Publications by Author: Lotfi Loucif

2022
Loucif L, Chelaghma W, Cherak Z, Bendjama E, Beroual F, Rolain J-M. Detection of NDM-5 and MCR-1 antibiotic resistance encoding genes in Enterobacterales in long-distance migratory bird species Ciconia ciconia, Algeria. Science of The Total Environment [Internet]. 2022;814. Publisher's VersionAbstract

β-lactams and colistin resistance in Enterobacterales is a global public health issue. In this study we aimed to investigate the occurrence and genetic determinants of Extended-Spectrum β-lactamases, carbapenemases and mcr-encoding-genes in Enterobacterales isolates recovered from the migratory bird species Ciconia ciconia in an Algerian city. A total of 62 faecal samples from white storks were collected. Samples were then subjected to selective isolation of β-lactams and colistin-resistant-Enterobacterales. The representative colonies were identified using Matrix-Assisted Laser Desorption-Ionisation Time-of-Flight Mass Spectrometry. Susceptibility testing was performed using the disk-diffusion method. ESBL, carbapenemases, and colistin resistance determinants were searched for by PCR and sequencing. The clonality relationships of the obtained isolates were investigated by multilocus sequence typing assays. Mating experiments were carried out to evaluate the transferability of the carbapenemase and mcr-genes. Forty-two isolates were identified as follows: Escherichia coli (n = 33), Klebsiella pneumoniae (n = 4), Proteus mirabilis (n = 4) and Citrobacter freundii (n = 1). Molecular analysis showed that twelve isolates carried the blaESBL genes alone, fifteen E. coli isolates were positive for the blaOXA-48 gene, six isolates were NDM-5-carriers (two P. mirabilis, two K. pneumoniae and two E. coli) and eight E. coli strains were positive for the mcr-1 gene. MLST results showed a high clonal diversity, where NDM-5-producing strains were assigned to two sequence types (ST167 for E. coli and ST198 for K. pneumoniae), whereas the mcr-1 positive E. coli isolates belonged to ST58, ST224, ST453, ST1286, ST2973, ST5542, ST9815 and the international high-risk resistant lineage ST101. To the best of our knowledge, this is the first report of blaNDM-5 gene in white storks and also the first describing the mcr-1 gene in white storks in Algeria. This study underlines the important role of migratory white storks as carriers of high-level drug-resistant bacteria, allowing their possible implication as indicators and sentinels for antimicrobial resistance surveillance.

Cherak Z, Loucif L, Moussi A, Bendjama E, Benbouza A, Rolain J-M. Emergence of metallo-β-lactamases and OXA-48 carbapenemase producing gram-negative bacteria in hospital wastewater in Algeria: a potential dissemination pathway into the environment. Microbial Drug Resistance [Internet]. 2022;28 (1) :23-30. Publisher's VersionAbstract

Antibiotic-resistant bacteria can leave hospitals and therefore contaminate the environment and, most likely, humans and animals, through different routes, among which wastewater discharge is of great importance. This study aims to assess the possible role of hospital sewage as reservoir and dissemination pathway of carbapenem-resistant Gram-negative bacilli (GNB). Carbapenem-resistant GNB were selectively isolated from wastewater collected from a public hospital in Batna, Algeria. Species identification was carried out using matrix-assisted laser desorption and ionization time-of-flight mass spectrometry, and antibiotic susceptibility was evaluated by the disc diffusion method. β-Lactamase production was investigated phenotypically using the double-disk synergy assay and the modified CarbaNP test, then the molecular mechanisms of β-lactam-resistance were studied by PCR and sequencing. Ten Enterobacteriaceae and 14 glucose-nonfermenting GNB isolates were obtained. All Enterobacteriaceae isolates were positive for OXA-48 and TEM-1D β-lactamases, where seven of them coproduced an extended-spectrum β-lactamase. VIM-2 carbapenemase was detected in six glucose-nonfermenting GNB isolates. However, three Pseudomonas aeruginosa, one Comamonas jiangduensis and one Acinetobacter baumannii isolates were positive for VIM-4 variant. In addition, NDM-1 enzyme was detected in four A. baumannii isolates. Our findings highlight the potential impact of hospital wastewater in the spread of drug resistance mechanisms outside of hospitals.

2021
Cherak Z, Loucif L, Moussi A, Rolain J-M. Carbapenemase-producing Gram-negative bacteria in aquatic environments: A review. Journal of Global Antimicrobial Resistance [Internet]. 2021;25 :287-309. Publisher's VersionAbstract

Antibiotic resistance is one of the greatest public-health challenges worldwide, especially with regard to Gram-negative bacteria (GNB). Carbapenems are the β-lactam antibiotics of choice with the broadest spectrum of activity and, in many cases, are the last-resort treatment for several bacterial infections. Carbapenemase-encoding genes, mainly carried by mobile genetic elements, are the main mechanism of resistance against carbapenems in GNB. These enzymes exhibit a versatile hydrolytic capacity and confer resistance to most β-lactam antibiotics. After being considered a clinical issue, increasing attention is being giving to the dissemination of such resistance mechanisms in the environment and especially through water. Aquatic environments are among the most significant microbial habitats on our planet, known as a favourable medium for antibiotic gene transfer, and they play a crucial role in the huge spread of drug resistance in the environment and the community. In this review, we present current knowledge regarding the spread of carbapenemase-producing isolates in different aquatic environments, which may help the implementation of control and prevention strategies against the spread of such dangerous resistant agents in the environment.

Cherak Z, Loucif L, Moussi A, Rolain J-M. Epidemiology of mobile colistin resistance (mcr) genes in aquatic environments. Journal of Global Antimicrobial Resistance [Internet]. 2021;27 :51-62. Publisher's VersionAbstract

Colistin is one of the last-line therapies against multidrug-resistant Gram-negative pathogens, especially carbapenemase-producing isolates, making resistance to this compound a major global public-health crisis. Until recently, colistin resistance in Gram-negative bacteria was known to arise only by chromosomal mutations. However, a plasmid-mediated colistin resistance mechanism was described in late 2015. This mechanism is encoded by different mobile colistin resistance (mcr) genes that encode phosphoethanolamine (pEtN) transferases. These enzymes catalyse the addition of a pEtN moiety to lipid A in the bacterial outer membrane leading to colistin resistance. MCR-producing Gram-negative bacteria have been largely disseminated worldwide. However, their environmental dissemination has been underestimated. Indeed, water environments act as a connecting medium between different environments, allowing them to play a crucial role in the spread of antibiotic resistance between the natural environment and humans and other animals. For a better understanding of the role of such environments as reservoirs and/or dissemination routes of mcr genes, this review discusses primarily the various water habitats contributing to the spread of antibiotic resistance. Thereafter, we provide an overview of existing knowledge regarding the global epidemiology of mcr genes in water environments. This review confirms the global distribution of mcr genes in several water environments, including wastewater from different origins, surface water and tap water, making these environments reservoirs and dissemination routes of concern for this resistance mechanism.

Cherak Z, Loucif L, Ben-Khedher M, Moussi A, Benbouza A, Baron SA, Rolain J-M. MCR-5-Producing Colistin-Resistant Cupriavidus gilardii Strain from Well Water in Batna, Algeria. Msphere [Internet]. 2021;6. Publisher's VersionAbstract

This paper presents the first description of the mcr-5.1 gene in a colistin-resistant Cupriavidus gilardii isolate from well water that supplies a maternity hospital in Algeria. The whole-genome sequence of this strain showed the presence of putative β-lactamase, aac(3)-IVa, and multidrug efflux pump-encoding genes, which could explain the observed multidrug resistance phenotype. Our findings are of great interest, as we highlight a potential contamination route for the spread of mcr genes. 

IMPORTANCE Colistin resistance mediated by mcr genes in Gram-negative bacteria has gained significant attention worldwide. This is due to the ability of these genes to be horizontally transferred between different bacterial genera and species. Aquatic environments have been suggested to play an important role in the emergence and spread of this resistance mechanism. Here, we describe the first report of an mcr-5-positive Cupriavidus gilardii aquatic isolate through its isolation from well water in Algeria. The significance of our study is in shedding the light on an important environmental reservoir of mcr genes.

Kalla A, Loucif L, Yahia M. Miscarriage Risk Factors for Pregnant Women: A Cohort Study in Eastern Algeria’s Population. The Journal of Obstetrics and Gynecology of India [Internet]. 2021;72 :1-12. Publisher's VersionAbstract

Background

Miscarriage is defined as an adverse and unexpected termination of pregnancy; it is the most frequent pregnancy complication. Here, we aimed to identify the factors predisposing to miscarriage in pregnant women in Eastern Algeria and the effect of the combination of several factors, including maternal Body Mass Index (BMI), maternal age, concomitant pathologies, and nutrients, and to predict the occurrence of miscarriage.

Methods

A total of 786 pregnant women from Eastern Algeria were interviewed between 2011 and 2015. Association between miscarriage exposure and identified risk factors was assessed using a Generalized Linear Model (GLM), ANOVA test, Multiple Correspondence Analysis (MCA), and Hierarchical Clustering Analysis (HCA). Throughout this study, we sought to find answers, discuss this association, and predict the occurrence of miscarriage.

Results

We developed a predictive model for miscarriage, and we found that miscarriage was significantly higher for pregnant women aged over 35 years (1.75; 95% CI: 0.75–4.37; p = 0.208), with a high BMI (> 25 kg/m2), (1.88; 95% CI:1.28–2.78; p = 0.001). We have highlighted that miscarriage is strongly associated with hypertension (1.67; 95% CI: 1.16–2.39; p = 0.006), diet rich in meat (0.60; 95% CI: 0.33–1.04; p = 0.075), and moderate in fish (2.32; 95% CI: 1.18–4.58; p = 0.015).

Conclusion

Our study proved that knowing these risk factors helps to establish predictive models and strategies to prevent tragic pregnancy outcomes and highlights the link between miscarriage and several risk factors; and thus, will allow protecting mother and fetus health.

Kalla A, Loucif L, Yahia M. Prevention of congenital malformations for pregnant women: A predictive model based on a study in eastern Algeria’s population. Journal of Biological Research-Bollettino della Società Italiana di Biologia SperimentaleJournal of Biological Research-Bollettino della Società Italiana di Biologia Sperimentale. 2021;94.
Chelaghma W, Loucif L, Bendahou M, Rolain J-M. Vegetables and Fruit as a Reservoir of β-Lactam and Colistin-Resistant Gram-Negative Bacteria: A Review. MicroorganismsMicroorganisms. 2021;9 :2534.
Cherak I, Bachir AS, Cherak L, Ghazi C, Loucif L, Sellami M. Diversity and distribution patterns of endophytic mycoflora of Atlas cedar, Cedrus atlantica (Endl) G. Manetti ex Carrière, needles in Belezma biosphere reserve (Batna, Algeria). Biodiversity Journal [Internet]. 2021;12 (3) :573–583. Publisher's VersionAbstract

This study aims to assess the diversity and distribution of fungal mycoflora developing on Cedrus atlantica (Endl) G. Manetti ex Carrière needles in three sites in the Belezma National Park (Biosphere Reserve, Northeast - Algeria). Three sites were sampled according to a cedar decline gradient, these are the massifs of: Telmet (healthy site), Boumerzoug (moderately depressed) and Tougurt (decayed site). Polymerase chain reaction (PCR) molecular analysis, allows identifying 19 endophytic mycotaxa. All the identified species have a weak occurrence frequency (less than 25%). In terms of specific richness, the moderately depressed site (Boumerzoug) homes the largest number of taxa (S = 17), followed by healthy site of Telmet (12 taxa), while the depressed site of Tougurt was the least populated (8 taxa). The hierarchical classification analysis (HCA) showed that the taxonomic composition of endophyte associations differs clearly from one site to another according to the cedar decline. The clustering representing healthy massif brings 2 species which are demanding phytoparasitic endophytes (Fusarium sp. and Xylaria sp.). The group associated to moderately depressed site hosts 7 taxa with a wide ecological valence, such as: Canariomyces notabilis, Canariomyces vonarxii, Chaetomium aegilopis, Coniolariella hispanica and Penicillium kubanicum. Then, mycoflora group noted in the decayed cedar includes 10 taxa, in particular, saprophytic mycotaxa relatively less demanding with a high ecological valence like: Biscogniauxia mediterranea, Alternaria arborescens, A. tenuissima and three species of Chaetomium genus. The mycotaxa distribution is related to the specific conditions of colonized trees. Taxa specific to healthy and decayed massifs would represent bio indicators of the phytosanitary and ecological conditions of colonized cedars.

2020
Bendjama E, Loucif L, Chelaghma W, Attal C, Bellakh FZ, Benaldjia R, Kahlat I, Meddour A, Rolain J-M. First detection of an OXA-48-producing Enterobacter cloacae isolate from currency coins in Algeria. Journal of Global Antimicrobial ResistanceJournal of Global Antimicrobial Resistance. 2020;23 :162-166.
2018
Loucif L, Chelaghma W, Helis Y, Sebaa F, Baoune RD, Zaatout W, Rolain J-M. First detection of OXA-48-producing Klebsiella pneumoniae in community-acquired urinary tract infection in Algeria. Journal of global antimicrobial resistanceJournal of Global Antimicrobial Resistance. 2018;12 :115-116.
Bouaziz A, Loucif L, Ayachi A, Guehaz K, Bendjama E, Rolain J-M. Migratory white stork (Ciconia ciconia): a potential vector of the OXA-48-producing Escherichia coli ST38 clone in Algeria. Microbial Drug ResistanceMicrobial Drug Resistance. 2018;24 :461-468.
Baoune H, Hadj-Khelil AOE, Pucci G, Sineli P, Loucif L, Polti MA. Petroleum degradation by endophytic Streptomyces spp. isolated from plants grown in contaminated soil of southern Algeria. Ecotoxicology and environmental safetyEcotoxicology and Environmental Safety. 2018;147 :602-609.
2017
Loucif L, Michelle C, Terras J, Rolain J-M, Raoult D, Fournier P-E. Draft Genome Sequence of Streptomyces specialis Type Strain GW41-1564 (DSM 41924). Genome AnnouncementsGenome Announcements. 2017;5 :e00101-17.
Loucif L, Cherak Z, Chamlal N, Bendjama E, Gacemi-Kirane D, Grainat N, Rolain J-M. First detection of VIM-2 metallo-β-lactamase-producing Pseudomonas putida in Blattella germanica cockroaches in an Algerian hospital. Antimicrobial agents and chemotherapyAntimicrobial Agents and Chemotherapy. 2017;61 :e00357-17.
Morakchi H, Loucif L, Gacemi-Kirane D, Rolain J-M. Molecular characterisation of carbapenemases in urban pigeon droppings in France and Algeria. Journal of global antimicrobial resistanceJournal of Global Antimicrobial Resistance. 2017;9 :103-110.
2016
Ramoul A, Loucif L, Bakour S, Amiri S, Dekhil M, Rolain J-M. Co-occurrence of blaNDM-1 with blaOXA-23 or blaOXA-58 in clinical multidrug-resistant Acinetobacter baumannii isolates in Algeria. Journal of global antimicrobial resistanceJournal of Global Antimicrobial Resistance. 2016;6 :136-141.
Loucif L, Gacemi-Kirane D, Cherak Z, Chamlal N, Grainat N, Rolain J-M. First report of German cockroaches (Blattella germanica) as reservoirs of CTX-M-15 extended-spectrum-β-lactamase-and OXA-48 carbapenemase-producing Enterobacteriaceae in Batna University Hospital, Algeria. Antimicrobial agents and chemotherapyAntimicrobial Agents and Chemotherapy. 2016;60 :6377-6380.
Loucif L, Gacemi-Kirane D, Cherak Z, Chamlal N, Grainat N, Rolain J-M. German cockroaches (Blattella germanica): reservoirs of CTX-M-15 ESBL and OXA-48 carbapenemase producing Enterobacteriaceae in Batna university hospital, Algeria: First report. Antimicrobial Agents and ChemotherapyAntimicrobial Agents and Chemotherapy. 2016.
Bourafa N, Abat C, Loucif L, Olaitan AO, Bentorki AA, Boutefnouchet N, Rolain J-M. Identification of vancomycin-susceptible major clones of clinical Enterococcus from Algeria. Journal of Global Antimicrobial ResistanceJournal of Global Antimicrobial Resistance. 2016;6 :78-83.

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