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23 October 2026

17 Pages

Predominance of Staphylococcus aureus in Peripheral Intravenous Catheter Colonization in Neonates: SCCmec Distribution and Antimicrobial Resistance

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1
Human Pathology Biomedicine and Environment Laboratory, Faculty of Medicine, Pharmacy and Dental Medicine, Sidi Mohamed Ben Abdellah University, Fez BP 1893, Morocco
2
Epidemiology and Health Science Research Laboratory, Faculty of Medicine, Pharmacy, and Dental Medicine, Sidi Mohamed Ben Abdellah University, Fez BP 1893, Morocco
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Author to whom correspondence should be addressed.
Antibiotics2026, 15(11), 1050;https://doi.org/10.3390/antibiotics15111050
This article belongs to the Special Issue Advances in Antimicrobial Action and Resistance
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Abstract

Background/Objectives: Peripheral intravenous catheters (PIVCs) are frequently used in neonatal intensive care units (NICUs) and can become major conduits of nosocomial infections, often colonized with clinically important bacteria, including methicillin-resistant Staphylococcus aureus (MRSA). Molecular data on PIVC-associated S. aureus in Moroccan NICUs remain limited. This study aimed to characterize bacterial colonization of PIVCs and investigate the phenotypic and molecular characteristics of recovered S. aureus, with particular emphasis on MRSA and staphylococcal cassette chromosome mec (SCCmec) types. Methods: 402 PIVC tips collected from 225 neonates hospitalized in the NICU of Hassan II University Hospital between June 2024 and May 2025 were analyzed using the Brun–Buisson quantitative culture method. Bacterial identification and antimicrobial susceptibility testing were performed, and S. aureus isolates were further characterized by PCR for 16S rRNA, mecA, and Panton–Valentine leukocidin (PVL) genes. SCCmec typing was performed on mecA-positive MRSA isolates. Results: Seventy-nine PIVC tips (19.7%, 95% CI: 16.1–23.8%) met the colonization criteria (≥1000 CFU/mL). A total of 152 bacterial isolates were recovered; S. aureus was the predominant species (n = 89, 58.6%), of which 15 (16.9%) were confirmed as MRSA. All MRSA isolates were mecA-positive. SCCmec typing identified two types; 12 isolates predominated and harboured SCCmec type IV (n = 12, 80.0%), while SCCmec type III was detected in three isolates (20.0%). No isolate harbored PVL genes, and no inducible clindamycin resistance was detected. MRSA isolates showed markedly higher resistance to gentamicin, fusidic acid, erythromycin, rifampicin, and clindamycin compared with MSSA isolates. Conclusions: S. aureus was the predominant bacterium recovered from PIVCs in our study. The predominance of SCCmec type IV among MRSA isolates provides original molecular epidemiological data from a Moroccan neonatal setting and highlights the need for continued surveillance of PIVC-associated MRSA and its molecular characteristics.

1. Introduction

Staphylococcus aureus is a Gram-positive pathogen that causes a wide range of clinical manifestations, ranging from superficial skin and soft tissue infections to severe invasive diseases such as bacteremia, endocarditis, osteomyelitis, and toxic shock syndrome [1,2]. The clinical importance of methicillin-resistant S. aureus strains (MRSA) has considerably increased due to their resistance to β-lactam antibiotics and their association with therapeutic difficulties. These strains were first identified shortly after the introduction of methicillin into clinical practice in 1959, and were described by Jevons in England in 1961 when clinical isolates exhibiting resistance to this semi-synthetic β-lactam were reported due to the acquisition of the mecA gene [3].
Methicillin resistance is primarily mediated by the acquisition of the mecA gene, which encodes the altered penicillin-binding protein 2a (PBP2a). This protein has a markedly reduced affinity for β-lactam antibiotics, allowing bacterial cell-wall synthesis to continue in their presence and resulting in broad-spectrum β-lactam resistance [4].
The mecA gene is acquired through a large mobile genetic element called the staphylococcal cassette chromosome mec (SCCmec), which integrates at a specific and conserved chromosomal locus, orfX; once integrated, SCCmec becomes a stable part of the bacterial chromosome [1,5]. These SCCmec elements are structurally defined by two essential genetic complexes: The mec gene complex and the cassette chromosome recombinase (ccr) complex. The mec complex consists of the mecA gene, its regulatory elements (mecI encoding a transcriptional repressor and mecR1 encoding a signal transducer) and finally flanking insertion sequences (IS431 or IS1272); all these elements together regulate the expression of methicillin resistance [5]. The ccr complex encodes site-specific recombinases, either a pair of genes (ccrA and ccrB) or a single ccrC gene, that mediate the integration and excision of SCCmec from the staphylococcal chromosome and its horizontal mobility [5,6]. These two complexes are delimited by three joining regions (J1, J2, J3) that may carry additional resistance determinants on integrated plasmids or transposons, conferring resistance to aminoglycosides, macrolides, or heavy metals depending on the SCCmec type [5]. According to the International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC), the SCCmec type is determined by the combination of the mec complex class and the ccr gene type; this has resulted in 15 SCCmec types that have been identified since 2022, which shows the genetic diversity of the SCCmec elements [6,7].
Molecular typing of SCCmec elements is not only a structural classification tool, but it is also considered a molecular key and an epidemiological approach that helps us trace the origin, clonal diversity and resistance profiles of circulating MRSA strains in clinical environments. In this context, a significant association between the SCCmec type and MRSA epidemiology has been reported. Large SCCmec elements like types I, II and III (34–67 kb) generally harbor several additional resistance determinants in their joining regions and are more commonly found in hospital-acquired MRSA (HA-MRSA) strains that are by definition multidrug-resistant [1,5]. In contrast, since types IV and V (20–28 kb) are smaller elements and contain fewer resistance genes besides the mecA gene, these types are more easily transferred between strains and are mainly found in community-acquired MRSA (CA-MRSA) [5,6]. The emergence of CA-MRSA since the mid-1990s has been well described as an epidemiologically and clinically distinct entity from HA-MRSA, differing in the patient populations affected, clinical presentation, and antimicrobial susceptibility pattern [8]. This distinction was further validated by a multi-center prospective cohort study conducted in U.S. laboratories that compared the epidemiology and microbiology of CA-MRSA and HA-MRSA infections [9].
However, SCCmec type alone cannot establish whether an isolate was acquired in the community or healthcare environment, determine its transmission pathway, or demonstrate clonality. Thus, SCCmec typing should be interpreted as a molecular epidemiological marker that provides useful context when combined with clinical, epidemiological, phenotypic, and other molecular data [8,9,10].
Neonatal intensive care units (NICUs) are high-risk environments for MRSA colonization and transmission because neonates are particularly vulnerable to infection and are frequently exposed to invasive medical devices [11]. Peripheral intravenous catheters (PIVCs) are widely used in this population for drug administration, fluid therapy, and nutritional support. Catheter insertion disrupts the skin barrier and provides a surface that may become colonized by microorganisms during catheter dwell time, making PIVCs relevant to infection-prevention surveillance in neonatal care [11,12]. Previous studies have documented bacterial colonization of peripheral venous cannulae in neonates and have identified staphylococci among the microorganisms recovered from catheter tips [12]. Quantitative bacteriological approaches have also been applied to peripheral venous catheter cultures in neonatal populations, supporting the assessment of bacterial colonization using quantitative catheter-tip culture.
Despite these observations, the molecular characteristics of S. aureus associated specifically with PIVC colonization in neonates remain insufficiently documented. In particular, information on MRSA recovered from neonatal PIVCs and the distribution of SCCmec types among these isolates remains limited. In Morocco, molecular studies have characterized MRSA in pediatric healthcare settings, including the study by Serray et al., which reported multiple SCCmec types among MRSA isolates recovered from a pediatric hospital [10]. However, these data were obtained from a broader pediatric population and different clinical specimens and therefore do not specifically characterize S. aureus associated with PIVC colonization in neonates. The molecular epidemiology of PIVC-associated S. aureus, particularly MRSA and SCCmec distribution, therefore remains insufficiently characterized in Moroccan neonatal settings.
Molecular characterization of S. aureus isolates, including SCCmec typing using multiplex PCR approaches [13,14], together with phenotypic antimicrobial susceptibility testing and detection of virulence determinants such as Panton–Valentine leukocidin (PVL), can provide complementary information on the characteristics of MRSA isolates circulating in clinical settings [10]. SCCmec typing is particularly useful for describing the structural diversity of the mecA-carrying element; however, SCCmec type alone should not be interpreted as definitive evidence of community acquisition, healthcare acquisition, transmission, or clonality. Such conclusions require integration with epidemiological information and, where appropriate, higher-resolution molecular or genomic methods.
The present study was conducted in the Neonatal Intensive Care Unit (NICU) of the Hassan II University Hospital of Fez, Morocco during the period June 2024 to May 2025. The aim was to characterize bacterial colonization of peripheral venous catheters in hospitalized neonates, and to investigate the phenotypic and molecular characteristics of the recovered S. aureus isolates. Molecular detection of the mecA gene was used to confirm methicillin resistance, while species identification was confirmed phenotypically and supported by molecular detection of the 16S rRNA and nuc genes. SCCmec typing was performed to characterize the molecular profiles of MRSA isolates and to describe the distribution of SCCmec types among PIVC-associated MRSA. Screening for Panton–Valentine leukocidin (PVL) genes was also performed to characterize selected virulence determinants among the recovered S. aureus isolates. Together, these approaches were used to address the limited molecular epidemiological data available on PIVC-associated S. aureus in Moroccan neonatal settings.

2. Results

2.1. Clinical and Catheter Characteristics

402 peripheral intravenous catheter (PIVC) tips were collected from 225 hospitalized neonates admitted to the Neonatal Intensive Care Unit (NICU) of Hassan II University Hospital, Fez, Morocco, between June 2024 and May 2025. Among the 225 neonates, male newborns predominated (n = 130, 57.8%) over females (n = 95, 42.2%). Regarding the gestational age, 135 (60.0%) neonates were full-term and 90 (40.0%) were born prematurely. A total of 179 neonates were born via vaginal delivery (79.6%), 51.6% (116/225) presented with respiratory distress, and 10.7% (24/225) had underlying congenital anomalies (Table 1A).
Table 1. (A): Baseline Demographic and clinical Characteristics of Hospitalized Neonates (n = 225). (B): Catheter Characteristics and Colonization Status among 402 Analyzed PIVCs.
Because catheter colonization is a device-specific event directly linked to insertion site, local handling, and dwell time, all demographic, clinical, and microbiological variables were calculated using the total number of evaluated catheters (n = 402) as the denominator.
At the catheter level (n = 402), most PIVCs were inserted in the hand (292/402, 72.6%), followed by the foot (65/402, 16.2%), arm (23/402, 5.7%), forearm (21/402, 5.2%), and cranial site (1/402, 0.2%). Left-sided insertion was more frequent than right-sided insertion (302/402, 75.1% vs. 100/402, 24.9%). The mean number of insertion attempts was 2 attempts, and the mean PIVC dwell time was 2 days. Of the 402 PIVCs, 60 (14.9%) were removed systematically, while 342 (85.1%) were removed due to a clinical indication, for example, suspected phlebitis, occlusion, infiltration, or catheter dislodgement.
Culture quantification revealed that 79 PIVC tips (19.7%, 95% CI: 16.1–23.8%) met the quantitative criterion for catheter colonization (≥1000 CFU/mL). Among the remaining 323 non-colonized PIVC tips (<1000 CFU/mL), 280 tips (86.7% of non-colonized; 69.7% of all PIVCs) were completely sterile (0 CFU/mL), whereas 43 tips (13.3% of non-colonized; 10.7% of all PIVCs) exhibited sub-threshold bacterial counts (1–999 CFU/mL). No statistically significant association was observed between catheter colonization status and insertion site, insertion side, or dwell time (Table 1B).

2.2. PIVC Colonization and Bacterial Distribution

Across all 402 analyzed PIVC tips, 152 bacterial isolates were recovered in total, including isolates from tips with sub-threshold bacterial counts (<1000 CFU/mL). Overall, S. aureus was the most frequently recovered species (89/152, 58.6%), followed by CoNS (51/152, 33.6%), E. coli (7/152, 4.6%), and K. pneumoniae (5/152, 3.3%) (Table 2).
Table 2. Distribution of bacterial isolates recovered from peripheral intravenous catheter tips in the NICU of Hassan II University Hospital, Fez, Morocco, 2024–2025.
Based on the Brun–Buisson quantitative criterion (≥1000 CFU/mL), 79 PIVC tips (19.7%, 95% CI: 16.1–23.8%) were classified as colonized.
Restricting the analysis strictly to the 79 colonized PIVC tips, a total of 106 bacterial isolates were recovered: 53 tips (67.1%) yielded a single bacterial species, including S. aureus (n = 32), coagulase-negative staphylococci (CoNS) (n = 14), E. coli (n = 4), and K. pneumoniae (n = 3) while polymicrobial growth was observed in 26 tips (32.9%), including 25 tips with two co-isolated organisms and one tip with three organisms. Within this colonized subset, S. aureus remained the predominant organism (recovered from 57/79 tips, 72.2%), followed by CoNS (38/79, 48.1%), E. coli (6/79, 7.6%), and K. pneumoniae (5/79, 6.3%). Among the 26 polymicrobial tips, the most frequent combination was S. aureus with CoNS (23/26), followed by S. aureus with K. pneumoniae (1/26), E. coli with K. pneumoniae (1/26), and one tip yielding S. aureus, CoNS, and E. coli together.
Notably, 57 of the total 89 S. aureus isolates and all 15 MRSA isolates originated from quantitatively colonized PIVC tips (≥1000 CFU/mL).
Given the overall predominance of S. aureus and its clinical relevance in neonatal healthcare-associated infections, all 89 S. aureus isolates were retained for subsequent phenotypic and molecular characterization.

2.3. Antimicrobial Susceptibility Profile of Staphylococcus aureus

Antimicrobial susceptibility testing was performed on all 89 S. aureus isolates recovered from the 402 sampled PIVC tips. These comprised 57 isolates recovered from PIVC tips meeting the predefined quantitative colonization threshold (≥103 CFU/mL) and 32 isolates recovered from tips with sub-threshold bacterial counts (<103 CFU/mL). Among the 89 S. aureus isolates, 74 (83.1%) were classified as methicillin-susceptible S. aureus (MSSA) and 15 (16.9%, 95% CI: 10.5–26.0%) as methicillin-resistant S. aureus (MRSA).
The highest proportion of resistance among all S. aureus isolates was observed for penicillin G (27/89, 30.3%), followed by gentamicin (14/89, 15.7%), fusidic acid (12/89, 13.5%), erythromycin (9/89, 10.1%), clindamycin (7/89, 7.9%), levofloxacin (5/89, 5.6%), and rifampicin (5/89, 5.6%). Resistance patterns according to methicillin-resistance phenotype are presented in Table 3.
Table 3. Antimicrobial susceptibility profile of the 89 Staphylococcus aureus isolates according to methicillin susceptibility.
Resistance was consistently more frequent among MRSA isolates than among MSSA isolates. Using two-sided Fisher’s exact tests, the difference between MRSA and MSSA was statistically significant for penicillin G (100% vs. 16.2%, p < 0.001), erythromycin (40.0% vs. 4.1%, p < 0.001), clindamycin (33.3% vs. 2.7%, p = 0.001), gentamicin (46.7% vs. 9.5%, p = 0.002), levofloxacin (26.7% vs. 1.4%, p = 0.003), rifampicin (33.3% vs. 0%, p < 0.001), and fusidic acid (46.7% vs. 6.8%, p < 0.001). As expected from the phenotypic classification, cefoxitin resistance was detected in all MRSA isolates (15/15, 100%) and in none of the MSSA isolates (0/74, p < 0.001).
Because the MRSA group comprised only 15 isolates, these statistical comparisons were considered exploratory. The small sample size limits statistical power and the precision of the estimated differences; therefore, the observed associations should not be interpreted as definitive estimates of differences in antimicrobial resistance between MSSA and MRSA.
Inducible clindamycin resistance was assessed according to the erythromycin–clindamycin susceptibility pattern. Seven of the nine erythromycin-resistant isolates were also resistant to clindamycin, whereas two isolates were erythromycin-resistant but clindamycin-susceptible. These two isolates were further evaluated using the D-test, and both showed a negative D-test, with no flattening of the clindamycin inhibition zone toward the erythromycin disk.

2.4. Molecular Characterization of Staphylococcus aureus

All 89 S. aureus isolates were confirmed at the species level by standard phenotypic and biochemical identification (API Staph) and were successfully amplified for the nuc gene, which encodes the thermostable nuclease used as a species-specific molecular marker for S. aureus, and the 16S rRNA gene, confirming adequate bacterial DNA quality and the absence of PCR inhibitors. All 15 isolates identified phenotypically as methicillin-resistant S. aureus (MRSA) were positive for the mecA gene, confirming methicillin resistance at the molecular level. All 89 S. aureus isolates were negative for the Panton–Valentine leukocidin genes (lukF-lukS), indicating that none of the isolates carried PVL-associated virulence determinants.

2.5. SCCmec Distribution Among MRSA Isolates

SCCmec typing was performed on all the 15 mecA-positive MRSA isolates using a multiplex PCR approach targeting characteristic SCCmec-associated loci. The amplicon of internal-control mecA (162 bp) was detected in all isolates. Amplification profiles were analysed based on the combination of type-specific products and the lack of competing amplicons, allowing definitive assignment to two SCCmec types (Figure S1). SCCmec type IV (n = 12, 80.0%, 95% CI: 54.8–93.0%) was the most prevalent and characterized by the presence of the amplification product of DCS (342 bp) with the amplicon mecA and the absence of all other amplicons specific for the type. The other 3 isolates (20.0%) had SCCmec type III which was identified by the RIF4 amplification product (243 bp) in addition to the mecA amplicon. No other SCCmec types were identified.

3. Discussion

This prospective study provides clinical, microbiological, and molecular epidemiological data on Staphylococcus aureus recovered from peripheral intravenous catheters (PIVCs) in a neonatal intensive care unit (NICU) in Morocco. Among 402 PIVCs collected from 225 neonates, 79 (19.7%, 95% CI: 16.1–23.8%) met the predefined quantitative criterion for catheter colonization. Among these colonized PIVC tips, S. aureus was the predominant organism, being recovered from 57/79 tips (72.2%). Overall, 89 S. aureus isolates were recovered from the 402 sampled PIVC tips, of which 74 (83.1%) were methicillin-susceptible S. aureus (MSSA) and 15 (16.9%) were methicillin-resistant S. aureus (MRSA). All MRSA isolates carried mecA, none carried the targeted PVL genes, and SCCmec type IV predominated among MRSA isolates (12/15, 80.0%), followed by type III (3/15, 20.0%).
The main contribution of the present study is therefore not simply the observation that S. aureus can colonize PIVCs, which has been documented previously, but the characterization of PIVC-associated bacterial colonization in a neonatal population using quantitative catheter culture combined with antimicrobial susceptibility testing and molecular characterization. In particular, the study provides local data on MRSA, SCCmec distribution, and antimicrobial resistance in PIVC-associated S. aureus in a Moroccan NICU.
The observed colonization rate of 19.7% indicates that PIVCs may provide an important surface for bacterial persistence in the neonatal setting. The predominance of S. aureus is clinically relevant because this organism is frequently associated with healthcare-associated infections in neonates and may originate from the skin microbiota. The presence of polymicrobial growth in approximately one-third of colonized PIVCs further indicates that catheter colonization may involve multiple bacterial species.
Among the 79 colonized PIVC tips, S. aureus was recovered from 57 tips (72.2%). This finding highlights the prominent contribution of S. aureus to PIVC colonization in this population. Importantly, this figure represents PIVC tips, whereas the subsequent molecular and antimicrobial analyses were performed on individual S. aureus isolates. The 89 S. aureus isolates identified in the study included 57 isolates recovered from PIVC tips meeting the predefined colonization threshold and 32 isolates recovered from tips with sub-threshold bacterial counts. Maintaining this distinction is essential for interpreting the microbiological and molecular findings.
Importantly, catheter-tip colonization should not be equated with catheter-related bloodstream infection (CRBSI). Recovery of microorganisms from a catheter tip alone does not establish bloodstream infection. CRBSI requires clinical evidence of infection together with microbiological evidence linking the catheter to the bloodstream infection, such as compatible blood culture and catheter-related microbiological findings [15].
The present study did not assess subsequent bacteremia, sepsis, or other clinical outcomes [16]. Therefore, the observed 19.7% frequency should be interpreted primarily as evidence of PIVC colonization rather than as an estimate of CRBSI incidence. Nevertheless, catheter colonization remains clinically relevant because colonized intravascular devices may represent an important microbiological reservoir and may contribute to the pathway leading to device-associated infection under appropriate clinical circumstances.
The distribution of SCCmec types among MRSA varies according to geographic region, healthcare setting, patient population, and study period. In the present study, SCCmec type IV was identified in 12 of 15 MRSA isolates (80.0%), whereas type III was identified in three isolates (20.0%).
This predominance of SCCmec type IV is consistent with observations from some neonatal and pediatric intensive-care settings. Pereira et al., who characterized MRSA isolates recovered from neonatology and pediatric intensive-care units of a university hospital, identified SCCmec type IV in 12 of 21 isolates (57.1%) and type III in nine (42.9%) [17]. Similarly, Reich et al., in a prospective study conducted in a level IV NICU, observed a predominance of SCCmec type IV among the community-associated MRSA isolates investigated [18].
In a New York NICU followed from 2000 to 2008, Carey et al. reported a change in the predominant MRSA clone from a healthcare-associated SCCmec type II during 2001–2004 to SCCmec type IV from 2005 onward, with USA300 appearing in 2007 [19]. These findings illustrate that SCCmec distributions within a single NICU may change substantially over time.
More recently, Rallis et al. emphasized the molecular and epidemiological diversity of MRSA in neonates and highlighted the importance of distinguishing healthcare-associated and community-associated strains using broader molecular and epidemiological characteristics rather than relying on a single marker such as SCCmec type [20].
The predominance of SCCmec type IV in the present study should be interpreted cautiously. SCCmec type IV has frequently been associated with community-associated MRSA, but its presence does not constitute definitive evidence of community acquisition. Chew et al. reported that SCCmec type IV can also occur among hospitalized neonates and healthcare-associated strains [21].
The traditional distinction between community-associated and healthcare-associated MRSA based primarily on SCCmec type has consequently become less clear. Community-associated MRSA lineages, particularly USA300, have spread into healthcare settings and have been implicated in healthcare-associated infections and outbreaks [22,23].
Accordingly, the predominance of SCCmec type IV in our NICU should be regarded as a molecular epidemiological finding rather than evidence of community acquisition or a specific transmission pathway. Determining the origin and epidemiological relationships of these isolates would require additional epidemiological information and higher-resolution molecular characterization.
Within Morocco, our findings differ from those reported by Serray et al., who investigated MRSA in a mother–child hospital at CHU Mohamed VI in Marrakech. Their study was conducted between December 2010 and May 2014 and included patients aged 2 days to 15 years, from whom 259 S. aureus isolates were recovered from various clinical specimens. Among these, 53 (20.46%) were identified as MRSA, including six MRSA isolates recovered from catheter specimens [10].
SCCmec type III was the predominant type among their MRSA isolates (25/53, 47.17%), followed by type IV (18/53, 33.96%), while types II, V, and I accounted for 11.32%, 5.66%, and 1.89%, respectively [10]. In contrast, the MRSA isolates characterized in our study were predominantly SCCmec type IV (12/15, 80.0%).
These differences may reflect variations in patient populations, clinical specimens, healthcare settings, and study periods. They may also reflect temporal or institutional differences in the MRSA populations circulating in Moroccan healthcare facilities. Nevertheless, comparisons should be interpreted cautiously because the two studies were not conducted in comparable populations or clinical settings.
The antimicrobial susceptibility results showed a broader resistance profile among MRSA than MSSA isolates, particularly for erythromycin, clindamycin, gentamicin, rifampicin, and fusidic acid. This finding is clinically relevant in neonatal care, where antimicrobial selection is constrained by patient age, toxicity considerations, and the need for targeted therapy.
The combination of phenotypic antimicrobial susceptibility testing with mecA detection provides complementary information for characterizing the resistance profile of the isolates. However, because only 15 MRSA isolates were identified, these resistance patterns should be considered descriptive rather than representative of the wider MRSA population in Moroccan NICUs. The small number of MRSA isolates also limits the statistical power and precision of subgroup comparisons.
Several potential reservoirs and routes of transmission may contribute to the acquisition and spread of MRSA in NICUs, including mothers, healthcare workers, neonates’ skin microbiota, environmental surfaces, family members, and expressed breast milk.
Saiman et al. investigated an outbreak of community-acquired MRSA in postpartum women and identified eight women with MRSA skin and soft-tissue infections. Although the outbreak strain was SCCmec type IV, the source of transmission was not identified through surveillance cultures of hospital employees, the hospital environment, and newborns [24].
Gastelum et al. subsequently documented transmission of community-associated MRSA associated with expressed breast milk in a NICU, providing a documented example of a maternal milk-associated route of neonatal exposure [25]. David et al. also demonstrated that community-associated MRSA can establish transmission within a neonatal healthcare setting. Their study involved four neonates and one staff member and identified a single clone carrying SCCmec type IVa, demonstrating that a strain with a community-associated molecular profile can subsequently undergo healthcare-associated spread in a neonatal unit [26].
More recently, Keneh et al. systematically reviewed MRSA carriage in non-outbreak NICUs and reported MRSA carriage among mothers, healthcare workers, and environmental samples, with pooled proportions of 2.1%, 9.6%, and 16.6%, respectively, although substantial heterogeneity was observed between studies [27].
In a level II NICU, Tiroumourougane Serane and Kothendaraman recovered bacteria from 22 of 154 catheter tips, predominantly methicillin-susceptible S. aureus. In five cases, the organism recovered from the catheter was identical to that identified on the neonate’s own skin, supporting skin flora as a potential source of PIVC colonization [28].
Collectively, these studies indicate that MRSA detected on neonatal vascular devices may potentially originate from multiple reservoirs and subsequently spread within the healthcare environment. However, our study did not systematically screen healthcare workers, mothers, family members, or environmental surfaces. Therefore, the precise source and direction of transmission cannot be established from the present data, and SCCmec typing alone cannot determine the transmission pathway.
The strengths of this study include prospective PIVC sampling, quantitative catheter culture, antimicrobial susceptibility testing, and molecular characterization using mecA, PVL, and SCCmec typing. The study also contributes data from a neonatal population that remains relatively underrepresented in Moroccan MRSA molecular epidemiology.
Several limitations should be considered. First, the study was conducted in a single NICU, which may limit the generalizability of the findings. Second, the study assessed PIVC colonization rather than catheter-associated bloodstream infection or other clinical outcomes. Third, SCCmec typing alone does not provide sufficient resolution for definitive clonal characterization or reconstruction of transmission chains; additional approaches such as spa typing, multilocus sequence typing (MLST), or whole-genome sequencing would provide greater discriminatory power.
Fourth, systematic screening of potential reservoirs such as healthcare workers, mothers, family members, and environmental surfaces was not performed. Accordingly, the precise sources and transmission pathways of the detected MRSA isolates could not be established. Fifth, the relatively small number of MRSA isolates (n = 15) limits the statistical power of comparisons between SCCmec types and between MRSA and MSSA resistance profiles. Finally, repeated PIVCs from some neonates may introduce within-patient clustering and should be considered when interpreting catheter-level analyses.
Because catheter tips were collected both at routine removal and following clinically indicated removal, differential sampling according to catheter complications or suspected local infection cannot be completely excluded. Consequently, the observed colonization frequency may have been influenced by the indications leading to catheter removal.
Future multicenter studies integrating clinical risk factors, catheter-related outcomes, systematic screening of potential reservoirs, and high-resolution genomic typing are warranted to clarify the genetic relatedness and epidemiological pathways of MRSA in Moroccan NICUs. Whole-genome sequencing could provide substantially greater resolution than SCCmec typing alone and could help distinguish related from unrelated isolates and investigate potential transmission events.
Future studies should also incorporate patient-level longitudinal analyses linking PIVC colonization with clinically relevant outcomes such as bacteremia and sepsis, while accounting for repeated PIVCs within individual neonates. Such studies would provide a stronger basis for determining the clinical implications of PIVC colonization and for developing targeted infection-prevention strategies.
Overall, the predominance of S. aureus among colonized PIVCs and the high proportion of SCCmec type IV among MRSA isolates provide relevant molecular epidemiological information from a Moroccan NICU. These findings support continued microbiological surveillance and rigorous PIVC-related infection-prevention practices while underscoring that SCCmec type IV alone cannot establish community acquisition or a specific transmission pathway. Higher-resolution genomic and epidemiological studies are needed to better understand MRSA.

4. Materials and Methods

4.1. Study Design and Setting

This prospective study was conducted during the period June 2024 to May 2025, in the Neonatal Intensive Care Unit (NICU) of the Hassan II University Hospital in Morocco, a tertiary-level hospital and a regional referral center for high-risk and critically ill newborns. The unit admits both pre-term and term neonates with a variety of conditions like respiratory distress, infections, neurological or metabolic disturbances, congenital malformations and surgical pathologies. It has a neonatal resuscitation unit for unstable or surgical patients, a unit for premature infants, which looks after neonates from 28 weeks of gestation or weighing approximately 1000 g, and a day hospital for emergency consultations and early follow-up after discharge.

4.2. Study Population, Inclusion/Exclusion Criteria, and Sampling Procedure

Neonates admitted to the NICU of Hassan II University Hospital of Fez, Morocco, during the study period who required peripheral intravenous catheterization were prospectively screened. Both preterm and full-term neonates were eligible for inclusion. Only standard 24-gauge (24 G) peripheral intravenous catheters (PIVCs) inserted and managed within the NICU during the infant’s hospitalization were eligible. Catheters inserted before NICU admission, including those placed in the delivery room, emergency department, or referring healthcare facilities, were excluded.
A total of 402 PIVC tips were collected from 225 neonates. Consecutive sampling was applied to all eligible PIVC tips removed during the NICU stay. Successive catheters from the same neonate were included, irrespective of the anatomical site or side of insertion. PIVCs were removed either systematically at the end of therapy or for clinical indications including phlebitis, extravasation, infiltration, occlusion, or suspected local infection, regardless of prior systemic antibiotic exposure. Non-hospitalized infants (such as day-hospital consultations), pre-admission catheters, specimens with missing clinical data, and catheter tips that were contaminated, improperly handled, or unavailable for analysis were excluded. Catheter removal was performed by trained neonatal nurses under strict aseptic conditions. Approximately 2 cm of the distal catheter tip was cut using sterile scissors and placed in a sterile container for immediate transport to the laboratory. All microbiological and molecular analyses were performed at the Microbiology and Molecular Biology Laboratory, Faculty of Medicine, Pharmacy and Dentistry, Sidi Mohamed Ben Abdellah University, Fez, Morocco.

4.3. Catheter Tip Culture

Catheter-tip colonization was evaluated using a quantitative culture method based on the Brun–Buisson protocol [15] with additional support from previous studies evaluating quantitative bacterial colonization of peripheral venous catheters, including neonatal populations [29]. Briefly, approximately 2 cm of the distal catheter tip was placed in 1 mL of sterile 0.9% physiological saline and vortexed for 1–3 min to dislodge adherent microorganisms. From this initial mother suspension, a series of five 10-fold dilutions was prepared in sterile physiological saline. Aliquots of 0.1 mL from the undiluted suspension and from each serial dilution step were spread onto 5% sheep blood agar plates (Oxoid, Dardilly, France) and incubated at 37 °C for 48 h; a single plate was cultured per dilution level (no duplicate plating). Colony-forming units (CFU) were quantified, adjusted for the dilution factor and inoculated volume, and expressed as CFU/mL, with a lower limit of detection of 10 CFU/mL. If no colonies were observed on any plate, including the undiluted suspension, the tip was recorded as negative (0 CFU/mL).
An uninoculated blood agar plate was incubated in parallel with every culture batch as a negative control to confirm medium sterility and rule out laboratory or handling contamination.
Catheter colonization was defined a priori as a colony count of ≥1000 CFU/mL (≥1000 CFU/mL). Although originally described for central venous catheters, this quantitative threshold (≥1000 CFU/mL) has since been applied to peripheral intravenous catheters in multicenter studies [30] as well as to catheter tip cultures in neonatal intensive care settings [31], supporting its suitability for the present study population.
Each morphologically distinct colony type (varying in size, pigmentation, margin, or hemolysis) was enumerated separately, and in cases of polymicrobial growth, every co-isolated bacterial species was quantified individually. For catheter tips displaying sub-threshold growth (<1000 CFU/mL, down to 10 CFU/mL), bacterial counts and species identities were systematically recorded into the study isolate inventory. All recovered S. aureus isolates from both quantitatively colonized (≥1000 CFU/mL) and sub-threshold (<1000 CFU/mL) PIVC tips were subsequently retained for full phenotypic antimicrobial susceptibility testing and molecular characterization. Laboratory personnel performing colony counts were not blinded to neonates’ clinical status, as this information was subsequently used for correlation with clinical outcomes in a related analysis of the same cohort.

4.4. Bacterial Identification

Colonies recovered from the primary blood agar cultures described in Section 4.3 were subcultured onto Mannitol Salt Agar (Oxoid, France) for selective isolation of staphylococci. On this medium, S. aureus normally grows as golden-yellow colonies due to fermentation of mannitol with production of acid and a change in color of the phenol red pH indicator. Eosin Methylene Blue (EMB) agar (Oxoid, France) was used for the isolation of Gram-negative bacteria. E. coli was identified by its characteristic metallic green sheen and K. pneumoniae formed large, mucoid, pink to purple lactose-fermenting colonies. Colony morphology and standard biochemical characteristics were used for preliminary identification. Further identification was confirmed by Gram stain and by conventional biochemical tests including catalase, coagulase, oxidase and DNase assays, and Analytical Profile Index (API) systems: API Staph for staphylococci and API 20E for Gram-negative isolates (BioMérieux, Marcy-l'Étoile, France).

4.5. Antimicrobial Susceptibility Testing and Phenotypic Detection of Methicillin Resistance

Antimicrobial susceptibility testing was performed using the Kirby-Bauer disk diffusion method on Mueller-Hinton agar (MHA) following the EUCAST/CA-SFM 2024 guidelines [32]. The bacterial suspension of each isolate was adjusted to a 0.5 McFarland turbidity standard and inoculated uniformly onto MHA plates. The antimicrobial agents used for testing of the S. aureus isolates were as follows: Penicillin G (1U), Gentamicin (10 µg), Levofloxacin (5 µg), Erythromycin (15 µg), Fusidic acid (10 µg), Clindamycin (2 µg), Cefoxitin (30 µg), and Rifampicin (5 µg). The diameters of the inhibition zones were measured and interpreted using the recommendations of EUCAST/CA-SFM 2024 [32]. Isolates were classified as Susceptible (standard dosing regimen), Susceptible with increased exposure, or Resistant. Staphylococcus aureus ATCC 25923 was used as a quality control strain throughout the study.
The cefoxitin disk (30 µg) was used for screening of methicillin resistance and isolates were categorized as methicillin-sensitive S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA). Isolates of S. aureus resistant to erythromycin but susceptible to clindamycin were also screened for inducible clindamycin resistance by the double-disk diffusion test (D-test) as recommended by EUCAST [32].

4.6. DNA Extraction

Genomic DNA was extracted from all confirmed S. aureus isolates using the rapid boiling method of Zhang et al. [33]. Briefly, 1–5 colonies from the nutrient agar plate were suspended in 50 µL of sterile distilled water and heated at 99 °C for 10 min. The suspension was then centrifuged for 10 min at 20,000× g, 4 °C. The supernatant containing the extracted DNA was collected and stored at −20 °C for further use.

4.7. Multiplex PCR for Detection of 16S rRNA, mecA and PVL Genes

Multiplex PCR was performed for the simultaneous detection of the mecA and lukF-lukS genes, with the 16S rRNA gene serving as an internal amplification control to verify DNA quality and the absence of PCR inhibitors [2,33,34]. The mecA gene was investigated as the primary molecular determinant of methicillin resistance, whereas the lukF-lukS genes were screened as markers encoding the two protein subunits of Panton–Valentine leukocidin (PVL).
PCR amplification conditions were based on the protocol described by McClure et al. [34], with a modified final extension step at 72 °C for 10 min as previously applied [2]; full primer sequences and thermocycling parameters are provided in Table 4.
Table 4. Primers used for multiplex PCR detection of mecA, nuc, 16S rRNA, and LukF-LukS genes.
Species-level molecular confirmation of S. aureus was performed independently, targeting the nuc gene, encoding the thermostable nuclease specific for S. aureus. Amplification of nuc was conducted as a separate simplex PCR using the species-specific primer pair nuc-F and nuc-R, generating an expected 359-bp amplicon [35].
Thermocycling parameters for the nuc simplex PCR are also detailed in Table 4.
PCR products from both assays were separated by electrophoresis (1.8% agarose gel for the multiplex reaction; 1% agarose gel for the nuc simplex reaction), stained with ethidium bromide, and visualized under UV illumination.
Quality control was rigorously maintained across all PCR runs. A well-characterized mecA-positive MRSA clinical isolate (ATCC BAA-44) was used as a positive control for methicillin resistance, and Staphylococcus aureus ATCC 25923 was included as a reference strain. A PVL-positive clinical isolate, previously characterized in earlier work, was used as a positive control for the lukF-lukS assay. A no-template control (sterile nuclease-free water replacing DNA) and a negative extraction control were included in every PCR run to monitor for potential contamination.

4.8. SCCmec Typing

SCCmec typing was performed only in confirmed MRSA isolates by multiplex PCR targeting six SCCmec types (I, IA, II, III, IV and IVA) based on loci located upstream and downstream of the mecA gene as described by Zetola et al. [37] and applied by Valle et al. [2]. The mecA gene was used as an internal control for amplification.
Thermal cycling conditions for the SCCmec multiplex PCR consisted of an initial denaturation at 94 °C for 4 min; 30 cycles of denaturation at 94 °C for 30 s, primer annealing at 53 °C for 30 s, and extension at 72 °C for 1 min; followed by a final extension at 72 °C for 5 min. Electrophoresis of the PCR products was performed on a 1.8% agarose gel, stained with ethidium bromide, and visualized under UV illumination. Primer sequences, target regions, and amplicon sizes are presented in Table 5 [2].
Table 5. Primers used for SCCmec typing by multiplex PCR.

4.9. Statistical Analysis

Data was analyzed with SPSS Statistics, Version 26 (IBM Corp., Armonk, NY, USA). Descriptive statistics were calculated for all variables and extreme or inconsistent data were re-checked for accuracy. Continuous variables were presented as mean ± standard deviation and categorical variables as absolute frequencies and percentages. The associations between categorical variables were assessed by the Chi-square test or Fisher’s exacttest, as appropriate. Because some neonates contributed more than one PIVC, observations at the catheter level are not fully independent; therefore, catheter-level statistical comparisons (Table 1B) are considered exploratory and aimed at identifying potential univariate associations. Statistical significance was considered at p ≤ 0.05.

5. Conclusions

Staphylococcus aureus was the predominant organism recovered from PIVC tips in the NICU of Hassan II University Hospital, Fez. The predominance of SCCmec type IV among the MRSA isolates provides original molecular epidemiological data from a Moroccan neonatal setting and demonstrates the coexistence of SCCmec type IV and III among PIVC-associated MRSA. These findings support continued microbiological surveillance and molecular characterization of MRSA in neonatal healthcare settings.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/antibiotics15111050/s1, Figure S1: Representative agarose gel electrophoresis images from SCCmec multiplex PCR typing.

Author Contributions

M.R. performed the sample collection, conducted the study, analyzed the data, and drafted the manuscript. M.B. assisted with manuscript writing and the scientific interpretation of the results. S.B. assisted with the study and provided essential resources for its execution. F.H. and B.O. provided continuous guidance and scientific supervision throughout the study, critically revised the manuscript, and offered expert advice to ensure the rigor, quality, and integrity of the work. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

This study was approved by the Ethics Committee of the Faculty of Medicine and Pharmacy and the Hassan II University Hospital of Fez, Morocco (number 05/24), and complied with the principles of the Ethics Declaration following the guidelines of the Declaration of Helsinki. Written informed consent to participate was obtained from the parents or legal guardians of all newborns included in the study.

Data Availability Statement

The data supporting the findings of this study are available within the article and its Supplementary Materials. Additional data related to this study are available from the corresponding author upon reasonable request.

Acknowledgments

Manal Rossi gratefully acknowledges the National Center for Scientific and Technical Research (CNRST), Morocco, for supporting this research through the PhD Associate Scholarship (PASS).

Conflicts of Interest

The authors declare no conflicts of interest.

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