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Saudi Journal of Kidney Diseases and Transplantation
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ORIGINAL ARTICLE Table of Contents   
Year : 2003  |  Volume : 14  |  Issue : 1  |  Page : 30-38
The Prevalence of Nasal Carriage of Staphylococcus aureus and Associated Vascular Access-Related Septicemia Among Patients on Hemodialysis in Al-Hasa Region of Saudi Arabia


1 Division of Nephrology, King Fahad Hospital, Hofuf, Al-Hasa, Saudi Arabia
2 Division of Microbiology, King Fahad Hospital, Hofuf, Al-Hasa, Saudi Arabia

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   Abstract 

A high Staphylococcus aureus nasal carriage rate is frequently seen among patients on hemodialysis (HD) and consequently, these patients appear to be at a higher risk for endogenous S. aureus associated vascular access-related septicemia (VARS). The prevalence of nasal carriage of S. aureus and it's impact on VARS with particular reference to age, sex and type of vascular access was studied in an HD cohort to recognize the most susceptible group(s) and plan prophylactic strategies accordingly. This study involved 208 end-stage renal disease (ESRD) patients on long-term HD from July 1997 to July 2000. Five standardized swabs from the anterior nares were taken. Persistent nasal carriage was defined by two or more positive cultures. Peripheral blood samples for culture and sensitivity were collected on clinical suspicion of septicemia. An overall prevalence of nasal carriage of 38.0% was observed. Nasal carriage rates were 85.7% among 75-84 year's and 50.0% in 65-74 year's age-groups. Central venous catheters (CVCs) recorded nine folds greater collective risk of developing S. aureus nasal carriage­related VARS than non-carrier group. No significant difference in S. aureus related incidence of VARS between non-carrier and nasal carrier groups was observed among those dialyzed through arteriovenous fistula (AVF). Elderly (>65 years) nasal carriers dialyzed through Central Venous Catheters, formed a high-risk group for S. aureus nasal carriage related VARS. The optimization of AVF placement might offer a safer, non-phamacological approach to reduce the S. aureus nasal carriage-related VARS besides possibly much desirable improvent in the quality of life of our senior citizens through decline in the frequency of hospitalizations.

Keywords: Nasal carriage, Vascular access, S. aureus, Septicemia.

How to cite this article:
Saxena AK, Panhotra B R. The Prevalence of Nasal Carriage of Staphylococcus aureus and Associated Vascular Access-Related Septicemia Among Patients on Hemodialysis in Al-Hasa Region of Saudi Arabia. Saudi J Kidney Dis Transpl 2003;14:30-8

How to cite this URL:
Saxena AK, Panhotra B R. The Prevalence of Nasal Carriage of Staphylococcus aureus and Associated Vascular Access-Related Septicemia Among Patients on Hemodialysis in Al-Hasa Region of Saudi Arabia. Saudi J Kidney Dis Transpl [serial online] 2003 [cited 2020 Oct 27];14:30-8. Available from: https://www.sjkdt.org/text.asp?2003/14/1/30/33085

   Introduction Top


Infection remains one of the most frequent causes of mortality and morbidity, next only to cardiovascular disease, among hemodialysis (HD) patients. [1] The United States Renal Data Service (USRDS) data base review (1997) revealed that 15-17% of hospitalizations were vascular access-related. [2] Staphylococcus aureus Scientific Name Search  is the commonest bacteria associated with vascular access-related sepsis (VARS) in HD patients. [3] Bacterial colonization of the vascular access site, which occurs most often either due to contamination of access­lumen or, migration of bacteria from skin through the entry-site, remains the common cause of VARS among long-term HD patients. [4]

Anterior nares are the most common sites, where the S. aureus colonizes and disseminates to other parts of the body. The nasal carriage of S. aureus is an independent risk factor for the development of VARS of endogenous origin in HD patients. [5] Von Eiff et al, reported that S. aureus blood isolates from septicemic patients were clonally indistin­guishable from those obtained from nasal specimens in 82.2% patients, suggesting that the organisms in the blood stream originated from the patient's own nasal flora. [6] S. aureus moves from nasal reservoir to hands and skin, consequently infecting the vascular access sites. Thus, nasal carriage of S. aureus appears to play a key role in the development of VARS in HD patients.

The risk of VARS depends on the type of vascular access used. Arterio-venous fistula (AVF) is the preferred type of access due to the lowest infection rates when compared with polytetrafluoroethylene grafts (PTFE) grafts and central venous catheters (CVCs). [7] Yet, about 60% of new patients with end­stage renal disease (ESRD) and 30% of prevalent patients have to depend upon less desirable modes of vascular access like CVCs, due to a variety of reasons. These include: the growing elderly population on HD with co-morbid conditions such as diabetes mellitus and malignancies, who usually have poor vascular framework, late-referrals, unpredictability of clinical course of chronic reanal failure (CRF) and lack of pre-ESRD programs. [8] Patients dialyzed through CVCs, appear to be more vulnerable to frequent episodes of endogenous S. aureus related VARS and consequential admini-stration of systemic antibiotics, often started empirically. The risk factors of nasal S. aureus flora getting modified include the administration of systemic antibiotics. [9] The recurrent episodes of S. aureus related VARS are a frequent cause of repeated hospitaliza-tions, thereby increasing the cost of ESRD management and affecting the quality of life of patients on HD.

The present study aims to determine the prevalence of nasal carriage of S. aureus and it's impact on VARS in patients on HD, with particular reference to the age and sex of the patients and the type of vascular access used. Also, we make an attempt to identify the most vulnerable group(s) of HD patients to endogenous S. aureus associated VARS, in order to plan prophylactic strategies for this group.


   Patients and Methods Top


The present study was performed on 208 ESRD patients of diverse etiologies on long-term HD twice or thrice/ week at the King Fahad Hospital, Hofuf, Saudi Arabia, from July 1997 to July 2000. Dialysis was performed using polysulphone membrane dialyzers through the following vascular accesses: [a] Femoral dual lumen catheter (FC) in 16 (7.6%), [b] Subclavian dual lumen catheter (SC) in 24 (11.5%), [c] Permanent subcutaneous tunneled cuffed catheter (PC) in 31 (14.9%), [d] Polytetrafluoroethylene (PTFE) graft in 35 (16.8%) and [e] Arterio­Venous Fistula (AVF) in 102 (49%) patients.

The procedure described for optimal screening of nasal carriage of S. aureus in patients on HD was used and the followed steps were followed: three cultures at intervals of one hour each, on day one; and the fourth and fifth cultures were taken at subsequent dialysis sessions with each inter-dialysis interval being not less than 48 hours. [10] One swab moistened in sterile 0.9% sodium chloride solution was rotated in both the anterior nares and placed into modified Amines charcoal transport medium (Eurotuba, Barcelona). These swabs were processed in the laboratory within 12 hours of collecting the material. Patients who were culture positive for S. aureus on more than two occasions were labelled as persistent nasal carriers for S. aureus. The nasal swabs were cultured on blood agar and mannitol salt agar. The culture plates were incubated at 35 o C for 48 hours. S. aureus was identified on the basis of colony morphology (golden pigmentation of colonies); gram-positive cocci in clusters on microscopic examination and positive results of tube coagulase, mannitol-fermentation, deoxyribo­nuclease (DNAse) and Staphaurex latexagglu­tination tests (Murex Bio Tech, Dartford, UK).

The widely accepted clinical criteria of Raad and Bodey was used for diagnosis of septicemia which is based on the presence of backache, fever, chills and rigors, unexplained nausea, vomiting, hypotension, mental changes and leukocytosis. [11] Peripheral blood culture samples were collected from the patients in blood culture bottles (Becton and Dickinson, USA) and were processed in Bectec 9240, blood culture analyzer. The catheter tips and insertion site swabs were cultured on MacConky , s and blood agar media and bacteria were identified by conventional microbiological method and API technique (API-System, La Balmes-Ies Grottes, France).

After the clinical diagnosis of septicemia was established and complete sepsis work-up was performed, patients with clinical VARS were started on empirical intravenous antibiotics, administered post-HD. Antibiotics were continued for five successive dialysis sessions in patients having VARS related to temporary vascular accesses (FC and SC) and for seven successive dialysis sessions in those with VARS and permanent vascular accesses (PC, PTFE and AVF). [12] Therapy was modified appropriately, once these culture and sensitivity reports were available. Patients with persistent hypotension and mental changes were hospitalized. Peripheral blood cultures were repeated on the 45 th day after completion of antibiotic therapy. A cure was defined as a 45-days symptom-free interval after antibiotic therapy was completed. Any bacteremia involving the original organism, that occurred within 45 days of treatment, was considered as treatment failure. [13]


   Statistical Analysis Top


The statistical analysis was performed using Web X 2 Calculator, Georgetown University, Washington DC, USA. Statistical significance was set at the 0.05 level.


   Results Top


The present study involved 208 patients on long-term HD. Overall, 125 clinically suspected and bacteriologically proven S. aureus associated episodes of VARS were recorded in the three years of study period (7488 patient-months), yielding 1.66 episodes/100 patient-months. Of the study patients, 79 (38.0%) were nasal carriers and had 93 S. aureus associated VARS episodes in 2,844 patient-months (1.24 episodes/100 patient-months). The other 129 (62.0%) patients were non-carriers and had 32 VARS episodes during 4,644 patient-months (0.42 episodes/100 patient-months) [Relative Risk (RR) = 3.98, p<0.0001].

The mean age of the HD population in this study was 47.5 years (range 15-84 years). The lowest prevalence of nasal carriage was observed in the 15-24 years age-group [assigned RR of one]. In this group, only one VARS episode occurred in eight patients giving a prevalence rate of 12.8%, (0.34 episodes/100 patient-months). In the 75-84 years age-group, the highest prevalence of nasal carriage of 85.7% (12/14) was observed with VARS incidence of 2.97 episodes/100 patient-months. This group had a 7.5 fold higher risk of developing S. aureus associated VARS than the 15-24 years age-group [RR=7.50, p<0.001]. The 65-74 years age­group recorded a prevalence of 50.0% (26/52) with VARS incidence of 1.70 episodes/100 patient-months, representing nearly five folds higher risk of developing S. aureus associated VARS than the 15-24 years age­group [RR=4.92, p<0.02] [Figure - 1], [Table - 1].

Of the 208 patients studied, 113 (54.3%) were females and 95 (45.7%) were males. Among females, 32% (36/113) were nasal carriers of S. aureus recording 1.10 episodes/100 patient-months. The remaining 68% (77/113) who were non-carriers, recorded just 0.29 episodes/100 patient­months. Thus, carrier females recorded six folds greater incidence of S. aureus associated VARS than non-carrier females on HD [RR = 6.34, p<0.0001]. Among males, 45% (43/95) were nasal carriers documenting 1.40 episodes/100 patient­months and 55% (52/95) were non-carriers with an average of 0.58 episodes/100 patient­months. Thus, nasal carrier males carried a 2.5 fold higher risk of developing S. aureus associated VARS than non-carrier males on HD [RR=2.57, p<0.0001] [Figure - 2], [Table - 2].

Among various types of vascular accesses used, patients being dialyzed through FC, recorded the highest incidence of VARS; 0.342 and 1.198 episodes/1000 catheter­days among non-carrier and nasal carrier groups respectively, with nasal carriers being at 3.5 folds [RR-3.502, p<0.0001] higher risk of developing S. aureus associated VARS than non-carriers. In the SC group, VARS incidence of 0.342 and 0.913 episodes/1000 catheter-days was observed among non-carriers and nasal carriers respectively [RR-2.939, p<0.0001]. The PC group had 0.176 and 0.736 episodes/1000 catheter-days among non­carriers and nasal carriers respectively [RR = 4.167, p<0.0001].

In the PTFE group, 0.057 and 0.142 episodes/patient-years were observed among non-carriers and nasal carriers respectively [RR = 2.50, p<0.019]. The lowest and comparable incidence of S. aureus associated VARS of 0.019 and 0.026 episodes/patient­ years among non-carriers and nasal carriers respectively was observed in the AVF group. Thus, patients dialyzed through AVF carried a trivial, statistically insignificant risk [RR=1.333, p-NS] of developing S. aureus associated VARS even if they carried S. aureus in their nostrils [Figure - 3], [Table - 3].


   Discussion Top


The overall prevalence of persistent nasal carriage of S. aureus observed in our study was 38.0% (79/208). A relatively lower prevalence of 25.4% among hospital personnel in Saudi Arabia has been reported. [14] However, the prevalence rate in our study is lower than the 44.0 to 84.0% reported in other studies. [15],[16],[17]

Persistent nasal carriage and ensuing risk of developing S. aureus linked VARS in HD patients is well recognized. [5] Our study showed a four-fold greater risk of developing S. aureus related VARS [RR-3.98, p< 0.0001] in the nasal carrier group over the non-carrier group (1.24 vs 0.42 episodes/100 patient-months) on HD. These results are in concordance with other studies reporting relative risk of 4.0 to 4.7. [16],[17]

The highest prevalence of nasal carriage (85.7%) and 7.5 times greater risk of developing S. aureus related VARS was observed in the very elderly (75-84 years age-group). The age-group (65-74 years) had 50.0% nasal carriage rate and five­times higher risk of developing S. aureus related VARS. Thus, patients > 65 years age had a significantly higher prevalence of nasal carriage of S. aureus and carried an approximately 12.5 times greater combined risk of developing S. aureus related VARS than the youngest age-group. It has been reported in several studies that hospitalization for six months or longer is a key risk factor for elevated nasal carriage in the elderly (>65 years) and carries an unfavorable outcome. [18],[19] Nonetheless, immunocompro­mise due to advanced age, malnutrition, CRF and co-morbid conditions such as diabetes mellitus and malignancies together with repeated punctures and cannulations for vascular access and HD itself, are additional key risk factors. [5] Male patients had a higher prevalence of S. aureus nasal carriage than females on HD (45.0% vs 32.0%). Also, male nasal carriers had 40% greater risk (RR-1.40) of developing S. aureus associated VARS. The overall risk factors significantly associated with S. aureus nasal colonization include male gender, elderly, hospitalization, and antibiotic therapy during the previous three months. [19],[20]

Patients dialyzed through CVCs had the highest incidence of S. aureus related VARS, both among and nasal carrier and non-carrier groups when compared to those dialyzed through PTFE or AVF. Thus, the risk of developing S. aureus related VARS is dependent on the type of vascular access used for perfoming HD. However, patients in nasal carriers' group dialyzed through CVCs had significantly higher incidence of S. aureus related VARS than those in the non-carrier group. Collectively, patients of nasal carriage group on HD through CVCs carried nearly nine times higher risk of developing S. aureus associated VARS than those of non-carrier group. Patients with functioning AVF had no statistically significant difference in the risk of developing S. aureus related VARS (RR­1.33%) between nasal carrier and non­carrier groups. Comparable findings have been reported in other studies with incidence of VARS ranging from 0.5 to 13 episodes/1000 catheter days. Additionally, a 7.64 fold higher relative risk of VARS in CVC group has been reported in comparison with those having functioning AVF. [21],[22]

The present study evidently specifies that elderly male ESRD patients with S. aureus nasal carriage, who constituted about one third of the HD cohort, carried exceedingly high risk of developing recurrent episodes of S. aureus related VARS when dialyzed through CVCs. Elderly people are less likely to have native AVFs and only 23% of this age-group in the United States were dialyzed through AVF in 1997. [23] Also, 46% of elderly patients on HD have at least two co-morbid factors and consequently, they spend 20% of their remaining life-time in the hospital. The most significant cause of death reported among the elderly was cardiovascular diseases (24%) followed by infections (22%) with 5-year survival rate of only 2.4% for the very elderly. [24] The patients who experience an episode of VARS have twice the risk of death from any cause and eight fold higher risk of death from VARS. [25] Recently, the type of vascular access has also been linked to mortality as CVCs and PTFE grafts have appreciably higher incidence of VARS as well as mortality, the latter caused by sepsis as well as due to cardiovascular causes. [26]

The efforts for long-term nasal decoloni­zation in elderly HD patients through oral administration of rifampicin or mupirocin nasal applications had been associated with development of side-effects, emergence of low or high level drug-resistance as well as recolonization once the drug is stopped. [27],[28]

In addition, these decolonizing agents do not have standardized schedules for application and their optimal duration of use is also not known, rendering them a relatively insecure option for the elderly.

Instead, using the AVF as the access of choice is convincingly safer and is the non­pharmacological approach of choice to reduce the incidence of VARS. Promoting the use of AVF in at least 50% of the HD popualtion, is recommended by the National Kidney Foundation-Dialysis Outcomes and Quality Initiative (NKF-DOQI) working panel, and has been reported to significantly reduce the over all mortality due to S. aureus associated VARS in HD patients, including diabetic ESRD patients. [7],[29],[30] Hence, optimization of AVF placement should be preferred and promoted to minimize the risk of S. aureus nasal carriage-related VARS, reduce the cost of hospitalization and possibly achieve much desirable improvement in quality of life of elderly HD patients.

 
   References Top

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2.US Renal Data System: US Renal Data System - annual report. 1999;Chapter IX:131-43.  Back to cited text no. 2    
3.Nielsen J, Ladefoged SD, Kolmos HJ. Dialysis catheter-related septicemia: focus on Staphylococcus aureus septicemia. Nephrol Dial Transplant 1998;13:2847-52.  Back to cited text no. 3  [PUBMED]  [FULLTEXT]
4.Kirkland KB, Saxton DF. Diaysis access infection, In: Conlon PJ, Nicholson MI, Schwab S. Hemodialysis vascular access practice and problems,Oxford, New York: Oxford University Press 2000, p-85-100.  Back to cited text no. 4    
5.Berman DS, Schaefler S, Simberkoff MS. Staphylococcus aureus colonization in intra­venous drug abusers, dialysis patients and diabetics. J Infect Dis 1987;155:829-31.  Back to cited text no. 5    
6.Von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. N Engl J Med 2001;344:11-6.  Back to cited text no. 6  [PUBMED]  [FULLTEXT]
7.NKF-DOQI Clinical Practice Guidelines for vascular access, National Kidney Foun­dation, New York, New York. Guideline 1997;3:22-3.  Back to cited text no. 7    
8.Tanriover B, Carlton D, Saddenkni S. Bacteremia associated with tunneled dialysis catheters: comparison of two treat­ment strategies. Kidney Int 1999; 55:1081-90.  Back to cited text no. 8    
9.Aly R, Maibach HI, Strauss WG, Shinefield HR. Effects of a systemic anti-biotic on nasal bacterial ecology in man. Appl Microbiol 1970;20:240-4.  Back to cited text no. 9  [PUBMED]  [FULLTEXT]
10.Geert JA, Peter MS, Annielies B, Egidia VG, Marrianne IK. Optimizing screening procedures for Staphylococcus aureus nasal carriage in patients on haemodialysis. Nephrol Dial Transplant 1998;13:1256-8.  Back to cited text no. 10    
11.Raad II, Baba M, Bodey GP. Diagnosis of catheter-related infections: the role of surveillance and targeted quantitative skin cultures. Clin Infect Dis 1995;20:593-7.  Back to cited text no. 11  [PUBMED]  
12.Raad II, Sabbagh MF. Optimal duration of therapy for catheter-related Staphylococcus aureus bacteremia: a study of 55 cases and review. Clin Infect Dis 1992; 14:1259-60.  Back to cited text no. 12    
13.Saxena AK, Panhotra BR, Naguib MB, et al. Vascular access related septicemia in hemodialysis: a focus on bacterial flora and antibiotic access salvage. Saudi J Kidney Dis Transplant 2002;13:29-34.  Back to cited text no. 13    
14.Alghaithy AA, Bilal NE, Gedebou M, Weily AH. Nasal carriage and antibiotic resistance of Staphylococcus aureus isolates from hospital and non-hospital personnel in Abha, Saudi Arabia. Trans R Soc Trop Med Hyg 2000;94:504-7.  Back to cited text no. 14    
15.Goldblum SE, Reed WP, Ulrich JA, Goldman RS. Staphylococcus aureus nasal carriage and infections in haemodialysis patients. Dial Transplant 1978;7:1140-63.  Back to cited text no. 15    
16.Yu VL, Goetz A, Wagener M, et al. Staphylococcus aureus nasal carriage and infections in patients on hemodialysis. Effi­cacy of antibiotic prophylaxis. N Engl J Med 1986;315:91-6.  Back to cited text no. 16    
17.Kaplowitz LG, Comstock JA, Landwehr DM, Dalton HP, Mayhall CG. Prospective study of microbial colonization of the nose and skin and infection of the vascular access site in hemodialysis patients. J Clin Micro­biol 1988;26:1257-62.  Back to cited text no. 17    
18.Parnaby RM, O'Dwyer G. Carriage of Staphylococcus aureus in the elderly. J Hosp Infect 1996;33:20-6.  Back to cited text no. 18    
19.O'Sullivan NR, Keane CT. The prevalence of methicillin resistant Staphylococcus aureus among the residents of six nursing homes for the elderly. J Hosp Infect 2000; 45:322-9.  Back to cited text no. 19  [PUBMED]  [FULLTEXT]
20.Morgan M, Salmon R, Keppie N, Evans­Williams D, Hosein I, Looker DN. All Wales surveillance of methicillin-resistant Staphy­lococcus aureus (MRSA): the first year's results. J Hosp Infect 1999;41:173-9.  Back to cited text no. 20  [PUBMED]  
21.Hoen B, Paul-Dauphin A, Hestin D, Kessler M. EPIBACDIAL: a multicenter prospe­ctive study of risk factors for bacte-remia in chronic hemodialysis patients. J Am Soc Nephrol 1998;9:869-76.  Back to cited text no. 21  [PUBMED]  
22.Sehgal AR, Silver MR, Covinsky KE, Coffin R, Cain JA. Use of standardized ratios to examine variability in hemo­dialysis vascular access across facilities. Am J Kidney Dis 2000;35:275-81.  Back to cited text no. 22  [PUBMED]  
23.Besarab A, Adams M, Amatucci S, et al. Unraveling the realities of vascular access: the network 11 experience. Adv Ren Replace Ther 2000;7:S65-70.  Back to cited text no. 23  [PUBMED]  
24.Munshi SK, Vijayakumar N, Taub Na, Bhullar H, LoTC, Warwick G. Outcome of renal replacement therapy in the very elderly. Nephrol Dial Transplant 2001; 16:128-33.  Back to cited text no. 24    
25.Jaar BG, Herman JA, Furth SL, Briggs W, Powe NR. Septicemia in diabetic hemo­dialysis patients : Comparison of incidence, risk factors and mortality with nondiabetic hemodialysis patients. Am J Kidney Dis 2000;35:282-92.  Back to cited text no. 25    
26.Dhingra RK, Young EW, Hulbert-Shearon TE, Leavey SF, Port FK. Type of vascular access and mortality in US hemodialysis patients. Kidney Int 2001;60:1443-51.  Back to cited text no. 26  [PUBMED]  [FULLTEXT]
27.Eltringham I. Mupirocin resistance and methicillin-resistant Staphylococcus aureus (MRSA). J Hosp Infect 1997;35:1-8.  Back to cited text no. 27  [PUBMED]  
28.Watanabe H, Masaki H, Asoh N, et al. Emergence and spread of low-level mupirocin resistance in methicillin-resistant Staphylococcus aureus isolated from a community hospital in Japan. J Hosp Infect 2001; 47:294-300.  Back to cited text no. 28  [PUBMED]  [FULLTEXT]
29.Saxena AK, Panhotra BR, Naguib M, et al. The impact of achieving goal for AV fistula set by NKF-DOQI, on Staphylococcus aureus septicemia. Dial Transplant 2002;31:16-23.  Back to cited text no. 29    
30.Saxena AK, Panhotra BR, Naguib M, et al. Outcome of dialysis access-related septicemia among diabetics following optimized AV fistula placement. Kidney Blood Press Res 2002;25:109-14.  Back to cited text no. 30  [PUBMED]  [FULLTEXT]

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Correspondence Address:
Anil K Saxena
Nephrology Division, King Fahad Hospital, Hofuf, Al-Hasa-31982
Saudi Arabia
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