Skip to main content

Antimicrobial resistance among GLASS pathogens in Morocco: an epidemiological scoping review



Monitoring of antimicrobial resistance (AMR) is of great importance due to the frequency of strains becoming increasingly resistant to antibiotics. This review, using a public health focused approach, which aims to understand and describe the current status of AMR in Morocco in relation to WHO priority pathogens and treatment guidelines.


PubMed, ScienceDirect and Google Scholar Databases and grey literature are searched published articles on antimicrobial drug resistance data for GLASS priority pathogens isolated from Morocco between January 2011 and December 2021. Articles are screened using strict inclusion/exclusion criteria. AMR data is extracted with medians and IQR of resistance rates.


Forty-nine articles are included in the final analysis. The most reported bacterium is Escherichia coli with median resistance rates of 90.9%, 64.0%, and 56.0%, for amoxicillin, amoxicillin-clavulanic acid, and co-trimoxazole, respectively. Colistin had the lowest median resistance with 0.1%. A median resistance of 63.0% is calculated for amoxicillin-clavulanic acid in Klebsiella pneumonia. Imipenem resistance with a median of 74.5% is reported for Acinetobacter baumannii. AMR data for Streptococcus pneumonie does not exceed 50.0% as a median.


Whilst resistance rates are high for most of GLASS pathogens, there are deficient data to draw vigorous conclusions about the current status AMR in Morocco. The recently join to the GLASS system surveillance will begin to address this data gap.

Peer Review reports


Antimicrobial resistance (AMR) is increasingly recognized as a global public health issue by leading to a high rate of morbidity and mortality [1, 2]. By 2050, the global mortality will have attributed to AMR that could reach 10 million per year; this will pose a significant threat to the global economy if measures are not taken to curb the problem [3]. The antimicrobials misuse and abuse in veterinary and human medicine have accelerated the growing worldwide phenomenon of AMR [4,5,6]. Moreover, the use of antimicrobials in the food chain endangers sustainable food production and food security [7].

In October 2015, the World Health Organization (WHO) launched the Global Antimicrobial Resistance Surveillance System (GLASS), as a necessary contribution to the global action plan against AMR. Morocco joined GLASS system by the end of 2018 [8]. Recent AMR data collected from two million patients over 66 countries show high rates of resistance among antimicrobials frequently used to treat common bacterial infections [9]. The main AMR profiles are defined as those identified by WHO as “priority pathogens” for the public health significance. There are eight organisms: Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii, Staphylococcus aureus, Streptococcus pneumoniae, Salmonella spp., Shigella spp., and Neisseria gonorrhoeae [9] (Additional file 2: Appendix 1). Pathogen-antimicrobial combinations under GLASS surveillance include penicillins, third- and fourth-generation cephalosporins, carbapenems, fluoroquinolones, aminoglycosides, tetracyclines, polymyxins, macrolides, and co-trimoxazole.

It is well known that E. coli and K. pneumoniae are the most common pathogens of urinary tract infections (UTIs), which are one of the most common bacterial infections [10,11,12,13]. Uropathogenic E. coli strains have a range of adhesins that allow the bacteria to aggregate and adhere to the cellular surfaces [11, 14]. In addition to UTIs, K. pneumonia causes a variety of infectious diseases, including bacteremia, pneumonia, and liver abscesses. K. pneumoniae multidrug-resistant strains are closely related to the antibiotic resistance genes encoded by plasmid [15, 16]. The extensive use and misuse of carbapenems to treat diseases and infections caused by multidrug-resistant gram-negative bacteria contribute to the evolution of plasmid-mediated carbapenemases [17]. A. baumannii and S. aureus are some of the more common opportunistic pathogens which cause community and nosocomial infections. Unfortunately, the number of multidrug-resistant A. baumannii isolates has increased significantly [18, 19]. Resistance to antibiotics is widespread in S. aureus, which methicillin-resistant S. aureus (MRSA) are the most important clinically [20].

S. pneumoniae is an opportunistic pathogen causes pneumonia, meningitis, sepsis, bacteremia, and otitis media, especially in individuals with underdeveloped, weakened, and or deteriorating immune systems. S. pneumoniae has developed increased resistance to multiple classes of antibiotics [21, 22]. Salmonella belongs to the family Enterobacteriaceae and causes especially gastroenteritis, bacteraemia and enteric fever [23]. Antimicrobial resistance in Salmonella strains is a serious health problem worldwide. Mechanisms of Salmonella resistance are related especially to genes encoding proteins related to drug transport [24, 25]. Shigella causes especially acute gastrointestinal infections and is increasingly becoming highly drug resistant [26,27,28]. In the same line, Neisseria gonorrhoeae has developed resistance to every antibiotic currently approved for treatment [29].

In Morocco, recently, the Ministry of Health creates the national coordination unit and the technical committee for the surveillance of AMR. However, earliest studies highlighted the resistance seriousness of microorganisms to antibiotics [30,31,32]. Hitherto, however, these data have not been combined to provide a perspective at a national level. This review aims to describe the recent published AMR data from Morocco and gives a summary of key AMR patterns in the country by focusing on the organisms identified by WHO-GLASS.


Sources of information and search strategies

PubMed, SciencDirect, and the Google Scholar were searched for papers from January 1, 2011 to December 20, 2021. Search strategy in PubMed database was performed on MeSH terms (see Additional file 2: Appendix 2). In addition, we researched related reviews and references for relevant studies. The design of this proposed scoping review methodology was informed by Arksey and O’Malley’s framework [33] and The Joanna Briggs Institute Reviewers’ Guidance [34]. The selection of articles for review is done by three-stage method whereby the title alone was examined, followed by looking at the abstract, and then examining the whole article (Fig. 1).

Fig. 1
figure 1

Flow diagram of the search results and selection of the included studies

Eligibility: inclusion and exclusion criteria

All original articles written in English or French languages reporting the prevalence of antibiotic resistance in bacteria strains isolated from humans by standard laboratory tests are included.

The inclusion criteria include:

  • Reports on AMR in humans from Morocco,

  • Information about antibiotic resistance of at least one bacterium,

  • The denominator as total isolates clearly described for population-based studies,

  • Correspondence and abstracts published with sufficient information on methodology and results.

The exclusion criteria include reports published before 2011, studies only focused on HIV or tuberculosis without AMR information, reviews, and studies without information on total studied isolates.

Article quality assessment

The quality of each article is assessed using the modified critical appraisal checklist recommended by the Joanna Briggs Institute [35] (Additional file 2: Appendix 3). Quality assessment of studies was performed by two reviewers independently. Disagreements were resolved by a consensus-based discussion. Nine items are used as quality criteria for assessing the design, details of sample collection, processing and reporting on AMR methodologies.

Data extraction and analysis

Data extraction is done using a predesigned and pretested database, developed for the purpose of this review using Microsoft Excel 2016 spreadsheet (Additional file 2: Appendix 4). Data extracted are name of first author, publication date, sample size, time and location of study, laboratory methodological information (pathogen identification and antimicrobial susceptibility testing methodology) and antibacterial resistance data.

Intermediate susceptibility, where reported, is considered as resistant. Where susceptibility rates are reported, without resistance rates, the resistance rates are calculated as the inverse of the susceptibility rates. Two authors independently collected data.


Data and study characteristics

In total, 14,662 articles are collected from the initial literature search, and from them only 61 are eligible for data abstraction (Fig. 1). However, after full assessment, 12 articles are excluded due to data overlapping or duplication [36,37,38] and for difficulties to abstract data [39,40,41,42,43,44,45,46,47]. Finally, 49 papers fulfilling the inclusion criteria are included in the final analysis. Characteristics of included studies are summarized in Table 1.

Table 1 Characterization of included studies

Of the 49 included studies, 13 reported isolates from children only, while 14 not reported age of patients. The majority of included studies [38] used the disk diffusion method as the antibiotic-susceptibility test. Some studies used agar dilution and broth dilution combined, referred to as MIC testing for the analysis. The most commonly reported organism was E. coli, with AMR data reported by 22 papers. In contrast, AMR data is reported by one paper for Shigella spp. [48], one paper for N. gonorrhoea [49] and two papers for Salmonella spp. [48, 50] (Table 1).

Microbial resistance patterns

Escherichia coli

The most commonly reported bacterium was E.coli. it is reported in 22 studies (Table 1). Median resistances are calculated as 64.0% (n = 21, IQR 47.1–71.4), 90.9% (n = 13, IQR 78.8–95.3), 34.0% (n = 23, IQR 26.3–71.7), 56.0% (n = 19, IQR 32.7–70.3), 23.0% (n = 23, IQR 15.8–53.7), 3.4% (n = 22, IQR 2.1–11.0), 47.8% (n = 9, IQR 34.9–72.5), and 15.1% (n = 11, IQR 6.6–23.9) for amoxicillin-clavulanic acid, amoxicillin, fluoroquinolones, co-trimoxazole, gentamicin, amikacin, nalidixic acid and cefoxitin, respectively (Fig. 2; Additional file 1: Table S1). For 3GC, median resistances are calculated as 28.7% (n = 8, IQR 15.7–49.3), 34.4% (n = 14, IQR 13.0–71.9), and 31.8% (n = 12, IQR 18.0–84.0) for ceftriaxone, cefotaxime and ceftazidime, respectively. Colistin resistance is reported as 0.1% (n = 7, IQR 0.0–11.9). Carbapenem resistance is studied in 21 papers and calculated as 3.0% (IQR 0.0–11.8).

Fig. 2
figure 2

AMR profile of E. coli in the form of median resistance with interquartile range. AK Amikacin, AMX-C Amoxicillin-clavulanic acid, AMX amoxicillin, Carb Carbapenems, CRO Ceftriaxone, CTX Cefotaxime, CAZ Ceftazidime, CFX Cefoxitin, Cs Colistin, Fluorq Fluoroquinolones, GN Gentamicin, NA Nalidixic acid, SXT Trimethoprim-sulfamethoxazole

Klebsiella pneumonia

AMR data on K. pneumonia is reported in 16 studies (Table 1). Median resistances are calculated as 63.0% (n = 15, IQR 59.5–80.9), 100.0% (n = 7), 42.9% (n = 15, IQR 29.8–73.9), 50.9% (n = 12, IQR 45.6–80.8), 50.0% (n = 15, IQR 36.8–86.7), 4.9% (n = 14, IQR 1.4–25.0), 42.9% (n = 5, IQR 36.4–48.2) for amoxicillin-clavulanic acid, amoxicillin, fluoroquinolones, co-trimoxazole, gentamicin, amikacin and nalidixic acid respectively (Fig. 3; Additional file 1: Table S2). Carbapenem resistance is reported by 15 papers with a median rate of 12.4% (IQR 6.7–35.0). For 3GC, median resistances are calculated as 58.6% (n = 6, IQR 52.5–77.5), 63.7% (n = 9, IQR 40.4–86.7), 61.9% (n = 10, IQR 42.1–85.9) for ceftriaxone, cefotaxime and ceftazidime respectively. Colistin resistance is reported as 17.0% (IQR 8.3–24.0) in four studies [51,52,53,54].

Fig. 3
figure 3

AMR profile of K. pneumonia in the form of median resistance with interquartile range. AK Amikacin, AMX-C Amoxicillin-clavulanic acid, AMX amoxicillin, Carb Carbapenems, CRO Ceftriaxone, CTX Cefotaxime, CAZ Ceftazidime, CFX Cefoxitin, Cs Colistin, Fluorq Fluoroquinolones, GN Gentamicin, NA Nalidixic acid, SXT Trimethoprim-sulfamethoxazole

Acinetobacter baumannii

Thirteen papers reported data for A. baumannii (Table 1). Except for El Mekes et al. study [55], all papers reported imipenem resistance with a median 74.5% (IQR 65.8–79.7). Three studies reported resistance rates of 90.9%, 64.0% and 65.6% to tetracyclines [56,57,58]. Higher resistance to ticarcillin and piperacillin is reported in nine studies (92.6%, IQR 89.3–100.0) (Fig. 4; Additional file 1: Table S3). AMR resistance to 3GC, especially represented by ceftazidime, was reported as a median of 85.5% (n = 10, IQR 82.9–92.6). Gentamicin and amikacin resistance was reported with rates of 87.0% (n = 9, IQR 79.8–94.0) and 52.3% (n = 11, IQR 47.5–62.8), respectively. Colistin resistance is reported in eight studies as 0.0%, (IQR 0.0–1.2). Cefepime (4CG) resistance is reported by four studies as 87.6% (IQR 86.2–91.2) [57,58,59,60].

Fig. 4
figure 4

AMR profile of A. baumannii in the form of median resistance with interquartile range. AMX-C Amoxicillin-clavulanic acid, SXT Trimethoprim-sulfamethoxazole

Salmonella spp.

Two papers report resistance data for Salmonella spp. in humans [48, 50]. In the study of Benmessaoud et al. [48], resistance to 3CG, 4CG, imipenem and amikacin is not detected. Resistance to tetracyclines, fluoroquinolones (ciprofloxacin and levofloxacin) and co-trimoxazole is reported as 60.0%, 20.0% and 40.0%, respectively. The results reported by Ed-Dra et al. [50] show that 84.6% (22/26) of the Salmonella infantis strains were susceptible to all of the 14 antibiotics tested. Three strains are resistant to tetracycline, two strains had low-level β-lactam resistance and one strain is resistant to streptomycin and sulfonamide.

Shigella spp.

One study reports AMR data for Shigella spp. among nine isolates including six S. sonnei [48]. No resistance found to 3CG, fluoroquinolones and imipenem. Resistance higher than 50% is reported to tetracycline (55.5%) and co-trimoxazole (66.7% for all strains and 83.3% for S. sonnei).

Neisseria gonorrhoeae

One study reports AMR data for N. gonorrhoeae among 72 isolates recruited from 171 men [49]. Resistance to ciprofloxacin is identified in 86.8% of N. gonorrhoeae strains, 16.2% are resistant to penicillin and 92.6% were resistant to tetracycline. All the isolates are 100% susceptible to ceftriaxone, cefixime and spectinomycin. In this study, evolution of resistance in N. gonorrhoeae strains isolated in 2001 and 2009 was reported. The AMR study in 2009 demonstrated an increasing trend of resistance in N. gonorrhoeae to tetracycline (from 59.7% in 2001 to 92.6% in 2009) and to ciprofloxacin (from 2.6% in 2001 to 86.7% in 2009).

Staphylococcus aureus

Six papers report S. aureus among human populations [61,62,63,64,65,66]. MRSA rates range from 1.6% to 31.1%. Diawara et al. [64] report that only one strain per 62 isolates (1.6%) expressed an inhibition around cefoxitin and moxalactam disks, which is confirmed as MRSA. In the study of Ed-dyb et al. [61], 49 strains of S. aureus are isolated and the prevalence of MRSA is 4% (2/49) of S. aureus isolates. The rate of MRSA in hemodialyzed patients is 2.1% (1/47) in the study of Elazhari et al. [65]. In the study of Frikh et al. [66], S. aureus is the second most prevalent isolate with a rate of 14.9%, of which 31.1% are MRSA. The prevalence of MRSA strains is 12.5% (3/24) in the study of Souly et al. [62]. The overall prevalence of MRSA in the study of Zrouil et al. [63] is 18.4%.

Streptococcus pneumoniae

AMR data for St. pneumonie is reported by seven studies and does not exceed 50.0% as a median (resistance to tertracycline with IQR 30.5–83.7) (Table 1; Fig. 5; Additional file 1: Table S4). Resistance to penicillin G, co-trimoxazole, erythromycin is reported as 36.7% (n = 6, IQR 10.0–86.1), 33.3% (n = 5, IQR 19.8–46.1) and 21.0% (n = 5, IQR 15.5–81.0), respectively. Ceftriaxone resistance is reported by four studies as a median of 5.8% (IQR 0.3–30.4).

Fig. 5
figure 5

AMR profile of St. pneumonie in the form of median resistance with interquartile range. SXT Trimethoprim-sulfamethoxazole

In a case study [67], Néhémie et al. reported characteristics of a 35-year-old female patient. An ovarian transposition is performed in the Ibn Rochd University Hospital Centre of Casablanca. Antibiotic susceptibility tests are performed by disc diffusion and E-test method. The strain isolated is resistant to oxacillin, erythromycin, ampicillin, clindamycin, penicillin G and co-trimoxazole. It is only susceptible to vancomycin, levofloxacin and chloramphenicol and intermediate to ceftriaxone.


Over the last decade in Morocco, there has been no comprehensive review dealing with the AMR prevalence using the global antimicrobial resistance surveillance system (GLASS). This attempt seeks, hopefully, to fill the gap and clarify the AMR status in the country’s regions. The AMR data depicts high heterogeneity due to unstandardized laboratory methods, clinical conditions, and a few isolates. This makes drawing firm conclusions highly challenging. However, resistance rates to several key clinically important antibiotics are found to be alarmingly high.

To this end, the European Committee on Antimicrobial Susceptibility Testing (EUCAST) standards are recommended over the Clinical and Laboratory Standards Institute (CLSI) guidelines. Moreover, improved access to quality assurance is needed to enhance the current WHO initiative, and scale up the global antimicrobial surveillance system (GLASS) based on country-specific priority pathogens [9].

In a recent systematic review conducted in the MENA region [68], it is shown that the lack of consistency and harmonization in the regional surveillance system is not a prerogative of the Middle East, as is the case in developed countries.

The most frequently GLASS pathogens belong to the Enterobacteriaceae family (E. coli and K. pneumoniae), A. baumannii, and S. aureus. They have been described in most of selected papers. Other systematic reviews, conducted on AMR in the Middle East [68] and Africa [69], have reported the same results. Concerning Shigella spp. and N. gonorrhoeae, each has been cited by only one paper. Shigella spp. is the second leading cause of diarrheal mortality, which accounts for 13.2% of diarrheal deaths globally [70] whereas, N. gonorrhoeae causes high levels of morbidity in LMICs, and shows the rapid development of AMR [8, 9].

Enterobacterales are a large order of different types of bacteria that commonly cause infections both in healthcare settings and communities. This family represented especially by E. coli and K. pneumoniae can produce extended-spectrum beta-lactamases (ESBLs) Enzymes. The latter break down some commonly used antibiotics such as penicillins and cephalosporins, which render them inefficient [71]. The WHO has recently published a global priority list of antibiotic-resistant bacteria, which includes ESBL-producing Enterobacteriaceae and carbapenemase-producing Enterobacteriaceae [8, 9]. Carbapenem belong to the category of β-lactams, which has a broader spectrum of activity. It bind to the bacterial cell wall and inhibits growth. It also results in damage to the cell wall, which frequently leads to cell lysis and death [13, 72, 73]. Carbapenem resistance may be caused by different mechanisms, one of them being inducible overexpression of chromosomal cephalosporinases combined with porin loss [74, 75]. Enterobacteriaceae with ESBL/carbapenemase genes are bestowed with highly multi-drug resistance among humans, animals, and food chains [76]. Moreover, careless use of these antibiotic classes would co-select for resistance genotypes against the others [76].

The proportion of AMR driven from this review is alarming. The highest proportion of studies on both E. coli and K. pneumoniae are related to UTIs. Such cases require more complex treatments [9]. Such infections might require hospitalization and intravenous injection of carbapenem antibiotics. In this review, the carbapenem-resistance proportion among GLASS Enterobacteriaceae appears like other reports from Africa [69] and the Middle East [68], but higher than those described in most European countries [77]. In this context, the prevalence of carbapenemase-producing K. pneumoniae and E. coli, per 10,000 hospital admissions, presents an average of 1.3 (6.0 in Italy, 0.02 in Norway). The incidence per 100,000 hospital patient-days ranged from 17.3 in Greece to 0.09 in Lithuania, with a mean of 2.5 across all the countries. In China, the overall carbapenem-resistant Enterobacteriaceae infection incidence per 10,000 discharges was 4.0 and varies significantly by region [78]. However, no carbapenem-resistant Enterobacteriaceae is found in a recent systematic review from Cambodia [79]. Carbapenemases have a global distribution, but substantial variability exists at the regional and continental levels.

Recently, different products are under evaluation and over thirty antibiotics are active against the most dangerous pathogens included in the WHO’s priority pathogens [80, 81]. Many of them consist of combinations of new β-lactams and β-lactam inhibitors. d-mannose derivatives and glycomimetics are reported as a promising, valuable, effective, feasible and cost-effective way to treat UTIs especially, urgent clinical trials [82, 83].

In the past decade, numerous review papers have highlighted the rising problem of colistin resistance worldwide, especially with E. coli, K. pneumonia, and A. Baumanii in the human community [16, 68, 69, 84,85,86,87]. Current and emerging colistin resistance may be explained by its high usage in the animal field, and this not only as an infection-healing drug but also as a growth promoter and protective agent [88]. Following this study, several reviews have also reported high 3GC, co-trimoxazole, fluoroquinolones, and gentamicin resistance among E. coli and K. pneumoniae isolates [68, 69, 87].

In the current review, the pathogens isolated from humans such as Salmonella spp., Shigella spp., and N. gonorrhoeae are understudied in the Morocco context. However, AMR in Salmonella spp. from foods and environmental sources is mentioned by several studies [89, 90]. Such finding is also revealed by other systematic reviews in other countries [68, 69]. On the other hand, N. gonorrhoeae is known for its high resistance to ciprofloxacin [91, 92]. Of note, ciprofloxacin, which is used to treat gonococcal infections, done by, was replaced by ceftriaxone in the Moroccan context [49]. This decision is sustained by previous studies [93] stating that penicillin, tetracycline, and ciprofloxacin should not be used for N. gonorrhoeae management in Morocco. For Salmonella spp., the prevalence of fluoroquinolone resistance has exceeded 30% in many areas of the Arab World [94]. This remains significantly high when compared with the Moroccan context, where it does not surpass 20%. As recommended by Ranjbar et al. [28] a clear virulence gene profile of Shigella may lead to have an accurate diagnosis and a definite treatment relating to different pathogenic strains. In a recent study on Shigella in Morocco, the dual contribution of SfGtr4 and SfPgdA genes to the pathogenicity and the regulation biofilm formation by S. flexneri is demonstrated [95].

The epidemiology of S. aureus, especially that of MRSA, has shown a rapid evolution over the last years. Global surveillance has emphasized that MRSA represents a problem in all countries showing an increase in the mortality and need to use last-resource antibiotics [8, 9, 96]. The proportion of MRSA (30%) reported in this review is still higher than that mentioned in the European countries (16.9%) [97], but lower than those reported in Asia (28–70%) [98], and Africa (53%) [99]. While the treatment options for MRSA are still limited, there are several new antimicrobials under development [100]. S. pneumoniae is reported as a major cause of community-acquired pneumonia, meningitis, sepsis, bacteremia, and otitis media [101, 102]. A decline in susceptibility of S. pneumoniae to commonly used beta-lactams, fluoroquinolones, and macrolides is mentioned by several studies [101, 103, 104].

Although the findings of this study may seem useful, some limitations must be considered when the interpretation of the results is required. The strict focus on GLASS bacteria might have led to oversight of important pathogens like Helicobacter pylori [105, 106], and Pseudomonas aeruginosa [107, 108], which are of significate public health concern in AMR. The Validity and generalizability of the findings to the entire country’s regions might be affected by the clinical-based, cross-sectional study design of the published papers, mainly collected from Casablanca and Marrakech cities. Besides, there is high variability among the criteria relevant to methodology and interpretation. This is consonant with the data depicted elsewhere in recent similar reviews [68, 69, 79, 87]. There are some calls to adopt standardized AMR data presented in published papers, wishing to make the findings interpretable and comparable from the perspective of scarce homogeneity [109]. Despite these limitations, the high proportion of AMR detected in this review has a certain degree of validity.


In summary, this review highlights that data on AMR in Morocco are limited but improving. Overall, there are significant similarities in AMR tendency in comparison with other countries worldwide. The recent joining of Morocco to the GLASS system will improve the accuracy, quality, and comparability of data collected on AMR.

Availability of data and materials

All data generated or analyzed during this study are included in this published article and its Additional files.



Acinetobacter baumannii resistant to imipenem


Agar dilution method




Antimicrobial resistance


Amoxicillin-clavulanic acid




Broth microdilution


Third-generation cephalosporins










Clinical and Laboratory Standards Institute








Disk diffusion method


Extended spectrum beta lactamase

E Test:

Epsilometer test

E. coli :

Escherichia coli


European Committee on Antimicrobial Susceptibility Testing


Global antimicrobial resistance surveillance system






Human immunodeficiency virus


Middle East and North Africa


Interquartile range


Minimum inhibitory concentration


Nalidixic acid


Methicillin-resistant Staphylococcus aureus




University Hospital


World Health Organization


  1. Limmathurotsakul D, Dunachie S, Fukuda K, Feasey NA, Okeke IN, Holmes AH, et al. Improving the estimation of the global burden of antimicrobial resistant infections. Lancet Infect Dis. 2019;19:e392–8.

    Article  PubMed  Google Scholar 

  2. Ferri M, Ranucci E, Romagnoli P, Giaccone V. Antimicrobial resistance: a global emerging threat to public health systems. Crit Rev Food Sci Nutr. 2017;57:2857–76.

    Article  CAS  PubMed  Google Scholar 

  3. O’Neill J. Tackling drug-resistant infections globally: final report and recommendations the review on antimicrobial resistance. 2016.

  4. Ferri M, Ranucci E, Romagnoli P, Giaccone V. Antimicrobial resistance: a global emerging threat to public health systems. Crit Rev Food Sci Nutri. 2017;57:2857.

    Article  CAS  Google Scholar 

  5. Pieri A, Aschbacher R, Fasani G, Mariella J, Brusetti L, Pagani E, et al. Country income is only one of the tiles: the global journey of antimicrobial resistance among humans, animals, and environment. Antibiotics. 2020;9:473.

    Article  CAS  PubMed Central  Google Scholar 

  6. Bourély C, Coeffic T, Caillon J, Thibaut S, Cazeau G, Jouy E, et al. Trends in antimicrobial resistance among Escherichia coli from defined infections in humans and animals. J Antimicrob Chemother. 2020;75:1525.

    Article  PubMed  CAS  Google Scholar 

  7. George A. Antimicrobial resistance (AMR) in the food chain: trade, one health and codex. Trop Med Infect Dis. 2019;4:54.

    Article  PubMed Central  Google Scholar 

  8. WHO. Global antimicrobial resistance surveillance system (GLASS) report. Early implementation 2017–2018. 2018.

  9. WHO. Global antimicrobial resistance and use surveillance system (GLASS) report. Early implementation 2020. 2020.

  10. Klein RD, Hultgren SJ. Urinary tract infections: microbial pathogenesis, host–pathogen interactions and new treatment strategies. Nat Rev Microbiol. 2020;18:211–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Behzadi P, Urbán E, Matuz M, Benkő R, Gajdács M. The role of gram-negative bacteria in urinary tract infections: current concepts and therapeutic options. Adv Exp Med Biol. 2021;1323:35–69.

    Article  CAS  PubMed  Google Scholar 

  12. Khonsari MS, Behzadi P, Foroohi F. The prevalence of type 3 fimbriae in Uropathogenic Escherichia coli isolated from clinical urine samples. Meta Gene. 2021;28:100881.

    Article  Google Scholar 

  13. Issakhanian L, Behzadi P. Antimicrobial agents and urinary tract infections. Curr Pharm Des. 2019;25:1409–23.

    Article  CAS  PubMed  Google Scholar 

  14. Hozzari A, Behzadi P, Kerishchi Khiabani P, Sholeh M, Sabokroo N. Clinical cases, drug resistance, and virulence genes profiling in Uropathogenic Escherichia coli. J Appl Genet. 2020;61:265–73.

    Article  CAS  PubMed  Google Scholar 

  15. Effah CY, Sun T, Liu S, Wu Y. Klebsiella pneumoniae: an increasing threat to public health. Ann Clin Microbiol Antimicrob. 2020;19:1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ahmadi M, Ranjbar R, Behzadi P, Mohammadian T. Virulence factors, antibiotic resistance patterns, and molecular types of clinical isolates of Klebsiella pneumoniae. Expert Rev Anti Infect Ther. 2022;20:463–72.

    Article  CAS  PubMed  Google Scholar 

  17. Queenan AM, Bush K. Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev. 2007;20:440–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sarshar M, Behzadi P, Scribano D, Palamara AT, Ambrosi C. Acinetobacter baumannii: an ancient commensal with weapons of a pathogen. Pathogens. 2021;10:387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gallagher P, Baker S. Developing new therapeutic approaches for treating infections caused by multi-drug resistant Acinetobacter baumannii. J Infect. 2020;81:857–61.

    Article  CAS  Google Scholar 

  20. Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12:547–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cherazard R, Epstein M, Doan T-L, Salim T, Bharti S, Smith MA. Antimicrobial resistant Streptococcus pneumoniae: prevalence, mechanisms, and clinical implications. Am J Ther. 2017;24:e361–9.

    Article  PubMed  Google Scholar 

  22. Kim L, McGee L, Tomczyk S, Beall B. Biological and epidemiological features of antibiotic-resistant Streptococcus pneumoniae in pre- and post-conjugate vaccine eras: a United States perspective. Clin Microbiol Rev. 2016;29:525–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Eng S-K, Pusparajah P, Ab Mutalib N-S, Ser H-L, Chan K-G, Lee L-H. Salmonella : a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci. 2015;8:284–93.

    Article  CAS  Google Scholar 

  24. Shaheen A, Tariq A, Shehzad A, Iqbal M, Mirza O, Maslov DA, et al. Transcriptional regulation of drug resistance mechanisms in Salmonella: where we stand and what we need to know. World J Microbiol Biotechnol. 2020;36:85.

    Article  CAS  PubMed  Google Scholar 

  25. Wójcicki M, Świder O, Daniluk KJ, Średnicka P, Akimowicz M, Roszko MŁ, et al. Transcriptional regulation of the multiple resistance mechanisms in salmonella—a review. Pathogens. 2021;10:801.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Moradi F, Hadi N, Akbari M, Hashemizadeh Z, Rouhi Jahromi R. Frequency and antimicrobial resistance of Shigella species in Iran during 2000–2020. Jundishapur J Health Sci. 2021;13.

  27. Muthuirulandi Sethuvel DP, Devanga Ragupathi NK, Anandan S, Veeraraghavan B. Update on: Shigella new serogroups/serotypes and their antimicrobial resistance. Lett Appl Microbiol. 2017;64:8–18.

    Article  CAS  PubMed  Google Scholar 

  28. Ranjbar R, Bolandian M, Behzadi P. Virulotyping of Shigella spp. isolated from pediatric patients in Tehran, Iran. Acta Microbiol Immunol Hung. 2017;64:71–80.

    Article  CAS  PubMed  Google Scholar 

  29. Aitolo GL, Adeyemi OS, Afolabi BL, Owolabi AO. Neisseria gonorrhoeae antimicrobial resistance: past to present to future. Curr Microbiol. 2021;78:867–78.

    Article  CAS  PubMed  Google Scholar 

  30. Filali E, Bell J, Elhouadfi M, Huggins M, Cook J. Antibiotic resistance of Escherichia coli strains isolated from chickens with colisepticaemia in Morocco. Comparat Immunol Microbiol Infect Dis. 1988;11.

  31. Amábile-Cuevas CF. Antimicrobial resistance in developing countries. New York: Springer, New York; 2010.

    Google Scholar 

  32. Ousaid A, Akrim J, Khayati Y. Overuse of antibiotics as a key driver to antibiotic resistance in Morocco: a short review with potential solutions. Int Arab J Antimicrob Agents. 2020;10.

  33. Arksey H, O’Malley L. Scoping studies: towards a methodological framework. Int J Soc Res Methodol. 2005;8:19–32.

    Article  Google Scholar 

  34. Peters MDJ, Godfrey CM, Khalil H, McInerney P, Parker D, Soares CB. Guidance for conducting systematic scoping reviews. Int J Evid Based Healthc. 2015;13:141.

    Article  PubMed  Google Scholar 

  35. Munn Z, Moola S, Lisy K, Riitano D, Tufanaru C. Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int J Evid Based Healthc. 2015;13:147.

    Article  PubMed  Google Scholar 

  36. Benmessaoud R, Jroundi I, Moraleda C, Alvarez-Martínez MJ, Pons MJ, Chaacho S, et al. Aetiology, epidemiology and clinical characteristics of acute moderate-to-severe diarrhoea in children under 5 years of age hospitalized in a referral paediatric hospital in Rabat, Morocco. J Med Microbiol. 2015;64:84–92.

    Article  PubMed  Google Scholar 

  37. el Bouamri MC, Arsalane L, Kamouni Y, Berraha M, Zouhair S. Évolution récente du profil épidémiologique des entérobactéries uropathogènes productrices de β-lactamases à spectre élargi à Marrakech. Maroc Progres Urol. 2014;24:451–5.

    Article  Google Scholar 

  38. El Bouamri MC, Arsalane L, Kamouni Y, Yahyaoui H, Bennouar N, Berraha M, et al. Profil actuel de résistance aux antibiotiques des souches d’Escherichia coli uropathogènes et conséquences thérapeutiques. Prog Urol. 2014;24:1058–62.

    Article  CAS  PubMed  Google Scholar 

  39. Barguigua A, el Otmani F, Talmi M, Zerouali K, Timinouni M. Emergence of carbapenem-resistant Enterobacteriaceae isolates in the Moroccan community. Diagn Microbiol Infect Dis. 2012;73:290–1.

    Article  PubMed  Google Scholar 

  40. Barguigua A, el Otmani F, Talmi M, Bourjilat F, Haouzane F, Zerouali K, et al. Characterization of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates from the community in Morocco. J Med Microbiol. 2011;60:1344–52.

    Article  CAS  PubMed  Google Scholar 

  41. Bourjilat F, Bouchrif B, Dersi N, David J, Gros Claude P, Amarouch H, et al. Emergence of extended-spectrum beta-lactamase-producing Escherichia coli in community-acquired urinary infections in Casablanca, Morocco. J Infect Dev Ctries. 2011;5:850.

    Article  CAS  PubMed  Google Scholar 

  42. el Hamzaoui N, Berguigua A, Nayme K, Mohamed S, Timinouni M, Louzi L. Prevalence of extended-spectrum beta-lactamases in uropathogenic Enterobacteriaceae isolated from a community setting, Meknes, Morocco. Gene Rep. 2020;19:100652.

    Article  Google Scholar 

  43. le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, et al. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis. 2013;13:672–9.

    Article  PubMed  Google Scholar 

  44. Natoubi S, Barguigua A, Diawara I, Timinouni M, Rakib K, Amghar S, et al. Epidemiology of extended-spectrum β-lactamases and carbapenemases producing Enterobacteriaceae in Morocco. J Contemp Clin Pract. 2020;6:75–85.

    Article  Google Scholar 

  45. Nejmi H, Laghla B, Boutbaoucht M, Samkaoui MA. Évolution des résistances de l’Escherichia coli au cours des péritonites communautaires. Méd Maladies Infect. 2011;41:218–20.

    Article  CAS  Google Scholar 

  46. Ambroise J, Benaissa E, Irenge LMWB, Belouad EM, Bearzatto B, Durant J-F, et al. Genomic characterisation of extended-spectrum β-lactamase-producing multidrug-resistant Escherichia coli in Rabat, Morocco. J Glob Antimicrob Resist. 2021;26:335–41.

    Article  PubMed  Google Scholar 

  47. Farih S, Saddari A, Noussaiba B, Araab A, Yacoubi L, Benaissa E, et al. Health vigilance concerning female urinary tract infections: epidemiological profile and antibiotic resistance. E3S Web Conf. 2021;319:01009.

    Article  CAS  Google Scholar 

  48. Benmessaoud R, Nezha M, Moraleda C, Jroundi I, Tligui H, Seffar M, et al. Antimicrobial resistance levels among diarrhoeagenic micro-organisms recovered from children under-5 with acute moderate-to-severe diarrhoea in Rabat, Morocco. J Glob Antimicrob Resist. 2016;7:34–6.

    Article  PubMed  Google Scholar 

  49. Hançali A, Ndowa F, Bellaji B, Bennani A, Kettani A, Charof R, et al. Antimicrobial resistance monitoring in Neisseria gonorrhoeae and strategic use of funds from the Global Fund to set up a systematic Moroccan gonococcal antimicrobial surveillance programme. Sexually Transmit Infect. 2013;89(Suppl):4.

    Google Scholar 

  50. Ed-Dra A, Karraouan B, Allaouiel A, Khayatti M, Ossmaniel H, Filali FR, et al. Antimicrobial resistance and genetic diversity of Salmonella Infantis isolated from foods and human samples in Morocco. J Glob Antimicrob Resist. 2018;14:297–301.

  51. Benaicha H, Barrijal S, Ezzakkioui F, Elmalki F. Prevalence of PMQR genes in E. coli and Klebsiella spp. isolated from North-West of Morocco. J Glob Antimicrob Resist. 2017;10:321–5.

    Article  PubMed  Google Scholar 

  52. Lachhab Z, Frikh M, Maleb A, Kasouati J, Doghmi N, Ben Lahlou Y, et al. Bacteraemia in intensive care unit: clinical, bacteriological, and prognostic prospective study. Can J Infect Dis Med Microbiol. 2017;2017:1–9.

    Article  Google Scholar 

  53. el Hamzaoui N, Barguigua A, Larouz S, Maouloua M. Epidemiology of burn wound bacterial infections at a Meknes hospital, Morocco. N Microb N Infect. 2020;38:100764.

    Article  Google Scholar 

  54. Loqman S, Soraa N, Diene SM, Rolain J-M. Dissemination of carbapenemases (OXA-48, NDM and VIM) producing enterobacteriaceae isolated from the Mohamed VI University Hospital in Marrakech, Morocco. Antibiotics. 2021;10:492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. El mekes A, Zahlane K, Ait said L, Tadlaoui Ouafi A, Barakate M. The clinical and epidemiological risk factors of infections due to multi-drug resistant bacteria in an adult intensive care unit of University Hospital Center in Marrakesh-Morocco. J Infect Public Health. 2020;13:637–43.

    Article  PubMed  Google Scholar 

  56. el Kettani A, Maaloum F, Diawara I, Katfy K, Harrar N, Zerouali K, et al. Prevalence of Acinetobacter baumannii bacteremia in intensive care units of Ibn Rochd University Hospital, Casablanca Iran. J Microbiol. 2017;9:318–23.

    Google Scholar 

  57. Uwingabiye J, Frikh M, Lemnouer A, Bssaibis F, Belefquih B, Maleb A, et al. Acinetobacter infections prevalence and frequency of the antibiotics resistance: comparative study of intensive care units versus other hospital units. Pan Afr Med J. 2016;23.

  58. Yacoubi L, Farih S, Benhamza N, Seddari A, Maleb A. Health vigilance concerning Acinetobacter baumannii bacteremia at the Mohammed VI University Hospital of Oujda (morocco): epidemiological profile and antibiotic resistance. E3S Web Conf. 2021;319:01003.

    Article  CAS  Google Scholar 

  59. Kabbaj H, Seffar M, Belefquih B, Akka D, Handor N, Amor M, et al. Prevalence of Metallo-β-lactamases producing Acinetobacter baumannii in a Moroccan Hospital. ISRN Infect Dis. 2013;2013:1–3.

    Google Scholar 

  60. el Hafa H, Nayme K, el Hamzaoui N, Maroui I, Sbiti M, Zerouali K, et al. Dissemination of carbapenem-resistant Acinetobacter baumannii strains carrying the blaGES, blaNDM and blaOXA23 in Morocco. Germs. 2019;9:133–41.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Ed-dyb S, Aboudourib M, Azzouzi F, Quiddi W, Akhdari N, Amal S, et al. Prevalence of community acquired methicillin resistant Staphylococcus aureus nasal carriage among children of consultation: experience of a Moroccan University Hospital. Arch Clin Microbiol. 2020;11.

  62. Souly K, Ait El kadi M, Lahmadi K, Biougnach H, Boughaidi A, Zouhdi M, et al. Epidemiology and prevention of Staphylococcus aureus nasal carriage in hemodialyzed patients. Med Maladies Infect. 2011;41:469–74.

    Article  CAS  Google Scholar 

  63. Zriouil SB, Bekkali M, Zerouali K. Epidemiology of Staphylococcus aureus infections and nasal carriage at the Ibn rochd university hospital center, casablanca, morocco, Brazilian. J Infect Dis. 2012;16:379–283.

    Google Scholar 

  64. Diawara I, Bekhti K, Elhabchi D, Saile R, Elmdaghri N, Timinouni M, et al. Staphylococcus aureus nasal carriage in hemodialysis centers of Fez, Morocco Iran. J Microbiol. 2014;6:175–83.

    Google Scholar 

  65. Elazhari M, Elothmani F, Errouagui A, Elhabchi D, Saile R, Timinouni M. Staphylococcus aureus nasal carriage in centers of Casablanca (Morocco). Afr J Microbiol Res. 2014;8:375–82.

    Article  Google Scholar 

  66. Frikh M, Abdelhay L, Jalal K, Imad Y, Yassine B, Bouchra B, et al. Profile and antibiotic susceptibility of bacteria isolates in burn patients hospitalized in a Moroccan Hospital: a cross-sectional study. Wounds. 2018;30:102–7.

    PubMed  Google Scholar 

  67. Néhémie N, Zerouali K, Diawara I, Katfy K, Maaloum F, Kabura S, et al. Surgical wound infection caused by a multi drug resistant Streptococcus pneumoniae Serotype 19A after a total coloproctectomy with ileostomy. Pan Afr Med J. 2020;35.

  68. Truppa C, Abo-Shehada MN. Antimicrobial resistance among GLASS pathogens in conflict and non-conflict affected settings in the Middle East: a systematic review. BMC Infect Dis. 2020;20.

  69. Tadesse BT, Ashley EA, Ongarello S, Havumaki J, Wijegoonewardena M, González IJ, et al. Antimicrobial resistance in Africa: a systematic review. BMC Infect Dis. 2017;17.

  70. Khalil IA, Troeger C, Blacker BF, Rao PC, Brown A, Atherly DE, et al. Morbidity and mortality due to shigella and enterotoxigenic Escherichia coli diarrhoea: the Global Burden of Disease Study 1990–2016. Lancet Infect Dis. 2018;18:1229.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Lutgring JD. Carbapenem-resistant Enterobacteriaceae: an emerging bacterial threat. Semin Diagnos Pathol. 2019;36:182.

    Article  Google Scholar 

  72. Aurilio C, Sansone P, Barbarisi M, Pota V, Giaccari LG, Coppolino F, et al. Mechanisms of action of carbapenem resistance. Antibiotics. 2022;11:421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Nicolau DP. Carbapenems: a potent class of antibiotics. Expert Opin Pharmacother. 2008;9:23–37.

    Article  CAS  PubMed  Google Scholar 

  74. Iredell J, Brown J, Tagg K. Antibiotic resistance in Enterobacteriaceae: mechanisms and clinical implications. BMJ. 2016.

    Article  PubMed  Google Scholar 

  75. Suzuki S, Horinouchi T, Furusawa C. Prediction of antibiotic resistance by gene expression profiles. Nat Commun. 2014;5.

  76. Rodríguez-Baño J, Gutiérrez-Gutiérrez B, Machuca I, Pascual A. Treatment of infections caused by extended-spectrum-beta-lactamase-, AmpC-, and carbapenemase-producing enterobacteriaceae. Clin Microbiol Rev. 2018;31.

  77. Grundmann H, Glasner C, Albiger B, Aanensen DM, Tomlinson CT, Andrasević AT, et al. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): a prospective, multinational study. Lancet Infect Dis. 2017;17.

  78. Zhang Y, Wang Q, Yin Y, Chen H, Jin L, Gu B, et al. Epidemiology of carbapenem-resistant enterobacteriaceae infections: report from the China CRE Network. Antimicrob Agents Chemother. 2017;62.

  79. Reed TAN, Krang S, Miliya T, Townell N, Letchford J, Bun S, et al. Antimicrobial resistance in Cambodia: a review. Int J Infect Dis. 2019;85:98–107.

    Article  PubMed  Google Scholar 

  80. Terreni M, Taccani M, Pregnolato M. New antibiotics for multidrug-resistant bacterial strains: latest research developments and future perspectives. Molecules. 2021;26:2671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Behzadi P, García-Perdomo HA, Karpiński TM, Issakhanian L. Metallo-ß-lactamases: a review. Mol Biol Rep. 2020;47:6281–94.

    Article  CAS  PubMed  Google Scholar 

  82. Miyanishi W, Ojika M, Akase D, Aida M, Igarashi Y, Ito Y, et al. d-Mannose binding, aggregation property, and antifungal activity of amide derivatives of pradimicin A. Bioorg Med Chem. 2022;55: 116590.

    Article  CAS  Google Scholar 

  83. Sarshar M, Behzadi P, Ambrosi C, Zagaglia C, Palamara AT, Scribano D. FimH and anti-adhesive therapeutics: a disarming strategy against uropathogens. Antibiotics. 2020;9:397.

    Article  CAS  PubMed Central  Google Scholar 

  84. Marchello CS, Dale AP, Pisharody S, Rubach MP, Crump JA. A systematic review and meta-analysis of the prevalence of community-onset bloodstream infections among hospitalized patients in Africa and Asia. Antimicrob Agents Chemother. 2019;64.

  85. O’Neal L, Alvarez D, Mendizábal-Cabrera R, Ramay BM, Graham J. Community-acquired antimicrobial resistant Enterobacteriaceae in Central America: a one health systematic review. Int J Environ Res Public Health. 2020;17:7622.

    Article  PubMed Central  Google Scholar 

  86. Agyeman AA, Bergen PJ, Rao GG, Nation RL, Landersdorfer CB. A systematic review and meta-analysis of treatment outcomes following antibiotic therapy among patients with carbapenem-resistant Klebsiella pneumoniae infections. Int J Antimicrob Agents. 2020;55:105833.

    Article  CAS  PubMed  Google Scholar 

  87. Bilal H, Khan MN, Rehman T, Hameed MF, Yang X. Antibiotic resistance in Pakistan: a systematic review of past decade. BMC Infect Dis. 2021;21.

  88. Rhouma M, Beaudry F, Letellier A. Resistance to colistin: what is the fate for this antibiotic in pig production? Int J Antimicrob Agents. 2016;48:119.

    Article  CAS  PubMed  Google Scholar 

  89. Amajoud N, Bouchrif B, el Maadoudi M, Skalli Senhaji N, Karraouan B, el Harsal A, et al. Prevalence, serotype distribution, and antimicrobial resistance of Salmonella isolated from food products in Morocco. J Infect Dev Countries. 2017;11:136–42.

    Article  CAS  Google Scholar 

  90. el Allaoui A, Rhazi Filali F, Ameur N, Bouchrif B. Contamination des élevages de dinde de chair par Salmonella spp. au Maroc: prévalence, antibiorésistances et facteurs de risque associés. Rev Sci Tech l’OIE. 2017;36.

  91. Shigemura K, Fujisawa M. History and epidemiology of antibiotic susceptibilities of Neisseria gonorrhoeae. Curr Drug Targets. 2015;16:272.

    Article  CAS  PubMed  Google Scholar 

  92. Allan-Blitz L-T, Wang X, Klausner JD. Wild-type gyrase A genotype of Neisseria gonorrhoeae predicts in vitro susceptibility to ciprofloxacin: a systematic review of the literature and meta-analysis. Sexually Transmit Dis. 2017;44.

  93. Karim S, Bouchikhi C, Banani A, el Fatemi H, Souho T, Erraghay S, et al. Molecular antimicrobial resistance of Neisseria gonorrhoeae in a Moroccan Area. Infect Dis Obstetr Gynecol. 2018;2018:1.

    Article  CAS  Google Scholar 

  94. Moghnieh RA, Kanafani ZA, Tabaja HZ, Sharara SL, Awad LS, Kanj SS. Epidemiology of common resistant bacterial pathogens in the countries of the Arab League. Lancet Infect Dis. 2018;18:e379–94.

    Article  PubMed  Google Scholar 

  95. Kaoukab-Raji A, Biskri L, Allaoui A. Inactivation of the sfgtr4 Gene of Shigella flexneri induces biofilm formation and affects bacterial pathogenicity. Microorganisms. 2020;8:841.

    Article  PubMed Central  CAS  Google Scholar 

  96. WHO. Global Antimicrobial Resistance Surveillance System Manual for Early Implementation. 2015.

  97. European Centre for Disease Prevention and Control. Surveillance of antimicrobial resistance in Europe Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2018. Stockholm; 2019.

  98. Chen C-J, Huang Y-C. New epidemiology of Staphylococcus aureus infection in Asia. Clin Microbiol Infect. 2014;20:605–23.

    Article  CAS  PubMed  Google Scholar 

  99. Wangai FK, Masika MM, Maritim MC, Seaton RA. Methicillin-resistant Staphylococcus aureus (MRSA) in East Africa: red alert or red herring? BMC Infect Dis. 2019;19.

  100. Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers. 2018;4.

  101. Cherazard R, Epstein M, Doan T-L, Salim T, Bharti S, Smith MA. Antimicrobial resistant Streptococcus pneumoniae: prevalence, mechanisms, and clinical implications. Am J Therapeut. 2017;24:e361.

    Article  Google Scholar 

  102. Feldman C, Anderson R. Recent advances in the epidemiology and prevention of Streptococcus pneumoniae infections. F1000 Res. 2020;9:338.

    Article  CAS  Google Scholar 

  103. Cornick JE, Bentley SD. Streptococcus pneumoniae: the evolution of antimicrobial resistance to beta-lactams, fluoroquinolones and macrolides. Microb Infect. 2012;14:573.

    Article  CAS  Google Scholar 

  104. Schroeder MR, Stephens DS. Macrolide resistance in Streptococcus pneumoniae. Front Cell Infect Microbiol. 2016;6.

  105. Bouihat N, Burucoa C, Benkirane A, Seddik H, Sentissi S, Al Bouzidi A, et al. Helicobacter pylori primary antibiotic resistance in 2015 in Morocco: a phenotypic and genotypic prospective and multicenter study. Microb Drug Resist. 2017;23:727–32.

    Article  CAS  PubMed  Google Scholar 

  106. Bouilhat N, Burucoa C, Benkirane A, el Idrissi-Lamghari A, Al Bouzidi A, El Feydi A, et al. High-level primary clarithromycin resistance of Helicobacter pylori in Morocco: a prospective multicenter molecular study. Helicobacter. 2015;20:422–3.

    Article  PubMed  Google Scholar 

  107. Rosenthal VD, Bat-Erdene I, Gupta D, Belkebir S, Rajhans P, Zand F, et al. International Nosocomial Infection Control Consortium (INICC) report, data summary of 45 countries for 2012–2017: device-associated module. Am J Infect Contr. 2020;48.

  108. Elmouaden C, Laglaoui A, Ennanei L, Bakkali M, Abid M. Virulence genes and antibiotic resistance of Pseudomonas aeruginosa isolated from patients in the Northwestern of Morocco. J Infect Dev Countries. 2019;13:892.

    Article  CAS  Google Scholar 

  109. Tsalik EL, Petzold E, Kreiswirth BN, Bonomo RA, Banerjee R, Lautenbach E, et al. Advancing diagnostics to address antibacterial resistance: the diagnostics and devices committee of the Antibacterial Resistance Leadership Group. Clin Infect Dis. 2017;64(Suppl_1):S41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Bouskraoui M, Soraa N, Zahlane K, Arsalane L, Doit C, Mariani P, et al. Étude du portage rhinopharyngé de Streptococcus pneumoniae et de sa sensibilité aux antibiotiques chez les enfants en bonne santé âgés de moins de 2 ans dans la région de Marrakech (Maroc). Arch Pediatr. 2011;18:1265–70.

    Article  CAS  PubMed  Google Scholar 

  111. Essayagh T, Zohoun A, Essayagh M, Elameri A, Zouhdi M, Ihrai H, et al. Épidémiologie bactérienne á l’unité des br̂lés de l’hôpital militaire d’instruction de rabat. Ann Biol Clin. 2011;69:71–6.

    Google Scholar 

  112. Benbachir M, Elmdaghri N, Belabbes H, Haddioui G, Benzaid H, Zaki B. Eleven-year surveillance of antibiotic resistance in Streptococcus pneumoniae in casablanca (Morocco). Microb Drug Resist. 2012;18:157–60.

    Article  CAS  PubMed  Google Scholar 

  113. Moukrad N, Rhazi Filali F, Makoudy Y. Prévalence de la multi-résistance bactérienne aux antibiotiques des infections urinaires dans la ville de Meknès (Maroc) et son évolution dans le temps. ScienceLib Edition Mersenne. 2012;4.

  114. el Mdaghri N, Jilali N, Belabbes H, Jouhadi Z, Lahssoune M, Zaid S. Epidemiological profile of invasive bacterial diseases in children in Casablanca, Morocco: antimicrobial susceptibilities and serotype distribution. Easter Mediterr Health J. 2012;18:1097.

    Article  Google Scholar 

  115. Arsalane L, Zouhair S, Lahlou Amine I, Louzi L, Bouskraoui M. Infection urinaire du nourrisson (376 cas) dans un hôpital marocain (2009–2010)—fréquence étiologique et prévalence de la résistance. Pathol Biol. 2012;60:e90–1.

    Article  CAS  PubMed  Google Scholar 

  116. Barguigua A, el Otmani F, Talmi M, Zerouali K, Timinouni M. Prevalence and types of extended spectrum β-lactamases among urinary Escherichia coli isolates in Moroccan community. Microb Pathog. 2013;61–62:16–22.

    Article  PubMed  CAS  Google Scholar 

  117. Zohoun AGC, Moket D, el Hamzaoui S. Résistance à l’imipénème par production de métallo-β-lactamases par Acinetobacter baumannii et Pseudomonas aeruginosa à l’Hôpital militaire d’instruction Mohammed V de Rabat. Ann Biol Clin. 2013;71:27–30.

    Google Scholar 

  118. Mouaffak Y, Boutbaoucht M, Soraa N, Chabaa L, Salama T, Oulad Saiad M, et al. Profil bactériologique des péritonites communautaires de l’enfant prises en charge au CHU de Marrakech. Annal Francaises Anesth Reanim. 2013;32:60–2.

    Article  CAS  Google Scholar 

  119. Warda K, Oufdou K, Zahlane K, Bouskraoui M. Antibiotic resistance and serotype distribution of nasopharyngeal isolates of Streptococcus pneumoniae from children in Marrakech region (Morocco). J Infect Public Health. 2013;6:473–81.

    Article  PubMed  Google Scholar 

  120. Fassi F el, Malki F el, Benaicha H, Idaomar M, Barrijal S. High levels multi-resistance to antibiotics among extended-spectrum β-lactamases-producing Enterobacteriaceae from Northwest Morocco. 2014.

  121. Es-Said I, Elfazazi H, Zouhdi M. In vitro activity of imipenem combination with colistin or rifampicin against clinical isolates of Acinetobacter baumannii and his antimicrobial susceptibility profil. Int J Innov Appl Stud. 2014;8:1252–7.

    Google Scholar 

  122. Es-Said I, Mahdoufi R, Yagoubi M, Zouhdi M. Isolation and antibiotic susceptibility of bacteria from Otitis media infections in children in Rabat Morocco. J Biol Agricult Healthc. 2014;4:153–9.

    Google Scholar 

  123. Barguigua A, Zerouali K, Katfy K, el Otmani F, Timinouni M, Elmdaghri N. Occurrence of OXA-48 and NDM-1 carbapenemase-producing Klebsiella pneumoniae in a Moroccan university hospital in Casablanca, Morocco. Infect Genet Evol. 2015;31:142–8.

    Article  CAS  PubMed  Google Scholar 

  124. Alem N, Frikh M, Srifi A, Maleb A, Chadli M, Sekhsokh Y, et al. Evaluation of antimicrobial susceptibility of Escherichia coli strains isolated in Rabat University Hospital (Morocco). BMC Res Notes. 2015;8.

  125. Moutachakkir M, Chinbo M, Elkhoudri N, Soraa N. La résistance aux antibiotiques chez les entérobactéries uropathogènes en milieu pédiatrique au CHU de Marrakech. J Pediatr Pueric. 2015;28:16–22.

    Google Scholar 

  126. el Hamzaoui N, Barguigua A, Timinouni M, Belhaj A. Epidemiology of extended spectrum beta-lactamase producing Escherichia coli isolated from hospital and community setting, Morocco. Int Multidiscip J. 2015;4:206–17.

    Google Scholar 

  127. el Bouamri MC, Arsalane L, el Kamouni Y, Zouhair S. Antimicrobial susceptibility of urinary Klebsiella pneumoniae and the emergence of carbapenem-resistant strains: a retrospective study from a university hospital in Morocco. N Afr Afr J Urol. 2015;21:36–40.

    Article  Google Scholar 

  128. El Bouamri MC, Arsalane L, Zerouali K, Katfy K, El Kamouni Y, Zouhair S. Molecular characterization of extended spectrum β-lactamase-producing Escherichia coli in a university hospital in Morocco, North Africa. Afr J Urol. 2015;21:161–6.

    Article  Google Scholar 

  129. Diawara I, Zerouali K, Katfy K, Barguigua A, Belabbes H, Timinouni M, et al. Phenotypic and genotypic characterization of Streptococcus pneumoniae resistant to macrolide in Casablanca, Morocco. Infect Genet Evol. 2016;40:200–4.

    Article  CAS  PubMed  Google Scholar 

  130. Chabah M, Chemsi M, Zerouali K, Alloula O, Lehlimi M, Habzi A, et al. Healthcare-associated infections due to carbapenemase-producing Enterobacteriaceae: bacteriological profile and risk factors. Med Maladies Infect. 2016;46:157–62.

    Article  CAS  Google Scholar 

  131. Arhoune B, Oumokhtar B, Hmami F, Barguigua A, Timinouni M, el Fakir S, et al. Rectal carriage of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae among hospitalised neonates in a neonatal intensive care unit in Fez, Morocco. J Glob Antimicrob Resist. 2017;8:90–6.

    Article  PubMed  Google Scholar 

  132. Arhoune B, Oumokhtar B, Hmami F, Fakir S el, Moutaouakkil K, Chami F, et al. Intestinal carriage of antibiotic resistant Acinetobacter baumannii among newborns hospitalized in Moroccan neonatal intensive care unit. PLoS ONE. 2019;14.

  133. Zahir H, Draiss G, Rada N, Abourrahouat A, Ait sab I, Sbihi M, et al. Écologie microbienne et sensibilité aux antibiotiques des bactéries isolées d’infections urinaires chez l’enfant au Maroc. Rev Francoph Lab. 2019;2019:65–70.

    Google Scholar 

  134. Torumkuney D, Hammami A, Mezghani Maalej S, ben Ayed N, Revathi G, Zerouali K, et al. Results from the survey of antibiotic resistance (SOAR) 2015–18 in Tunisia, Kenya and Morocco: data based on CLSI, EUCAST (dose-specific) and pharmacokinetic/pharmacodynamic (PK/PD) breakpoints. J Antimicrob Chemother. 2020;75.

  135. Arhoune B, el Fakir S, Himri S, Moutaouakkil K, el Hassouni S, Benboubker M, et al. Intense intestinal carriage and subsequent acquisition of multidrug-resistant enterobacteria in neonatal intensive care unit in Morocco. PLoS ONE. 2021;16: e0251810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Kettani Halabi M, Lahlou FA, Diawara I, el Adouzi Y, Marnaoui R, Benmessaoud R, et al. Antibiotic resistance pattern of extended spectrum beta lactamase producing Escherichia coli isolated from patients with urinary tract infection in Morocco. Front Cell Infect Microbiol. 2021;11.

  137. Rafik A, Abouddihaj B, Asmaa D, Kaotar N, Mohammed T. Antibiotic resistance profiling of Uropathogenic Enterobacteriaceae, Casablanca, Morocco. E3S Web Conf. 2021;319:01002.

    Article  CAS  Google Scholar 

  138. Benaissa E, Elmrimar N, Belouad E, Mechal Y, Ghazouani M, Bsaibiss F, et al. Update on the resistance of Escherichia coli isolated from urine specimens in a Moroccan hospital: a review of a 7-year period. GERMS. 2021;11:189–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references


The authors would like to thank language-editing service monitored by Professor Kamal EL AISSAOUI and would also like to thank referees for their valuable comments.


This study is sponsored by Sothema, which included compensation for services related to preparing this manuscript.

Author information

Authors and Affiliations



Study concept and design: CN and YE. Acquisition of data: CN and YE, Analysis and interpretation of data: CN, YE, AB and CA. Drafting of the manuscript: CN and YE. Critical revision of the manuscript for important intellectual content: All authors. All the authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Youness El Achhab.

Ethics declarations

Ethics approval and consent to participate

Not applicable in virtue of the study design (systematic literature review).

Consent for publication

Not applicable in virtue of the study design (systematic literature review).

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1:

Table S1. Resistance rates for E. coli isolates. Table S2. Resistance rates for K. pneumonia isolates. Table S3. Resistance rates for A. baumannii isolates. Table S4. Resistance rates for S. pneumonia isolates.

Additional file 2: Appendix 1

. GLASS specific antibiotic susceptibility testing against individual organisms (WHO, 2020). Appendix 2. Search strategy. Appendix 3. Joanna Briggs Institute’s critical appraisal checklist for studies reporting prevalence data. Appendix 4. Data extraction form

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nejjari, C., El Achhab, Y., Benaouda, A. et al. Antimicrobial resistance among GLASS pathogens in Morocco: an epidemiological scoping review. BMC Infect Dis 22, 438 (2022).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: