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American Journal of Infection Control 44 (2016) 465-9

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American Journal of Infection Control American Journal of


Infection Control

j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g

Major article

Recovery of resistant bacteria from mattresses of patients under


contact precautions
Roberta El Hariri Viana MSN a, Simone G. dos Santos PhD b, Adriana C. Oliveira PhD, RN c,*
a Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
b Department of Microbiology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
c Department of Basic Nursing, School of Nursing, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

Key Words: Background: Microorganisms may contaminate hospital mattresses even after terminal cleaning. We in-
Patient safety vestigated the recovery of resistant bacteria from the mattresses of patients under contact precautions
Disinfection at a university hospital.
Antibiotic-resistant bacteria
Methods: We conducted a cross-sectional study. Samples were obtained from the surface of mat-
Hospital infection
tresses, spread on replicate organism detection and counting plates, and cultivated at 37°C for 48 hours.
After collecting samples, we identified microorganisms and tested for antimicrobial susceptibility using
the Vitek 2 (bioMérieux SA, Marcy-l’Etoile, France) automation system.
Results: We evaluated 51 mattresses. A total of 26 had resistant bacteria on the surface; the predomi-
nant species were Acinetobacter baumannii (69.2%), Klebsiella pneumoniae (11.5%), and Pseudomonas aeruginosa
(11.5%). The median length of hospital stay was 41 days; the bed occupancy for patients under contact
precautions and the time at which the patient was diagnosed as a carrier of resistant bacteria was 18
days.
Conclusions: The phenotypic similarity of A baumannii in inpatient units (mattresses) suggests circula-
tion of the same strain. These results highlight the importance of controlling the potential spread of
microorganisms through hospital mattresses.
© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier
Inc. All rights reserved.

INTRODUCTION try of Health has reported that the overall incidence is 9%-15%, with
14% mortality.1,3,4
Health care-associated infection (HAI) is an infection that pa- Pathogens responsible for HAIs often spread by cross-
tients acquire while receiving treatment for other conditions within contamination; the main sources are colonized patients, patients
a health care setting.1 HAIs are a worldwide health problem that with infectious diseases, and the hands of health professionals.
result in long periods of hospitalization, increased hospital costs, However, several studies point to possible environment sources in
increased use of antimicrobial agents, and high mortality rates. Above the maintenance and spread of pathogens that increase the likeli-
all, they adversely affect the productivity and quality of life of pa- hood that hospitalized patients will acquire HAIs.1,2,5-8
tients and their families.1,2 Although the role of the environment in the acquisition of patho-
The World Health Organization estimates that 5%-10% of pa- gens is unclear, epidemiologically relevant microorganisms have been
tients admitted to hospitals acquire 1 or more infections.1 In 2002, isolated in different hospital settings. Evidence exists that environ-
1.7 million patients were diagnosed with HAIs and in 2004 HAIs had ments occupied by patients infected with resistant bacteria may
an economic impact of $6.5 billion in the United States. Brazil does also become contaminated and contribute to the spread of
not have systematic data on the incidence of HAIs, but the Minis- pathogens.6,7,9-11
Hospital bed mattresses, which are prone to contamination, are
a potential reservoir of pathogens. The surfaces of mattresses may
be contaminated by microorganisms that colonize a patient’s skin,
* Address correspondence to Adriana C. Oliveira, PhD, RN, Department of Basic by body fluids such as urine and wound exudates, or by feces. Mat-
Nursing, School of Nursing, Universidade Federal de Minas Gerais, Rua Aimorés, 2162,
tresses with a high microbial load may contribute to the horizontal
apto 1601, 30140072 Belo Horizonte, Minas Gerais, Brazil.
E-mail address: adrianacoliveira@gmail.com (A.C. Oliveira). transmission of microorganisms between patients and other
Conflicts of interest: None to report. surfaces.12,13

0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ajic.2015.10.027
466 R. El Hariri Viana et al. / American Journal of Infection Control 44 (2016) 465-9

A better understanding of the role of environment surfaces in 2014.15 Antimicrobial drugs were selected based on microbial char-
the chain of pathogen transmission, especially surfaces in direct acteristics and clinical relevance.
contact with patients and frequently touched by health profession- We characterized the previous occupants of mattresses by search-
als, such as mattresses, is critically important. Such understanding ing the microbiology records of the institution to determine when
would help health care professionals to establish new strategies to the patients had been diagnosed as beingresistant bacteria carriers.
control the spread of microorganisms that may influence the oc- We tabulated and processed data using Stata version 12.0 (Stata
currence of HAIs and antimicrobial-resistant bacteria. We investigated Corp, College Station, TX), carried out univariate and multivariate
the recovery of resistant bacteria from the mattresses of patients analysis using Poisson regression, and calculated coefficients with
under contact precautions at a university hospital. 95% confidence intervals.

MATERIALS AND METHODS Ethical procedures

Trial design and characteristics of the evaluated service In accordance with Resolution 466/2012 of the National Health
Council, we conducted this study with approval from the Re-
We carried out a cross-sectional study in 9 inpatient units of a search Ethics Committee of the Federal University of Minas Gerais
547-bed public general university hospital in Belo Horizonte, Minas (CAAE-0386.0.203.000-11).
Gerais, Brazil. Two of the 9 inpatient units were intensive care units
(ICUs)—the adult intensive care and the coronary care unit; 7 were RESULTS
clinical units.
We analyzed 51 mattresses used by patients colonized or in-
Data collection fected by resistant bacteria. The median length of hospital stay was
We analyzed all beds occupied by patients colonized or in- 41 days; the bed occupancy for patients under contact precaution
fected by resistant bacteria between May 2014 and July 2014. We and the time at which the patient was diagnosed as a carrier of re-
collected 3 samples from each mattress, the first in the upper area sistant bacteria was 18 days.
(near the head of the mattress), the second in the middle, and the Specimens were collected in the mornings before bed-bath and
third in the bottom area (near the foot). We collected samples from environment cleaning. We obtained 306 samples, and bacteria were
the face of the mattress; that is, the surface on which a patient lies. cultured from 61.4% (188 out of 306) (Table 1).
All mattresses were analyzed in the early morning before the We obtained 473 isolates from the 188 positive samples; 275
patient’s bed bath and environment cleaning. were gram positive (58.1%) and 198 (41.9%) were gram negative. Plate
counts of colony forming units indicated that most mattresses (31
Laboratory procedures: Microbiologic evaluation of mattress out of 51) had an uncountable microbial load (Table 2).
Twenty-six (51.0%) of the 51 mattresses analyzed had resistant
We carried out microbiologic evaluation of mattress surfaces bacteria on their surface, predominantly Acinetobacter baumannii,
using BBL replicate organism detection (BBL, Biomérieux, Marcy- Klebsiella pneumoniae, and Pseudomonas aeruginosa (Fig 1).
l’Étoile, France) and counting (RODAC) plates to identify the genus All resistant microorganisms recovered from the mattresses had
and species of bacteria present in samples; antimicrobial suscep- a profile of resistance in accordance with the resistance marker pro-
tibility profiles were established using the disk diffusion in agar posed by CLSI.16 Staphylococcus aureus was resistant to methicillin,
method. Enterococcus faecium was resistant to all antibiotics tested, and En-
RODAC plates containing brain heart infusion broth and terococcus faecalis was resistant to vancomycin.
MacConkey culture media were seeded with mattress samples and The A baumannii strains were all resistant to ciprofloxacin,
incubated in the laboratory at 37°C for 48 hours in a bacteriologic ceftriaxone, and imipenem, and many were resistant to ceftazidime.
incubator. For each culture medium used, we registered the char- All P aeruginosa strains were resistant to imipenem, and some were
acteristics of the colonies and performed a semiquantitative resistant to ciprofloxacin or ceftazidime.
assessment of bacterial growth. We estimated the microbial load
present on the surface of each mattress from the number of colony-
Table 1
forming units identified on plates. With respect to total microbial Bacterial growth under culture medium
load, we categorized mattresses that had RODAC plates with bac-
Culture media
terial growth up to 300 CFU as countable; those with plates showing
growth of >300 CFU were categorized as uncountable. Brain heart MacConkey
Bacterial growth infusion broth agar Total
We identified microorganisms on the basis of morphology and
Gram’s staining pattern. Biochemical, physiologic, or enzymatic char- Positive 148 (78.7) 40 (21.3) 188 (61.4)
acteristics were determined with use of the Vitek 2 system Negative 05 (4.2) 113 (95.8) 118 (38.6)
Total 153 153 306
(bioMérieux SA, Marcy-l’Etoile, France), gram-negative bacteria and
gram-positive bacteria. To test antibiotic susceptibility, we per- NOTE. Values are presented as n (%).
formed the disk diffusion method for isolated bacteria according to
guidelines from the Clinical and Laboratory Standards Institute Table 2
Resistant bacteria of epidemiologic relevance recovered according to the total mi-
(CLSI).14 Bacterium inoculates were prepared by direct colony sus-
crobial load identified in the mattresses of patients under contact precautions
pension in saline solution to obtain a density equivalent to a 0.5
McFarland standard (about 8.0 log CFU/mL). The inoculum suspen- Recovery of resistant
bacteria of epidemiologic
sion was spread in 3 directions on a Mueller Hinton agar (Difco PR (95%
relevance
Laboratories, Detroit, MI) plate surface with a sterile swab and in- Total microbial Confidence
load Yes No interval) P value
cubated at 35°C ± 2°C aerobiosis for 16-18 hours. After incubation,
we measured the diameter of inhibition zones using an electronic Countable 8 (40.0) 12 (60.0) 1 .239
digital caliper (Series 727, Starrett, Athol, MA). We interpreted the Uncountable 18 (58.1) 13 (41.9) 1.45 (0.78-2.70)

results according to the critical points recommended by CLSI in NOTE. Values are presented as n (%). PR, poison regression.
R. El Hariri Viana et al. / American Journal of Infection Control 44 (2016) 465-9 467

20 73.1%

18

16

14

Number of Matress
12

10

4 11.5% 11.5%
7.7% 7.7% 7.7%
2

0
Acinetobacter Klebisiella VRE Pseudomonas Escherichia MRSA
baumannii pneumoniae aeruginosa coli
Antimicrobial resistant bacterial isolate

Fig 1. Distribution of resistant bacteria recovered from mattresses of patients under contact precautions.

10
9
8
Number of mattresses

7 Acinetobacter baumannii
6 Klebisiella pneumoniae
5 Pseudomonas aeruginosa
4 MRSA
3 Escherichia coli
2
Enterococcus faecium
1
Enterococcus faecallis
0
AICU 7 East* 8 East* 3 South* CCU 8 South* 10 South*
Inpatient units (*Clinical units)

Fig 2. Distribution of resistant bacteria recovered from mattresses according to the inpatient unit. AICU, adult intensive care unit; CCU, coronary care unit.

All K pneumonia strains were resistant to at least 2 antibiotic according to the microbiology records of the institution. The species
agents, usually ampicillin, imipenem, or ceftriaxone. All Escheri- were especially K pneumoniae, P aeruginosa, and methicillin-
chia coli strains were resistant to ampicillin, ceftriaxone, and resistant Staphylococcus aureus (MRSA). In other words, mattresses
imipenem. previously occupied by patients with K pneumoniae, P aeruginosa,
We observed that 80.7% (21 out of 26) of the analyzed mat- and MRSA remained contaminated even after terminal cleaning.
tresses were contaminated by only 1 of the identified antimicrobial- For antimicrobial therapy, vancomycin was the antibiotic most
resistant bacteria, but 19.2% (5 out of 26) were contaminated often used (75.5%) in patients under contact precautions in this study,
by >1 bacterium. The area of mattresses from which bacteria were followed by meropenem (73.4%), polymyxin (51%), cefepime (36.7%),
most often recovered was the lower region (73.1%), followed by the and others. Data of duration in days for antimicrobial therapy for
upper region (50%), and the middle (42.3%). patients under contact precautions are presented in Table 3.
A baumannii strains were present in most contaminated mat-
tresses (19 out of 26) (Fig 2) and 77.7% (7 out of 9) of inpatient units
in the study. DISCUSSION
In 13 of 26 beds (50.0%) from which resistant bacteria were re-
covered, the phenotype was the same as that registered for the Evidence of microbial growth was present in all evaluated mat-
patient occupying the bed at the time the mattress samples were tresses and, in most cases, the identified species involved resistant
taken, especially A baumannii in 92% of the isolates. bacteria. The detection of microorganisms on mattress surfaces re-
In cases in which the isolated microorganism on the mattress inforces the fact that the surroundings of colonized or infected
was different from that associated with the bed’s current occu- patients can become contaminated with bacteria and confirms that
pant, 54% (7 out of 13) of the microorganisms phenotypically mattresses are a potential reservoir of pathogens in health
resembled those associated with the bed’s previous occupant, facilities.11,12,15-17
468 R. El Hariri Viana et al. / American Journal of Infection Control 44 (2016) 465-9

Table 3 In this study, the rate of contamination of mattresses with re-


Average length of antimicrobial therapy in patients under contact precautions sistant bacteria was highest in ICUs. Several studies around the world
Average time of have provided evidence of environment contamination in ICUs; the
Antimicrobial agent antimicrobial use, d high prevalence of resistant microorganisms in ICUs may be attrib-
Clarithromycin 10.0 uted to factors such as the severity of patients’ illnesses, extended
Metronidazole 10.4 periods of hospitalization, use of invasive procedures, low-quality
Daptomycin 12.5
cleaning and disinfection, physical structures of ICUs, and low ad-
Ceftriaxone 13.1
Amikacin 13.7 herence to hand hygiene.4,10
Vancomycin 13.8 The bacteria most often associated with cases of colonization were
Moxifloxacin 14.0 vancomycin-resistant enterococci. The high frequency of coloniza-
Polymyxin 15.4 tion of patients with this bacteria can be attributed to the significant
Ceftazidime 16.0
Meropenem 18.5
increase in the presence of vancomycin-resistant enterococci in hos-
Trimethoprim-sulfamethoxazole 19.2 pitals since 1990, when it was first isolated in the United States. The
Cefazolin 21.0 use of antibiotics is an important risk factor for colonization by re-
Ampicillin 24.7 sistant pathogens; in this study the antibiotic most frequently
Oxacillin 27.0
administered to patients was vancomycin (75.5%).23,24
The widespread use of antimicrobial agents reported in this study
reinforces concerns about the continuing emergence of resistant mi-
The predominant microorganisms recovered from mattresses in croorganisms in health institutions and even in the community.2,25
the study sample were resistant A baumannii strains, which can The emergence of resistance among microorganisms is a con-
survive in different environments and on dry surfaces from 3 days- stant challenge to researchers and to the pharmaceutical industry.
11 months.18 They can also form biofilm owing to various virulence Such resistance reduces the effectiveness of medicines, increases
factors and versatile metabolic capacity, which increases the chances duration of hospital stays, increases cost of treatment, and contrib-
of outbreaks. utes to increased morbidity and mortality associated with
The varied strains of A baumannii were recovered especially from infections.25
the lower regions of the mattress surface. This finding corrobo- Bacterial resistance to antimicrobial agents may result from either
rates similar research and correlates to how mattresses are typically novel mutation or transfer of genes causing resistance and
cleaned, from the upper region toward the lower region, which may environment-related stresses. Adaptation may occur naturally
move microorganisms but not eliminate them.15,19 because of the presence of genes that confer resistance to certain
The protocol of the hospital involved in the study recommends antimicrobial agents in various ways, and deserve special atten-
cleaning the frame, undercarriage, mattress, and base of the bed. tion in health care facilities.10
Beds should be decontaminated after each patient leaves (ie, ter- The lag between the time at which an individual is diagnosed
minal cleaning) and once per week when the bed is occupied by as a carrier of resistant bacteria and the recovery of epidemiologi-
same patient. This cleaning schedule aims to prevent dust accu- cally relevant numbers of bacteria from a mattress is probably
mulation and the harboring of microorganisms. During terminal because of the time required for microbial growth.
cleaning, lockers, bed tables, nurse call systems, bed controls, patient Knowledge of the factors associated with the recovery of resis-
chairs, oxygen and suction canisters, and other items need to be de- tant bacteria from mattresses can contribute to the development
contaminated. Environment surfaces that the patient contacts of improved cleaning procedures and changes in the behavior of
frequently (eg, bedside table, bed rails, and mattress) can be con- health professionals who treat patients under contact precautions.
taminated with epidemiologically relevant microbes. Hospital This study supports the idea that the environment is a poten-
protocol recommends the use of Glucoprotamin as an effective, tial source of transmission of microorganisms, especially when
rapidly acting bactericidal and fungicidal cleaning agent. Among terminal cleaning is not efficient. In addition, the findings show that
other institutions in Brazil, the local committee of hospital infec- greater attention should be given to units occupied by patients with
tion control may have other recommendations about which resistant microorganisms where the chance of survival of these mi-
disinfectant to use for cleaning the patient unit.20 croorganisms is increased.
When the bacteria recovered from the mattress were pheno- One limitation of the study was the use of a convenience sample;
typically different from the bacteria associated with the bed’s current cultures were not taken after terminal cleaning. The collection of
occupant, we sought to identify if the bed’s previous occupant had samples after terminal cleaning (ie, cleaning that occurs upon a
been a carrier of a resistant microorganism. In those cases, micro- patient’s departure) was beyond the scope of the study. Patients
biology laboratory records of the institution pointed out that could depart at any time of day, and we were not able to collect
especially the strains of K pneumoniae, P aeruginosa, and MRSA iso- samples at all times within a 24-hour period. In addition, the high
lated from the mattresses were phenotypically similar to the rate of patient turnover meant that beds needed to be prepared
microorganism carried by the bed’s previous occupant. This result quickly for other patients, which left little time to collect samples
aligns with studies that refer to a small but significant increase in before environment cleaning occurred. However, the study was not
the risk of acquiring MRSA if patients are admitted into rooms pre- intended to evaluate the immediate effectiveness of terminal clean-
viously occupied by carrier patients21 and reinforces flaws in terminal ing but rather to examine the potential for resistant microorganisms
cleaning procedures. Other studies also reinforce the premise that to be transmitted through the mattresses of patients under contact
2.4%-64.3% of mattresses previously occupied by patients colo- precautions.
nized or infected with resistant bacteria remain contaminated even
after terminal cleaning.9,15,18,19
The results should prompt health care facilities to consider their CONCLUSIONS
cleaning procedures. Surfaces are usually cleaned mechanically with
disinfecting, germicidal agents, but such cleaning procedures and We recovered resistant bacteria from the majority of analyzed
their duration may be insufficient to act against microorganisms and mattresses, most often from the lower region of the surface. Patho-
reduce microbial contamination to safe levels.22 gens phenotypically similar to the microorganisms associated with
R. El Hariri Viana et al. / American Journal of Infection Control 44 (2016) 465-9 469

the patient currently occupying the mattress, and other species not 9. Datta R, Platt R, Yokoe DS, Huang SS. Environmental cleaning intervention and
risk of acquiring multidrug-resistant organisms from prior room occupants. Arch
associated with the current occupant, were present in mattresses.
Intern Med 2011;171:491-4.
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nated with resistant bacterial species associated with the current of resistant microorganisms present in reserves from an intensive care unit. Am
patient. The majority of microorganisms unrelated to the current J Infect Control 2012;40:186-7.
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