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We report here the emergence of VIM-2 and IMP-15 carbapenemases in a series of clinical isolates of carbapenem-resistant Pseudomonas aeruginosa in Lebanon. We also describe the disruption of the oprD gene by either mutations or insertion sequence (IS) elements ISPa 1328 and ISPre 2 isoform. Our study reemphasizes a rapid dissemination of the VIM-2 carbapenemase-encoding gene in clinical isolates of P. aeruginosa in the Mediterranean basin.

Carbapenem resistant Pseudomonas aeruginosa were isolated among multidrug-resistant (CR-MDR) organisms from tertiary hospitals in Thailand. Decreased expression of oprD mRNA (93.65%) was predominant followed by increased expression of mexAB-oprM mRNA (92.06%) and mexXY mRNA (63.49%). Interestingly, 23 of 126 (18.25%) isolates were susceptible to imipenem with down-regulated oprD expression and non-up-regulated mexCD-oprJ mRNA expression. Metallo-β-lactamases production was clearly positive in 24 isolates (18.46%) and weakly positive in 12 isolates (9.23%). Among both of these sets of isolates, imp-1, imp-14 and vim-2 were identified. Hyperproduction of AmpC β-lactamase had the lowest prevalence rate (3.97%). It was concluded that CR-MDR P. aeruginosa clinical isolates in Thailand possess multifactorial resistance mechanisms.

We reviewed 37 patients treated for bacteremia due to carbapenem-resistant (CR) Pseudomonas aeruginosa . Although 65% of isolates were multiple-drug resistant, therapeutic options were available, as all were susceptible to ≥1 antibiotic. A total of 92% of patients received active antimicrobial therapy, but only 57% received early active therapy (within 48 h). Fourteen-day mortality was 19%. Microbiologic failure occurred in 29%. The Pitt bacteremia score ( P = 0.046) and delayed active therapy ( P = 0.027) were predictive of death and microbiologic failure, respectively.

Background Multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii are common causes of health care associated infections worldwide. Carbapenems are effective against infections caused by multidrug resistant Gram-negative bacteria including Pseudomonas and Acinetobacter species. However, their use is threatened by the emergence of carbapenemase-producing strains. The aim of this study was to determine the prevalence of carbapenem-resistant P. aeruginosa and A. baumannii at Mulago Hospital in Kampala Uganda, and to establish whether the hospital environment harbors carbapenem-resistant Gram-negative rods. Results Between February 2007 and September 2009, a total of 869 clinical specimens were processed for culture and sensitivity testing yielding 42 (5 %) P. aeruginosa and 29 (3 %) A. baumannii isolates, of which 24 % (10/42) P. aeruginosa and 31 % (9/29) A. baumannii were carbapenem-resistant. Additionally, 80 samples from the hospital environment were randomly collected and similarly processed yielding 58 % (46/80) P. aeruginosa and 14 % (11/80) A. baumannii, of which 33 % (15/46) P. aeruginosa and 55 % (6/11) A. baumannii were carbapenem-resistant. The total number of isolates studied was 128. Carbapenemase genes detected were blaIMP-like (36 %, 9/25), blaVIM-like (32 %, 8/25), blaSPM-like (16 %, 4/25); blaNDM-1-like (4 %, 1/25) in carbapenem-resistant P. aeruginosa, and blaOXA-23-like (60 %, 9/15), blaOXA-24-like (7 %, 1/15), blaOXA-58-like (13 %, 2/15), and blaVIM-like (13 %, 2/15) in carbapenem-resistant A. baumannii. Furthermore, class 1 integrons were detected in 38 % (48/128) of P. aeruginosa and Acinetobacter, 37 % (26/71) of which were in clinical isolates and 39 % (22/57) in environment isolates. Gene cassettes were found in 25 % (12/48) of integron-positive isolates. These were aminoglycoside adenylyltransferase ant(4′)-IIb (3 isolates); trimethoprim-resistant dihydrofolate reductase dfrA (2 isolates); adenyltransferase aadAB (3 isolates); QacE delta1 multidrug exporter (2 isolates); quinolone resistance pentapeptide repeat protein qnr (1 isolate); and metallo-β-lactamase genes blaVIM-4-like, blaIMP-19-like, and blaIMP-26-like (1 isolate each). Gene cassettes were missing in 75 % (36/48) of the integron-positive isolates. Conclusions The prevalence of carbapenem-resistant P. aeruginosa and Acinetobacter among hospitalized patients at Mulago Hospital is low compared to rates from South-East Asia. However, it is high among isolates and in the environment, which is of concern given that the hospital environment is a potential source of infection for hospitalized patients and health care workers. Electronic supplementary material The online version of this article (doi:10.1186/s40064-016-2986-7) contains supplementary material, which is available to authorized users.

Se analizaron 17 cepas de Pseudomonas aeruginosa resistentes a carbapenémicos aisladas en cuatro hospitales del oriente y sur de Venezuela colectadas entre los años 2007 y 2010. En todas las cepas se demostró la producción de metalo-β-lactamasas (MBLs) por el método de discos combinados. Mediante la amplificación por la reacción de polimerasa en cadena (RPC) de los genes que codifican para las metalo-β-lactamasas de las familias IMP, VIM y SPM, y su posterior secuenciación, se confirmó la presencia de MBLs de tipo VIM-2 en todas las cepas. Mediante la electroforesis de campos pulsantes (ECP), las cepas se clasificaron en tres grupos de similaridad. El grupo dominante (A) estuvo constituido por 13 cepas provenientes de los cuatro hospitales, con similaridad superior al 83% entre ellas. Dos cepas del hospital de Cumaná conformaron el Grupo B y otras dos el Grupo C con similaridad de 73 y 65%, respectivamente, con el Grupo A. Estos resultados confirmaron que en los hospitales del oriente y sur de Venezuela, circulan cepas de P. aeruginosa productoras de MBLs de tipo VIM-2, con un origen clonal común. Asimismo, en el hospital de Cumaná circulan cepas de origen policlonal.

One hundred sixty-nine nonreplicate imipenem-resistant Pseudomonas aeruginosa strains isolated in a large hospital on the coastal region of Croatia were studied. The most active antibiotics were colistin and amikacin. Most of the isolates were multiresistant. The most prevalent serotype was O12, followed by O11. Six strains carried the bla VIM-2 gene located in a novel class 1 integron composed in its variable part of the bla VIM-2 - bla oxa-10 -Δ qacF-aacA4 genes. Metallo-β-lactamase-producing strains belonged to sequence types ST235 and ST111.

An outbreak of a multidrug-resistant Pseudomonas aeruginosa producing metallo-β-lactamase (MBLPA) in a haemato-oncology unit was controlled using multidisciplinary interventions. The present study assesses the effects of these interventions by active surveillance of the incidence of MBLPA infection at the 1,240-bed tertiary care Kyoto University Hospital in Kyoto, Japan. Infection control strategies in 2004 included strengthening contact precautions, analysis of risk factors for MBLPA infection and cessation of urine collection. However, new MBLPA infections were identified in 2006, which prompted enhanced environmental cleaning, routine active surveillance, and restricting carbapenem usage. Between 2004 and 2010, 17 patients in the unit became infected with indistinguishable MBLPA strains. The final five infected patients were found by routine active surveillance, but horizontal transmission was undetectable. The MBLPA outbreak in the haemato-oncology unit was finally contained in 2008.

The existence of Gram-negative bacilli producing metallo-β-lactamase has been increasingly reported in many countries. The polyresistant strains of Pseudomonas aeruginosa isolated from patients’ urine were studied. The sensitiveness of strains to imipenem was assessed. The production of carbapenem-hydrolysing enzymes in resistant and moderately resistant strains was investigated. A high level of prevalence of the metallo-β-lactamase according to phenotypical test was showed. The necessity of monitoring of the distribution of carbapenem-hydrolysing enzymes producers is grounded.

Acquired metallo-beta-lactamases (MBLs) can confer broad-spectrum beta-lactam resistance (including carbapenems) not reversible by conventional beta-lactamase inhibitors and are emerging resistance determinants of remarkable clinical importance. In 2001, multidrug-resistant Pseudomonas aeruginosa carrying bla(VIM) MBL genes were found to be widespread (approximately 20% of all P. aeruginosa isolates and 70% of the carbapenem-resistant isolates) at Trieste University Hospital. Clonal diversity and heterogeneity of resistance determinants (either bla(VIM-1)-like or bla(VIM-2)-like) were detected among MBL producers. This evidence is the first that acquired MBLs can rapidly emerge and establish a condition of endemicity in certain epidemiologic settings.

Objective To investigate an outbreak of carbapenem-resistant Pseudomonas aeruginosa (CRPA) in a urology ward. Methods Patients infected or colonized with CRPA were prospectively identified by daily laboratory surveillance. Routine infection-control measures were reinforced, disinfection protocols were revised, and a surveillance program was set up, analyzing cross-transmission in the nursing ward and environment cultures from urology wards and the operating theater. CRPA isolates from clinical and environment samples were studied by pulsed-field gel electrophoresis (PFGE), following Xba I and Spe I restriction. Results From February 1998 to September 2000, 59 adult urology patients were colonized or infected by CRPA. All patients had been operated on prior to identification of the CRPA isolate and 79% of these procedures were performed in the same cystoscopy room. No patients had received prior carbapenem therapy. No cross-transmission was detected, and environment cultures from the urology ward and theater were negative except for five samples collected in the cystoscopy room. PFGE identified a single clone in the isolates from different patients and the environment samples. Conclusions The PFGE analysis indicated that the CRPA outbreak resulted from the contamination of the cystoscopy room via an unsealed drain. The outbreak ended when the drain was sealed.

Background: The Pseudomonas aeruginosa porin OprD is a substrate-specific porin that facilitates the diffusion of basic amino acids, small peptides, and carbapenems into the cell. OprD-mediated resistance occurs as a result of decreased transcriptional expression of oprD and/or loss of function mutations that disrupt protein activity. Objectives: In this study, we examined the level of oprD expression in P. aeruginosa clinical isolates to determine the contribution of OprD porins in carbapenem resistance. Materials and Methods: Included strains were divided into two groups, comprised of multidrug-resistant (MDR) and isolated carbapenem-resistant (ICR) strains. The transcription product level of oprD was identified using real-time polymerase chain reaction (qPCR). Results: Of the 18 clinical isolates, a decrease in the oprD level was found to be significant in 13 isolates. Nine of eighteen isolates with a significant decrease were determined in the first group and comprised MDR isolates that showed a statistically significant difference compared with the ICR group (P = 0.001). In the ICR group, oprD levels were found to be significantly low in 4 isolates. Six different patterns were determined by comparing band profiles in AP-PCR. Conclusions: Although the data support the idea that the basic mechanism of imipenem resistance could be via the loss of oprD, they do not fully explain the role of oprD and indicate that other mechanisms may play an important role. Additionally, the significant decrease in the oprD levels in MDR strains suggests that oprD also plays a role in the emergence of both carbapenem and non-carbapenem resistance. © 2015, Ahvaz Jundishapur University of Medical Sciences.

Background: Carbapenems are important drugs used for the treatment of Pseudomonas aeruginosa infections, however metallo-βlactamases (MBL) are able to efficiently hydrolyze these classes of drugs. Immediate detection of the MBL-producing P. aeruginosa is necessary in order to accurately treat infections caused by this organism. Objectives: To determine the prevalence of MBL producing P. aeruginosa in burn and non-burn patients by two phenotypic tests and polymerase chain reaction (PCR) and to compare phenotypic tests with PCR. Materials and Methods: A total of 223 non-duplicate strains of P. aeruginosa were collected from three teaching hospitals of Ahvaz, Iran. Antimicrobial susceptibility and minimum inhibitory concentrations (MICs) of carbapenems (imipenem, meropenem, doripenem and ertapenem) were determined by the Kirby-Bauer and E-test methods. Combined disk (CD) test, MBL E-test and PCR were performed for carbapenem-resistant P. aeruginosa isolates. Results: Amongst all the P. aeruginosa isolates, 58.7% were resistant to imipenem while 31.8%, 13.5% and 74.4% were resistant to meropenem, doripenem and ertapenem, respectively. Amongst all the P. aeruginosa isolates, 44.4% were multidrug resistant and 13.45% were resistant to all of the carbapenems. The CD test with doripenem disk / 750 μg ethylene diamine tetra acetic acid (EDTA) had the highest efficiency compared to the other phenotypic tests. bla IMP and bla VIM genes were detected in 11.7% and 0.4% of isolates, respectively. bla SPM and bla NDM genes were not observed. Conclusions: Epidemiological and regional evaluation of MBL-producing P. aeruginosa through simple and inexpensive methods should be considered for effective treatment of carbapenem-resistant P. aeruginosa infections.

The present work describes a prevalence of 36.2% of carbapenemases IMP-, VIM-, and GES-type on 124 imipenem-resistant Pseudomonas aeruginosa clinical isolates. The ESBL GES-19 and carbapenemase GES-20 genes were the most prevalent (84.4%) β-lactamases among imipenem-resistant P. aeruginosa clinical isolates in Mexico. These genes are chromosomal encoded on embedded class 1 integron arrays.

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In Brazil, carbapenem-resistant Pseudomonas aeruginosa isolates are closely related to the São Paulo metallo-β-lactamase (SPM) Brazilian clone. In this study, imipenem-resistant isolates were divided in two sets, 2002/2003 and 2008/2009, analysed by pulsed field gel electrophoresis and tested for the Ambler class B metallo-β-lactamase (MBL) genes blaSPM-1, blaIMP and blaVIM. The results show a prevalence of one clone related to the SPM Brazilian clone in 2002/2003. In 2008/2009, P. aeruginosa isolates were mostly MBL negative, genetically diverse and unrelated to those that had been detected earlier. These findings suggest that the resistance to carbapenems by these recent P. aeruginosa isolates was not due to the spread of MBL-positive SPM-related clones, as often observed in Brazilian hospitals.

This study was conducted to investigate the molecular occurrence and dissemination of Pseudomonas aeruginosa producing MBLs recovered from the different wards in the affiliated hospital, Jilin. Antibiotic susceptibility test was determined using standard agar diffusion in conjunction with MBL screening methods. Plasmid profiles and pulsed-field gel electrophoresis were used to study the relatedness of isolates. The total of 120 were isolated from three wards and 89 strains (74.8%) produced MBLs, the number of 31 strains (25.2%) didn't produce MBLs. All MBLs isolates showed identical antimicrobial susceptibility profiles. Among P. aeruginosa producing MBLs, 79 strains (88.9%) were positive for bla VIM-2 gene, 12 strains (11.1%) contained bla IMP-3 gene, which were located on transferable plasmids with class 1 integron. All MBLs isolates were closely related by PFGE and plasmid analysis. This study confirmed the potential risk of dissemination of carbapenem-resistant Pseudomonas aeruginosa with inter-and intrahospital clonal transfer of patients.

IOT – Institute of Orthopedics and Traumatology(Instituto de Ortopedia e Traumatologia), Clinical Hospital,School of Medicine, Sao Paulo University, started theadministration of ertapenem in March 2006. The ClinicalHospital is a tertiary and quaternary healthcare center andthe Institute of Orthopedics and Traumatology isexclusively designed to treat highly complex cases,counting on 200 beds. That antibiotic (ertapenem) wasincluded in the standardization of the use of antimicrobialagents intended to treat hospital-acquired infectionsassociated to enterobacteriaceae producing ESBL (extendedspectrum beta-lactamase), including cases of post-surg icalor post-traumatic bone and soft tissues infections. At IOT,the Gram-negative bacillus most frequently found in thatgroup of infections is

Aim: MBL E test for MBL screening in carbapenem resistant Pseudomonas aeruginosa isolates is recommended as a fast and reliable phenotypic screening test. However, as it has been put forward by some reserachers, because of variations in antibiotic susceptibility tests or MBL E test with different brands of Mueller- Hinton Agar (MHA) media, the possibility that carbapenem MIK values and MBL E test results can, therefore, be influenced by these media. To this end, we aim to determine the most suitable MHA media to be used in search for MBL E test in routine microbiology laboratories by employing five different brands of MHA media. Materials and Methods: 29 carbapenem resistant Pseudomonas aeruginosa strains isolated from hospitalised patients have been used in this study. P.aeruginosa isolates were identified by conventional methods. Imipenem and meropenem E test were used for verification of carbapenem resistance. MBL E test was used for detecting MBL production by five different brands of Mueller Hinton agar plates and the results of these tests were compared with polymerase chain reaction (PCR) results. Results: IMP, VIM, GIM, SIM and SPM type genes were found to be negative with polymerase chain reaction for 29 isolates that were resistant to carbapenem. One isolate with BBL brand MHA, two isolates with Oxoid brand MHA, 19 isolates with Himedia brand MHA, 21 isolates with Merck brand MHA, and 27 isolates with Plasmatec brand MHA gave positive results. Conclusion: The present results indicate that use of BBL or Oxoid brand MHA media, especially in laboratories without any fascilities for molecular diagnosis, can be more reliable compared to other brands.

Metallo-beta-lactamase production is emerging worldwide as an important mechanism of carbapenem resistance among nonfermentative Gram-negative isolates, and this mechanism is becoming frequently observed in Brazil. This study documents the occurrence and characteristics of an epidemic SPM-1-producing Pseudomonas aeruginosa strain in a teaching hospital located in Rio de Janeiro City, Brazil. The bla (SPM-1) gene and a class 1 integron were detected in 13 isolates, representing 20% of the 65 imipenem-resistant P. aeruginosa isolates obtained from January, 2000, to August, 2001. DNA sequencing revealed that this integron carries three gene cassettes that confer resistance to antimicrobials, aacA4, bla (OXA-56), and aadA7, and an orf1 encoding a putative transposase. All 13 SPM-producing P. aeruginosa isolates had closely related pulsed-field gel electrophoresis (PFGE) profiles, designated as clonal group A, suggesting nosocomial spread of the strain. This clonal group was the same as that observed in other SPM-1-producing P. aeruginosa isolates from distinct Brazilian states. The dissemination of this clone throughout Brazil could not be explained by transfer of infected patients and/or sharing of common health-care staff. It is likely that the spread of these strains occurred indirectly via the community.

Background Pseudomonas aeruginosa is a ubiquitous organism that is easily recovered from moist environments. It is encountered as a nosocomial pathogen and has become one of the most serious causes of nosocomial bacterial infections particularly in the immunocompromised and burned hosts as well as in patients with cystic fibrosis. Increasingly, Pseudomonas aeruginosa that are multidrug or pan-resistant are being isolated from clinical specimens. Metallo-b-lactamases (MBLs) which belong to Ambler class B b-lactamase have emerged as a therapeutic threat, as they often confer high-level resistance to all b-lactams except aztreo-nam. Aim The aim of this study is to identify the number of isolates that are carbapenem resistant due to the presence of an IMP type MBL from a storage collection in Queensland and to review the characteristics and epidemiology of these isolates. The secondary aim is to analyse whether the MBL genotypes correlate well with phenotypic detection. Method Previously stored carbapenem resistant Pseudomonas aeruginosa clinical isolates were retrieved. The minimum inhibitory concentrations (MICs) to two carbapenems (meropenem and imipenem) were defined using E-test (bioMerieux, France). Template DNA was prepared by heat lysis and polymerase chain reaction (PCR) was performed using IMP-1A and IMP-1B primers. Phenotypic testing was done using the same subculture by the modified Hodge test (MHT) and double disc synergy testing (DDST) methods. Results A total of 69 isolates was included in this study of which 14.5% (10 isolates) were positive for IMP type MBL. Of the 10 isolates, five were collected from intensive care units, three from medical wards and one each from the surgical ward and outpatients department. Phenotypic testing of the 10 isolates with the IMP type MBL showed negative results on MHT but was positive for the DDST. Conclusion This is the first study from Australia looking at the prevalence of IMP type MBL in carbapenem resistant Pseudomonas aeruginosa . The prevalence of IMP type MBL is 14.5% in carbapenem resistant Pseudomonas aeruginosa isolates in Queensland from as early back as 2002. Laboratory screening is important in identifying and preventing the further spread of MBL-producing organisms. The DDST is a relatively simple and economic test for this purpose. A positive screening test will need molecular confirmation to identify the MBL involved.

Pseudomonas aeruginosa is an opportunistic pathogen that causes frequently nosocomial infections, currently becoming more difficult to treat due to the various resistance mechanisms and different virulence factors. The purpose of this study was to determine the risk factors independently associated with the development of bacteremia by carbapenem-resistant P. aeruginosa, the frequency of virulence genes in metallo-β-lactamases producers and to evaluate their ability to produce biofilm. We conducted a case–control study in the Uberlândia Federal University – Hospital Clinic, Brazil. Polymerase Chain Reaction was performed for metallo-β-lactamases and virulence genes. Adhesion and biofilm assays were done by quantitative tests. Among the 157 strains analyzed, 73.9% were multidrug-resistant, 43.9% were resistant to carbapenems, 16.1% were phenotypically positive for metallo-β-lactamases, and of these, 10.7% were positive for blaSPM gene and 5.3% positive for blaVIM. The multivariable analysis showed that mechanical ventilation, enteral/nasogastric tubes, primary bacteremia with unknown focus, and inappropriate therapy were independent risk factors associated with bacteremia. All tested strains were characterized as strongly biofilm producers. A higher mortality was found among patients with bacteremia by carbapenem-resistant P. aeruginosa strains, associated independently with extrinsic risk factors, however it was not evident the association with the presence of virulence and metallo-β-lactamases genes.

Background The prevalence and clinical impact on mortality of carbapenem-resistant Pseudomonas aeruginosa (CRPA) is unclear in Taiwan. We aim to clarify these clinical issues by using data from the Taiwan Surveillance of Antimicrobial Resistance (TSAR) program. Methods Patients from five hospitals with their P. aeruginosa isolates collected by TSAR II-VII (2000–2010) program were considered as the potential study population. All patients with CRPA were enrolled as case patients. Patients with carbapenem-susceptible P. aeruginosa were randomly selected in a 1:1 ratio to case patients as control patients. CRPA isolates were tested for the presence of carbapenemase-producing genes. The clinical data were collected to identify risk factors for CRPA carriage and mortality of P. aeruginosa infection. Results The overall prevalence of CRPA was 10.2% (349/3408), which increased significantly by the TSAR period ( p = 0.007). Among the 164 enrolled patients, the risk factor for carrying CRPA was previous fluoroquinolone exposure ( p = 0.004). The risk factors for mortality among 80 patients with infection by P. aeruginosa included: intensive care unit (ICU) setting, receipt of antifungal therapy, and presence of invasive devices ( p = 0.001, 0.010, and 0.017; respectively). Carbapenem resistance did not play a role. Among the 82 CRPA isolates enrolled in this study, 15 isolates were found to carry carbapenemase-producing genes. Conclusion In Taiwan, the prevalence of CRPA and carriage of carbapenemase-producing genes was high. However, carbapenem resistance did not play a role in the mortality of patients with P. aeruginosa infections.

Background Patients with Pseudomonas aeruginosa infections from blood or sterile sites were evaluated to determine risk factors associated with carbapenem resistance (CRPA) compared to carbapenem sensitivity (CSPA) as well as prior carbapenem use and the development of resistance. Findings Retrospective chart review of 80 patients hospitalized with a documented P. aeruginosa infection during 2010–2011. Stored isolates were retested with both Kirby–Bauer disk diffusion and E-tests. Clinical characteristic of patients in the CRPA (N = 21) and the CSPA (N = 59) groups were similar. Hospital acquired (HA) infections were more common in the CRPA group compared to the CSPA group (71 vs 44 %, p = 0.04) and CRPA patients were more likely to have a Foley catheter at the time of infection (71 vs 37 %, p = 0.01). There was more carbapenem use in the CRPA group prior to onset of infection (59 vs 22 %, OR 5.1, 95 % CI 1.3–20.8, p = 0.01). Length of stay was significantly longer in the CRPA group (mean 44 days) compared to the CSPA group (mean 23 days), p = 0.02. Mortality between the two groups was similar and there were no differences between groups for death attributable to Pseudomonas. Conclusions Patients with CRPA were more likely to have HA infections and to have a multidrug resistant profile. Other identifiable risks included a Foley catheter in place at the time of infection and exposure to a carbapenem prior to infection. Prompt removal of devices and judicious use of antibiotics may be interventions that can impact the development of this kind of infections.

This study evaluated the clonal spread of carbapenem-resistant P. aeruginosa producing SPM-1 type metallo-beta-lactamase (MBL), at the university hospital of Florianopolis, Santa Catarina, Brazil, compared to an epidemic clone previously reported, as well as strains collected in other three Brazilian states. Among the isolates, 17 (62%) were clonal and highly related to strains from other regions of Brazil. Six clonal strains harbored the bla(SPM-1) gene. the finding of a unique SPM-1 producer clone suggests that its dissemination has contributed to the high resistance to carbapenems in Brazilian hospitals. Univ Fed Parana, Hosp Clin, Serv Anal Clin, BR-80060000 Curitiba, Parana, Brazil Univ Fed Santa Catarina, Univ Hosp, Serv Patol Clin, BR-88040900 Florianopolis, SC, Brazil Universidade Federal de São Paulo, Dept Doencas Infecciosas, São Paulo, Brazil Hosp Clin Porto Alegre, Serv Patol Clin, Porto Alegre, RS, Brazil Univ Catolica Goias, Dept Enfermagem, Goiania, Go, Brazil Univ Catolica Goias, Dept Med, Goiania, Go, Brazil Fac Pequeno Principe, Inst Pesquisa Pele Pequeno Principe, Curitiba, Parana, Brazil Universidade Federal de São Paulo, Dept Doencas Infecciosas, São Paulo, Brazil Web of Science