Staphylococcus aureus Nasal Carriage and Blood Stream Infection among Conventional Hemodialysis Patients in Thailand: a Prospective Multicenter Cohort Study

doi:10.21203/rs.3.rs-1727557/v1

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Staphylococcus aureus Nasal Carriage and Blood Stream Infection among Conventional Hemodialysis Patients in Thailand: a Prospective Multicenter Cohort Study

https://doi.org/10.21203/rs.3.rs-1727557/v1

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Objective: Staphylococcus aureus nasal carriage screening among hemodialysis patients is not a standard practice in Thailand, because of lacking data in prevalence and the correlation with subsequent infection. We aimed to investigate the prevalence of S. aureus nasal carriage and its association with blood stream infection among hemodialysis patients. In this prospective multicenter cohort study, each participant was screened for S. aureus nasal carriage once weekly for two consecutive weeks. Incidence of S. aureus bloodstream infection within 12 months after the last sample collection was observed.

Results: The prevalence of S. aureus nasal carriage was 11.67%. Incidence of S. aureus bacteremia among participants presenting S. aureus nasal carriage and non-carriers were 7.1 % and 3.8%, respectively. The odds ratio for nasal carriage to develop bacteremia was 1.96 (95% CI 0.04-21.79; p=0.553). Survival analysis showed that time to bacteremia among participants with and without nasal carriage did not significantly differ (p =0.531). Prevalence of S. aureus nasal carriage among hemodialysis patients in Thailand was low. Patients presenting S. aureus nasal carriage did not have increased risk of S. aureus bacteremia after 12-month follow-up. Nasal S. aureus screening and decolonization should not be encouraged in this setting.

end-stage chronic kidney disease

hemodialysis

S. aureus nasal carriage

S. aureus bloodstream infection

The most common infection among hemodialysis patients is blood stream infection, with Staphylococcus aureus as the main causative pathogen[1]. S. aureus can colonize in humans, with anterior nares as the most common site of colonization. S. aureus nasal carriage is recognized as an important risk factor for S. aureus blood stream infection [2].

An observational study reported a high rate of S. aureus nasal carriage among hemodialysis patients (40%), compared with normal populations (27%) [3]. An artificial nasal colonization study found that average duration of S. aureus colonization was 4 days in the non-carriage group, and 14 days in the intermittent S. aureus nasal carriage group. However, among patients with persistent S. aureus nasal carriage, the duration of colonization could persist up to 157 days [4].

Screening of S. aureus nasal carriage among hemodialysis patients and decolonization using mupirocin ointments exhibited 87% reduced S. aureus infection and 82% reduced S. aureus bacteremia [5]. Therefore, screening of S. aureus nasal carriage among hemodialysis patients is routinely practiced in several countries [6, 7].

In Thailand, the epidemiology of pathogens differs from western countries in the lack of community-acquired methicillin resistant S. aureus (CA-MRSA) [8]. Moreover, no data is available regarding the prevalence of S. aureus nasal carriage and its association with invasive diseases. Thus, S. aureus nasal carriage screening is not a standard practice in Thailand. We aimed to investigate the prevalence of S. aureus nasal carriage and its association with S. aureus blood stream infection among hemodialysis patients.

Study Setting and Design

We conducted a prospective multicenter cohort study. The target population was patients with end-stage renal disease (ESRD) who received hemodialysis at Phramongkutklao Hospital and Ananda Mahidol Hospital hemodialysis centers from July 2020 to September 2020. According to the related reported prevalence of S. aureus nasal carriage among ESRD patient at 40%[3], the estimated sample size of 145 participants was needed to ensure 80% power to demonstrate the correlation between S. aureus nasal carriage and S. aureus bacteremia, with a two-sided alpha level of 0.05. The inclusion criteria included age over 18 years, diagnosis of ESRD, receiving conventional hemodialysis, and regular follow up at two study hospitals. We excluded patients with acute hemodialysis conditions.

Nose Swab And Bacterial Isolate

All patients completed questionnaires regarding their sociodemographic data and medical history. Swabs were obtained from the nasal mucosa at anterior nares once weekly for two consecutive weeks in each participant, by two trained and validated investigators. On each occasion, the cotton tip was inserted at 1 cm in one nostril, rotated four times with slight pressure against the nasal septum and transported with Amies transport medium. Each specimen was gently rolled and streaked on 5% sheep blood agar (BA). Then, the BA plates were incubated at 37°C up to 24 h. Identification of S. aureus was carried out following standard microbiologic methods recommended by Clinical and Laboratory Standards Institute (CLSI) guidelines [9]. Positive swab was defined as colony forming unit (CFUs) of > 10³. S. aureus isolates were inoculated in Mueller Hinton Agar and methicillin susceptibility was identified by disc diffusion method using 30 µg cefoxitin disc. The zone diameter of ≥ 25 mm was classified as susceptible whereas the zone diameter of ≤ 24 mm was classified as resistant, according to CLSI guidelines [9].

S. aureus Nasal Carriage and S. aureus Bacteremia

S. aureus nasal carriage was classified in three groups: no nasal carriage, intermittent nasal carriage, and persistent nasal carriage. Intermittent nasal carriage was defined as positive nasal swab in only one of the two specimens, while persistent nasal carriage was defined as positive nasal swab in both specimens [10, 11]. All participants were followed up until 12 months after the last nasal swab collection for their status of S. aureus bacteremia, defined as at least one isolation from blood culture. Participants lost to follow up were excluded from the analysis but were interviewed by phone for the admission with signs or symptoms compatible with bacteremia. Participants and primary doctors were not informed of the carrier status and all participants presenting S. aureus nasal carriage did not receive any decolonization intervention.

Statistical Analysis

Baseline characteristics were analyzed using descriptive statistics. Categorical data were presented as percentages while mean and standard deviation (SD) were used for continuous data. For categorical variables, Fisher’s exact test or the Chi-square test was used, while Mann–Whitney test or Student’s T-test was used to compare continuous variables. The relationship between S. aureus nasal carriage and S. aureus blood stream infection was analyzed using odds ratios and was presented with a 95% confidence interval. We used Kaplan–Meier method to estimate the cumulative bacteremia and stratified log-rank statistic to assess the risk of nasal carriage compared with non-nasal carriage. For all analyses, a two-sided p-value of 0.05 was considered significant. All statistical analyses were performed using Stata 12.0 Software (StataCorp, USA).

From July 2020 to September 2020, 141 hemodialysis patients at the two hemodialysis centers were enrolled. Nine participants declined to participate in the study and 12 participants were excluded owing to the changes in hemodialysis center during this period. These participants were all non-carriers. They did not report admission with signs or symptoms compatible with bacteremia upon phone interview. Hence, we recruited 120 participants (FigureS1).

Patient Characteristics

Of 120 participants, the average age was 54.9 ± 16.07 years. A half of participants were female. The two most common routes of hemodialysis were arteriovenous fistula, and tunneled hemodialysis catheter, respectively. Common underlying diseases were hypertension, dyslipidemia, and diabetes, respectively. Female sex and dyslipidemia were significantly more common in the carrier group (OR 4.11; 95%CI:1.08–15.56, p = 0.027, and OR 4.60; 95%CI: 1.21–17.45, p = .008 respectively). Baseline characteristics are described in Table 1.

Table 1

Baseline characteristics of hemodialysis patients presenting *S. aureus* nasal carrier and non-carrier.
Characteristic	Carrier (n = 14)	Noncarrier (n = 106)	Total (n = 120)	p-value
	n (%) \| Mean ± SD	n (%) \| Mean ± SD	n (%) \| Mean ± SD
Age	55.14 ± 17.15	54.89 ± 16.10	54.9 ± 16.07	0.959
Female	11(78.57%	50(47.17%)	61(50.83%)	0.027
BMI	22.01 ± 6.12	23 ± 4.32	21.4 ± 4.57	0.566
Route of hemodialysis
Double lumen catheter	1(7.14%)	5(4.72%)	6(5%)	0.696
Tunneled hemodialysis catheter	5(35.71%)	35(33.02%)	38(31.67%)	0.841
AVF	6(42.86%)	57(53.77%)	63(52.5%)	0.442
AVG	2(14.29%)	9(8.49%)	11(9.17%)	0.480
Prior Antibiotic	9(32.14%)	20(21.74%)	29 (24.17%)	0.260
Immunosuppressive use	1(7.14%)	8(7.54%)	9(7.5%)	0.957
Underlying disease
Hypertension	12(85.71%)	98(92.45%)	110(91.67%)	0.391
Diabetic	4(28.57%)	29(27.36%)	33(27.5%)	0.924
Dyslipidemia	11(78.57%)	47(44.34%)	58(48.33%)	0.008
SLE	1(7.14%)	3(2.83%)	4(3.33%)	0.398
Skin disease	1(7.14%)	5(4.72%)	6(5%)	0.696
Malignancy	1(3.57%)	2(2.17%)	3(2.5%)	0.678
Renal cell cancer	1(7.14%)	0	1(0.83%)	1
Prostatic cancer	0	2(1.89%)	2(1.67%)	1
Abbreviation; AVF: Arteriovenous fistula, AVG: Arteriovenous Graf, SLE: Systemic lupus erythematous

The prevalence of S. aureus nasal carriage was 11.67% (14 /120), with ten cases classified as intermittent and four cases classified as persistent nasal carriage. The prevalence of S. aureus nasal carriage in hemodialysis patients of Phramongkutklao and Ananda Mahidol Hospital was 10.71% and 11.96%, respectively (p = 0.858). All S. aureus isolates were susceptible to methicillin (methicillin-susceptible S. aureus; MSSA).

S. aureus bacteremia occurred in five participants after 12-month follow-up (incidence = 4.17%). Among participants presenting S. aureus nasal carriage, one participant in the intermittent nasal carriage group had S. aureus bacteremia (incidence = 7.1%; 1/14), while 4 participants in the non-nasal carriage group had S. aureus bacteremia (3.8%; 4/106). Participants with nasal carriage were not more likely to develop bacteremia than participants presenting non nasal carriage at 12 months (OR 1.96; p = 0.553).

Clinical characteristics of participants presenting bacteremia are described in Table 2. All S. aureus isolated in blood culture were MSSA.

Table 2

Clinical characteristics of *S. aureus* bacteremia participants
No.	Age/Sex	Vascular access	Nasal carriage status	Hemoculture (Bacteremia)	Clinical syndrome	Treatment/Outcome
1	35/Female	DLC IJV	Intermittent	MSSA	CRBSI	IV Cloxacillin, removed catheter/ Cured
2	60/Male	Tunneled hemodialysis catheter	None	MSSA	CRBSI	IV Cloxacillin, removed catheter/ Cured
3	59/Male	Tunneled hemodialysis catheter	None	MSSA	CRBSI	IV Cloxacillin, removed catheter/ Cured
4	74/Female	Tunneled hemodialysis catheter	None	MSSA	CRBSI	IV Cefazolin, removed catheter / Cured
5	67/Male	AVG	None	MSSA	Infected AVG	IV Cefazolin, debridement/ Cured
Abbreviation; AVF: Arteriovenous fistula, AVG: Arteriovenous graf, DLC: Double lumen catheter, IJV: Internal jugular vein, MSSA; Methicillin-susceptible Staphylococcus aureus, CRBSI: Catheter related blood stream infection.

Among participants presenting bacteremia, nasal carriage patients developed bacteremia in 41 days while non nasal carriage patients developed bacteremia at 89, 89, 111 and 153 days, respectively. Cumulative bacteremia did not significantly differ between the two groups (p = 0.531) (Fig. 1).

In this prospective multicenter cohort study among hemodialysis patients, the prevalence of S. aureus nasal carriage was 11.7%. This number was lower than reported in other studies. For example, a related systematic review and meta-analysis among 2,374 participants revealed the prevalence of S. aureus nasal carriage at 26% [5]. Another report also found a 40% prevalence of S. aureus nasal carriage among hemodialysis patients.[3] Several factors may have influenced this effect. Firstly, the prevalence of S. aureus nasal carriage in the general population in Thailand is low. Related studies in Thailand reported prevalence of S. aureus nasal carriage at 20, 13.9, and 3.6% among patients with allergic rhinitis, patients undergoing elective cardiac surgery, and pre-admission screening, respectively [12–14]. These proportions are fewer than the reported prevalence in the US and Germany at 22% and 40%, respectively [4, 15]. Although prevalence of nasal carriage among hemodialysis patients are usually higher than general population [3], the prevalence in our cohort resembled general Thai population. This also correlated with the lower emergence and spreading of S. aureus in local hospitals and the lower colonization rate among health care personnel. [11, 15–18]. Secondly, in this present study, most participants had permanent vascular access. This was associated with a lower risk of S. aureus nasal carriage compared with temporary dialysis access [19]. Finally, the prevalence of S. aureus nasal carriage may depend on several factors particularly, ethnicity, previous antibiotic use, socioeconomic status, and geographic differences between countries, as well as personal hygiene [19, 20].

The present study revealed factors associated with carrier groups were female and dyslipidemia. Association between sex and S. aureus nasal carriage status remains controversial. [21, 22] Woman with low levels of circulating testosterone may have increased probability of S. aureus persistent carriage [23]. The nasal colonization of S. aureus among patient undergoing hemodialysis depends on host underlying condition especially skin disease and diabetic mellitus. Nevertheless, dyslipidemia has not been established as a risk factor in related studies [24]. However, the association that we found in this present study did not represent the true relationship, because other confounding variables were not explored or minimized. Well-designed studies are warranted to resolve this situation.

This study did not find any association between S. aureus nasal carriage and bacteremia. This may be explained by the unexpectedly low prevalence of S. aureus nasal carriage, compared with the prevalence at 40 to 65% reported in several studies which found associations between S. aureus nasal carriage and bacteremia [3, 10, 25]. However, the rate of invasive infection within 6 to 20 months of nasal carriage was 19% [26], much higher than the 4.17% found in this study. Therefore, another possible explanation is the difference in the virulence of S. aureus between the studies. Although this study was conducted in tertiary hospital hemodialysis centers, we could not find MRSA. This conforms with the related data in Thailand which indicated an extremely low rate of MRSA nasal colonization either among patients or healthcare personnel [13, 14, 17]. The molecular basis of S. aureus in each strain plays a major role in the ability of colonization and developing invasive diseases [2]. Molecular characterization of the isolated S. aureus nasal carriage strain should be further investigated.

To our knowledge, this study constitutes the first report of the prevalence of S. aureus nasal carriers and the relationship between nasal S. aureus carriers and S. aureus blood stream infection among hemodialysis patients in Thailand. Because of the low prevalence of S. aureus colonization and low proportion of hemodialysis patients with colonization to develop subsequent infection, implementing nasal S. aureus screening and decolonization might not be a beneficial strategy.

strategy.

Prevalence of S. aureus nasal carriage among hemodialysis patients at two Thai tertiary hospitals was 11.67%. Patients who had S. aureus nasal carriage did not have increased risk of S. aureus bacteremia after 12-month follow-up. Among the center which has a low prevalence of S. aureus nasal carriage, nasal S. aureus screening and decolonization should not be encouraged.

First, some participants were lost to follow up, which might have influenced the study result. However, this subset of patients were all non-carriers and did not report admission with signs or symptoms compatible with bacteremia. Therefore, the true incidence of bacteremia of non-carrier group, but not in carrier group, might be underreported. Second, the molecular characteristics of the S. aureus isolates were not identified. Therefore, we could not confirm the linkage between colonization and bacteremia. Nevertheless, only one patient was found in this group. Finally, the adherence to basic infection prevention strategies among hemodialysis centers was not monitored. Therefore, we could not ensure that the lower rate of S. aureus nasal colonization and infection was due to good adherence to basic infection control. However, no difference was found in colonization between the two study sites.

AVF; Arteriovenous fistula, AVG; Arteriovenous Graft, DLC; Double lumen catheter, CKD; Chronic kidney disease, RRT; Renal replacement therapy, S. aureus; Staphylococcus aureus, ESRD; End stage renal disease, CA; Cancer, RCC; Renal cell carcinoma, HT; Hypertension, DLP; Dyslipidemia, SLE; Systemic lupus erythematous, MRSA; Methicillin-resistant Staphylococcus aureus, MSSA; Methicillin-susceptible Staphylococcus aureus

CRBSI: Catheter related blood stream infection,

Ethics Approval and Consent to Participate

The study was reviewed and approved by the Institutional Review Board, Royal Thai Army Medical Department in compliance with the Declaration of Helsinki, the Belmont Report, CIOMS Guidelines and the International Conference on Harmonization of Technical Requirements for Registration of Pharmaceuticals for Human Use—Good Clinical Practice (ICH-GCP), approval number R071h/63. Informed consent was obtained in written from all participants in the study.

Consent for publication

Not applicable

Availability of data and materials

Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

Competing interests

The authors declare they have no potential conflict of interest relevant to this article

Funding

This study was supported by the Department of Internal Medicine, Phramongkutklao Hospital and Phramongkutklao Hospital Foundation. The funder provided budget in the patient data collection process and all research equipment expenses, e.g., laboratory equipment and office supplies.

Author Contributions

Conceptualization, T.T., W.N., N.V., N.R. and V.V.; methodology, T.T., W.N. and V.V.; software, T.T., W.N. and V.V.; validation, T.T., W.N. and V.V.; formal analysis, T.T., W.N. and V.V.; investigation, T.T., W.N., N.V., N.R. and V.V.; resources, T.T., W.N., N.V., N.R. and V.V.; data curation, T.T., W.N., N.V., N.R. and V.V.; writing—original draft preparation, T.T., W.N. and V.V.; writing—review and editing, T.T., W.N., N.V., N.R. and V.V. visualization, T.T., W.N. and V.V.; supervision, W.N., and V.V.; project administration, W.N. ; funding acquisition, W.N., and T.T. All authors have read and agreed to the published version of the manuscript.

Acknowledgements

The results of this study were presented in part at 32^nd European Congress of Clinical Microbiology & Infectious Diseases, April 23-26, 2022, in Lisbon, Portugal.

We thank Division of Clinical Microbiology, Department of Clinical Pathology, Phramongkutklao Hospital and Ananda Mahidol Hospital for bacterial isolation and standard antimicrobial susceptibility test.

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Staphylococcus aureus Nasal Carriage and Blood Stream Infection among Conventional Hemodialysis Patients in Thailand: a Prospective Multicenter Cohort Study

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Abstract

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Introduction

Material And Methods

Study Setting and Design

Nose Swab And Bacterial Isolate

S. aureus Nasal Carriage and S. aureus Bacteremia

Statistical Analysis

Result

Patient Characteristics

Discussion

Conclusion

Limitations

Abbreviations

Declarations

References

Supplementary Files

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