https://doi.org/10.52973/rcfcv-e33196
Received: 15/11/2022 Accepted: 27/12/2022 Published: 07/02/2023
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Revista Científica, FCV-LUZ / Vol. XXXIII, rcfcv-e33196, 1 – 7
ABSTRACT
The effect of excessive use of biocides during the COVID-19, on the
resistance of Escherichia coli to Tobramycin in poultry, meat was
examined in this observational epidemiological study (Before and after
COVID–19). Tobramycin E. coli resistant strains isolated from poultry
meat before COVID-19 appearance were compared with those isolated
after COVID-19 emergence. Univariable analyses were performed
using t-test and chi-squared test. Odds ratios and 95% condence
intervals were used for statistically signicant risk factor. Multivariate
analysis was done with the binary logistic regression to detect an
independent predictor, and with the principal component analysis
(PCA), to analyze whether the Tobramycin resistance in E. coli was
linked with the COVID-19 outbreak. Statistical signicance was set
at P<0.05. The frequency of Tobramycin E. coli resistant isolates
was more important after COVID-19 emergence (12.5%) than before
COVID-19 (2.1%). Graphical representation of PCA qualitative variables
shows the interfactor relationship. A signicant relationship between
Tobramycin E. coli resistance and COVID-19 emergence (P=0.014), and
the effect of the emergence of COVID-19 on the Tobramycin E. coli
resistance was OR = 6.57 (95% Condence interval (CI) 1.61-7.94). The
probability of Tobramycin E. coli resistance linked with poultry meat
bought after COVID-19 was 1.88 times more than before COVID-19
emergence. Poultry meat purchased after COVID-19 found related to
Tobramycin resistance in E. coli. It seems possible that the overuse
of biocides during COVID-19 increased the risk of Tobramycin E. coli
resistance in poultry meat.
Key words: Antibiotic; antimicrobial-resistance; biocide; cross-
resistance; risk-factor
RESUMEN
En este estudio epidemiológico observacional (Antes y después del
COVID-19) se examinó el efecto del uso excesivo de biocidas, durante
la pandemia de COVID-19, sobre la resistencia de Escherichia coli
a la tobramicina en la carne de aves (CA). Las cepas resistentes a
la tobramicina E. coli aisladas de la CA antes de la aparición de la
COVID-19 se compararon con las aisladas después de la aparición
de la pandemia COVID-19. Los análisis univariables se realizaron
mediante la prueba t y la prueba de Ji-cuadrado. Se utilizaron razones
de probabilidad e intervalos de conanza del 95 % para el factor de
riesgo estadísticamente signicativo. El análisis multivariante se
realizó con la regresión logística binaria para detectar un predictor
independiente y con el análisis de componentes principales (PCA) para
analizar si la resistencia a la tobramicina en E. coli estaba relacionada
con el brote de COVID-19. La signicación estadística se jó en P<0,05.
La frecuencia de aislamientos de E. coli resistentes a la tobramicina
fue más importante después de la aparición de la COVID-19 (12,5 %)
que antes de la COVID-19 (2,1 %). La representación gráca de las
variables cualitativas de PCA muestra la relación interfactorial. Una
relación signicativa entre la resistencia a la tobramicina E. coli y la
aparición de COVID-19 (valor de P=0,014), y el efecto de la aparición de
COVID-19 en la resistencia a la tobramicina E. coli fue Odds Ratio (OR)
= 6,57, intervalo de conanza (IC) del 95 %: (1,61-7,94). La probabilidad
de resistencia a la tobramicina E. coli vinculada con la CA comprada
después de la COVID-19 fue 1,88 veces mayor que antes de la aparición
de la COVID-19. La CA comprada después de COVID-19 se encontró
relacionada con la resistencia a la tobramicina en E. coli. Parece
posible que el uso excesivo de biocidas durante el COVID-19 haya
aumentado el riesgo de resistencia a la tobramicina E. coli en la CA.
Palabras clave: Antibiótico; biocida; factor de riesgo; resistencia
antimicrobiana; resistencia cruzada
Emergence of Tobramycin Escherichia coli resistance in poultry meat linked
to biocides overuse during COVID-19
Aparición de resistencia a la tobramicina en Escherichia coli en la carne de aves de corral
vinculada al uso excesivo de biocidas durante COVID-19
Nadjah Guergueb* and Nadir Alloui
The University of Batna 1, Department of Veterinary Medicine. Batna, Algeria.
*Email: nadjah.guergueb@univ-batna.dz
Overuse of biocides increased the risk of tobramycin E. coli resistance / Guergueb and Alloui _____________________________________
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INTRODUCTION
Repercussions of Coronavirus disease 2019 outbreak (currently
known as COVID-19) on future global health are still being investigated,
including the pandemic’s potential effect on the emergence, and
spread of global antimicrobial resistance (AMR) [3]. According to
World Health Organization (WHO) data, AMR causes about 700,000
deaths annually, which has been estimated to increase reaching
10 million deaths worldwide by 2050 [24].The post-COVID-19 study
is expected to alter this data, and the death attributed to AMR is
expected to approach a much higher number due to a global change
in antibiotic consumption patterns [27].Further, concerns such as
biocides (disinfectants, sanitizing agents, and cleaning chemical
agents) use during COVID-19 pandemic could also increase AMR [3].
Massive additional quantities of disinfectants have been applied
during the COVID-19 pandemic as infection preventive and control
measures [1].
Antimicrobials are valuable therapeutics whose efficacy is
seriously compromised by the emergence and spread of antimicrobial
resistance [18]. However, recent data from food animal studies
showed that limiting the use of antibiotics in food animal production
resulted in modest reductions in the prevalence of resistance, instead
of elimination of resistance, in certain bacteria [37]. Several articles
exemplify resistance stabilization and induction mechanisms,
independent of a corresponding antibiotic exposure [33].
Long-term sub-lethal exposure to biocides can exert a selective
pressure leading to the emergence of microbial strains with a reduced
susceptibility to the used antimicrobials, which can colonize food-
processing environments and recurrently contaminate food [25].
Microbial tolerance to biocides does not only compromise food safety
but also threatens Public Health (PH) mainly because the mechanisms
that convey tolerance to biocides are similar to those observed in
antimicrobials of clinical importance in a phenomenon known as
cross-resistance [8, 25].
There is now considerable evidence that transfer of AMR from
food-producing animals to humans directly via the food chain is
a likely route of spread [36].Bacteria tolerant to a wide range of
antimicrobial compounds (including biocides) are becoming more
frequent in the food chain [20]. According to the Food and Agriculture
Organization (FAO) statistics, poultry has become the most widely
consumed meat worldwide [12]. The use of antimicrobials in animal
farming is likely to accelerate the development of antimicrobial
resistance in pathogens, as well as in commensal organisms [21].
Animal products may contain antimicrobial resistant bacteria as
a result of fecal contamination during slaughter [32]. Commercial
broilers can be reservoirs of virulent and resistant genes as well as
Escherichia coli causing extra-intestinal infections, which can be a
potential threat to humans via direct contact and food [16]. During the
processing of meat, the bacteria from animal origin can contaminate
other food items, the processing plant, or workers. On the other
hand, it is possible that resistant organisms are introduced from the
outside, e.g. by food handlers into the production line [36]. Sanitizers
are used in the disinfection process to control, reduce, and inactivate
foodborne pathogens. They reduce microorganisms of PH importance
to levels considered safe, based on established parameters, without
adversely affecting either the quality of the product or its safety [9].
Due to the current COVID-19 pandemic, the use of biocides has hugely
increased in private, community and hospital settings [3]. The role of
biocides or sanitizing agents in food production and manufacturing
facilities, as well as in hospital settings, has been linked to the risk
of increasing antibiotic resistance [6].
Many in vitro studies have investigated genetic changes in
standard culture collection strains following biocide exposure [17].
Unsurprisingly, this preconditioning reduces the susceptibility of
these strains, often resulting in reduced susceptibility to biocides
and increased minimal inhibitory concentrations for antimicrobial
agents [6]. However, lifestyle modications due to pandemics are
changing the usage pattern of these disinfectants and have a realistic
potential to enhance AMR development [27].
The objective of this study was to examine the effect of excessive
use of disinfectants and biocides as a means of controlling the spread
of the virus during the COVID-19 pandemic on the resistance of E. coli
to Tobramycin in poultry meat (PM).
Tobramycin is an aminoglycoside antibiotic, used in the treatment
of systemic and ocular infections, mainly caused by Gram-negative
bacteria andStaphylococcus aureus. It is especially effective against
species of Pseudomonas [22]. However, is not allowed for poultry use
in Algeria [19]. Hence the risk of antibiotic resistance linked to its use in
poultry farming is thus eliminated and the confusion bias is controlled.
MATERIALS AND METHODS
Sample collection
The study lasted from January 2018 to July 30, 2020. A total of
159 different cuts of PM samples were bought from ten butcher
shops in the Algerian City, Biskra. All samples were subjected to a
bacterial examination. Following the Food and Drug Administration's
(FDA) Bacteriological Analytical Manual [9], 134 E. coli isolates were
identied from PM samples. Ninety four E. coli strains were isolated
from PM samples purchased from the butcher's shop prior to the
COVID-19 emergence, from January 2018 to January 2020, and 40
E. coli strains were isolated from PM samples purchased from the
same butcher's shops (10 shops) after the COVID-19 outbreak, from
June 15 to July 30, 2020.
E. coli isolation and identication
Positive lactose isolated bacteria from MacConkey agar (Liolchem,
Italy), were investigated by microscope (OPTIKA-B150 microscope,
Optika, Italy) after Gram stain, the identication of characteristic
Gram-negative bacilli was then conrmed by biochemical tests:
•
Brilliant Green Bile Broth with Durham Tube (BGLB) : positive
gas production,
•
Triple Sugar Iron agar (TSIA) : Acid/Acid, gas Positive, H
2
S
negative,
• Citrate : negative,
• Urease : negative,
• Indole : positive.
Finally, E. coli was conrmed using API-20E strips (Biomerieu,
France).
E. coli antimicrobial susceptibility testing
The disc diffusion method was used to assess antibiotic susceptibility
of all identied isolates (n=134). Mueller-Hinton agar (Himedia, India),
FIGURE 1. Boxplot of Tobramycin E. coli resistance proles estimated
from inhibition zone deviations
FIGURE 2. Frequency histogram showing the percentage of the
Tobramycin E. coli resistance before and after COVID-19 emergence
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was used to distribute bacterial suspensions. Tobramycin (TOB, 10
microgram -µg-) was utilized as the antibacterial. The antibiotic discs
were incubated for 18 to 24 h at 37°C. The diameter of the inhibitor
zone was determined in millimeters (mm). The interpretations were
made in accordance with the European Committee on Antimicrobial
Susceptibility Testing guidelines (EUCAST); Recommendations 2019
V.2.0 Mai [29] and Recommendations 2020 V.1.1 Avril [30].
Statistical analysis
Tobramycin resistance in E. coli isolated from PM, before COVID-19
appearance, was compared with those isolated after COVID-19
emergence.
Means ± standard error mean (SEM) of the inhibited zone was
calculated and data distribution was checked with boxplot diagram.
Univariable analyses were performed using the Student’s t-test (t) for
continuous variables while the chi-squared test (X
2
) for categorical
variables. Odds ratios (OR) and 95% condence intervals (CI) were used
for statistically signicant risk factor. Multivariate analysis was done
with the principal component analysis (PCA), to examine whether the
Tobramycin resistant in E. coli was linked with COVID-19 outbreak. The
binary logistic regression used to detect the independent predictor.
The goodness of t for the logistic regression model was assessed with
Nagelkerke test. A receiver operating characteristic (ROC) analysis was
used to determine the area under the curve (AUC). A P-value of 0.05 was
considered to indicate statistical signicance. The statistical package
for the Social Sciences (SPSS, version 21) [14] was used for descriptive
and regression statistics while principal component analysis (PCA) was
performed with R software version 3.1.3 [26].
RESULTS AND DISCUSSION
The objective of this study was to examine the effect of excessive
use of biocides, during the COVID-19, on the resistance of E. coli to
Tobramycin in PM.
Independent t-test
A disc diffusion assay was used to estimate the antibiotic
susceptibilities to Tobramycin (10 µg) of E. coli isolated from PM.
Results showed that inhibition zones before COVID-19 emergence
were signicantly larger than those of after COVID-19 appearance
(P-value=0.023, t-test of differences, TABLE I). Indicating that E. coli
isolated from PM purchased after the emergence of COVID-19 were more
resistant to Tobramycin than those isolated before the appearance of
COVID-19. Boxplot was used to present the distribution of inhibitor zone
size obtained before and after the appearance of COVID-19 (FIG. 1).
Chi-squared test (X
2
) and Odds ratio (OR)
FIG. 2 shows that the frequency of Tobramycin E. coli resistant
isolates is more important after COVID-19 emergence (12.5%) than
before COVID-19 (2.1%). From the TABLE II, there was a signicant
relationship between Tobramycin E. coli resistance and COVID-19
emergence (Pearson's Chi-squared test P=0.014), furthermore the
effect of COVID-19 time enlapsed (period) on the Tobramycin E. coli
resistance was OR=6.57 (95% CI 1.22 – 35.45).
TABLE I
Comparison of mean zone size of inhibition in
Tobramycin E. coli resistance isolated in poultry
meat before and after COVID-19 emergence
Variable class N (%) Mean ± SEM SD T P-value
Before COVID-19 94 (70.15) 16.07 ± 0.17 1.64
2.30 0.023
After COVID-19 40 (29.85) 15.37 ± 0.24 1.53
N: Sample size. SEM: Standard Error Mean. SD: Standard Deviation. t :
Student’s
t-test
FIGURE 3. Principal component analysis (PCA) of Tobramycin resistance
in E. coli strains obtained before and after COVID-19
FIGURE 4. Receiver operating characteristic (ROC) curves with
respective area under the curve (AUC) binary logistic validation
Overuse of biocides increased the risk of tobramycin E. coli resistance / Guergueb and Alloui _____________________________________
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Principal component analysis (PCA)
PCA was carried out to show relationship between Tobramycin
resistance in E. coli strains and the appearance of COVID-19.
The distribution of qualitative factors according to the dimensions
of the rst (80.02% of the total variance) and second (19.98% of the
total variance) was shown in FIG. 3.
Results of logistic regression indicated that after COVID-19
emergence (OR 6.57, 95%CI: 1.22-35.45; P-value=0.029) was found
to be independent risk factor associated with Tobramycin resistant
in E. coli isolated in PM (TABLE III).
TABLE II
Results of Chi-square analysis on Tobramycin E. coli resistance
Variable X
2
Df P–value OR 95% CI
Befor/After COVID-19 6.10 1 0.014 6.57 [1.22 – 35.45]
Df : Degrees of freedom. CI: Condence Interval
PM purchased after the appearance of COVID-19 was associated
with Tobramycin E. coli resistant strains isolated from PM (FIG. 3).
PCA of qualitative variables reveals that the rst two principal
components (Dim1 and Dim2) explained 80.02 and 19.98% of the total
variance. The PCA results show the relationship between Tobramycin
E. coli resistance and the period of COVID-19. Before = PM purchased
before the appearance of COVID-19, After = PM purchased after the
appearance of COVID-19,Not R = not resistant to Tobramycin, R =
resistant to Tobramycin.
Binary logistic regression
A binary logistic regression was used to estimate and to predict
the probability of Tobramycin resistance in E. coli, associated to the
overuse of biocides after COVID-19 emergence. From the Omnibus
Tests of Model Coecients, Chi-square X
2
= 5.45 (P-value=0.02),
it means the logistic model was signicant. Nagelkerke R
2
= 0.12,
suggests that the model explains roughly 12% of the variation in the
outcome. Sensitivity and specicity analyses (ROC curves) were
performed in order to assess the ability of overuse biocides (during
COVID-19) to predict Tobramycin resistant in E. coli isolated in PM.
The area under the ROC curve (AUC) was = 71.9% (95% CI: 0.52-0.92,
P-value=0.05), indicating that the model discriminates well (FIG. 4).
The estimates of regression coecients of the predictors B, Wald
statistic and P-values were presented in TABLE III.
TABLE III
Binary logistic regression
Equation
variables
Regression
coecient B
Wald Signicance Exp (B)
95%CI for
Exp (B)
Lower
limit
Upper
limit
Before/After
COVID–19
1.88 4.79 0.029 6.57 1.22 35.45
Constant -3.82 28.69 0.001 0.022
E. coli strains isolated from PM purchased after COVID-19 outbreak
were 5.57 times more likely to be Tobramycin resistant than E. coli
strains isolated from PM purchased before COVID-19.
The probability of resistance to Tobramycin in E. coli linked with
PM bought after COVID-19 was 1.88 times more than before COVID-19
emergence: Logit P = (-3.82) + 1.88 (After COVID-19)
Tobramycin E. coli resistance before COVID-19 appearance
Resistance rates to Tobramycin of E. coli strains isolated from PM,
before COVID-19 appearance, found in the current study was 2.13%
(FIG.2). The results agree with those of Kocúreková et al. [16] in Slovakia
who found Tobramycin E. coli resistance from broilers in 1.96%. The
most common mechanism of acquired resistance to aminoglycosides
is the modication of the chemical structure of the antibiotic by
bacterial enzymes. This mechanism of resistance is thought to be
more frequent in the presence of Tobramycin and Gentamicin than for
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other aminoglycosides [7]. Furthermore, Tobramycin and Gentamicin
are not allowed for aviculture use in Algeria [19]. As a consequence,
the risk of antibiotic resistance linked to its use in poultry farming is
thus reduced and the confusion bias is reduced.
Tobramycin E. coli resistance after COVID-19 appearance
After COVID-19 emergence, Tobramycin E. coli resistance in PM, found
in the current study, increased to 12.5% (FIG. 2). Even so,Tobramycin
is always not allowed for aviculture use.Similar result of Tobramycin
E. coli resistance in raw PM samples collected from retail PM market
of Bhubaneswar, India was 11.16% [28].
Antibiotic resistance persists in spite of the restricted use of several
key antibiotics, which indicates that there are components governing
the evolution, dissemination, and perpetuation of these resistance
systems, many of which are independent of antibiotic usage [4, 31].
TABLE I and FIG. 1, indicate that E. coli isolated from PM purchased
after the emergence of COVID-19 were more resistant to Tobramycin
than those isolated before the appearance of COVID-19 (P-value=0.023,
TABLE I). In that study, PM purchased after COVID-19 was statistically
related to Tobramycin resistance in E. coli (P=0.014, OR= 6.57 (95%
CI 1.22-35) in TABLE II. Graphical representation of PCA qualitative
variables shows the interfactor relationship (FIG. 3). The results of
this study show that PM purchased after COVID-19 (OR=6.57, 95% CI
1.22-35) was an independent predictor of Tobramycin resistance at
logistic regression analysis (TABLE III). And the probability of resistance
to Tobramycin in E. coli linked with PM bought after COVID-19 was 1.88
times more than before COVID-19 emergence.
The explanation for this increase in Tobramycin E. coli resistance
could be attributed to the excessive use of biocides in Algeria,
during the COVID-19 outbreak, according to WHO recommendations.
The Algerian government has issued several decrees laying down
additional measures to prevent the spread of Coronavirus. These
measures include making disinfectant products available to users
and customers, in particular hydro-alcoholic gels, and daily cleaning
and disinfection of business premises [23]. Hydroalcoholic solution
was available for employees in 85% and for customers only in 4%. In
more than 70% of cases, disinfection of surfaces, oors and door
handles took place frequently according to survey of 115 service
sector companies carried out in the prefecture of Setif City (Algeria)
in order to evaluate the preventive measures taken by the service
sector companies against the spread of the virus [13].
The Algeria Press Service stated, on March 21, 2020, that several
companies in the public and private sectors of the sanitation,
disinfection and personal hygiene products sector have doubled their
production capacity with the spread of the Corona virus (COVID-19)
in Algeria. The production capacity of the public sector companies
specialized in the production of disinfectants and personal hygiene
products is 1,000 units·days
-1
(U·d
-1
) for disinfectant gel and liquid
soap, 4,000 liters (L)·d
-1
for surface cleaners as well as 4,500 U of
bleach. This should increase its production capacity to 3,000 U·d
-1
of disinfectant gel and liquid soap, 20,000 L of oor cleaner as well
as 10,000 bottles of bleach [2].
Constant selective pressures exerted on microbiota not only
can increase their tolerance to biocidal agents but their resistance
to certain antibiotics. Such risks are likely to be exacerbated by
the non-diverse portfolio of active ingredients used in current 535
disinfectant products approved for COVID-19 [5]. Recent studies
suggest that exposure to sub-inhibitory biocide concentrations
facilitates the evolution of resistance to the biocide and may also lead
to co-resistance and cross-resistance to other antimicrobial agents
such as antibiotics [11]. Repeated exposure of bacteria to certain
microbicides (biocides) in vitro can result in decreases in antimicrobial
susceptibility [10]. In accordance with the present results, Westgate
et al. [34] observed unstable clinical resistance to Tobramycin
(10μg) in E. coli, after exposure to the cationic biocide and oxidizing
agent. Westgate et al. [35] demonstrated that exposure of E. coli to
Triclosan (0.00002%) altered the antibiotic susceptibility prole to
Tobramycin suciently to change the clinical interpretation from
susceptible to intermediate. Biocidal agents used for disinfection in
healthcare, Veterinary Medicine, food production, food handling or
in the domestic setting may also have a risk of enhancing antibiotic
resistance, especially during low level exposure [15].
CONCLUSIONS
Many in vitro experimental studies have often resulted in
reduced susceptibility to biocides and increased minimal inhibitory
concentrations for antimicrobial agents in a phenomenon known as
cross-resistance. This observational epidemiological study showed
the association between the overuse of biocides during COVID-19
emergence and the increase in Tobramycin resistance in E. coli
isolated in PM. The resistance to Tobramycin level of E. coli in PM
purchased before the emergence of COVID-19, found in this study
was 2.1%. This rate increased after COVID-19 emergence to 12.5%.
PM purchased after COVID-19 found related to Tobramycin resistance
in E. coli.It seems possible that the excessive use of biocides during
COVID-19 increases the risk of Tobramycin E. coli resistance in PM.
Conict of interest
The authors declare that they have no conicts of interest in the
research.
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