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American Journal of Infection Control 42 (2014) e47-e53

Contents lists avai

American Journal of Infection Control

journal homepage: www.aj ic journal .org

American Journal of Infection Control

Major article

Evaluating the quality of outbreak reports on health care-associatedinfections in São Paulo, Brazil, during 2000-2010 using the ORIONstatement findings and recommendations

Amanda Luiz Pires Maciel RN a, Denise Brandão de Assis MD, MSc b,Geraldine Madalosso MD, MSc b, Maria Clara Padoveze RN, MSc, PhD a,*aDepartment of Collective Health Nursing, School of Nursing, University of São Paulo, São Paulo, Brazilb São Paulo State Health Department, Centro de Vigilância Epidemiológica Prof Alexandre Vranjac, Hospital Infection Division, São Paulo, Brazil

Key Words:Cross-infectionDisease outbreak

* Address correspondence to Maria Clara Padoveze,Carvalho Aguiar, 419, CEP - 05403-000, São Paulo, SP

E-mail address: padoveze@usp.br (M.C. Padoveze)Conflicts of interest: None to report.

0196-6553/$36.00 - Copyright � 2014 by the Associahttp://dx.doi.org/10.1016/j.ajic.2013.12.017

Background: The standard of outbreak reports must be improved to a level where they are robustenough to properly influence preventive strategies. We aimed to verify compliance with mandatoryoutbreak notification, describing epidemiologic characteristics and management, and evaluating thequality of outbreak reports on health care-associated infections in São Paulo State, Brazil.Methods: A systematic search was carried out on PubMed, the Latin American and Caribbean HealthSciences Literature database, Embase, Outbreak Database, the Annals of Brazilian Conferences onHealthcare-Associated Infection Prevention and Infectious Diseases, and reports from the São Paulo StateHospital Infection Division. The quality of reports was evaluated according to the Outbreak Reports andIntervention studies of Nosocomial Infection (ORION) statement guidelines.Results: A total of 87 outbreak reports were identified; however, only 15 outbreaks (17.2%) were reportedto the São Paulo State Hospital Infection Division. Bloodstream infection and neonatal intensive careunits were mostly implicated (23% and 19.5%, respectively). Quality, evaluated according to ORIONstatement recommendations, was generally poor. The ORION categories of Background, Objectives,Participants, Setting, Infection-Related Outcomes, and Generality were properly described in 32.2%,74.7%, 2.3%, 46%, 2.3%, and 12.6% of reports, respectively. Interventions and Culture-Typing weredescribed with details in 51.9% and 55.2% of outbreak reports, respectively.Conclusions: Our findings pointed out the need for strategies to improve competence in outbreak re-ports, and the ORION statement guidelines may help in this matter. Efforts to promote confidence andconsequent compliance with mandatory notification of outbreak reports are essential.

Copyright � 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc.Published by Elsevier Inc. All rights reserved.

Health care-associated infections (HAIs) are usually endemic,but it is estimated that 2%-5% of these infections are due to noso-comial outbreaks.1,2 Despite low frequency, outbreaks can causeconcern, increasing morbidity and mortality, and require extensivepersonnel and financial resources in addition to being very timeconsuming.3,4

Outbreak investigations can provide insight into the field ofhealth care epidemiology and infection control by describing

RN, MSc, PhD, Av Dr Enéas de, Brazil..

tion for Professionals in Infection C

cause and evaluating the most appropriate interventions for-prevention.5-7

Since 1998, reporting outbreak investigation to health agenciesis mandatory in Brazil.8 Vonberg and Gastmeier9 estimated thatabout 75% of all nosocomial outbreaks published in the medicalliterature support new ideas for the prevention of nosocomial in-fections. In agreement with this, the quality of outbreak reports andinterventions in infection control must be improved to a levelwhere they are robust enough to influence policy as well asgovernmental guidelines and practice in health care.9-12

During the 1990s, when evidence-based medicine gatheredmomentum, the quality of research reporting was required evenmore. In that decade, to improve transparency and consistency ofresearch reports, efforts were initiated by researchers, editors, and

ontrol and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Fig 1. Distribution of outbreaks reports evaluated according to the reference sources, São Paulo State, Brazil, 2000-2010. HAI, health care-associated infection; LILACS, LatinAmerican and Caribbean Health Science Literature database.

A.L.P. Maciel et al. / American Journal of Infection Control 42 (2014) e47-e53e48

methodologists to develop and recommend specific standards forpublished research. Since 1996 multiple statements and checklistshave been developed for publishing a variety of study types, such asthe Consolidated Standards of Reporting Trials, the TransparentReporting of Evaluations with Nonrandomized Designs statement,and the Strengthening the Reporting of Observational Studies inEpidemiology statement.13-16 In the field of hospital epidemiology,the Outbreaks Report and Intervention Studies of NosocomialInfection (ORION) statement was created; it consists of a 22-itemchecklist and a summary table that facilitates the synthesis of ev-idence and promotes transparency of reporting.10-12,16-18

Our study aimed to review outbreaks reported in São PauloState, Brazil, and verify compliance with mandatory outbreaknotification, describe epidemiologic characteristics and manage-ment, and evaluate the quality of outbreak reports.

METHODS

A systematic search was performed to describe nosocomialoutbreaks occurring in São Paulo State and reported during thetime period 2000-2010. São Paulo State has approximately41,262,199 inhabitants, representing 21.6% of the total population ofBrazil,19,20 and 891 hospitals that represent 14.2% of all health in-stitutions in the country.21

Data sources

The following databases were used for a systematic search ofavailable articles describing nosocomial outbreaks: Embase, theLatin American and Caribbean Health Science Literature database,and PubMed. We adopted the controlled vocabulary used for sub-ject indexing in Embase (hospital infection, epidemics, and Brazil),the descriptors in health sciences for the Latin American andCaribbean Health Science Literature database, and the MedicalSubject Headings for PubMed (cross-infection, disease outbreak, andBrazil). The Annals of the Brazilian Conference on HAI Preventionand Hospital Epidemiology and Brazilian Conference on InfectiousDisease were reviewed and abstracts describing nosocomial out-breaks were included. The freely accessible worldwide database ofhealth care-associated outbreaksdknown as Outbreak Database(www.outbreak-database.com)dwas accessed and searched using

the term Brazil. Outbreaks reported to the Hospital Infection Divi-sion at the São Paulo State Health Department were also included.

Inclusion criteria

We included HAI outbreaks occurring in São Paulo State andreported during 2000-2010. Articles focusing exclusively on phe-notyping or genotyping methodologies of the pathogens withoutan epidemiologic approach were excluded.

Data collection

The data extraction was done by 1 researcher (A.L.P.M.), and allthe process of data extraction was supervised by a secondresearcher (M.C.P.). These researchers discussed all of the outbreakreports in case of uncertainty during the data extraction.

Two instrumentswereused to capture all the information required.The first was for epidemiologic characteristics, such as geographiclocation and investigation methods applied. The second instrumentwas the ORION Authors (or Reviewers) Checklist, which evaluatesinformation to determine the quality of an outbreak report.10

Variables

To describe the features of the reports the following variableswere selected: geographic location (ie, city, type of health care facility,and ward), descriptive characteristics (ie, infection sites, pathogens,and antimicrobial resistance), investigation methods applied (ie,genotyping methods, epidemiologic approach, and source of trans-mission), and control measures adopted. The ORION items and de-scriptors were used to evaluate the quality of the studies.

Data analysis

A descriptive analysis of the selected variables was carried outusing EPI-INFO version 3.5.2 software (Centers for Disease Controland Prevention, Atlanta, GA).

RESULTS

A total of 87 outbreak investigation reports were identified.Most frequently the publications were from the Annals of Brazilian

Table 1Sources of transmission related to the outbreaks reported in São Paulo State, Brazil, 2000-2010

Source of transmission n (%) Details of the source in reports (n)

Unknown 55 (63.2) Not provided23-25,28,32,33,36-40,42,44,45,47,48,51-54,56-61,63,65,69,70,72-74,77-80,82-84,86-91,93,95,96,99-102,107

Contaminated substances 10 (11.5) Anticoagulant substance (2),26,67 manitol (1),27 parenteral nutrition (2),75,76 enteral nutrition (1),31

chemotherapeutic substance (1),35 lactated Ringer’s solution (1),68 saline (1),30

chlorhexidine (1)34

Colonized staff 3 (3.4) Staff contaminated with Klebsiella pneumoniae associated to onychomycosis in hands (3)29,50,92

Environmental contamination 4 (4.6) Water (3),22,66,105 dialysis equipment (1)55

Infect or colonized patient 4 (4.6) Scabies (2),49,81 incubation period of chickenpox (1),97 and respiratory syncytial virus (1)103

Foods 2 (2.3) Meal (1),108 dessert (1)85

Sick visitor 1 (1.1) Respiratory syncytial virus (1)62

Contaminated substances and environmentalcontamination

1 (1.1) Saline and dialysis reservatory (1)43

Device contamination 1 (1.1) Contamination of urinary catheter by health care workers during patient care (1)94

Pseudo-outbreaks 6 (6.8) Contaminated sample (3),41,64,71 surveillance system (2),98,104 contaminated saline andwater (1)46

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Conferences on HAI Prevention and Hospital Epidemiology (50.6%,n ¼ 44) (Fig 1).

Compliance with mandatory outbreak reporting

Only 15 outbreaks (17.2%) were reported to the Hospital Infec-tion Division at the São Paulo State Health Department, in accor-dance with federal law.

Epidemiologic characteristics

Outbreaks that were reported occurred mainly in large cities suchas São Paulo (57.5%; n ¼ 50),22-71 Campinas (10.3%; n ¼ 9),72-80 andRibeirão Preto (5.7%; n ¼ 5).81-85 These cities are quite different intheir scale; São Paulo is the most populated city in Brazil, with10,659,386 inhabitants and 202 hospitals, whilst Ribeirão Preto is amedium-size city with 583,842 inhabitants and 16 hospitals.19-21

Inpatient health care facilities accounted for 75.9% (n ¼ 66) of theoccurrences, outpatient settings for 14.9% (n ¼ 13), long-term carefacilities for 1.1% (n ¼ 1), and health care workers for 2.3% (n ¼2).22,23,26-48,50-66,68-79,81-108 The remaining 5.7% (n ¼ 5) of outbreakreports did not mention the setting of the event, according to ORIONrecommendations (Item 8).24,25,49,67,80 The most common inpatientsetting was neonatal intensive care units (19.5%; n ¼ 17), followed byadult intensive care units (13.8%; n¼ 12). The occurrence of outbreaksaffecting >1 unit were found in 14.9% (n ¼ 13) of the outbreaksreported, and 11.5% (n ¼ 10) of them involved the entire hospi-tal.23,29,31,34,37-42,44,45,47,48,51,52,58-61,63-66,69-76,79,81,82,84,86,94,96-99,101,103

Bloodstream infections were the most frequently reported site(23.0%; n ¼ 20), followed by skin and soft tissue (9.2%; n ¼ 8). Out-breaks presenting>1 infection site occurred in 16.1% of reports (n¼14). Pyrogenic reaction was the outcome in 6 outbreaks reported(6.9%) and surgical site or gastrointestinal infectionswere describedas the main outcome in 5 reports each (5.7%). Surprisingly, theinfection site was not mentioned in 16 reports (18.4%).23,25-27,29-32,34,40,42,50-55,58-61,63,65-70,72,74-77,79,81-88,90-93,95-99,101,102,104,106-108

Themajorityof outbreakswerecausedbybacteria (72.4%;n¼63)with a predominance of gram-negative bacillus (49.4%; n¼ 43). Themost frequent agents associated with the outbreaks wereAcinetobacter baumanni (11.5%; n¼ 10),Klebsiella pneumonia (10.3%;n ¼ 9), Enterococcus sp (8%; n ¼ 7), and Pseudomonas aeruginosa(6.9%; n¼ 6).22-29,31,32,34,35,37-40,42-44,46-48,50-53,55,58-61,63,64,66-69,71,72,74-76,79,82-84,86-102,104,107,108

The source of transmissionwas identified in only 36.8% (n¼ 32)of the reports (Table 1). Among the reports where this informationwas provided, contaminated substances were frequentlyidentified as the cause of the outbreak (n ¼ 10), mainly intrinsic

contamination (n ¼ 7). Gram-negative bacillus was the mostcommon agent isolated in contaminated substances (n ¼9).22,26,27,29-31,34,35,41,43,46,49,50,55,62,64,66-68,71,75,76,81,85,92,94,97,98,103-105,108

Managementeinfection control measures

Interventions were reported in 89.7% (n ¼ 78) of the studies.Contact precautions was the most common intervention describedto prevent the spread of pathogens (39.1%; n ¼ 34), followed byaudit of units by an infection control team (28.4%; n ¼ 25), patientscreening/surveillance (25%; n ¼ 22), hand hygiene improvement(25%; n ¼ 22), drugs screening (20.5%; n ¼ 18), and enhancedenvironmental cleansing (19.3%; n ¼ 17).19-35,37,38,40,42-66,68-76,78-82,86-92,94-106,108

Quality assessmenteORION statement recommendations

No report achieved full compliance with the ORION checklist(Table 2). Most relevant flaws were identified in the Methods sec-tions of the reports evaluated. Regarding study design, descriptiveepidemiology (85.1%; n ¼ 74) was more common than analyticmethods (14.9%; n ¼ 13); cohort studies and case-control studieswere carried out in 10.3% (n ¼ 9)45,46,48,52,53,55-57,78 and 4.6% (n ¼4)24,85,90,96 of the outbreaks, respectively.

As for the Introduction sections, the organism was described asepidemic or endemic in 62.1% (n ¼ 54) and the clinical backgroundwas explained in 57.5% (n ¼ 50) (ORION item 2).24-27,30-38,40-47,49-62,64,65,67-74,86,87,90,92,93,95,103,105,106,108

Participants (ORION item 7) were found to be unclear in most ofthe reports; for example, the case definition was described only in33.3% (n ¼ 29) and relevant information such as age and length ofstay was rarely presented (9.2%; n ¼ 8 and 13.8%; n ¼ 12, respec-tively).24,26,27,30-33,36-39,45,46,48,50,52-58,62,64,67-73,76-80,83,85,87,90-93,95-103

Failures in describing the setting (ORION item 8) occurred in 22(25.2%) of the reports. Although information on the number of bedswas given in 44.8% (n ¼ 39) and the presence of infection controlteam in 86.2% (n ¼ 75) of studies, the patient to staff ratio was notreported in any of the studies.22-108

Interventions (ORION item 9) were described without details,using generic language such as “reinforcement of infection controlpractices,” “environmental cleaning,” and “cohort.” In 7 cases theinterventions were implemented in phases, due to initial insuffi-ciency in controlling the outbreak.22,25-38,40,41,43,45-51,53-57,62,69,71-73,76-78,81-87,89,90,92,94,95,97-106,108

Cultures were performed in 88.6% (n ¼ 77) of studies and in18.4% (n¼ 16) of reports details of the culture media or antibiogram

Table 2Analysis of outbreak reports in São Paulo State, Brazil, 2000-2010, according to theOutbreak Reports and Intervention studies of Nosocomial Infection (ORION)statement

ORION itemAt least 1 descriptoraccording to ORION

All the descriptorsaccording to ORION

Title and abstract 73/87 (83.9) 58/87 (66.7)Introduction 73/87 (83.9) 28/87 (32.2)BackgroundType of paper 85/87 (97.7) 85/87 (97.7)Dates ey 82/87 (94.3)Objectives ey 65/87 (74.7)

MethodsDesign 66/87 (75.8) 29/87 (33.3)Participants 51/87 (58.6) 2/87 (2.3)Setting 87/87 (100) 40/87 (46)Interventions 42/87 (51.9) 42/87 (51.9)Culturing and typing 60/87 (69) 48/87 (55.2)Infection-related outcomes 72/87 (82.8) 2/87 (2.3)Economic outcomes Not relevantPotential threats to

internal validity*ey 3/13 (23.1)

Sample size Not relevantStatistical methods* ey 11/13 (84.6)

ResultsRecruitment Not relevantOutcomes and estimation ey 34/87 (39.1)Ancillary analyses* ey 8/13 (61.5)Harms Not relevant

DiscussionInterpretation 78/87 (89.7) 78/87 (89.7)Generalizability 34/87 (39) 11/87 (12.6)Overall evidence ey 34/87 (39)

NOTE. Values are given as n (%).*Only for cohort or case-control study.yItems with only 1 descriptor.

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were not given (ORION item 10). Genotyping was reported for48.9% (n ¼ 43) of outbreaks, with pulsed field gel electrophoresisbeing the most common method (33.3%; n ¼ 29), followed by po-lymerase chain reaction (4.6%; n¼ 4).22-35,37-48,50-53,55-80,82-108 Onlyin scabies reports were there no biological tests performed 4.7%(n ¼ 4), with clinical symptoms considered as the criteria forcases.36,49,54,81 We identified that 74.7% (n ¼ 65) of reports clearlydefined outcomes (ORION item 11), and in 14.9% (n ¼ 13) a chartwas donewith duration of patient stay and dates of detection of theorganism. In the 13 reports where analytic epidemiology was per-formed, the description of potential bias and confounders (ORIONitem 13) were found in 23.1% (n ¼ 3).24,45,46,48,52,53,55-57,78,85,90,96

In the Discussion sections authors were able to showconcern forthe clinical significance of observations they made during theirinterpretation of the findings (89.7%; n ¼78) and explanatory hy-potheses were generated in all of the reports (89.7%; n ¼ 78)(ORION item 20). Only 36.8% (n ¼ 32) of the Discussion sectionscovered how results could be generalized to different target pop-ulations or settings (ORION items 21 and 22) and the feasibility ofinterventions was also poorly described (this was present in 13.8%[n ¼ 12] of reports).22-38,40,41,43,45-67,69-99,103-105,108

DISCUSSION

Our study summarizes a sample of the outbreaks occurring inSão Paulo State, Brazil, over a given period. In fact, there is a highprobability that many other outbreaks occurred without beingdivulged or reported to the appropriate health authorities. Thislimits our knowledge of the epidemiologic features of the out-breaks, and therefore this may not be an unbiased sample,leading to a point where certain studies are published and others

are not. Some researchers have noted that studies associatedwith multidrug-resistant pathogens may have a greater likeli-hood of being published, and outbreaks with higher attack ratesare more likely to be reported than those with lower attackrates.109,110 Fear of being exposed may prevent health care facil-ities from sharing, in scientific media, the knowledge gatheredfrom outbreak experiences. The concern for potential penaltymay explain the low proportion of outbreak notification to thehealth authorities.111

Only a few of the outbreak investigation reports we reviewedwere designed as analytic epidemiologic studies. This may be dueto a lack of resources or limited availability of infection control staff.On the other hand, almost half of the reports used some kind ofmolecular fingerprinting method. In accordance, Gastmeier et al111

observed an increasing number of outbreak investigations that usegenotyping methods, whereas application of analytic epidemio-logic studies was still below expectations. This can be attributed topublication bias, because a study using genotyping methods mighthave a better chance of publication.

The predominance of outbreak reports in intensive care unitshas been previously identified and neonatal intensive care unitsappear to be the most important subgroup.111-114 The vulnerabilityof these patients, the degree of invasiveness, and the systematicsurveillance system in these areas contributed to these results.Bloodstream infection appeared as an important site of infectiondue to both the severity of the disease and its association withcontaminated substances or devices that can infect numerous pa-tients.111 Many reports we reviewed described multiple sites ofinfection in the same outbreak, a fact that was not observed in otheroutbreak reviews.114,115

A large variety of infection control measures were identified andthe reinforcement of standard infection control practices was themost common action applied, including environmental cleaning,which is known to have a positive influence on the control ofoutbreaks.116 It is of the utmost urgency to reinforce efforts forcontinuous educational programs aimed at preventing HAIs,thereby avoiding the occurrence outbreaks.

In a previous study dealing with outbreak investigations, thesource of transmission was identified in 61.3% of the outbreaks re-ported, and the most common source was index patients.115 In ourstudy, we observed quite a different situation; the source of trans-mission was identified in fewer than half of investigations and thelead position was held by contaminated substances. Interestingly,we found that most substances became contaminated intrinsically,in contrast to what was reported by Vonberg,117 who identifiedcontamination happening more frequently during the use of aproduct. This suggests that the overall quality control of medicaldevices and products could be below acceptable levels, pointing tothe need for better sanitary control. The lack of case definition foundin many reports suggests defective investigation methods, possiblycontributing to misleading information because investigators mighthave included patients not necessarily qualifying as a case.

By using the ORION checklists, we found that important infor-mation associated with outbreak investigations was missing inmany of the reports evaluated in our study. It is highly probable fora similar situation to occur in other regions of Brazil and abroad. Itis possible that in conferences the space provided for abstractscould be a limitation to showing all of the information required foroutbreak reports according to ORION recommendations.

Methodologic weaknesses and inadequate reporting are com-mon in hospital infection control literature, and concern for thestandards of research publication in infection control has beendiscussed in the scientific community. The ORION statement wascreated to help remedy this problem and encourage improvedreporting and higher standards of research.118 The Outbreak

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Database has endorsed the statement, as have some journals, andthe Society for Healthcare Epidemiology of America and the Euro-pean Congress of Clinical Microbiology and Infectious Disease haveused the ORION abstract checklist for studies submission for theirconferences.9-12,17,18,118

Our findings highlight that the ORION statement contributes tothe development of a stronger evidence base for sound infectioncontrol policies because it can make case reports much more usefulin the prevention and control of HAIs, and it may also improve thequality of case-control, cohort, and cross-sectional studies.

Notification of outbreaks to relevant health authorities isfundamental in driving governmental measures aimed at prevent-ing new cases, deaths, and epidemics. The role of such authoritiesgoes beyond dealing with an outbreak at the point at which it oc-curs. Strategies to support health care facilities via strong educa-tional programs for preventive measures and hospital epidemiologyare essential. It is of the utmost importance that authorities create atolerant environment to promote confidence within health caresettings to report such events, thusminimizing fear of repercussionsand empowering proactiveness for prevention.

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