CC BY
02023, Scienceline Publication
Worlds Veterinary Journal
World Vet J, 13(1): 32-44, March 25, 2023
DOI: https://dx.doi.org/10.54203/scil.2023.wvj4
Occurrence of Antibiotic Resistance in Salmonella Serotypes Isolated from Environment, Humans, Animals, and Animal Products in Morocco: A Systematic Review
Motassim El Hanafi1* , Bouchriti Nourredine2 , Nassik Saadia2 , and Karib Hakim2
'Veterinary Service of Rabat, National Food Safety Office, Rabat, Morocco
2Department of Veterinary Pathology and Public Health and Food, Hassan II Agronomic and Veterinary Institute, Rabat, Morocco *Corresponding author's Email: e.motassim@iav.ac.ma
ABSTRACT
Several studies have been carried out in Morocco on Salmonella contamination in humans, domestic and wild animals, food products, and the environment. This bacterial genus is responsible for several infections and foodborne illnesses worldwide. The epidemiological situation of contamination by Salmonella is worsened by the development of antibiotic resistance to the main antibiotics used in human and veterinary medicine. The purpose of this study was to review the leading research carried out in this field, emphasizing the antibiotic resistance of this bacterium to antibiotics in humans and animals. Although some studies could not demonstrate the presence of Salmonella in the environments studied, the prevalence of contamination remained relatively high in humans, animals, food products, and the environment. The most critical contaminations were observed in poultry farms and poultry meat. Salmonella causes 42.8% of food poisoning cases in Morocco. It is the second most common cause of poisoning after pesticide poisoning. Morocco ranks first in the Middle East and North Africa for human salmonellosis, with a prevalence of 17.9% (1997-2012). Its prevalence in food products, especially those of animal origin, is very high and could reach 52.9% in turkey meat. Food products have been studied more for their contamination by Salmonella species. Meat products accounted for 17.35% of food poisoning cases. This study revealed that the isolation rate of Salmonella from food products of animal origin was dominated by isolations from meat products, with prevalence rates of 41.76 % from red meat and meat products and 25.88% from poultry meat, followed by prevalence rates of 12.44 % from fish products and 11.80 % from eggs. On the coast of Agadir, the incidence rates of Salmonella were 6.8% and 4.1% in sediment and seawater, respectively. This occurrence was 2.38% in the surface waters of Oued Khoumane. The development of resistance, particularly multi-resistance to antibiotics of therapeutic interest in both humans and animals, is alarming, especially with the ease of transmission of the bacterium to humans and facilitates its dissemination. Research findings indicated that 93.02% of isolates of Salmonella from humans, 79.37% of the strains isolated from poultry, and 46.27% of isolates from food products were resistant to at least one antibiotic.
Keywords: Animals, Environment, Food products, Foodborne disease, Salmonella, Resistance INTRODUCTION
The increasing emergence of salmonellosis threatens the effective control of human foodborne diseases (Ziyate et al., 2016). In European countries, salmonellosis is the second most frequently reported zoonotic infection (Schmid and Baumgartner, 2013). Non-typhoidal Salmonella enterica is a leading bacterial that causes acute gastroenteritis in both children and adults (Al-Rifai et al., 2020).
From 2007 to 2011, more than 6960 cases of food poisoning, including 24 deaths, were listed by the Moroccan Poison Control and Pharmacovigilance Center (Rebgui et al., 2013). Salmonella would be responsible for 42.8% of food poisoning cases in Morocco, knowing that the incidence of foodborne disease is often underestimated (Cohen et al., 2007). Similarly, a retrospective study conducted by the Moroccan Poison Control and Pharmacovigilance Center covering the period of 2010-2016 revealed 17,076 foodborne diseases, of which 2,963 (17.35%) were linked to the consumption of flesh foods. The majority of cases occurred in urban areas, with a rate of 67.06% (Boukili et al., 2019). The risk assessment of foodborne bacterial pathogens in axis Rabat-Casablanca Morocco revealed that the raw products, particularly poultry meat and red meat, were most contaminated by Salmonella with the respective prevalence of 21.05% and 5% (Oba et al., 2014)
On a local scale, the analysis of the epidemiological characteristics of foodborne diseases at the prefecture of Agadir over 3 years (2015-2017) showed 11 foodborne disease outbreaks concerning 163 poisoned individuals with 2 cases of death. Salmonella species and Escherichia coli (E. Coli) were identified in four of six samples subjected to microbiological analysis (Bouchriti et al., 2021). In a similar study in Kenitra, Morocco, 43 foodborne disease outbreaks were reported between 2001 and 2018, affecting 367 poisoned individuals, including 69 hospitalized and 2 death cases. In that study, 25% of the samples revealed the presence of Salmonella (Elkhal et al., 2021).
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As part of the salmonellosis epidemiological surveillance in some European countries, salmonellosis cases are often reported in people who have stayed in Morocco. Thus, the European Center for Disease Prevention and Control reported an increase in salmonellosis cases in six European countries due to Salmonella Chester in patients who would have traveled to Morocco between 2014 and 2015 (Fonteneau et al., 2017). Other countries have reported isolation in people with digestive disorders who have recently traveled to Morocco, including travelers from France during 20002011 (Le Hello et al., 2013), Switzerland during 2011-2012 (Schmid and Baumgartner, 2013), Finland during 1995-2009 (Hinkka, 2011) and in Norway during 2000-2016 (Siira et al., 2019).
The widespread multidrug resistance to antibiotics in human, avian, aquacultural, and environmental Salmonella is increasing and has been confirmed by numerous epidemiological studies in Morocco. Thus, En-nassiri et al. (2017) reported the emergence of multiresistant Salmonella to fluoroquinolones and third-generation cephalosporins, prescribed in the treatment of severe salmonellosis in adults and children, which is a real public health problem.
The current study aimed to review the leading research and highlight the prevalence, serotypes distribution, profiles, and importance of Salmonella isolated from humans, animals, food products, and the environment in Morocco.
METHODOLOGY
The current review covered the studies addressing prevalence, serotype, and antibiotic resistance tests in Salmonella isolates in Morocco. The study was performed using the descriptive literature review method. The diagram of the article selection process is inspired by the methodology adopted by Al-Rifaia et al. (2020). The eligibility criteria for studies included the completion of the study on animals, animals' products, the environment, and humans in Morocco in the last 25 years. The studies must be related to the serotyping of the isolated Salmonella, and the antibiotic resistance test must be carried out on the isolates. This review study aimed at elucidating the isolation of Salmonella from the environment, animals, animal products, and humans.
Since there has been a limited number of studies in Morocco, a general search of several databases was performed to collect the maximum number of studies on Salmonella and salmonellosis in Morocco. The search was operated on ProQuest, Cochrane Library, Web of Science, PubMed, CABDirect, Agricultural Documentation Center (CDA-IAV Hassan II), IMIST library, GeoScienceWorld, and EBSCO. The number of bibliographical resources consulted for this study consisted of 114 studies. Several articles, end-of-study dissertations, and research theses in Morocco or having a relationship with Salmonella carriage at the national level were derived from the studies abroad on isolates from humans who would have consumed Moroccan food products. Exclusion criteria are shown in Figure 1.
1 Studies about Salmonella in Morocco (n = 114) 1
Rest (n=112) Duplicates (n=2)
Rest (n=93) General subject and not specific (n=19)
Rest (n=74) No Salmonella isolation (n= 19)
Figure 1. Flowchart of the study eligibility process. * Ancient food of vegetable origin, results not precise, and typhoid (not NTS)
The number of bibliographical resources eligible for this study consists of 21 references from scientific publications. Among these sources, the number of references for serotyping and antibiotic resistance of isolated Salmonella was 13 for food products, 6 for humans, 3 for the environment, and 2 for those isolated from animals (poultry). Some source studies have been concerned with more than the studied factors (animal and animal product/environment). The collected data were classified in Excel spreadsheets for their exploitation. Data were classified in terms of food product isolation (animal
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species, and food product), serotype, and antibiotic resistance profiles. Table 1 shows the list of studies selected for this study.
Table 1. List of studies eligible for this analysis
Authors Product/species concerned by the study
Amajoud et al. (2017) Dairy products, Red meat and meat products, Poultry meat
Ammari et al. (2009) Food products, Humans
Ben Moussa (2014) River water
Bouchrif et al. (2009) Dairy products, Red meat and meat products, Poultry meat, Fish products
Boutaib et al. (2011) Fish products (bivalve mollusk)
Dejlil et al. (2000) Food products
Ed-Dra et al. (2018) Food products
Ed-Dra et al. (2019) Meat products (Chicken)
El Allaoui et al. (2013) Turkey meat
El Allaoui et al. (2017) Turkey
Elared et al. (2001) Eggs
Fonteneau (2017) Humans
Karraouan et al. (2010) Turkey meat
Khallaf M. et al. (2014) Chicken meat
Le Hello et al. (2013) Humans
Siira et al. (2019) Humans
Murgia et al. (2015) Dairy products, red meat and meat products, Poultry meat, Fish products, Snails
Nassri et al. (2021) Spring water
Ohmani et al. (2010) Humans
Zahli et al. (2022) Chicken meat
Ziyate et al. (2016) Laying hens
RESULTS
Animals
Most of the studies carried out in Morocco on the Salmonella contamination and carriage of animals have addressed the poultry sector since it is the sector most concerned by the presence of Salmonella, particularly broiler chickens and turkeys. Several studies on the search for the genus Salmonella have been conducted in this sector. The data relating to the analysis of these studies are listed in Table 2, which concerns only two publications on poultry farms.
Studies revealed a highly variable prevalence of Salmonella contamination in poultry farms depending on the region and the sub-sector. It was found that 24% of broiler farms were infected with Salmonella spp. in Meknes (Chaiba and Rhazi Filali, 2016). In laying hen farms, 76.7% were contaminated by the Salmonella genus, with very significant regional variations ranging from 100% in farms in the Greater Casablanca region to 50% of contaminated farms in the Rabat Sale Zemmour Zaer region to 87.5% in the Sous Massa Draa region (Ziyate et al., 2016).
However, in a recent study performed in the region of Azemmour (El Jadida-Morocco), the absence of Salmonella in breeder farms, broiler farms, and laying hen farms was reported due to size-reduced samples (4 farms per category), and the low quality of health supervision and the establishment of health barriers or vaccination in laying hens (Karib et al. 2021). Furthermore, the reported prevalence in broiler turkey farms in the Khemisset region was 35% (El Allaoui et al., 2014). In local free-range chicken farms, still called traditional or more commonly "Beldi" chicken, the prevalence of Salmonella was 6%, 10%, and 5.6% in the locality of Zemamra (El Jadida), Marrakech, and Khenifra, respectively. Seroprevalences of typhosis and pullorosis were 7.6% and 4.4%, respectively (Fagrach, 2021). It is well established that the "Beldi" chicken is a reservoir of Salmonella Gallinarum and Salmonella that continually threatens the industrial poultry sector (Bouzoubaa et al., 1992; Fagrach et al., 2021).
The serotyping of 126 strains of Salmonella isolated from broiler chickens and broiler turkeys is described in Table 2. Ziyate et al. (2016) and El-Allaoui et al. (2017) found that the strains belonged to 12 different serotypes. The predominance of the S. Kentucky serotype is notable, with a frequency of 32.54%, of which 51.2% is isolated in turkeys and 48.8% in laying hens, followed by the S. Enteritidis serotype representing 22.22% of the isolated serotypes, mainly in laying hens with a percentage of 85.71% of the isolates.
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Table 2. Distribution and antibiotic resistance patterns of salmonella species isolated from poultry farms in Morocco
Animals Authors Serotype Number of Isolates Sensitive Amx Na Cip Caz Amc Ctx C S Te Tmp Cro SxT CEP Gm Am k SU Spt
By animal species Total
Laying hens Ziyate et al. (2016) S. Amsterdam 2 2 2
Laying hens Ziyate et al. (2016) S. Enteritidis 24 28 1 23
Turkey El Allaoui et al. (2017) 4 2 1 2 2 2
Turkey El Allaoui et al. (2017) S. Agona 7 10 0 3 2 3 4 4 3 3 3 1 5
Laying hens Ziyate et al. (2016) 3 3
Laying hens Ziyate et al. (2016) S. Thompson 4 4 4
Laying hens Ziyate et al. (2016) S. Infantis 7 7 7
Turkey El Allaoui et al. (2017) S. Heidelberg 4 4 1 2 2 3
Turkey El Allaoui et al. (2017) S. Newport 3 3 0 1 2 3 3 1 1
Turkey El Allaoui et al. (2017) S. Parkroyal 10 10 0 2 2 9 10 3 3 2 5 1
Turkey El Allaoui et al. (2017) S. Ruzizi 2 2 0 1 2 1
Turkey El Allaoui et al. (2017) S. Saintpaul 6 6 0 1 5 5 3 5 1 3
Laying hens Ziyate et al. (2016) S. Typhimurium 4 9 1 3 1 3
Turkey El Allaoui et al. (2017) 5 1 1 2 2 1 3 1
Laying hens Ziyate et al. (2016) S. Kentucky 20 41 4 13 16 16 11 14 13 6 11
Turkey El Allaoui et al. (2017) 21 0 21 20 5 1 21 20 3 4 0 12 9 3 18
Total 126 126 26 16 62 36 3 12 3 8 57 66 19 3 15 13 19 21 11 14 19
Percentage 20.63 12.7 49.21 28.6 2.38 9.52 2.38 6.35 45.2 52.38 15,08 2.38 11.9 10.3 15.1 16.7 8.73 11 15.1
Am : Ampicilline
Amc : Amoxicilline/acide clavulanique
Amx : Amoxicilline
C : Chloramphenicol
Caz : CEP : Cip : Cro :
Ceftazidime Cephalothin Ciprofloxacin Ceftriaxone
Ctx : Cefotaxime
Gm : K : Na :
Gentamycine Kanamycine Nalidixic acid
S : Streptomycin
Spt : Spectinomycine
SU : Sulfametoxaozal
Sxt : Sulfametoxaozal/ trimethoprim
Te : Tetracycline Tmp : Trimethoprim
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T3BB3SB0BSBBSSS El Hanafi M, Nourredine B, Saadia N, and Hakim K (2023). Occurrence of Antibiotic Resistance in Salmonella Serotypes Isolated from Environment, Humans, Animals, and Animal Products in Morocco: A Systematic Review. World Vet. J., 13 (1): 32-44. DOI: https://dx.doi.org/10.54203/scil.2023.wvj4
In the same studies, the antibiotic resistance profile of strains isolated from poultry farms showed that 79.37% of the strains were resistant to at least one antibiotic (Ziyate et al., 2016; El Allaoui et al., 2017). Salmonella presents significant antibiotic resistance to tetracyclines, nalidixic acid, and streptomycin at 52.38 %, 49.21%, and 45.20%, respectively. All S. Newport, S. Parkroyal, S. Ruzizi, S. Saintpaul, S. Kentucky, and S. Agona strains isolated from turkey are antibiotic-resistant. However, all isolated strains, including S. Thompson, S. Infantis, and S. Amsterdam, as well as all S. Agona isolates from laying hens, indicated sensitivity to all the antibiotics studied (Ziyate et al., 2016; El Allaoui et al., 2017). The studies carried out in Morocco on the carriage of Salmonella by other domestic or wild animal species are old, fragmentary, and limited to certain areas of the country. The study by El Jai et al. (2003) on the causes of abortions in sheep allowed the isolation of Salmonella Abortusovis from the vaginal swabs of aborting ewes with a prevalence of 4.8% (n = 8820). With the same objective, a similar study on the same species in the regions of Zaer and the Middle Atlas allowed the detection of Salmonella antibodies with seropositivity rates in sheep herds of up to 5% (n = 604, El Idrissi et al., 1995).
Food products with animal origin
Prevalence at the product level
The Salmonella prevalence depends on the size of the sample studied; thus, the systematic review and meta-analysis of data on the prevalence of non-typhoid Salmonella in food products marketed in the countries of the MENA region (Middle East and North Africa) concluded that the prevalence in studies on less than 100 samples was 13.4%, whereas, it was only 4.1% in studies performed on more than 100 samples (Al-Rifai et al., 2020). As shown in Table 3, contamination of food products with non-typhoid Salmonella enterica is relatively common in food products consumed in MENA countries, with a combined global prevalence of 8.8% (Al-Rifai et al., 2020). The variable trend in detection rates between countries could be attributed to the variability of the laboratory methods used, the types of food products analyzed, and their origins (local or imported, Habib et al., 2021). Meat products are the most frequently contaminated by Salmonella, predominately in poultry meat and offal. The highest prevalence reported in Morocco is 52.9% in turkey meat (Amajoud et al., 2017) and minced meat and poultry liver, with prevalence rates of 40% and 33.33%, respectively (Bennani et al., 2016). The highest prevalence (30.6%) for red meats and meat products was found in artisanal sausages (Ed-Dra et al., 2018).
Table 3. Meta-analyses of studies reporting non-typhoidal Salmonella in Morocco according to the tested food products
Number of studies Analyzed samples Salmonella positive Salmonella prevalence
Food products Range (%) Morocco Median (%) Pooled prevalence Morocco MENA
Animal products 18 9622 227 0.0-52.9 5.4 6.8
Fish products 6 893 46 0.0-38.4 8.9 7.7
Plant products 4 2342 6 0.0-2.0 0.1 0.0
Mixed products 4 858 11 1.7-2.0 1.6 1.1
Overall 32 13715 290 0.0-52.9 2.8 4.5
Source: Al-Rifai et al. (2020)
Distribution of isolates by serotype and by food products
Table 4 shows the results of serotypes of Salmonella isolated from food products of animal origin in Morocco. The findings indicated that 510 strains of Salmonella were isolated from food products distributed on 43 Salmonella serotypes, including Salmonella isolates that were not typable or on which serotyping was not done.
The most isolated serotypes from food products of animal origin are in descending order as S. Enteritidis (n = 74) at 14.51%, S. Infantis (n = 71) at 13.92%, S. Kentucky (n=54) at 10.59% S. Typhimurium (n = 31) at 6.08%, S. Bredeney (n = 30) at 5.88%, S. Mbandaka (n = 28) at 5.49%, S. Blockley (n=23) at 4.51%, S. Saintpaul (n = 18) at 3.53%, S. Corvallis (n = 16) at 3.14%, S. Agona (n = 15), and S. Hadar (n=15) at 2.94%. Non-typable Salmonella, or those on which serotyping has not been carried out constituted a significant part of the isolations, including 16 isolates (3.14%).
As shown in figures 2 and 3, the genus Salmonella is essentially linked to meat products since 67.65% of isolates were made from these products, particularly from red meats and meat products (41.76% of isolates) and poultry meat (25.88% of isolates). However, some serotypes are much more food products bound than others. Thus, the isolation from red meat and meat products of the following serotypes was in descending order, including S. Montevideo (100%), S. Kiambu (100%), S. Mbandaka (96.43%), S. Braenderup (88.89%), S. Anatum (87.5%), S. Indiana (85.71%) and S. Infantis (63.38). The isolation of S. Saintpaul (94.44%), S. Agona (86.67%), and S. Muenster (83.33%) was made mainly from poultry meat. Similarly, the S. Glostrup and S. Newport serotypes were more closely linked to fishery and aquaculture products, with isolation rates of 100% and 69.23%, respectively. Moreover, 77.03% of S. Enteritidis isolations were from eggs.
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Table 4. Distribution of Salmonella isolates by serotype and by food products in Morocco
FOOD PRODUCTS
Isolates Poultry meat Red meat and meat products Fish products Dairy product Eggs Food products Snail
Serotype of Salmonella No. (%)** No. (%)** No. (%)** No. (%)** No. (%)** No. (%)** No. (%)** No. (%)**
Enteritidis 74 14.51 2 2.70 6 8.11 57 77.03 9 12.16
Infantis 71 13.92 2 2.82 45 63.38 2 2.817 22 30.99
Kentucky 54 10.59 18 33.33 8 14.81 26 48.15 2 3.704
Typhimurium 31 6.08 12 38.71 16 51.61 1 3.226 1 3.226 1 3.23
Bredeney 30 5.88 4 13.33 24 80.00 2 6.667
Mbandaka 28 5.49 1 3.57 27 96.43
Blockley 23 4.51 7 30.43 6 26.09 10 43.48
Saintpaul 18 3.53 17 94.44 1 5.56
ND* 16 3.14 11 68.75 3 18.75 2 12.5
Corvallis 16 3.14 4 25.00 12 75.00
Agona 15 2.94 13 86.67 2 13.33
Hadar 15 2.94 8 53.33 1 6.67 6 40
Glostrup 13 2.55 13 100
Newport 13 2.55 4 30.77 9 69.23
Montevideo 10 1.96 10 100
Braenderup 9 1.76 1 11.11 8 88.89
Anatum 8 1.57 7 87.50 1 12.5
Indiana 7 1.37 1 14.29 6 85.71
Muenster 6 1.18 5 83.33 1 16.67
Kiambu 6 1.18 6 100
Reading 6 1.18 1 16.67 5 83.33
Bovismorbificans 4 0.78 4 100
Chester 4 0.78 4 100
Give 4 0.78 4 100
Altona 3 0.59 1 33.33 2 66.67
Heidelberg 3 0.59 3 100
Schwarzengrund 3 0.59 3 100
Berta 2 0.39 2 100
Labadi 2 0.39 1 50.00 1 50
Senftemberg 2 0.39 2 100
Aalbert 1 0.20 1 100
Bareilley 1 0.20 1 100
Cerro 1 0.20 1 100
Derby 1 0.20 1 100
Djugu 1 0.20 1 100
Gallinarum 1 0.20 1 100
Hatford 1 0.20 1 100
Israel 1 0.20 1 100
Kiel 1 0.20 1 100
Livingstone 1 0.20 1 100
Othmarschen 1 0.20 1 100
Salamae (type II) 1 0.20 1 100
Tennessee 1 0.20 1 100
Zerifin 1 0.20 1 100
Overall 510 100 132 213 66 10 57 31 1
Percentage (%) 100 25.88 41.76 12.94 1.96 11.18 6.08 0.2
* ND: isolates not serotypable or serotyping not carried out; **: Percentage isolation of the serotype from the food product; ***: The definition of the nature of the food products was not specified by the authors of the original study; No: Number
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Figure 3. Percentage of isolates of Salmonella spp. from food products
Antibiotic resistance of isolates
Although some cases of salmonellosis can come directly from pets or contaminated water, the transmission rate through food was estimated at 95% (Korsak et al., 2004). Table 5 shows the antimicrobial resistance of Salmonella strains isolated from animal products in Morocco. Thus, the study of the antibiotic resistance of these isolates showed that 46.27% were resistant to at least one antibiotic. However, 53.73% of isolates were fully susceptible to the antibiotics tested. Including all isolates (n = 510), the antibiotic resistance was highest for Salmonella isolated from food products of animal origin against antibiotics with resistance rates of 17.88%, 16.67%, 15.29%, 11.76%, and 10.98% for amoxicillin, ampicillin, tetracyclines, nalidixic acid, and streptomycin, respectively.
The isolates showed a wide range of antibiotic resistance profiles that varied from one serotype to another or even within the same serotype. Some isolated serotypes showed a higher rate of antibiotic resistance. The S. Glostrup and S. Muenster serotypes are fully antibiotic resistant, followed by resistance rates of 92.59%, 86.67%, 83.33%, 77.42%, and 75% for S. Kentucky, S. Hadar, S. Saintpaul, S. Typhimurium, and S. Corvallis, respectively. On the other hand, the S. Bredeney, S. Infantis, and S. Anatum serotypes presented the lowest rate of antibiotic resistance at 10% and 11.27%, and 12.50%, respectively. The serotype S. Typhimurium isolated from food products of animal origin has antibiotic resistance to a wide range of antibiotics, including 30 different molecules with antibiotic resistance rates varying from 3.23% to 58.06%, depending on the molecules studied. Regarding S Typhimurium isolates from food products, it was found that 58.06% were resistant to amoxicillin, 48.39% to streptomycin, 45.16% to chloramphenicol, and 45.16% to amoxicillin-clavulanic acid. Boutaib et al. (2011) reported S. Glostrup serotype from aquaculture products (bivalve mollusks), with 13 isolates presenting the same multiresistant profile to tetracyclines, nalidixic acid, and ampicillin. Another most isolated serotype of the genus Salmonella with antibiotic resistance to antibiotics and anti-infectives among the dominant serotypes in food products was S. Kentucky, which showed antibiotic resistance to more than 22 molecules of different antibiotics. Furthermore, no resistance to cefquinome and imipenem has been reported; however, this finding should be taken cautiously, knowing that the range of antibiotics tested could vary from one study to another.
The antibiotic resistance profile of isolates is very diverse, ranging from resistance to one antibiotic, the most dominant profile, to multi-resistance to 18 different molecules of antibiotics. Of note, 15 different antibiotic resistance profiles have been identified in isolates from food products of animal origin; resistance to a single antibiotic constitutes was 38.30%, followed by multi-resistance to 3, 2, and 4 molecules of antibiotics at the rates of 18.72%, 17.87%, and 6.38%, respectively. Other profiles are illustrated in Table 6. Most isolates are resistant or multiresistant to less than 6 antibiotics with a rate of 91.91%.
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Table 5. Antimicrobial resistance of Salmonella strains isolated from animals' products in Morocco
Isolats Sensible Amx Cs Na Cip Caz Amc Ct1 B C S Te Tmp Cro SSS SxT CEP Gm Am Nor Cn Ipm k Cef SU Cxm Enr Ofx UB MA Ak CQ F Tic FF Lvx Mec Tim PIP Cfm NN ATM FEP
Enteritidis 74 58 2 6 2 4 2 5 5 2 2
Infantis 71 63 1 5 2
Kentucky 54 4 17 22 36 13 2 10 11 8 6 3 8 2 10 4 4 4 2 1 2 2 2 2
Typhimurium 31 7 8 3 2 14 2 4 14 15 13 6 5 4 7 2 3 18 1 3 2 9 5 1 2 2 3 3 3 2 3 1
Bredeney 30 27 1 1 1 1 1 1 1
Mbandaka 28 15 2 1 2 5 6 3 0 1
Blockley 23 12 1 0 7 7 1 0 0
Saintpaul 18 3 8 5 1 10 4 8 3 4 1 1 1
Corvallis 16 4 4 2 1 7 1 1 8 4 1
ND* 16 9 1 3 1 4 3 2
Agona 15 8 5 1 1 1 1 6 2 0 4 1 1
Hadar 15 2 13 1 4 1 5 9 1 1 4 1 0 2 1 1
Glostrup 13 0 13 13 13
Newport 13 7 1 3 1 0 4 1 0 1 1
Montevideo 10 6 3 3 0 3 1
Braenderup 9 4 0 1 0 3 1
Anatum 8 7 1 1 0 1 0
Muenster 6 0 1 1 4
Reading 6 5 1
Bovismorbifican 4 2 2 2
Chester 4 0 2 2 4 1
Give 4 0 4 4
Heidelberg 3 0 3 1
Schwarzengrund 3 0 1 2 2 1 2 2 2 1 2 2
Aalbert 1 0 1 1 1 1
Derby 1 0 1 1 1 1
Gallinarum 1 0 1 1
Israel 1 0 1 1 1
Livingstone 1 0 1
Sérotypes sensibles 31 31
Overall 510 274 49 23 60 39 1 36 3 25 28 56 78 23 6 18 24 10 12 85 10 3 0 9 2 37 6 4 4 5 4 2 0 2 2 3 5 4 8 8 3 2 3 1
Percentage (n = 510) 100 53.3 17.88 4.51 11.76 7.65 0.20 7.06 0.59 4.90 5.49 10.98 15.29 4.51 1.18 3.53 4.71 1.96 2.35 16.67 1.96 0.59 0.00 1.76 0.39 7.25 1.18 0.78 0.78 0.98 078 0.39 0.00 0.39 0.39 0.59 0.98 0.78 1.57 1.57 0.59 0.39 0.59 0.20
Ak: Amikacin CEP: Cephalothin Enr: Enrofloxacin MA: Cefamandole SSS: Sulfonamide
Am: Ampicilline Cfm: Cefixime F: Furane Mec: Mecillinam SU: Sulfametoxaozal
Amc: amoxicillin-clavulanic acid Cip: Ciprofloxacin FEP Cefepime Na: Nalidixc Acid SxT: Sulfametoxaozal/ trimethoprim
Amx: Amoxicilline Cn: Cefalexine FF: Fosfomycin NN: Tobramycin Te: Tetracycline
ATM: Aztreonam CQ: Céfquinome Fox: Cefoxitin Nor: Norfloxacine Tic: Ticarcillin
B: Bacitracin Cro: Ceftriaxone Gm: Gentamycine Ofx: Ofloxacin Tim: Ticarcillic-Clavulanic acid
C: Chloramphenicol Cs: Colistine Ipm: Imipénème PIP: Piperacillin Tmp: Trimethoprim
Caz: Ceftazidime Ctx: Cefotaxime K: Kanamycine S: Streptomycin UB: Flumequine
Cef: Cefazoline Cxm: Cefuroxime sodium Lvx: Levofloxacin Spt: Spéctinomycine
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TQBRBBBlBEfflBI El Hanafi M, Nourredine B, Saadia N, and Hakim K (2023). Occurrence of Antibiotic Resistance in Salmonella Serotypes Isolated from Environment, Humans, Animals, and Animal Products in Morocco: A Systematic Review. World Vet. J., 32-44. DOI: https://dx.doi.org/10.54203/scil.2023.wvj4
13 (1):
Table 6. Resistance profile regarding the number of antibiotics resistant to Salmonella isolated from food products in Morocco
Total
Number of antibiotics 1 2 3 4 5 6 7 8 9 10 11 12 13 16 18 15 Number of isolates 90 44 42 15 13 12 3 3 2 2 1 4 2 1 1 235 Percentage 38.30 18.72 17.87 6.38 5.53 5.11 1.28 1.28 0.85 0.85 0.43 1.70 0.85 0.43 0.43 100
Occurrence of Salmonella in the environment
There are a few studies concerning the presence of Salmonella in Morocco. When Salmonella is isolated from the environment, additional investigations such as serotyping and antibiotic resistance are rarely done. The significant contamination of poultry farms, particularly turkey and laying hen farms, by resistant Salmonella promotes the spread and dissemination of this bacterium in other ecosystems, such as the sea coast (Karraouan et al., 2017). Similarly, Salmonella contamination can be introduced into the Atlantic coast (between Essaouira and Anza) by sewage or precipitation flows (Mannas et al., 2014). The poultry farming activity developed under the impetus of private investors with sustained growth from the 1960s around the major cities of the Atlantic zone (Srairi, 2011). The presence of clinically important Salmonella enterica in natural waters follows the same trends as infection in humans and wildlife in the same area, suggesting a common origin of this germ (Nassri et al., 2021).
Most of the research work on Salmonella in the environment has been carried out in water environments, such as wells (Lotfi et al., 2020, Nassri et al., 2021), running waterways (Ben Moussa et al., 2014), water from dams (Chahboune et al., 2014), wastewaters (Ait Melloul and Hassani, 1999), and seawater (Setti et al., 2009). However, the complete study by serotyping and the study of antibiotic resistance is generally not carried out or not reported. Therefore, a comparative study addressing the contamination of the environment by Salmonella cannot be carried out.
Occurrence of Salmonella in humans
An increase in international traveling, immigration, and trade accelerates the spread of Salmonella pathogens (Hinkka, 2011). Salmonella gastroenteritis was the first disease source, with more than 39,983 cases reported in an investigation conducted between the years 1995 and 2015 in Finland on the risk of acquiring foodborne diseases and notifiable sexually transmitted infections among Finnish international travelers (Zoldia et al., 2018). Human movement facilitates the spread of resistant bacteria and antimicrobial resistance genes globally. The enteric species accounted for 65% of the 26 identified bacterial species with drug resistance (Bokhary et al., 2021). The analysis demonstrated an increase in the total number of resistant Salmonella spp. associated with travel from 1553 in 1990-1999 (25.75%) to 3549 in 2000-2009 (58.84%). The rates of reporting quinolone-resistant and multidrug resistance Salmonella spp. increased from 9.52% and 22.94% in 1990-999 (n = 283 and 329) to 84.40% and 29.08% in 2000-2009 (2510 and 417), respectively (Bokhary et al. 2021).
Morocco comes first among the MENA region countries with the highest Salmonella prevalence rate at 17.9%, far exceeding the general average for this region, which is estimated at 6.6% (Al- Rifai et al., 2019). The lack of widespread wastewater treatment and its use in irrigation contributes to the increase in the prevalence of salmonellosis in the exposed population. The prevalence of Salmonella carriage is higher in children exposed to wastewater (32.56%) than those who are not exposed with a high risk in male children younger than 10 years and sons of farmers, compared to daughters and children aged over 10 and sons of non-farmers (Ait Melloul and Hassani, 1999).
However, Salmonella isolated from wastewater and stool samples from hospitalized children living in the sewage-spreading field of the city of Marrakech showed a different profile from the general finding of antibiotic resistance. The percentage of antibiotic resistance is higher in isolates from children's stools, compared to isolates taken directly from wastewater. In addition, these isolates are rather very sensitive to cefotaxime, gentamicin, trimethoprim-sulfamethoxazole complex, nalidixic acid, kanamycin, trimethoprim, and chloramphenicol with the respective percentages of 100%, 99.88%, 98.04%, 98.04%, 97.30%, 97.07%, and 96.07%, respectively. In comparison, the highest levels of antibiotic resistance were observed for cephalothin, amoxicillin, sulfamethoxazole, and ampicillin, with respective percentages of 29.27%, 26.44%, 26.7%, and 25.21%, respectively (Ait Melloul and Hassani, 1999).
In terms of resistance profile based on the number of antibiotic resistance molecules, the number of isolates resistant to a single antibiotic molecule is dominant, with more than 79.17% of isolates, 90.53% of which are resistant to nalidixic acid. In comparison, resistance profiles to 2 and 4 molecules of antibiotics are 7.5% and 5%, respectively, which are of less importance. The presence of isolates multiresistant to a wide range of antibiotics in humans is worrying, although their percentage is small. Le Hello et al. (2013) reported that some S. Kentuchy isolates are simultaneously multiresistant to 11, 13, 14, or 15 antibiotics; this broader antibiotic resistance profile is only observed in this serotype (Le Hello et al., 2013).
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The S. Kentuchy serotype is fully multiresistant, while the S. Enteritidis and S. Chester serotypes showed significant antibiotic resistance of 92.54% and 92.45%, mainly to nalidixic acid with rates of 79.1% and 88.68%, respectively.
However, there is a limited number of publications and an insufficient study of antibiotic resistance to Salmonella isolated from humans in Morocco. Nevertheless, the data analysis shows that S. Enteritidis and S. Chester are the most frequently isolated at the rates of 51.94% and 41.09% of isolates of Salmonella in humans in Morocco, respectively. The S. Kentuchy is occasionally isolated at a rate of 4.65%, occupying the third place or among international travelers (Europeans) who have been infected following their stays in Morocco.
Regarding the conducted studies, the antibiotic resistance of Salmonella isolates in humans shows that 93.02% of isolates are resistant to at least one antibiotic. These isolates are resistant to a wide range of antibiotic molecules composed of 23 molecules. The majority of isolated Salmonella species are resistant to nalidixic acid, with a percentage of 82.3% of all isolates. In addition, less resistance was noticed to tetracyclines, sulfametoxaozal/trimethoprim, and ampicillin at the rates of 14.6%, 11.5%, and 10%, respectively.
DISCUSSION
Salmonella is among the leading causes of collective food poisoning, which can be considered one of the primary causes of infant mortality in developing countries. Control measures are established through control strategies at the level of the different countries in different ways but which remain insufficient (Nacer et al., 2021).
In Morocco, epidemiological studies show the emergence of multi-resistance in Salmonella of human, avian, aquaculture, and environmental origins. The main cause is the uncontrolled use of antibiotics in public health and veterinary medicine (En-Nasiri et al., 2017). Thus, the survey was conducted on the use of antibiotics in poultry farms carried out considering the leading private veterinary practices whose main activity is the health supervision of these farms. The findings revealed that 93% of flocks received at least one antibiotic treatment for a minimum of 3 days in Morocco broiler farms (Rahmatallah et al., 2018). In another study, 96.55% of practicing veterinarians surveyed in the eastern region of Morocco considered the abuse of antibiotics in poultry farms by self-medication, 93.11% of them linked it to the purchase of drugs without a prescription, and 89.66% of respondents judged that it was related to the use of contraband antibiotics (El-Youbi et al., 2016).
The emergence of poultry units and the food chain of Salmonella strains resistant to antibiotics is considered a cross-sectoral problem. Resistant bacteria and antibiotic-resistance genes can quickly spread through each stage of the food production chain and can cause human infections (Nacer et al., 2021).
Salmonella is ubiquitous in different environments and food products. Their prevalence can reach 52.9%, recorded in turkey meat by Amajoud et al. (2017). All the studies carried out in Morocco agree that the prevalence of Salmonella is high in the poultry sector, in particular, in farms intended to produce meat and eggs for consumption. The rate of antibiotic resistance and multi-resistance is alarming. In addition, Morocco comes first among Arab countries in terms of the prevalence of Non-Typhoidal Salmonella in humans according to a systematic review and meta-analysis in Arab countries with a prevalence of 17.9%, ranging from 5.7 to 34.8% during 1997-2012 (Habib et al., 2021). In the same geographical area, the predominant serotypes isolated from an environment or food products may not be the same reported in humans (Setti et al., 2009).
Whatever the medium of origin of Salmonella, it will eventually be transmitted to humans and therefore constitute a public health problem. However, studies concerning the circulation of Salmonella in different environments and Salmonella carrier food products are rare. Most studies relating to Salmonella are limited to an animal species, a category of products, or a circumscribed region or carried out over a limited period, and even when they exist. The analysis is often not exhaustive since it does not convert the serotyping of the Salmonella isolates or not studying their antibiotic resistance profiles.
Thus, the control of the expansion of antibiotic resistance should be considered a public health priority adopting an intersectoral and intermenstrual approach according to the concept "One Health" advocated by the World Health Organization (WHO) and the World Organization for Animal Health (WOAH). This is the case of the USA, which has decided to ban several antibiotics used in humans in poultry farms so that currently, 95% of the chicken produced in the USA is antibiotic-free (Nacer et al., 2021). Similarly, since non-typhoid Salmonella are often associated with increased morbidity and mortality, the determination of antibiotic resistance patterns should be considered an essential part of the surveillance of this Salmonella in food safety laboratories for public health in Arab countries (Habib et al., 2021).
CONCLUSION
The food products are the most studied in Morocco for the contamination of Salmonella. In animals, most studies investigated Salmonella contamination in poultry farms. The other animals have been rarely studied especially domestic
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animals, such as cattle, sheep, goats, and camels. Isolation of Salmonella from humans and the environment are seldom studied. The contamination with non-typhoid Salmonella is relatively common in food products consumed in Morocco, with a global prevalence of 4.5%, meat products are the most frequently contaminated by Salmonella, with a predominance in red meat and meat products.
The antibiotic resistance of Salmonella isolated in Morocco is alarming both from the nature of antibiotics and the number of multidrug resistances. The antibiotic resistance profile of strains isolated from poultry farms shows that 79.37% are resistant to at least one antibiotic; 93.02% of isolates of Salmonella from humans are resistant to at least one antibiotic. A rate of 46.27% of the Salmonella isolated from food products is resistant to at least one antibiotic. Considering the number of antibiotics to which the isolates are resistant, resistance ranges from resistance to one antibiotic, which is the most dominant profile (38.30% of resistance), to multi-resistance to 18 different molecules of antibiotics.
Although there are many studies on Salmonella contamination in Morocco, they remain specific, partial, sectoral, and often incomplete. This shows the importance of setting up a national observatory for surveillance and epidemiological monitoring and coordinating actions between the various departments, particularly those acting in food safety and public health. The national observatory must focus on the evolution of the antibiotic resistance character in the genus Salmonella, Campylobacters, E. coli and all pathogens transmitted by food. The study of all animal species producing food products is necessary, especially Salmonella contamination of meat products, while the study of contamination in ruminant breeding is rarely reported. The use of new identification methods, such as Whole Genome Sequencing is essential in the epidemiological investigations of cases of foodborne diseases for tracing the routes of transmission and origin of Salmonella.
DECLARATIONS
Authors' contribution
All the authors contributed to the research of the notification data, their analyses, and the writing of the final manuscript. Pr Karib Hakim and Pr Nassik Saadia participated in the collection of scientific articles and the writing of the french version. Pr Bouchriti Nourreddine and Pr Nassik participated in translating the document; Dr Motassim El Hanafi participated in data collection and analysis, and coordination. All authors participated in the advancement of the research, the development of the document, and data analysis.
Competing interests
The authors of the present study declared that there is no financial or unethical conflict related to this work, which can negatively impact its publication.
Acknowledgments
The authors acknowledge Prof. Dahani Said and Pr. Bouchrif Brahim for their precious contributions and guidance. Ethical considerations
The authors have checked for ethical issues, such as plagiarism, approval of public misconduct, data fabrication or falsification, duplicate publishing or submission, and redundancy.
REFERENCES
Ait Melloul A and Hassani L (1999). Antibiotic resistance of Salmonella strains isolated from children living in the wastewater-spreading field of Marrakesh city (Morocco). World Journal of Microbiology and Biotechnology, 15: 81-85. DOI: https://www.doi.org/10.1023/A:1008874630153
Al-Rifai RH, Chaabna K, Denagamage T, and Alali WQ (2019). Prevalence of enteric non-typhoidal Salmonella in humans in the Middle East and North Africa: A systematic review and meta-analysis. Zoonoses Public Health, 66(7): 701-728. DOI: https://www.doi.org/10.1111/zph.12631
Al-Rifaia RH, Chaabnab K, Denagamagec T, and Alalid WQ (2020). Prevalence of non-typhoidal Salmonella enterica in food products in the Middle East and North Africa: A systematic review and meta-analysis. Food Control, 109: 106908P. DOI: https://www.doi.org/10.1016/j.foodcont.2019.106908
Amajoud N, Bouchrif B, El Maadoudi M, Skalli SN, Karraouan B, El Harsal A, and El Abrini J (2017). Prevalence, serotype distribution, and antimicrobial resistance of Salmonella isolated from food products in Morocco. The Journal of Infection in Developoing Countries, 11(2): 136142. DOI: https://www.doi.org/10.3855/jidc.8026
Ammari S, Laglaoui A, En-nanei L, Bertrand S, Wildemauwe C, Barrijal S, and Abid M (2009). Characterization of Salmonella Enteritidis isolated from foods and patients in northern Morocco. The Journal of Infection in Developing Countries, 3(9): 695-703. DOI: https://www.doi.org/10.3855/jidc.617
Ben Moussa A, Chahlaoui A, Rour E, Chahboune M, AboulkacemA, Karraouan B, and Bouchrif B (2014). Prévalence et gènes de virulence des Salmonella isolées des eaux superficielles de l'Oued Khoumane, Maroc. Lebanese Science Journal, 15(2): 3-12. Available at: http://lsj.cnrs.edu.lb/wp-content/uploads/2015/12/benmoussa.pdf
42
Bennani I, Berrada S, Salame B, Aabouch M, and El Ouali Lalami A (2016). Evaluation of the hygienic quality the meat and some meat products collected from Fez city, Morocco. International Journal of Innovation and Applied Studies, 15(3): 547-554. Available at: http://www.ijias.issr-journals.org/abstract.php?article=IJIAS-16-026-01#google vignetteh
Bokhary H, Pangesti KNA, Rashid H, Abd El Ghany M, and Hill-Cawthorne MGA (2021). Travel-related antimicrobial resistance: A systematic review. Tropical Medicine and Infectious Disease, 6(1): 11. DOI: https://www.doi.org/10.3390/tropicalmed6010011
Bouchrif B, Paglietti B, Murgia M, Piana A, Cohen N, Ennaji My M, Rubino S, and Timinouni M (2009). Prevalence and antibiotic-resistance of Salmonella isolated from food in Morocco. The Journal of Infection in Developing Countries, 3(1): 35-40. DOI: https://www.doi.org/10.3855/jidc.103
Bouchriti Y, Kabbachi B, Achbani A, Ben Daoud B, Zag N, Taoussi H, and Ezaidi S (2021). Analysis on epidemiological characteristics of food poisoning events in Agadir prefecture, Morocco, from 2015 to 2017. International Congress on Health Vigilance. E3S Web Confrence, 319: 01028. DOI: https://www.doi.org/10.1051/e3sconf/202131901028
Boukili M, Filali FR, Benlarabi S, Hmimou R, Soulaymani-Bencheikh R, and Sefiani M (2019). Foodborne diseases related to the consumption of flesh foods in Morocco (2010-2016). World's Veterinary Journal, 9(1): 8-15. DOI: https://www.doi.org/10.36380/scil.2019.wvj2
Boutaib R, Marhraoui M, Oulad AMK, and Bouchrif B (2011). Comparative study on faecal contamination and occurrence of Salmonella spp. and Vibrio parahaemolyticus in two species of shellfish in Morocco. Open Environmental Sciences, 5: 30-37. DOI: https://www.doi.org/10.2174/1876325101105010030
Chahboune M, Chahlaoui A, Zaid A, Ben Moussa A, Aboulkacem A, and Bouchrif B (2014). Prévalence et gènes de virulence des salmonelles dans les eaux superficielles du barrage Hassan II et de ses affluents (Province de Midelt Maroc). John Libbey Eurotext, 13(3): 244-255. DOI: https://www.doi.org/10.1684/ers.2014.0699
Chaiba A and Rhazi FF (2016). Prévalence de la contamination par Salmonella des élevages de poulet de chair au Maroc. Cahiers Agriculture, 25(3): 35007. DOI: https://www.doi.org/10.1051/cagri/2016017
Cohen N, Ennaji H, Bouchrif B, Hassar M, and Karib H (2007). Comparative study of microbiological quality of raw poultry meat at various seasons and for different slaughtering processes in Casablanca (Morocco). The Journal of Applied Poultry Research, 16(4): 502-508. DOI: https://www.doi .org/10.3382/j apr.2006-00061
Dejli J, Chibani A, Zouhdi M, El Messoui M, Alaoui MA, and El Yachioui M (2000). Antibiorésistance de certains germes isolés dans les aliments en milieu hospitalier (CHU Avicenne, Rabat). Médecine et Maladies Infectieuses, 30(10): 661-664. DOI : https://www.doi .org/10.1016/S0399-077X(00)80038-4
Ed-Dra A, Karraouan B, El Allaoui A, Khayatti M, El Ossmani H, Rhazi FF, El Mdaghri N, and Bouchrif B (2018). Antimicrobial resistance and genetic diversity of Salmonella infantis isolates from foods and human samples in Morocco. Journal of Global Antimicrobial Resistance, 14: 297301. DOI: https://www.doi.org/10.1016/j.jgar.2018.05.019
Ed-Dra A, Filali FR, Khayi S, Oulghazi S, Bouchrif B, El Allaoui A, Ouhmidou B, and Moumni M (2019). Antimicrobial resistance, virulence genes, and genetic diversity of Salmonella enterica isolated from sausages. European Journal of Microbiology and Immunology, 9(2): 56-61. DOI: https://www.doi.org/10.1556/1886.2018.00035
El Allaoui A, Rhazi Filali F, Ameur N, and Bouchrif B (2017). Contamination des élevages de dinde de chair par Salmonella spp. au Maroc: prévalence, antibiorésistances et facteurs de risque associés. Revue Scientifique et Technique, 36(3): 935-946. DOI: https://www.doi .org/10.20506/rst.36.3.2726
El Allaoui A, Rhazi FF, Essahale A, Bouchrif B, Karraouan B, Ameur N, and Aboulkacem (2013). Characterization of antimicrobial susceptibility, virulence genes and identification by 16S ribosomal RNA gene sequencing of Salmonella serovars isolated from turkey meat in Meknes, Morocco. International Journal of Microbiology and Immunology Research, 1(7): 068-079. Available at: http://academeresearchjournals.org/print.php?id=526a983bc80f8
El Allaoui A, Rhazi FF, Ameur N, Nassri I, Oumokhtar B, Aboulkacem A, Essahale A, Derouich A, and Bouchrif B (2014). Prevalence, antibio-resistance and risk factors for salmonella in broiler turkey farms in the province of khémisset (Morocco). Journal of World's Poultry Research, 4(1): 20-29. https://jwpr.science-line.com/attachments/article/23/J%20%20World's%20Poult%20%20Res%20%204(1)%2020-29,2014.pdf
El Idrissi AH, Manyari A, and Benkirane A (1995). Fréquence des avortements infectieux des ovins au Maroc (régions des Zaer et du Moyen Atlas). Actes Insttitut Agronomique et Veterinaire, 15(4) : 11-14. Available at:
https://www. agrimaroc. org/index. php/Actes IAVH2/article/view/233/212
El Jai S, Bouslikhane M, and El Idrissi AH (2003). Suivi épidémiologique des avortements de petits ruminants dans les zones pastorales du Maroc. Actes Institut Agronomique et Vetétérinaire Maroc, 23(2-4): 95-100. Available at:
https://www.agromaroc.com/index.php/Actes_IAVH2/article/view/127
Elared O, Amara A, Faid M, Alaoui MA, and El Hassane T (2001). Antibiorésistance des souches de Salmonella enteritidis isolées dans la zone Rabat-Casablanca à partir de l'œuf de consommation, de l'aliment et des fientes de poules pondeuses. Actes Institut Agronomique et Vetétérinaire Maroc, 21(3): 147-150. Available at: https://www.agrimaroc.org/index.php/Actes IAVH2/article/view/151
Elkhal A, Attarassi B, Aujjar N, Jayche S, and Lahmam M (2021). Epidemiological study of food poisoning during the period 2001-2018 in the province of Kenitra. E3S Web of Conferences, 319: 01055. DOI: https://www.doi.org/10.1051/e3sconf/202131901055
El-Youbi M, Belbachir C, Monir A, and Saalaoui E (2016). Antibiotics in broiler: Exhaustive survey among private veterinarians in eastern Morocco. Moroccan. Journal of Biololgie, 13: 60-68. Available at: http://www.fst.ac.ma/mjb/vol1/Iss13/ARTs/7 MJB 2016 13 M El-Youbi et al.pdf
En-nassiri H, Es-soucratti K, Bouchrif B, Karraouan B, and Hammoumi A (2017). Emergence of multi-resistant Salmonella in Morocco. Rennova, 1(3). DOI: https://www.doi.org/10.34874/IMIST.PRSM/reinnova-v1i3.8696
Fagrach A, Abdeladim R, Fellahi S, and Bouslikhane M (2021). Etude rétrospective des systèmes d'élevage et dominantes pathologiques du poulet traditionnel beldi au Maroc. Revue Marocaine des Sciences Agronomiques et Vétérinaires, 9(3): 370-376. Available at: https://www. agrimaroc.org/index.php/Actes IAVH2/article/view/1010
Fonteneau L, Jourdan DSN, Fabre L, Ashton P, Torpdahl M, Muller L, Bouchrif B, El Boulani A, Valkanou E, Mattheus et al. (2017). Multinational outbreak of travel-related Salmonella Chester infections in Europe, summers 2014 and 2015. Euro Surveillance, 22(7): 30463. DOI: https://www.doi.org/10.2807/1560-7917.ES.2017.22.730463
Habib I, Mohamed MI, and Khan M (2021). Current state of Salmonella, campylobacter and listeria in the food chain across the Arab countries: A descriptive review. Foods, 10(10): 2369. DOI: https://www.doi.org/10.3390/foods10102369
Hinkka N (2011). Salmonella infections acquired abroad and detected in Finland, 1995-2009. Master Thesis, University of Tampere, Medical School, Finland. pp. 10-41. Available at: https://urn.fi/urn:nbn:fi:uta-1-21747
Karib H, Bouchriti N, Gheyoub S, and Dahani S (2021). Prévalence de Salmonella et Campylobacter dans quelques élevages avicoles et établissements d'abattage au Maroc. Revue. Marocaine des Science Agronomique et Vétérinaire, 9(3): 500-503. Available at: https://agrimaroc.org/index.php/Actes IAVH2/article/view/1026/1468
43
Karraouan B, Fassouane A, El Ossmani H, Cohen N, Charafeddine O, and Bouchrif B (2010). Prévalence et gènes de virulence des Salmonella isolées des viandes hachées crues de dinde à Casablanca (Maroc). Revue Médecine Vétérinaire, 161(3): 127-132. Available at: https://www.yumpu.com/fr/document/view/25735141/prevalence-et-genes-de-virulence-des-salmonella-isolees-des-
Karraouan B, Ziyate N, Ed-dra A, Amajoud N, Boutaib R, Akil A, El Allaoui A, El Ossmani H, Zerouali K, Elmdaghri N et al. (2017). Salmonella Kentucky: Antimicrobial resistance and molecular analysis of clinical, animal and environment isolates, Morocco. Journal of Infection in Developing Countries, 11(4): 368-370. DOI: https://www.doi.org/10.3855/jidc.8171
Khallaf M, Ameur N, Terta M, Lakranbi M, Senouci S, and Ennaji MM (2014). Prevalence and antibiotic-resistance of Salmonella isolated from chicken meat marketed in Rabat, Morocco, International Journal of Innovative Space of Scientific Research Journals, 6(4): 1123-1128. Available at http://www.ijias.issr-journals.org/abstract.php?article=IJIAS-14-161-08
Korsak N., Clinquart A. and Daube G. (2004). Salmonella spp. dans les denrées alimentaires d'origine animale: un réel problème de santé publique ?.
Annales de Médecine Vétérinaire, ISSN 0003-4118, 148 : 174-193. Available at : http://www.facmv.ulg.ac.be/amv/articles/2004_148_4_03.pdf
Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, Zerouali K, and Weill FX (2013). Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: A microbiological study. The Lancet Infectious Diseases, 13(8): 672-679. DOI: https://www.doi.org/10.1016/S1473-3099(13)70124-5
Lotfi S, Chakit M, Najy M, Talbi FZ, Benchahid AF, El Kharrim K, and Belghyti D (2020). Assessment of microbiological quality of groundwater in the Saïs plain (Morocco). Egyptian Journal of Aquatic Biology and Fisheries, 24(1): 509-524. DOI: https://www.doi.org/10.21608/EJABF.2020.73595
Mannas H, Mimouni R Chaouqy N, Hamadi F, and Martinez-Urtaza J (2014). Occurrence of Vibrio and Salmonella species in mussels (Mytilus galloprovincialis) collected along the Moroccan Atlantic coast. SpringerPlus, 3: 265. DOI: https://www.doi.org/10.1186/2193-1801-3-265
Murgia M, Bouchrif B, Timinouni M, Al-Qahtani A, Al-Ahdal MN, Pietro C, Rubino S, and Paglietti B (2015). Antibiotic resistance determinants and genetic analysis of Salmonella enterica isolated from food in Morocco. International Journal of Food Microbiology, 215: 3-39. DOI: https://www.doi.org/10.1016/j.ijfoodmicro.2015.08.003
Nacer S, El Ftouhy F, Nassik S, and Lkhider M (2021). Salmonella spp. Entre l'aspect zoonotique et l'antibiorésistance, quel enjeu pour le secteur de l'aviculture la filière avicole?. Salmonelles en aviculture et en santé publique. Revue Marocaine des Science Agronomique et Vétérinaire, 9(3): 490-499. Available at: https://www.agrimaroc.org/index.php/Actes_IAVH2/article/view/1004
Nassri I, Tahri L, Saidi A, Ameur N, and Fekhaoui M (2021). Prevalence, diversity and antimicrobial resistance of Salmonella enterica and Pseudomonas aeruginosa isolates from spring water in a rural area of northwestern Morocco. Biodiversitas Journal of Biological Diversity, 22(3): 1363-1370. DOI: https://www.doi.org/10.13057/biodiv/d220337
Oba MS, Bezzari M, Belhouari A, Kettani A, Saile R and Bennani H (2014). Risques liés à la restauration rapide et collective: Présence des germes pathogènes susceptibles de causer des toxi-infections alimentaires. International Journal of Current Research, 6(1): 4420-4425. Available at: http://docplayer.fr/147777195-Available-online-at-international-journal-of-current-research-vol-6-issue-01-pp-january-2014.html
Ohmani F, Khedid K, Britel S, Qasmaoui A, Charof R, Filali MA, and El Aouad R (2010). Antimicrobial resistance in Salmonella enterica serovar Enteritidis in Morocco. Journal of Infection in Developing Contries, 4(12): 804-809. DOI: https://www.doi.org/10.3855/jidc.806
Rahmatallah N, El Rhaffouli H, Lahlou AI, Sekhsokh Y, Fassi FO, and El Houadfi M (2018). Consumption of antibacterial molecules in broiler production in Morocco. Veterinary Medicine and Science, 4(2): 80-90. DOI: https://www.doi.org/10.1002/vms3.89
Rebgui H, Nekkal N, Benlarabi S, El Hattimy F, Hadrya F, Soulaymani R, Soulaymani-Bencheikh A, and Mokhtari A (2013). Food poisoning in Morocco: Evolution and risk factors. International Journal of Scientific and Engineering Research, 4(11): 1015-1021. Available at: https://www.ij ser.org/paper/Food-poisoning-in-Morocco-Evolution-and-Risk-factors.html
Schmid H and Baumgartner A (2013). Epidemiology of infections with enteric Salmonellae in Switzerland with particular consideration of travelling, activities. Swiss Medical Weekly, 143: w13842. DOI: https://www.doi.org/10.4414/smw.2013.13842
Setti I, Rodriguez-Castro A, Pata MP, Cadarso-Suarez C, Yacoubi B, Bensmael L, Moukrim A, and Martinez-Urtaza J (2009). Characteristics and dynamics of Salmonella contamination along the coast of Agadir, Morocco. Applied and Environmental Microbiology, 75(24): 7700-7709. DOI: https://www.doi .org/10.1128/AEM.01852-09
Siira L, Naseer U, Alfsnes Kr, Hermansen NO, Lange H, and Brandal LT (2019). Whole genome sequencing of Salmonella chester reveals geographically distinct clusters. Norway, 2000 to 2016. Europe's Journal on Infectious Disease Surveillance, Epidemiology Prevention and Control, 24(4): 1800186. DOI: https://www.doi.org/10.2807/1560-7917.ES.2019.24.4.1800186
Sraïri MT (2011). Le développement de l'élevage au Maroc: Succès relatifs et dépendance alimentaire. Courrier de l'environnement de l'INRA. n° 60, mai 2011, pp. 91-101. Available at: https://hal.archives-ouvertes.fr/hal-01196901/file/C60TaherSrairi.pdf
Zahli R, ScheuAnn K, Abrini J, Copa-Patino JL, Amajoud N, and Soliveri J (2022). Salmonella spp: Prevalence, antimicrobial resistance and molecular typing of strains isolated from poultry in Tetouan-Morocco. LWT - Food Science and Technology. 153: 112359. DOI: https://www. doi.org/10.1016/j.lwt.2021.112359
Ziyate N, Karraouan B, Kadiri A, Darkaoui S, Soulaymani A, and Bouchrif B (2016). Prevalence and antimicrobial resistance of Salmonella isolates in Moroccan laying hens farms. The Journal of Applied Poultry Research, 25: 539-546. DOI: https://www.doi.org/10.3382/japr/pfw036
Zöldi V, Jussi S, Anu K, Ruska RF, Saara S, and Outi L (2018). Destination specific risks of acquisition of notifiable food- and waterborne infections or sexually transmitted infections among Finnish international travelers 1995-2015. Travel Medicine and Infectious Disease, 25: 35-41. DOI: https://www.doi.org/10.1016/j.tmaid.2017.10.006
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