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Is the use of supermarket trolleys microbiologically safe? Study of microbiological contamination

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Microbial contamination in shopping trolleys (eighty five) by considering different supermarkets (seven) from three major food companies in Las Palmas de Gran Canaria (Spain) was determined. The two sampled areas were trolley handles and food trolley baskets-child seats. Samples were analyzed by selective and differential microbiological culture media. E. coli four (2.4%) indicative of faecal contamination, Klebsiella pneumoniae twelve (6.5%) and Citrobacter freundii, six (5.1%), which have been isolated from human faecal samples, were isolated from trolleys; Pseudomonas rhodesiae, five (4.25%), and Pseudomonas fluorescens, three (2.55%), which both evidenced environmental contamination. Significant differences among the companies were found for the Enterobacteriaceae and coliforms. Regarding location, these differences (p < 0.003) were observed only for the coliform rates, which were higher in trolleys located outside. The results of this study suggest the implementation of cleaning and disinfection programmes to improve trolley sanitation, and to reduce exposure to both potential pathogenic and transmitting bacterial infections.
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Journal of Applied Animal Research
ISSN: 0971-2119 (Print) 0974-1844 (Online) Journal homepage: http://www.tandfonline.com/loi/taar20
Is the use of supermarket trolleys
microbiologically safe? Study of microbiological
contamination
Conrado Carrascosa, Esther Sanjuán, Rafael Millán, Sara Martín, Pedro
Saavedra, António Raposo, Cristóbal del Rosario-Quintana & José Raduán
Jaber
To cite this article: Conrado Carrascosa, Esther Sanjuán, Rafael Millán, Sara Martín, Pedro
Saavedra, António Raposo, Cristóbal del Rosario-Quintana & José Raduán Jaber (2019) Is the use
of supermarket trolleys microbiologically safe? Study of microbiological contamination, Journal of
Applied Animal Research, 47:1, 17-23, DOI: 10.1080/09712119.2018.1555091
To link to this article: https://doi.org/10.1080/09712119.2018.1555091
© 2018 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group
Published online: 12 Dec 2018.
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Is the use of supermarket trolleys microbiologically safe? Study of microbiological
contamination
Conrado Carrascosa
a
, Esther Sanjuán
a
, Rafael Millán
a
, Sara Martín
a
, Pedro Saavedra
b
, António Raposo
c,d
,
Cristóbal del Rosario-Quintana
e
and José Raduán Jaber
f
a
Department of Animal Pathology and Production, Bromatology and Food Technology, Faculty of Veterinary, Universidad de Las Palmas de Gran
Canaria, Arucas, Spain;
b
Department of Mathematics, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain;
c
Department for
Management of Science and Technology Development, Ton Duc Thang University, Ho Chi Minh City, Vietnam;
d
Faculty of Environment and Labour
Safety, Ton Duc Thang University, Ho Chi Minh City, Vietnam;
e
Microbiology Service, Complejo Hospitalario Materno-Insular de Gran Canaria, Canary
Health Service, Las Palmas de Gran Canaria, Spain;
f
Department of Morphology, Faculty of Veterinary, Universidad de Las Palmas de Gran Canaria,
Arucas, Las Palmas, Spain
ABSTRACT
Microbial contamination in shopping trolleys (eighty ve) by considering dierent supermarkets (seven)
from three major food companies in Las Palmas de Gran Canaria (Spain) was determined.
The two sampled areas were trolley handles and food trolley baskets-child seats. Samples were
analyzed by selective and dierential microbiological culture media.
E. coli four (2.4%) indicative of faecal contamination, Klebsiella pneumoniae twelve (6.5%) and
Citrobacter freundii, six (5.1%), which have been isolated from human faecal samples, were isolated
from trolleys; Pseudomonas rhodesiae,ve (4.25%), and Pseudomonas uorescens, three (2.55%), which
both evidenced environmental contamination. Signicant dierences among the companies were
found for the Enterobacteriaceae and coliforms. Regarding location, these dierences (p< 0.003) were
observed only for the coliform rates, which were higher in trolleys located outside.
The results of this study suggest the implementation of cleaning and disinfection programmes to
improve trolley sanitation, and to reduce exposure to both potential pathogenic and transmitting
bacterial infections.
ARTICLE HISTORY
Received 1 August 2018
Accepted 27 November 2018
KEYWORDS
Food baskets-child seats;
handles; microbiological
contamination; shopping
trolleys; surfaces
Introduction
Inanimate objects (fomites) for public use, such as shopping
trolley handles, lift buttons, handrails, etc, which come into
direct contact with usershands, are a source of contamination
of potential pathogenic microorganisms. They come into
contact either directly by surface-to-mouth contact or indirectly
by contaminated ngers and subsequent hand-to-mouth
contact (Gerba and Maxwell 2012; Irshaid et al. 2014). Some
studies have reported frequent exposure to pathogenic Staphy-
lococcus aureus on shopping trolley handles, suggest that it is a
hidden reservoir of this organism, and indicate a shopping
basket/trolley sanitation necessity (Mizumachi et al. 2011).
Shopping trolley contamination may occur from directly hand-
ling raw food products or trolleys contaminated by previous
users (Gerba and Maxwell 2012). Nevertheless, cross-contami-
nation in shopping trolley baskets occurs when disease-
causing microorganisms are transferred from one food type
to surfaces or, as in this case study, when dirty hands transfer
microorganisms to trolley handles or baskets. For example,
raw meat products are often contaminated with foodborne bac-
teria, such as Salmonella and Campylobacter (Bier et al. 2004),
which may be transferred to surfaces. However, the level of bac-
terial contamination on shopping trolleys or shopping baskets
is limiting making health assessment dicult (Mizumachi
et al. 2011). It is believed that up to 80% of common infections
can be spread through coming into contact with contaminated
surfaces (Reynolds et al. 2005). Pathogenic organisms, i.e.
viruses, bacteria and protozoa, may be excreted in large
numbers in biological substances, including blood, mucus,
saliva, faeces and urine (Hall and Douglas 1981; Hall et al.
1981; Feachem et al. 1983; Uhnoo et al. 1990; Weber et al.
1994; Islam et al. 2001). Some microbes are infectious at very
low concentrations and can survive on dierent surfaces like
countertops and telephone handpieces for hours, and even
for weeks (Noskin et al. 1995; Bures et al. 2000; Abad et al. 2001).
Hands are frequently involved in such episodes, and act as
vehicles that spread infections in both the community and hos-
pitals (Pittet et al. 2000). Several studies have been published
about microorganism contagion from contaminated fomites
with pathogens to healthcare workershands in hospitals
(Kramer et al. 2006; Mizumachi et al. 2011). However, a corre-
lation between the burden of contamination on hands and the
likelihood of transmission to patients has not yet been estab-
lished (Bellissimo-Rodrigues et al. 2017). Nonetheless, common
infectious diseases still feature among the top 10 leading
causes of death (Liu et al. 2012; Willmott et al. 2016), and health-
care-associated infections are recognized as a major cause of
preventable death in healthcare settings (Willmott et al. 2016).
© 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group
This is an Open A ccess artic le distributed under the terms of the Creative Common s Attributio n License (http://creativecommons.org/licenses/by/4.0/), which pe rmits unrestricted use,
distributio n, and reprod uction in any medium, prov ided the original work is properly cited .
CONTACT António Raposo antonio.raposo@tdtu.edu.vn
JOURNAL OF APPLIED ANIMAL RESEARCH
2019, VOL. 47, NO. 1, 1723
https://doi.org/10.1080/09712119.2018.1555091
Regarding bacterial persistence on surfaces, enterococci
species are able to survive for 24 h with no signicant reduction
in colony counts. Most gram-positive bacteria, such as Entero-
coccus spp. (including VRE), S. aureus (including MRSA) or Strep-
tococcus pyogenes, survive for months on dry surfaces (Kramer
et al. 2006). Many gram-negative species can also survive for
months, such as Acinetobacter spp., Escherichia coli,Klebsiella
spp., Pseudomonas aeruginosa,Serratia marcescens or Shigella
spp. A few others, like Bordetella pertussis,Haemophilus inuen-
zae,Proteus vulgaris or Vibrio cholerae, persist only for days
(Kramer et al. 2006).
Interestingly, vancomycin-resistant enterococci are
capable of prolonged survival on hands, gloves and environ-
mental surfaces, they persist for 60 min on telephone hand-
pieces and for 30 min on the diaphragmatic surface of a
stethoscope (Noskin, et al. 1995). Other authors (Wade et al.
1991) have documented the survival of vancomycin-resistant
E. faecium on hands for up to 30 min and bacteria such as
S. aureus,Acinetobacter,Klebsiella aerogenes,Escherichia coli,
Serratia marcescens,andPseudomonas aeruginosa (Casewell
and Desai 1983). Hence hand washing is considered an essen-
tial aspect of infection control to prevent microorganisms
from being transmitted. A 30-second wash with soap and
water is necessary to completely eradicate bacteria from
hands (Noskin et al. 1995).
The increased availability of shopping trolleys in supermar-
kets, handled by numerous users on a daily basis, and the fact
that trolleys are not routinely disinfected, are a potentially
excellent opportunity for contaminating microorganisms to
be transmitted (Anderson and Palombo 2009). This is particu-
larly true for infants and children under the age of 5 years
with reported 2- to 10-fold higher risk rates than for people
aged 5 years or more (Jones et al. 2006; Ailes et al. 2008).
Riding infants in a shopping trolley next to packaged raw
meat and poultry has been shown to be an important risk
factor for Salmonella spp. and Campylobacter spp. infection,
with attributable risks of 11% and 7%, respectively (Jones
et al. 2006; Fullerton et al. 2007; Patrick et al. 2010) as these
microorganism have been isolated from outer packages of
meat and poultry products at retail outlets (Harrison et al.
2001; Wong et al. 2004; Burgess et al. 2005).
The aim of this study was to determine the microbial con-
tamination and bacterial species on shopping trolley handles
and baskets in dierent supermarkets on the Gran Canaria
Island (Spain). In addition, the statistic relationship between
metal and plastic shopping trolleys microbiological contami-
nation was studied, as was the location of trolleys, either
outside or inside supermarkets.
Material and methods
Sampling was performed in three dierent supermarket compa-
nies of Las Palmas de Gran Canaria (A, B, C), the Canary Islands
(Spain), for 3 months. Eighty-ve shopping trolleys from seven
supermarkets were sampled to determine the microbiological
contamination on trolleys. We collected 85 swabs from trolley
handles and 83 other swabs from the food baskets-child seats
(basket-seat). The latter samples were considered from a
single site (Figure 1).
Sampling the contact surfaces of trolleys
To this end, a maximum 100-cm
2
area was sampled per swab.
Shopping trolleys were sampled for microbial contamination,
and were subsequently tested for the qualitative analyses of
pathogenics (Gerba and Maxwell 2012). A sterile rayon-tipped
swab (Copan Flock Technologies Srl., Brescia, Italy), moistened
with sterile saline solution (preservative-free), was moved over
the entire surface of trolley handles and a new swap was
used over baskets-seats. Swabs were aseptically transferred to
a tube that contained 10 ml of sterile 0.1% peptone water
(adapted from Salo, et al. 2002), and were delivered 2 h after
being packed on ice to be sent to the Hygiene Laboratory of
Veterinary Faculty of Las Palmas de Gran Canaria University,
where samples were processed before 24 h had elapsed.
The total number of shopping trolleys from each sampled
company was determined by a statistical stratied analysis,
where the following were sampled: 35 (2,700 in all) shopping
trolleys in one supermarket of company A; 30 (2,200 in all) shop-
ping trolleys in three supermarkets of company B; 20 (800 in all)
shopping trolleys in three supermarkets of company C.
Microbiological analysis and identication
Decimal dilutions in peptone water solution (0.85% NaCl with
0.1% peptone; Cultimed, Barcelona, Spain) were used for
microbial enumeration purposes. Tubes were shaken vigor-
ously. Appropriate dilutions were prepared by using sterile
0.1% peptone water and were plated by the pour plate
method on dierent bacteria selection agar (Figure 1). After
incubating the plate, the morphological characteristics of
microorganisms were associated with each growth medium.
Data are reported as colony-forming units (CFU/cm
2
). All the
counts were taken in duplicate.
Total viable counts (TVCs) and mesophilic bacteria were deter-
mined using Plate Count Agar (PCA Cultimed, 413799), and were
incubated at 31°C for 72 h (Pascual and Calderón 2002; Broekaert
et al. 2011). Enterobacteriaceae were determined using Violet
Red Bile Glucose Agar (VRBG), (Cultimed, 413745, Barcelona
Spain). Incubation was done at 37°C for 24 h. Bacteria were rep-
resented as large colonies with purple haloes, as described by
other authors (Pascual and Calderón 2002).
S. aureus was isolated by Baird Parker+Rabbit Plasma Fibro-
nogen agar (bioMerieux, Marcy ĺEtoile, France; ISO 68882;
ISO, 1999), and was incubated at 37°C for 2448 h. Escherichia
coli was identied by ChromID coli® (bioMerieux; AFNOR,
2014) and was incubated at 37°C for 2448 h.
E. faecalis was determined in kanamycin-esculin-azide broth
(KAA) (Canamicina Esculina Azida, Cultimed, 464695.0922), and
was incubated at 35°C for 48 h following the manufacturers
instructions. Positive growth was considered if the tube
changed to blackish-green. E. faecalis was spread on KAA agar
and incubated at 35°C for 2448 h. Finally, grown colonies
were conrmed as E. faecalis when they were gram-positive
cocci with a negative catalase test, and were able to grow on
bile esculin agar (BEA) incubated at 42°C by esculin hydrolysis
(Greenberg et al. 1992; Dionisio and Borrego 1995).
The microorganisms isolated from VRBG plates were identied
using gram stain, colony counts, morphology, and catalase and
18 C. CARRASCOSA ET AL.
oxidase reactions. Gram-negative bacteria were identied by API
20 E and mass spectrometry in a Bruker Biotyper matrix-assisted
laser desorption ionisation-time of ight mass spectrometry
(MALDITOF MS) system (Bruker Daltonics, Germany) with a
higher score level than 2,200 for species identication.
The Analytical Prole Index (API) 20 E test kit (BioMerieux®,
Marcy ĺEtoile, France) was used following the manufacturers
instructions. Strips were examined after 24 and 48 h. Isolates
were identied according to the API 20 E identication online
instructions (http://apiweb.biomerieux.com).
There are no standards available for fomites surface counts.
However, a general microbial target value of <2.5 CFU/cm
2
after
disinfection has been found to be attainable for a range of sur-
faces in food industries (Carrascosa et al. 2012). The preliminary
data obtained in this study showed that the total viable counts
in non-disinfected objects were considerably higher. Even so,
were obtained an average of 753 CFU/cm
2
, a minimum of
80 CFU/cm
2
and a maximum of 18,700 CFU/cm
2
.
Statistical analysis
The contamination rates for the considered microorganisms
were summarized as frequencies and percentages, and were
compared by the Chi-square (χ
2
) or the exact Fisher test when-
ever appropriate. Odd ratios by means of 95% condence inter-
vals (95%CI) were used for the comparisons that showed
statistical signicance. Statistical signicance was set at p
< .05. Data were analyzed with the R package, version 3.3.1 (R
Development Core Team 2016).
Figure 1. Flowchart of sampling in the trolleys.
Table 1. Contamination rates of surfaces at dierent supermarket companies (A, B,
C) locations and shopping trolley materials.
Factor Microorganism Level n/ total (%)*
P-
value OR (95%CI)
Company Enterobacteria
(1)
A 22/35 (62.9)
a
.003 1
B 7/30 (23.3)
b
0.180 (0.061
0.534)
C 6/20 (30.0)
b
0.253 (0.078
0.821)
Coliforms (1) A 14/25 (56.0)
a
.013 1
B 6/30 (20.0)
b
0.196 (0.060
0.648)
C 2/10 (20.0)
a,b
0.196 (0.035
1.118)
Enterobacteria
(2)
A 24/35 (68.6)
a
.008 1
B 9/30 (30.0)
b
0.196 (0.068
0.566)
C 9/18 (50.0)
a,b
0.458 (0.143
1.473)
Coliforms (2) A 15/25 (60.0)
a
.028 1
B 10/30 (33.3)
b
0.333 (0.111
1.004)
C 7/9 (77.8)
a
2.333 (0.400
13.609)
(*) Distinct superscripts (
a, b, c
) indicate signicant dierences for p< .05.
Surface sampled: 1, handles; 2, food baskets-child seats.
JOURNAL OF APPLIED ANIMAL RESEARCH 19
Results
Eighty-ve shopping trolleys were sampled, and the enteric
bacteria species on handles and baskets-child seats were iso-
lated. Shopping trolley handles were found to be contaminated
by enterobacteria on thirty ve (41.17%) surfaces and on forty
three (50.6%) baskets-child seats. Coliforms were growing on
handles on twenty two (25.9%) trolleys and on thirty nine
(45.9%) baskets-child seats. E. coli was identied only on three
(2.55%) basket-child seats. Neither S. aureus nor E. faecalis was
detected by specic agar medium.
Table 1contains the contamination rates of the sampled sur-
faces of the dierent supermarket companies (A, B, C). This table
also summarizes the contamination rates according to super-
market companies, location and material (Table 2). Company B
showed signicantly lower contamination rates than those
obtained for Company A for enterobacteria on handles (23.3%
vs. 62.9%), coliforms on handles (20% vs. 56%), enterobacteria
on baskets (30% vs. 68.6%) and coliforms on baskets (33.3% vs.
60%). All the results obtained from Companies A, B and C
showed signicant dierences for the coliforms and enterobac-
teria rates on both surfaces. E. coli on baskets was detected only
on one Company A trolley, whereas S. aureus and E. faecalis were
not detected on any analyzed trolley from companies A, B, C.
For the relationship of the location (outside or inside) of
shopping trolleys in supermarkets and their contamination,
we found signicant dierences, but only for the coliforms
rates (56.0% vs. 20.0%, p= .003) on handle surfaces. Contami-
nation was higher outside than it was inside (Table 2). Likewise,
the comparison made of the plastic and metal material used to
manufacture shopping trolleys showed no signicant
dierences (Table 2). The highest contamination rates on
handles and on basket-child seats were on plastic material,
except for coliforms contamination on handles, which was
higher for metal trolleys (Table 2).
In addition, E. coli and other potential pathogenic bacteria
were also isolated from both surfaces, but showed dierent
rates. The isolations of the bacteria that belonged to the Enter-
obactericeae family were particularly interesting, including Kleb-
siella pneumoniae isolated from 11 (6.5%) shopping trolleys,and
Citrobacter freundii isolated from 6 (5.1%), which may be found
in human faeces. Pseudomonas rhodesiae and P.uorescens
were isolated from ve (4.25%) and three (2.55%) shopping trol-
leys, respectively, and these bacteria evidenced environmental
contamination. Table 3shows other bacteria of special interest
that were isolated from trolleys.
Discussion
Microbiological counts in the analyzed shopping trolleys from
dierent supermarkets showed a high contamination rate on
both sampled surfaces, which was slightly higher on baskets-
child seats. Most studies about fomites contamination have
been undertaken on hospital equipment surfaces (Kramer
et al. 2006; Bellissimo-Rodrigues et al. 2017), but very few
studies have determined contaminated shopping trolleys (Al-
Ghamdi et al. 2011; Ashgar and El-Said 2012; Gerba and
Maxwell 2012; Irshaid et al. 2014), which indicates that consu-
mers are exposed to enteric bacteria from grocery shopping
trolleys on a regular basis. In our study, total bacterial levels
were far higher than those found in public restrooms and
other public places (airports, bus stations, public bathroom,
shopping malls, etc.) reported by other authors (Gerba and
Maxwell 2012). Those studies had sampled dierent surfaces
with the same swab (handles-child seat) and obtained a
single result for all the surfaces.
In the present study, we found up to 45.9% of coliforms and
2.45% of E. coli, whereas Gerba and Maxwell (2012) found
higher rates (72% and 21.17%, respectively). Similar results
were shown by Reynolds et al. (2005) and Al-Ghamdi et al.
(2011) and who determined 20% of coliform and 7% of faecal
coliform contamination, respectively. Regarding contamination
sources, Reynolds et al. (2005) found no relationship to link bio-
chemical markers, protein and bacterial contamination on
public surfaces, including shopping trolley handles. While the
presence of biochemical markers and protein provides
Table 2. Contamination rates of surfaces at dierent locations and shopping
trolley materials.
Factor Microorganism Level n/ total (%)*
P-
value OR (95%CI)
Location Enterobacteria
(1)
Inside 13/40 (32.5) .125 1
Outside 22/45 (48.9) 1.987 (0.822
4.803)
Coliforms (1) Inside 8/40 (20.0) .003 1
Outside 14/25 (56.0) 5.091 (1.684
15.390)
Enterobacteria
(2)
Inside 16/39 (41.0) .100 1
Outside 26/44 (59.1) 2.076 (0.864
4.989)
Coliforms (2) Inside 17/39 (43.6) .200 1
Outside 15/25 (60.0) 1.941 (0.700
5.384)
Material Enterobacteria
(1)
Metal 7/24 (29.2) .158 1
Plastic 28/61 (45.9) 2.061 (0.747
5.681)
Coliforms (1) Metal 6/14 (42.9) .527 1
Plastic 16/51 (31.4) 0.610 (0.181
2.049)
Enterobacteria
(2)
Metal 9/22 (40.9) .289 1
Plastic 33/61 (54.1) 1.702 (0.634
4.572)
Coliforms (2) Metal 6/13 (46.2) .756 1
Plastic 26/51 (51.0) 1.213 (0.358
4.113)
(*) Distinct superscripts (
a, b, c
) indicate signicant dierences for p< .05.
Surface sampled: 1, handles; 2, food baskets-child seats.
Table 3. Relation of the bacteria of special interest isolated from trolleys identied
with MALDITOF.
Isolated Bacteria n/ total (%)
E. coli 4 (2.4)
Klebsiela pneumoniae 11 (9.3)
Citrobacter freundi 9 (5.3)
Pseudomonas rhodesiae 4 (2.3)
Pseudomonas uorescens 3 (1.7)
Enterococcus faecalis 3 (1.7)
Staphylococcus haemolyticus 3 (1,7)
Streptococcus gallolyticus 3 (1.7)
Morganella morganii 2 (1.2)
Proteus mirabilis 2 (1.2)
Enterobacter asburiae 2 (1.2)
20 C. CARRASCOSA ET AL.
information on the relative hygiene of various environments,
very little is known about their correlation with infectious
microbes (Reynolds et al. 2005). Nonetheless, other authors
have described longer microbial persistence with higher inocu-
lum in the presence of protein (Neely 2000), serum (Elmos 1977;
Hirai 1991) or without dust (Wagenvoort and Penders 1997), but
these studies were undertaken on fomites in hospitals.
Thus persistence of bacteria on surfaces can vary subject to
intrinsic factors from microorganisms: gram-negative bacteria
have been described to persist longer than gram-positive bac-
teria (Dickgiesser 1978; Hirai 1991). The latter are transmitted
readily from environmental surfaces, followed by viruses and
gram-negative bacteria (Rusin et al. 2002). Humid conditions
and low temperatures, e.g. 4°C or 6°C, also improve the persist-
ence of most bacteria types, such as Listeria monocytogenes
(Helke and Wong 1994), Salmonella typhimurium (Helke and
Wong 1994), Methicillin-resistant Staphylococcus aureus
(MRSA) (Noyce et al. 2006), or Escherichia coli (Wilks et al.
2005; Williams et al. 2005). These risks can be minimized by
applying a shopping trolley cleaning and disinfection pro-
gramme using antimicrobial agents, according to the data
reported in this eld (Rutala and Weber 2001; Engelhart et al.
2002), and by devising ecient planning to rotate the periodical
cleaning of all supermarket trolleys (between 800 and 2,700
trolleys per supermarket).
The potential pathological microorganism ndings on the
shopping trolleys included in this study agree with those
reported by other authors (Reynolds et al. 2005; Al-Ghamdi
et al. 2011; Ashgar and El-Said 2012; Gerba and Maxwell
2012). Our results revealed the importance of cleaning and dis-
infecting shopping trolleys to avoid the presence of K. pneumo-
nia, which is an opportunistic pathogen responsible for a high
proportion (48%) of nosocomial infections (Podschun and
Ullmann 1998).
In addition, many studies have clearly shown that E. coli is
the only coliform that is an undoubted inhabitant of the gastro-
intestinal tract. While Klebsiella spp., Citrobacter freundii and
Enterobacter have been isolated from human faecal samples,
they are in small numbers when present (Edberg et al. 2000).
However, these opportunistic pathogens isolated herein such
as C. freundii, which can cause systemic infections (Kim et al.
2003; Pereira et al. 2010; Chen et al. 2011). Moreover, C. freundii
has been used to control good healthy measures, like periodical
cleaning of tools and abattoir surfaces (Milhem et al. 2016).
P. uorescens has been reported to cause infections like blood
transfusion-related septicaemia (Khabbaz et al. 1984). Thus,
results of epidemiological studies have shown that a risk of
infection from common enteric bacteria is related to the
placing of small children in shopping carts (Fullerton et al.
2007; Patrick et al. 2010) and it increases the risk of coming
into contact with a disease-causing organism.
When comparing plastic or metal shopping trolleys, plastic
ones showed higher contamination, but dierences were not
signicant. Nevertheless, larger sample sizes should be con-
sidered to obtain signicant dierences (p< 0.05). the tested
material types gave no consistent results for nosocomial persist-
ent pathogenics on inanimate surfaces. Although some
researchers have reported that this type of material has no
inuence on persistence (Bale et al. 1993; Wendt et al. 1997),
other authors have described longer persistence on plastic
(Neely and Maley 2000). This topic can be clearly observed in
food industries, where the ability of many bacteria to adhere
to surfaces and to form biolms has major implications. Proper-
ties like surface roughness, cleanability, disinfectability, wett-
ability and vulnerability to wear inuence the ability of cells
to adhere to a particular surface, and thus determine the hygie-
nic status of materials (Van Houdt and Michiels 2010). Other
authors (Bellissimo-Rodrigues et al. 2017) have described a
direct relationship between the bacterial load present on
hands and the risk of cross transmission following a single
hand-to-hand contact. Under the described experimental con-
ditions, at least 1 log
10
CFU of E. coli must be present on
hands for it to be potentially transmitted to another person.
This threshold may be useful to develop an evidence-based
safe handsmicrobiological concept that can be applied in
the healthcare setting, and in the general community to
prevent infections and antimicrobial resistance from spreading
(Bellissimo-Rodrigues et al. 2017).
Conclusions
The obtained results suggest the need to establish adequate
cleaning and disinfection programmes for shopping trolleys in
order to avoid exposing shopping trolley users to infections.
The most eective measure could be the use of an alkaline deter-
gent and quaternary ammonium as a disinfectant, washing the
shopping trolleys once a month and doing a proper rotation of
them. The material (metal or plastic) and location (outside or
inside) of the shopping trolleys in the supermarkets should be
taken into consideration during the preparation of the cleaning
and disinfection plan, to reduce microbial contamination more
eectively. As additional measures, some studies have proposed
using disinfecting wipes or disposable plastic barriers for
handles. In the future, we hope to compare our contamination
results and potential pathogenic rates with other studies done
on supermarket trolleys, which have established a cleaning
and disinfection programme to assess their ecacy and to
nally answer the age-old debate about the relevance of
environmental contamination.
Highlights
.Determination of microbial contamination in shopping trol-
leys located in Las Palmas.
.Isolation and identication of several pathogenic bacteria.
.Environmental contamination was evidenced.
.High microbiological contamination of supermarket trolleys
was evidenced.
Disclosure statement
No potential conict of interest was reported by the authors.
ORCID
António Raposo http://orcid.org/0000-0002-5286-2249
JOURNAL OF APPLIED ANIMAL RESEARCH 21
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JOURNAL OF APPLIED ANIMAL RESEARCH 23
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Placing children in grocery shopping carts has been implicated recently as a source of infection with Salmonella and Campylobacter in young children. This study was conducted to assess the occurrence total bacteria, coliform bacteria and Escherichia coli on grocery shopping cart handles and seats. A total of 85 shopping carts in parking lots of grocery stores were tested in five major metropolitan areas across the United States. The total numbers of heterotrophic bacteria were as great as 1.1 × 107 on the handle and seat. Coliforms were detected on 72% (62) of the carts. E. coli was identified on 18 of 35 carts (51%) on which coliform identification was conducted. The results of this study suggest the need for improved sanitation of shopping cards/baskets to reduce exposure to pathogens and potential transmission of microbial infections among shoppers.
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Background: The hygiene of environmental surfaces from shopping, ATM machines, telephones and computers and miscellaneous sites play role in spreading fecal and total coliform bacteria as well as pathogenic bacteria. Objectives: This study addresses the contaminated common sites by pathogenic or potentially pathogenic bacteria in Mecca, SA. Materials and Methods: A total 648 swab samples were collected and analyzed for presence or absence of pathogenic bacteria. Results: Of the total samples 422 were negative bacterial count (71%) and 226 (29%) were positive. All collected samples (100%) of glass windows in the fish markets were bacterial counted; most dominated was Bacillus spp. (n = 97) and the highest population of species was Enterococcus faecalis (n = 40) and E. coli (n = 16). Conclusion: Some public sites were very contaminated with different types of fecal coliform group of bacteria such as shopping cart handles, inner surfaces and child seats in supermarkets, and the glass windows in the fish market. Acinetobacter haemolyticus and other hemolytic bacteria were isolated from more than site.