Research Article | Open Access
Rike Syahniar1 , Adinta Anandani1, Aning Subiyatin2 and Hanif Ahmad Mubarok3
1Department of Microbiology, Faculty of Medicine and Health, Universitas Muhammadiyah Jakarta, Jakarta, Indonesia.
2Department of Midwifery, Faculty of Medicine and Health, Universitas Muhammadiyah Jakarta, Jakarta, Indonesia.
3Medical Study Program, Faculty of Medicine and Health, Universitas Muhammadiyah Jakarta, Jakarta, Indonesia.
Article Number: 8957 | © The Author(s). 2024
J Pure Appl Microbiol. 2024;18(2):1319-1325. https://doi.org/10.22207/JPAM.18.2.54
Received: 31 August 2023 | Accepted: 30 April 2024 | Published online: 02 June 2024
Issue online: June 2024
Abstract

Most S. aureus infections are multidrug resistant. S. aureus infections often occur with prolonged conditions, causing increased treatment costs and mortality rates. There is a need to understand the antibiotic susceptibility pattern to S. aureus in mothers and infants because the burden of S. aureus infection in infants is high. This study aims to determine the prevalence of nasal carriers of S. aureus in lactating mothers and their infants and their antibiotic susceptibility patterns. This cross-sectional study involved 59 pairs of breastfeeding mothers and infants aged 0 to 6 months. The research was conducted in the work area of the South Tangerang City Health Office. We take a nasal swab of the mother and the baby. We used Vitek-2 to determine antibiotic resistance against S. aureus. Overall, we found 22/59 (37%) S. aureus in infants’ noses, 18% of whom were MRSA. In mothers, we found 18/59 (30%) S. aureus isolates and 17% were MRSA. The majority of S. aureus isolates from infants were sensitive to cefoxitin (82%), gentamicin (86%), ciprofloxacin (91%), levofloxacin (95%), moxifloxacin (91%), vancomycin (100%), clindamycin (82%), erythromycin (86%), nitrofurantoin (100%), linezolid (100%) and tetracycline (77%). The majority of S. aureus isolates from mothers are sensitive to cefoxitin (83%), gentamicin (94%), ciprofloxacin (89%), levofloxacin (89%), moxifloxacin (89%), vancomycin (100%), clindamycin (89%), erythromycin (89%), nitrofurantoin (100%), linezolid (100%) and tetracycline (83%). MRSA monitoring of mothers and babies in the community needs to be done to prevent and control the spread.

Keywords

Antibiotics, Infant, MRSA, Staphylococcus aureus, Lactating Mothers

Introduction

Staphylococcus aureus infections range from soft tissue infections to bacteremia, which causes morbidity or mortality in hospital and community settings.1 S. aureus infections that should be treated with antibiotics have been found to have S. aureus strains resistant to several antibiotics.2 Infants appear especially susceptible to colonization and infection with Methicillin-Resistant Staphylococcus aureus (MRSA). Colonization or MRSA infection in neonates is associated with significant morbidity, causing a burden of medical care costs for affected infants.3 MRSA colonization rates in neonatal infections range from 3.9% to 32%. This is of particular concern among important pathogens causing infections in hospitals.4 MRSA transmission is most likely through the birth canal and/or through contact with surrounding people, namely parents, health workers, visitors, or a contaminated hospital environment.4

The prevalence of S. aureus resistance in Asia, both methicillin resistance acquired in healthcare and the community, is the highest in the world.2 The systematic review study that we have done has found the prevalence of MRSA 0.3%-52% from various clinical isolates in Indonesia.5 The results of a meta-analysis study found that infants who were colonized with MRSA were approximately five times more likely to develop MRSA infection than infants who were not colonized.4

In recent decades, the prevalence of infections caused by MRSA has increased among healthy people, especially children.1 S. aureus carried maternally was identified as a risk factor for early colonization in postnatal infants.6 Newborns acquire S. aureus, including MRSA, from adult sources because many healthy individuals can carry it as part of their normal microflora. There are few studies on the pattern of S. aureus sensitivity to antibiotics in nursing mothers and infants. The aim of this study was to determine the prevalence of nasal carriers of S. aureus in lactating mothers and their infants and their pattern of antibiotic susceptibility.

Materials and Methods

Study design and research subject
This research was a cross-sectional study involving infants who were taken in the South Tangerang City. We took samples from June 2022 to July 2023. The inclusion criteria for breastfeeding mothers are not suffering from mastitis or breast abscess infections and not taking antibiotics for the last two weeks. Inclusion criteria for infants are aged 0-6 months in good health, and not taking antibiotics for the previous two weeks. Exclusion criteria for breastfeeding mothers were experiencing severe infection and suffering from flu, and samples were not met from the mother’s nasal swab. Exclusion criteria for infants included severe infection, flu, and samples from the baby’s nasal swab were not met. Using a questionnaire, we interviewed respondents to obtain information on demographic characteristics and birth history.

Specimen collection
We took baby and mother nasal swabs using a sterile cotton swab by inserting it into the nose about 2 cm deep and then rotating it 360° for about 3 seconds. Nasal swabs are moistened with sterile phosphate buffered saline before being inserted into the nostrils. The swab was inserted into the Amies transport medium. All specimens were brought to the FMH UMJ laboratory for culture.

Isolation, identification, and antibiotic sensitivity test
All specimens were grown on mannitol Salt Agar (MSA). All media were incubated at 37°C for 24-48 hours under aerobic conditions—initial identification by observation of colonies and gram staining. S. aureus identification and sensitivity test using the VITEK®2 System (BioMérieux, Marcy-l′ Etoile, France) with GP cartridges according to the manufacturer’s instructions. The results were based on the antimicrobial susceptibility guidelines of the Clinical Laboratory Standards Institute (CLSI)—determination of MRSA based on cefoxitin antibiotic resistance. The antibiotics tested included cefoxitin, linezolid, ciprofloxacin, clindamycin, erythromycin, moxifloxacin, vancomycin, tetracycline, benzylpenicillin, levofloxacin, gentamicin, and nitrofurantoin.

Data analysis
Data was entered into Microsoft Excel and presented as tables and graphs. Chi-square test or Fisher’s exact test was used for analysis data on characteristics with S. aureus carriage in infants using the Statistical Package for the Social Sciences (version 22.0; SPSS). The determination of statistical significance used is p<0.05.

RESULTS

A total of 59 pairs of mothers and babies became the subject of this study. The babies’ ages range from 1 to 5 months, with an average of 2.6±1.39 months. Maternal age ranged from 16 to 42 years, averaging 29.76±5.97 years. In this study, 49% of infants aged less than two months and more than two months were the same at 51%. Thirty-six (61%) babies were girls, and 23 (39%) were boys. Most of the babies (91.5 %) were fully breastfed, and the rest received formula or mixed breast milk and formula. Thirty-three (56%) were delivered by cesarean section, and the remainder by vaginal delivery. A total of 54 (91.5%) babies were born normally (≥2500 grams). Twenty-two (37%) mothers had primiparity, and thirty-seven (63%) had no primiparity. Table 1 shows that all characteristics have no relationship with S. aureus carrier in infants (p<0.05).

Table (1):
Characteristics of participants and their relationship to S. aureus carriers

Characteristic Range Mean (SD) Frequency S. aureus Infant Carrier (n=59) p-value
Yes No
Mother’s Age 16-42 29.76 (5.97)
Baby’s Age (mo)a
2
> 2
1-5 2.6 (1.39) 29 (49%)
30 (51%)
13
9
16
21
0.239
Baby’s Gendera
Female
Male
36 (61%)
23 (39%)
15
7
21
16
0.384
Get fully breastfeda
Yes
No
54 (91.5%)
5 (8.5%)
19
3
35
2
0.272
Delivery Typea
Vaginal
Cesarean
26 (44%)
33 (56%)
9
13
17
20
0.706
Birthweight (gram)a
<2500
≥2500
5 (8.5%)
54 (91.5%)
3
19
2
35
0.272
Primiparitya
Yes
No
22 (37%)
37 (63%)
7
15
15
22
0.503
Total 58 (100%) 22 (37%) 37 (63%)

Overall, we found 22/59 (37%) S. aureus in the noses of the babies and 18/59 (30%) mothers. Table 2 shows that the pattern of antibiotic susceptibility showed that of the 18 maternal S. aureus isolates, 15/18 (83%) were Methicillin Sensitive Staphylococcus aureus (MSSA), and the remaining 3/18 (17%) were MRSA. The majority of S. aureus isolates from mothers are sensitive to cefoxitin (83%), gentamicin (94%), ciprofloxacin (89%), levofloxacin (89%), moxifloxacin (89%), vancomycin (100%), clindamycin (89%), erythromycin (89%), nitrofurantoin (100%), linezolid (100%) and tetracycline (83%). Most of the isolates were resistant to benzylpenicillin (78%).

Table (2):
Antibiotic Susceptibility Pattern of S. aureus Isolated from Mother’s Nasal Swab

Antibiotic Agent
Susceptible
n (%)
Intermediate
n (%)
Resistant
n (%)
Cefoxitin
15 (83)
0 (0)
3 (17)
Gentamicin
17 (94)
1 (6)
0 (0)
Benzylpenicillin
4 (22)
0 (0)
14 (78)
Ciprofloxacin
16 (89)
0 (0)
2 (11)
Levofloxacin
16 (89)
0 (0)
2 (11)
Moxifloxacin
16 (89)
0 (0)
2 (11)
Vancomycin
18 (100)
0 (0)
0 (0)
Clindamycin
16 (89)
0 (0)
2 (11)
Erythromycin
16 (89)
0 (0)
2 (11)
Nitrofurantoin
18 (100)
0 (0)
0 (0)
Linezolid
18 (100)
0 (0)
0 (0)
Tetracycline
15 (83)
0 (0)
3 (17)

The results of antibiotic susceptibility patterns showed that of the 22 infant S. aureus isolates, 18/22 (82%) were Methicillin Sensitive Staphylococcus aureus (MSSA), and the remaining 4/22 (18%) were MRSA. The majority of S. aureus isolates from infants were sensitive to cefoxitin (82%), gentamicin (86%), ciprofloxacin (91%), levofloxacin (95%), moxifloxacin (91%), vancomycin (100%), clindamycin (82%), erythromycin (86%), nitrofurantoin (100%), linezolid (100%) and tetracycline (77%). Most of the isolates were resistant to benzylpenicillin (82%) (Table 3).

Table (3):
Antibiotic Susceptibility Pattern of S. aureus Isolated from Baby’s Nasal Swab

Antibiotic Agent
Susceptible
n (%)
Intermediate
n (%)
Resistant
n (%)
Cefoxitin
18 (82)
0 (0)
4 (18)
Gentamicin
19 (86)
1 (5)
2 (9)
Benzylpenicillin
4 (18)
0 (0)
18 (82)
Ciprofloxacin
20 (91)
1 (5)
1 (5)
Levofloxacin
21 (95)
0 (0)
1 (5)
Moxifloxacin
20 (91)
0 (0)
2 (9)
Vancomycin
22 (100)
0 (0)
0 (0)
Clindamycin
18 (82)
0 (0)
4 (18)
Erythromycin
19 (86)
0 (0)
3 (14)
Nitrofurantoin
22 (100)
0 (0)
0 (0)
Linezolid
22 (100)
0 (0)
0 (0)
Tetracycline
17 (77)
0 (0)
5 (23)

Of the seven pairs of mothers and babies, four pairs of mothers and babies had the same pattern of antibiotic sensitivity (Table 4). In sample 22, there were differences in the susceptibility pattern to gentamicin and tetracyclin antibiotics, sample 32 to benzylpenicillin antibiotics, and sample 56 to the antibiotics moxifloxacin and clindamycin.

Table (4):
Antimicrobial Susceptibility Pattern of S. aureus Isolated from Mother and Baby’s Nasal Swab

Sample Number
Participant
FOX
GEN
BEN
CIP
LEV
MOX
VAN
CLIN
ERY
NIT
Lin
TET
22
Mother/ Baby
S/S
S/R
R/R
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
R/S
27
Mother/ Baby
R/R
S/S
R/R
R/R
R/R
R/R
S/S
R/R
R/R
S/S
S/S
S/S
30
Mother/ Baby
S/S
S/S
R/R
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
32
Mother/ Baby
S/S
S/S
R/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
36
Mother/ Baby
S/S
S/S
R/R
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
53
Mother/ Baby
S/S
S/S
R/R
S/S
S/S
S/S
S/S
S/S
S/S
S/S
S/S
R/R
56
Mother/ Baby
S/S
S/S
S/S
S/S
S/S
S/R
S/S
S/R
S/S
S/S
S/S
S/S

Abbreviations: Cefoxitin (FOX); Gentamicin (GEN); Benzylpenicillin (BEN); Ciprofloxacin (CIP); Levofloxacin (LEV); Moxifloxacin (MOX); Vancomycin (VAN); Clindamycin (CLIN); Erythromycin (ERY); Nitrofurantoin (NIT); Linezolid (LIN); Tetracycline (TET)

DISCUSSION

Studies estimate that at least 70-90% of the general population are intermittent carriers of S. aureus.7 About 20% of the people are persistent carriers, and about 60% of colonization occurs intermittently, with a high level of colonization in children.7,8 Only about 20-30% of the population are not carriers and have never hosted
S. aureus.7

In this study, we obtained nasal carriage of S. aureus in mothers (30%) and infants (37%). This result was lower than the Schaumburg study,9 which got 41.7%, and Accorsi EK10 got 56% S. aureus from nasal swabs in infants. In mothers, the results of this study were higher than those of Aylana et al. Getting S. aureus in healthy mothers is 19.3%. The anterior nares are the main reservoir of S. aureus and a significant risk factor for developing a patent staphylococcal infection, either community-acquired or health-care-acquired.11 When S. aureus begins to enter the host and the host’s defenses are overcome, S. aureus begins to spread and settle into the anterior nose so that the host becomes a nasal carrier of S. aureus.12

The infant’s age is in the range of 1 to 5 months. In this study, 49% of infants aged less than two months and more than two months were the same at 51%. The average carriage rate in the first eight weeks of life is around 40-50%, after which it drops to 21% at six months.11 Colonization of S. aureus generally peaks in newborns until 1-2 months of age and then declines at six months of age.13 In contrast to this study, there was more S. aureus in babies more than 2 months old. In addition, we found no difference in infant age in S. aureus carriers (p=0.412). This can be caused by environmental influences, including interference from pathogenic flora and other non-pathogenic NPs.13 Additionally, the hygiene practices of better mothers or caregivers can lead to decreased bacterial clearance. Most of the babies (62%) were female. Studies found that the female sex was a risk factor for MSSA and MRSA colonization,14 but in this study, we found no difference (p=0.587).

Most of the babies (93%) were fully breastfed, and the rest received formula or mixed breast milk and formula. This study did not show the effect of full breastfeeding on the presence of S. aureus in the infant’s nose. Most babies (55%) have been born by cesarean section, and the rest through the vaginal process. In this study, we found no difference between vaginal and cesarean delivery in the presence of S. aureus in the baby’s nasal passages (p=0.437). This result is similar to another study.12 Although vertical transmission via the vaginal route of the mother concomitantly and early infant colonization may occur, horizontal transmission in early neonatal life appears to be more common.6 Another study found vaginal delivery to be a risk factor for MSSA but not for MRSA colonization.14

In this study, most isolates were sensitive to almost all antibiotics. However, we found MRSA isolates in mothers (17%) and infants (18%). This result is similar to a study in Ethiopia in healthy children, namely 18.8%.15 However, this result is higher than Denmark at 0.11%16 and Taiwan, which found that the rate of nasal MRSA carriage was 10.2% in children aged 2-6 months, significantly associated with MRSA carriage.17 Differences in MRSA detection results may be caused by differences in diagnostic methods used to confirm/detect MRSA other than the cefoxitin disc detection method, differences in geographic distribution, study population characteristics, sampling quality, and culture techniques.

More than 50% of maternal and infant S. aureus isolates in this study were sensitive to cefoxitin (82%), gentamicin (86%), ciprofloxacin (91%), levofloxacin (95%), moxifloxacin (91%), vancomycin (100%), clindamycin (82%), erythromycin (86%), nitrofurantoin (100%), linezolid (100%) and tetracycline (77%). However, benzylpenicillin has a resistance of 83%. These results are in line with many studies on healthy people in Ethiopia (99.3%), China (87.5%), Nigeria (100%), and Ghana (95%).8,18-20 This may be observed because penicillin and ampicillin have been on the market for a long time, are cheap, and easy to obtain without a prescription (despite being prescription drugs). Therefore, penicillin may have been widely abused.

Tetracycline, clindamycin, and erythromycin are commonly prescribed antibiotics in the community. The emergence of resistance to other essential antimicrobials, such as clindamycin, has a meaningful impact on clinical outcomes and treatment choices. Clindamycin is associated with reduced relapse rates and a lower risk of treatment failure for S. aureus and other types of skin & soft tissue infections (SSTIs). Clindamycin is usually used to treat uncomplicated infections in the pediatric population. Given the increasing prevalence of clindamycin resistance in MSSA isolates from clinically significant infections, it is necessary to encourage clinicians to re-evaluate this prescribing practice. In addition, it should be a concern, especially if local data shows that clindamycin is not routinely active against S. aureus isolates.21

The high-risk population of newborns generally receives broad-spectrum antimicrobial agents as empiric therapy. The initial administration of antimicrobials by the clinician is based on initial clinical suspicion because microbiological examination evidence takes time. Identification results from culture results usually only come out 24 to 72 hours later. Vancomycin can be used as both empirical and definitive therapy because it is still susceptible to most MRSA infections. Newer agents, such as linezolid, may also be used as alternative oral regimens if available and considered cost-effective.22 This research is limited to only taking samples from one site. Therefore, we may miss MRSA colonies in the axillae, throat, perineum, and anal areas, although the anterior nose is the site of the highest colonization. In addition, this study did not identify cohort factors that influence carriers of S. aureus.

CONCLUSION

We found MRSA in mothers (17%) and their babies (18%). Although most antibiotics are still susceptible to S. aureus, some antibiotics are resistant, such as benzylpenicillin, tetracycline, clindamycin, erythromycin, oxacillin, moxifloxacin, gentamicin, ciprofloxacin, and levofloxacin. Education, ongoing surveillance, and decolonization of carriers are essential to prevent transmission in the community.

Declarations

ACKNOWLEDGMENTS
The authors would like to thank the Ministry of Education, Culture, Research, and Technology of the Republic of Indonesia, LLDIKTI Region 3, and LPPM Universitas Muhammadiyah Jakarta for their funding and facilitation. Authors are also thankful to the South Tangerang City Health Office for granting permission for the research location.

CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.

AUTHORS’ CONTRIBUTION
RS conceptualized the study. RS, AA, AS and HAM collected the data and organized the samples. RS and AA performed laboratory analysis. RS performed data analysis. RS wrote the manuscript. All authors reviewed and approved the final manuscript for publication.

FUNDING
This research was supported by a PDUPT grant with reference number 179/E5/PG.02.00/PL/2023 from the Ministry of Education, Culture, Research and Technology of the Republic of Indonesia, a derivative contract LLDIKTI Region 3, and UMJ Number: 454/LL3/AL.04/2023, Researcher UMJ Derivative Contract Number: 429/R-UMJ/VI/2023.

DATA AVAILABILITY
All datasets generated or analyzed during this study are included in the manuscript.

ETHICS STATEMENT
The study protocol involved humans was performed in accordance with the Declaration of Helsinki and approved by the Commission of Health Research Ethics, Faculty of Medicine and Health, Universitas Muhammadiyah Jakarta (No.113/PE/KE/FKK-UMJ/VI/2022).

INFORMED CONSENT
Written informed consent was obtained from the participants before enrolling in the study.

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