrobial resistance among P. aeruginosa isolates from intensive care unit patients in the United States from 1993 to 2002 by using the Intensive Care Unit Surveillance Study database. Over the 10-year period, susceptibility of 13,999 nonduplicate isolates of P. aeruginosa was analyzed. From 1993 to 2002, nationwide increases in antimicrobial resistance were greatest for ciprofloxacin, imipenem, tobramycin, and aztreonam. Rates of multidrug resistance (resistance to ≥3 of the following drugs: ceftazidime, ciprofloxacin, tobramycin, and imipenem) increased from 4% in 1993 to 14% in 2002. The lowest dual resistance rates were observed between aminoglycosides or fluoroquinolones with piperacillin-tazobactam while the highest were for those that included β-lactams and ciprofloxacin. Ongoing surveillance studies are crucial in monitoring antimicrobial susceptibility patterns and selecting empirical treatment regimens.
PMCID: PMC529178  PMID: 15561832
19.  Evaluation of Current Activities of Fluoroquinolones against Gram-Negative Bacilli Using Centralized In Vitro Testing and Electronic Surveillance 
Given the propensity for Enterobacteriaceae and clinically significant nonfermentative gram-negative bacilli to acquire antimicrobial resistance, consistent surveillance of the activities of agents commonly prescribed to treat infections arising from these organisms is imperative. This study determined the activities of two fluoroquinolones, levofloxacin and ciprofloxacin, and seven comparative agents against recent clinical isolates of Enterobacteriaceae, Pseudomonas aeruginosa, Acinetobacter baumannii, and Stenotrophomonas maltophilia using two surveillance strategies: 1) centralized in vitro susceptibility testing of isolates collected from 27 hospital laboratories across the United States and 2) analysis of data from The Surveillance Network Database-USA, an electronic surveillance network comprising more than 200 laboratories nationwide. Regardless of the surveillance method, Enterobacteriaceae, P. aeruginosa, and A. baumannii demonstrated similar rates of susceptibility to levofloxacin and ciprofloxacin. Susceptibilities to the fluoroquinolones approached or exceeded 90% for all Enterobacteriaceae except Providencia spp. (≤65%). Approximately 70% of P. aeruginosa and 50% of A. baumanii isolates were susceptible to both fluoroquinolones. Among S. maltophilia isolates, 50% more isolates were susceptible to levofloxacin than to ciprofloxacin. Overall, the rate of ceftazidime nonsusceptibility among Enterobacteriaceae was 8.7%, with fluoroquinolone resistance rates notably higher among ceftazidime-nonsusceptible isolates than ceftazidime-susceptible ones. Multidrug-resistant isolates were present among all species tested but were most prevalent for Klebsiella pneumoniae and Enterobacter cloacae. No gram-negative isolates resistant only to a fluoroquinolone were encountered, regardless of species. Thus, while levofloxacin and ciprofloxacin have maintained potent activity against Enterobacteriaceae, the potential for fluoroquinolone resistance, the apparent association between fluoroquinolone and cephalosporin resistance, and the presence of multidrug resistance in every species examined emphasize the need to maintain active surveillance of resistance patterns among gram-negative bacilli.
PMCID: PMC90271  PMID: 11120976
20.  Effectiveness and Limitations of Hand Hygiene Promotion on Decreasing Healthcare–Associated Infections 
PLoS ONE  2011;6(11):e27163.
Limited data describe the sustained impact of hand hygiene programs (HHPs) implemented in teaching hospitals, where the burden of healthcare-associated infections (HAIs) is high. We use a quasi-experimental, before and after, study design with prospective hospital-wide surveillance of HAIs to assess the cost effectiveness of HHPs.
Methods and Findings
A 4-year hospital-wide HHP, with particular emphasis on using an alcohol-based hand rub, was implemented in April 2004 at a 2,200-bed teaching hospital in Taiwan. Compliance was measured by direct observation and the use of hand rub products. Poisson regression analyses were employed to evaluate the densities and trends of HAIs during the preintervention (January 1999 to March 2004) and intervention (April 2004 to December 2007) periods. The economic impact was estimated based on a case-control study in Taiwan. We observed 8,420 opportunities for hand hygiene during the study period. Compliance improved from 43.3% in April 2004 to 95.6% in 2007 (p<.001), and was closely correlated with increased consumption of the alcohol-based hand rub (r = 0.9399). The disease severity score (Charlson comorbidity index) increased (p = .002) during the intervention period. Nevertheless, we observed an 8.9% decrease in HAIs and a decline in the occurrence of bloodstream, methicillin-resistant Staphylococcus aureus, extensively drug-resistant Acinetobacter baumannii, and intensive care unit infections. The intervention had no discernable impact on HAI rates in the hematology/oncology wards. The net benefit of the HHP was US$5,289,364, and the benefit-cost ratio was 23.7 with a 3% discount rate.
Implementation of a HHP reduces preventable HAIs and is cost effective.
PMCID: PMC3217962  PMID: 22110610
21.  High Prevalence of Antimicrobial Resistance among Clinical Streptococcus pneumoniae Isolates in Asia (an ANSORP Study) 
A total of 685 clinical Streptococcus pneumoniae isolates from patients with pneumococcal diseases were collected from 14 centers in 11 Asian countries from January 2000 to June 2001. The in vitro susceptibilities of the isolates to 14 antimicrobial agents were determined by the broth microdilution test. Among the isolates tested, 483 (52.4%) were not susceptible to penicillin, 23% were intermediate, and 29.4% were penicillin resistant (MICs ≥ 2 mg/liter). Isolates from Vietnam showed the highest prevalence of penicillin resistance (71.4%), followed by those from Korea (54.8%), Hong Kong (43.2%), and Taiwan (38.6%). The penicillin MICs at which 90% of isolates are inhibited (MIC90s) were 4 mg/liter among isolates from Vietnam, Hong Kong, Korea, and Taiwan. The prevalence of erythromycin resistance was also very high in Vietnam (92.1%), Taiwan (86%), Korea (80.6%), Hong Kong (76.8%), and China (73.9%). The MIC90s of erythromycin were >32 mg/liter among isolates from Korea, Vietnam, China, Taiwan, Singapore, Malaysia, and Hong Kong. Isolates from Hong Kong showed the highest rate of ciprofloxacin resistance (11.8%), followed by isolates from Sri Lanka (9.5%), the Philippines (9.1%), and Korea (6.5%). Multilocus sequence typing showed that the spread of the Taiwan19F clone and the Spain23F clone could be one of the major reasons for the rapid increases in antimicrobial resistance among S. pneumoniae isolates in Asia. Data from the multinational surveillance study clearly documented distinctive increases in the prevalence rates and the levels of antimicrobial resistance among S. pneumoniae isolates in many Asian countries, which are among the highest in the world published to date.
PMCID: PMC415617  PMID: 15155207
22.  Nationwide survey of the development of drug resistance in the pediatric field in 2007 and 2010: drug sensitivity of Haemophilus influenzae in Japan (second report) 
The Drug-Resistant Pathogen Surveillance Group in Pediatric Infectious Disease conducted national surveillance for Haemophilus influenzae in 2007 (phase 3) and 2010 (phase 4), following the previous surveillance conducted from 2000 to 2001 (phase 1) and in 2004 (phase 2). We examined the antimicrobial susceptibility for H. influenzae derived from clinical specimens of pediatric patients collected nationwide from 27 institutions during phases 3 (386 strains) and 4 (484 strains). The frequency of β-lactamase-nonproducing ampicillin (ABPC)-resistant (BLNAR) strains, which rapidly increased from 11.4 % in phase 1 to 43.4 % in phase 2, has gradually decreased from 38.3 % in phase 3 to 37.8 % in phase 4. In contrast, On the other hand, the frequency of β-lactamase-producing strains, which continuously decreased from 8.3 % in phase 1 to 4.4 % in phase 3, has increased to 8.7 % in phase 4. Prevalence of β-lactamase-producing clavulanic acid/amoxicillin-resistant (BLPACR) strains, especially, has increased from 1.6 % in phase 3 to 4.8 % in phase 4. The oral antimicrobial agents with the lowest MIC90 were levofloxacin in both phases, and tosufloxacin in phase 4 (≤0.063 μg/ml), whereas for intravenous use the corresponding agent was tazobactam/piperacillin in both phases (0.125 μg/ml). There was no increase in the MIC90 of most β-lactams between phase 3 and phase 4. In relationship to sex, age, presence of siblings, attendance at a daycare center, siblings’ attendance at a daycare center, and prior administration of antimicrobial agents within 1 month, the frequency of β-lactamase-nonproducing ABPC-intermediately resistant (BLNAI) strains + BLNAR strains was high (P = 0.005) in cases with prior administration of antimicrobial agents in phase 3.
PMCID: PMC3682095  PMID: 23564330
Pediatric infectious disease; Surveillance; Haemophilus influenzae sensitivity; Drug resistance
23.  Correlation of Antimicrobial Resistance with β-Lactamases, the OmpA-Like Porin, and Efflux Pumps in Clinical Isolates of Acinetobacter baumannii Endemic to New York City▿  
Acinetobacter baumannii strains resistant to all β-lactams, aminoglycosides, and fluoroquinolones have emerged in many medical centers. Potential mechanisms contributing to antimicrobial resistance were investigated in 40 clinical isolates endemic to New York City. The isolates were examined for the presence of various β-lactamases, aminoglycoside-modifying enzymes, and mutations in gyrA and parC. Expression of the genes encoding the β-lactamase AmpC, the efflux systems AdeABC and AbeM, and the OmpA-like porin was also examined by real-time reverse transcription-PCR. No VIM, IMP, KPC, OXA-23-type, OXA-24-type, or OXA-58 β-lactamases were detected, although several isolates had acquired blaSHV-5. Most cephalosporin-resistant isolates had increased levels of expression of ampC and/or had acquired blaSHV-5; however, isolates without these features still had reduced susceptibility to cefepime that was mediated by the AdeABC efflux system. Although most isolates with ISAba1 upstream of the blaOXA-51-like carbapenemase gene were resistant to meropenem, several remained susceptible to imipenem. The presence of aminoglycoside-modifying enzymes and gyrase mutations accounted for aminoglycoside and fluoroquinolone resistance, respectively. The increased expression of adeABC was not an important contributor to aminoglycoside or fluoroquinolone resistance but did correlate with reduced susceptibility to tigecycline. The expression of abeM and ompA and phenotypic changes in OmpA did not correlate with antimicrobial resistance. A. baumannii has become a well-equipped nosocomial pathogen; defining the relative contribution of these and other mechanisms of antimicrobial resistance will require further investigation.
PMCID: PMC2533509  PMID: 18591275
24.  Types and Prevalence of Carbapenem-Resistant Acinetobacter calcoaceticus-Acinetobacter baumannii Complex in Northern Taiwan 
The frequency of the carbapenem-resistant Acinetobacter calcoaceticus-Acinetobacter baumannii (CRACB) complex increases annually in our hospitals. However, the types and prevalence of carbapenemases among isolates still remain unclear. In this study, we identified and collected 672 carbapenem-resistant isolates from a medical center in Northern Taiwan between April and December of 2010. There were 577 genospecies 2 (Acinetobacter baumannii), 79 genospecies 13TU, and 16 genospecies 3 isolates. The isolates had an acquired blaOXA-24-like gene, which was confirmed by sequencing for the encoded OXA-72 carbapenemase, and were often associated with high-level carbapenem resistance. These CRACB complex isolates remained susceptible to colistin (100%). The genotyping of isolates was conducted using pulsed-field gel electrophoresis with ApaI digestion. In most clonally related groups, patients were from both branch hospitals. The results indicate that interhospital dissemination of clones occurred. This study provides updated data on the types and prevalence of the CRACB complex. In addition, it presents a warning on the emergence and spread of CRACB complex harboring blaOXA-24-like genes in northern Taiwan.
PMCID: PMC3910724  PMID: 24145535
25.  An Integrated Syndromic Surveillance System for Monitoring Scarlet Fever in Taiwan 
To develop an integrated syndromic surveillance system for timely monitoring and early detection of unusual situations of scarlet fever in Taiwan, since Hong Kong, being so close geographically to Taiwan, had an outbreak of scarlet fever in June 2011.
Scarlet fever is a bacterial infection caused by group A streptococcus (GAS). The clinical symptoms are usually mild. Before October, 2007, case-based surveillance of scarlet fever was conducted through notifiable infectious diseases in Taiwan, but was removed later from the list of notifiable disease because of improved medical care capacities. In 2011, Hong Kong had encountered an outbreak of scarlet fever (1,2). In response, Taiwan developed an integrated syndromic surveillance system using multiple data sources since July 2011.
More than 99% of the Taiwan population is covered by National Health Insurance. We first retrospectively evaluated claims data from the Bureau of National Health Insurance (BNHI) by comparing with notifiable diseases reporting data from Taiwan Centers for Disease Control (TCDC). The claims data included information on scarlet fever diagnosis (ICD-9-CM code 034.1), date of visits, location of hospitals and age of patients from outpatient (OPD), emergency room (ER) and hospital admissions. Daily aggregate data of scarlet fever visits or hospitalizations were prospectively collected from BNHI since July 2011. Over 70% of the deaths in Taiwan are reported to the Office of Statistics of Department of Health electronically. We obtained daily data on electronic death certification data and used SAS Enterprise Guide 4.3 (SAS Institute Inc., Cary, NC, USA) for data management and analysis. Deaths associated with scarlet fever or other GAS infections were identified by text mining from causes of death with keywords of traditional Chinese ‘scarlet fever’, ‘group A streptococcus’ or ‘toxic shock syndrome’ (3).
From January 2006 to September 2007, the monthly OPD data with ICD-9-CM code 034.1 from BNHI showed strong correlation with TCDC’s notifiable disease data (r=0.89, p<0.0001). From July 6, 2008 (week 28) through July 28, 2012 (week 30), the average weekly numbers of scarlet fever visits to the OPD, ER and hospital admissions were 37 (range 11–70), 7 (range 0–20) and 3 (range 0–9). Eighty-five percent of the scarlet fever patients were less than 10 years old. In Taiwan, scarlet fever occurred year-round with seasonal peaks between May and July (Fig. 1). From January 2008 to July 2012, we identified 12 potential patients (9 males, age range 0–82 years) who died of GAS infections. No report had listed ‘scarlet fever’ as cause of death during the study period.
Taiwan has established an integrated syndromic surveillance system to timely monitor scarlet fever and GAS infection associated mortalities since July 2011. Syndromic surveillance of scarlet fever through BNHI correlated with number of scarlet fever cases through notifiable disease reporting system. Text mining from cause of death with the used keywords may have low sensitivities to identify patients who died of GAS infection. In Taiwan, syndromic surveillance has also been applied to other diseases such as enterovirus, influenza-like illness, and acute diarrhea. Interagency collaborations add values to existing health data in the government and have strengthened TCDC’s capacity of disease surveillance.
PMCID: PMC3692810
syndromic surveillance; Taiwan; scarlet fever; claims data

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