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Tunneled-Cuffed Catheter Associated Infections in Hemodialysis Patients Who Are Seropositive for the Human Immunodeficiency Virus

MICHELE H. MOKRZYCKI^*,,, BERND SCHRÖPPEL^*,, GERO VON GERSDORFF^*,, HEATHER RUSH^*,, MIROSLAW P. ZDUNEK^*, and ROBERT FEINGOLD^*,

^* Division of Nephrology, Albert Einstein College of Medicine, Bronx, New York.
Departments of Medicine, Jacobi Medical Center, Bronx, New York.
Montefiore Medical Center, Bronx, New York.

Correspondence to Dr. Michele H. Mokrzycki, Associate Professor of Clinical Medicine, 3332 Rochambeau Avenue, Centennial 423, Montefiore Medical Center, Bronx, NY 10467. Phone: 718-920-5442; Fax: 718-652-8384; E-mail: mokrzm{at}aol.com

	Abstract

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Abstract. Infection rates in tunneled-cuffed catheters (TCC) are reported to be higher in immunocompromised patients. The purpose of this study was to evaluate TCC-associated infection rates in patients with HIV infection (HIV+). Data were collected in 40 HIV + patients and 41 controls (C), and in 118 TCC (HIV+, 58; C, 60) for 28,146 catheter days (HIV+, 16,227; C, 11,919). There were no significant differences in the TCC bacteremia rates (HIV+, 2.23 versus C, 2.53 per 1000 TCC days, P = NS) or in the TCC exit site infection rates (HIV+, 2.20 versus C, 2.24 per 1000 TCC days, P = NS) between the groups. The number of TCC removed due to infection was also similar, (HIV+ versus C: 17 versus 15%, P = NS). In the HIV+ group, the association of hepatitis B surface antigenemia with TCC exit site infection was dependent on the history of injection drug use. Black race was a significant risk factor for higher TCC exit site infection rates, whereas prophylactic antibiotic use and high CD4 count were significantly associated with lower TCC exit site infection rates. None of the factors significantly predicted bacteremia rate in either group (HIV+ or C). In comparison to controls, HIV+ patients had a fivefold increased risk of having a Gramnegative organism (P = 0.02) and a sevenfold increased risk of a fungal isolate (P = 0.08), although the latter finding was not statistically significant. HIV infection is not a significant risk factor for TCC-associated infection but is associated with a higher prevalence of Gram-negative and fungal species.

	Introduction

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Tunneled-cuffed catheters (TCC) are an important means of hemodialysis vascular access. They have a utility for short-term use—in patients who are awaiting arteriovenous fistula maturation—and for chronic use—in patients with poor venous anatomy in whom arteriovenous fistula or graft creation is not possible (1). In data from the 1996 United States Renal Data System report, 19% of hemodialysis patients were being dialyzed using a TCC in the first 60 d of hemodialysis initiation, and 13% of patients were using a TCC after this 60-d period (2).

Infection is a major complication of TCC use. The incidence of TCC exit site infections has been reported to be between 0.4 to 4.5 per 1000 catheter days, and the incidence of bacteremia has been estimated to be between 0.2 and 3.9 per 1000 catheter days (3,4,5). Hemodialysis vascular access infection rates have been reported to be higher in immunocompromised states, such as with malignancy and during therapy with immunosuppressive medications (4,6). In one study that analyzed the prevalence of TCC-associated infections, immunocompromised patients had a significantly higher prevalence of bacteremia compared with immunocompetent patients: 59 versus 35% (relative risk [RR] = 1.6 [1.0 to 2.5]) (5). Of these patients, only five were HIV positive (HIV+). HIV infection is associated with a marked reduction in T helper lymphocyte number and with impaired B lymphocyte function, including abnormal neutrophil chemotaxis and bactericidal activity (7). Thus, it might be anticipated that HIV+ patients are more prone to TCC infection. To better characterize TCC-associated infections in HIV-infected patients, we performed a retrospective cohort study to compare HIV seropositive patients and low-HIV risk chronic hemodialysis patients.

	Materials and Methods

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All HIV seropositive hemodialysis patients dialyzing with a TCC from June 1992 to May 1999 were identified by a review of the patient census. The control group of low-HIV risk chronic hemodialysis patients who were using a TCC as their hemodialysis access during this period was selected from the chronic hemodialysis population. Low HIV risk was defined as the absence of a history of injection drug use (IDU), homosexual or bisexual risk, or promiscuous heterosexual risk. Controls were age-matched to the HIV + group and were selected without regard to TCC infection history. The participating dialysis units all were Albert Einstein College of Medicine affiliates and consisted of three freestanding outpatient chronic units and three hospital-based units.

All catheters were tunneled, cuffed, dual lumen, silastic catheters used only for hemodialysis (Quinton PermCath, Quinton Instrument Company, Bothell, WA, or Medcomp, Medical Components Inc., Harleysville, PA). Standard catheter care during this period consisted of cleansing the catheter exit site with povidone-iodine solution alone or povidone-iodine followed by isopropyl alcohol and covering with a transparent, oxygen-permeable dressing (OpSite^TM, Smith and Nephew Ltd.) with or without gauze. Catheter dressings were changed thrice weekly by one of the hemodialysis staff.

Demographic and clinical data were obtained by performing a retrospective review of inpatient hospital charts, outpatient hemodialysis charts, and computerized records. Microbiologic data were retrieved by accessing the hospital laboratory computer database. Data regarding age, gender, race, ethnicity, cause of end-stage renal disease, presence of diabetes mellitus (DM), malignancy, HIV risk, IDU, or the use of immunosuppressive medications were recorded. In the HIV+ group, additional data regarding the use of prophylactic antibiotics for AIDS-related illnesses and antiretroviral therapy were retrieved. Pertinent laboratory data at the time of catheter insertion, including the serum albumin, CD4 count, and the presence of hepatitis B surface antigen and hepatitis C antibody, were extracted. Data regarding the date and site of catheter insertion, days of survival, reason for removal, number of hospitalizations, and number of catheter-related infections were recorded.

Catheter-related infections were categorized as an isolated exit site infection or a bacteremia. A description of the appearance of the TCC exit site was recorded for every dialysis treatment by a member of the medical staff. An isolated exit site infection was defined as (1) erythema at the catheter insertion site for which antibiotic therapy was instituted or (2) a culture-positive exudate from the exit site in the setting of negative blood cultures. A bacteremic episode was determined to be catheter related when blood cultures taken from the catheter turned positive during a period in which an exit site infection was also present or when other primary sources of bacteremia were absent (by physical examination, urinalysis, chest radiograph). Because of difficulty distinguishing catheter exit site and tunnel infections, all instances in which the catheter exit site appearance was abnormal and blood cultures were negative were classified as exit site infections. Data regarding wound and blood culture isolates and antibiotic administration were recorded.

All continuous variables were reported as the mean ± SEM and were analyzed using a two-tailed independent t test ( = 0.05). Categorical variables were evaluated using ² analysis for comparisons between groups. A multivariate analysis was performed using linear regression when outcome variables were continuous, and logistic regression was used when outcome variables were dichotomous. Covariates were removed using the backward elimination method; criterion for entry was P = 0.05, and criterion for removal was P = 0.07. A Cox regression was performed to analyze factors associated with patient survival.

	Results

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Demographic and Laboratory Data
A total of 54 HIV+ hemodialysis patients were dialyzed using a TCC during the 7-yr study period. Fourteen patients were excluded because of incomplete records. The remaining 40 HIV+ patients were included in the analysis and were age-matched with 41 controls. The cause of end-stage renal disease (ESRD) in the control group was as follows: diabetic nephropathy (44%), hypertensive nephrosclerosis (22%), idiopathic focal segmental glomerulosclerosis/documented HIV negative (10%), systemic lupus erythematosus (7%), other glomerulonephritides (7%), polycystic kidney disease (5%), reflux nephropathy (3%), and dysplastic kidneys (3%). Three patients in the control group were receiving intermittent steroids for asthma. In the HIV+ group, the cause of ESRD was determined by the patient's individual physician and renal biopsy was performed in only one case. One hepatitis C—positive patient was diagnosed as having membranoproliferative glomerulonephritis, and HIV-associated nephropathy was diagnosed in all other cases.

Data regarding patient demographics are provided in Table 1. As might be anticipated, there were fewer diabetics in the HIV+ group than in the control group. In the HIV+ group, the proportion of IDU and non-IDU with hepatitis B surface antigenemia was not significantly different. Hepatitis C was significantly more prevalent in the HIV+ group compared with controls. HIV+ patients with a history of IDU were 10 times more likely to be hepatitis C positive (RR = 10.1; 95% CI = 1.9 to 52.9; P = 0.003). The majority of HIV+ patients were receiving antiretroviral agents and prophylactic antibiotics for AIDS-related illnesses. Before 1997, antiretroviral therapy consisted of single-agent therapy using a reverse transcriptase inhibitor. After 1997, highly active antiretroviral therapy was administered. At the time of TCC insertion, 11 patients were receiving an reverse transcriptase inhibitor and 16 were on highly active antiretroviral therapy. An analysis comparing individual antiretroviral regimens was not performed because frequent changes in antiretroviral therapy occurred, due to the availability of new agents or regimens, or adverse drug effects requiring discontinuation of one or more agents. The prophylactic antibiotic regimens also varied but in all patients were initiated before TCC insertion and continued throughout the period of observation. Trimethoprim-sulfamethoxazole was used as a single agent in 16 patients, in combination with fluconazole in 5 patients, with clarithromycin in 1 patient, and with both fluconazole and clarithromycin in 3 patients; dapsone was used as single therapy in 3 patients and in combination with clarithromycin in 1 patient; and solo therapy with clarithromycin was used in 1 patient, and fluconazole was used alone in 1 patient.

Laboratory data at the time of catheter insertion for all patients are provided in Table 2. The HIV+ patients had a significantly lower mean serum albumin relative to controls. The mean number of days between the serum albumin determination and the TCC insertion was 3.8 ± 1.3, and with the exception of three values, all were obtained before TCC insertion. There were no significant differences in the rates of hospitalization or the number of deaths between the groups during the observation period (Table 2).

In the control group, three patients were receiving immuno-suppressive therapy. One patient was receiving low-dose oral corticosteroid therapy for systemic lupus erythematosus, another was receiving intermittent oral corticosteroids for asthma, and the third patient was given oral azathioprine and corticosteroids for Wegener's granulomatosis.

Catheter-Related Data
Data were collected on 118 TCC for a total of 28,146 catheter days. Of these, 58 catheters (16,227 d) were present in HIV+ patients and 60 catheters (11,919 d) were present in control patients (Table 2). The TCC bacteremia and TCC exit site infection rates were similar between the groups, as were the number of TCC removed because of infection.

A multivariate analysis was performed to determine factors associated with the TCC infection rate in the HIV+ group using the following variables: age, race, albumin, CD4 count, hepatitis B surface antigenemia, hepatitis C antibody, IDU, antiretroviral therapy, and prophylactic antibiotic therapy (Table 3). In the HIV+ group, a subgroup analysis was performed so as to control for IDU, which which was found to be a confounding factor. Hepatitis B surface antigenemia was associated with higher exit site infection rates in the IDU subset but was associated with lower exit site infection rates in the non-IDU subset. Although these were statistically significant findings (P < 0.001), they are derived from data in a small number of patients (only three hepatitis B/HIV+ co-infected patients: one IDU, two non-IDU). In the IDU subset, hepatitis C antibody positively correlated with that TCC exit site rate, whereas the CD4 count inversely correlated with the TCC exit site infection rate; however, these findings did not reach statistical significance. In the non-IDU HIV+ group, black race was a significant risk factor for TCC exit site infection, whereas prophylactic antibiotic use and the CD4 count were inversely associated with TCC exit site infection rates. In the HIV+ group, there was an association between IDU and higher TCC bacteremia rates, although this was not significant.

In a multivariate analysis, controlling for age, race, albumin, hepatitis C, and DM, there were no significant factors associated with the TCC exit site infection or bacteremia rate in the control population. The TCC bacteremia rate was not significantly different in diabetic controls as compared with nondiabetic controls (1.8 versus 3.2 episodes per 1000 TCC days, respectively; P = NS), nor was the exit site infection rate (1.7 versus 2.7 episodes per 1000 TCC days, respectively; P = NS). In the control population, DM was not a significant risk factor for TCC bacteremia or exit site infection in both univariate and multivariate analyses, adjusted for serum albumin, age, and race. When all 81 patients (HIV and controls) were analyzed, adjusting for all of the above variables, including the HIV status, none of the laboratory or clinical variables were significant risk factors for TCC bacteremia or exit site infection.

Microbiologic Isolates
A comparison of the microbiologic isolates from both TCC bacteremias and TCC exit site infections (diagnosed by culture in 65% cases) in the HIV+ and control groups are provided in Table 4. In the HIV+ group, there were 27 episodes of TCC bacteremia from which 29 organisms were isolated (2 mixed) and 23 episodes of TCC exit site infection from which 7 organisms were isolated. In the control group, 28 organisms were isolated during 27 episodes of TCC-bacteremia (1 mixed), and 29 organisms were isolated during 32 episodes of TCC exit site infection (2 mixed). The spectrum of organisms was significantly different between the HIV+ and the control groups. There was a significantly lower prevalence of Gram-positive organisms in the HIV+ patients relative to controls. HIV + patients were almost 5 times more likely to be infected with a Gram-negative isolate. HIV+ patients were also 7 times more likely to have a fungal isolate, although this did not reach statistical significance. The prevalence of mixed organisms from the same culture was similar in the two groups (HIV+ versus C: 9 versus 8%).

All fungal isolates occurred in HIV+ patients who were previously treated for bacterial TCC infections, and all were receiving prophylactic antibiotic therapy for AIDS-related illnesses; however, this was not a significant risk (RR = 1.1; 95% CI = 0.99 to 1.2). Overall, no significant association was found between the use of individual antibiotics/antifungals and the microbiologic isolates, although in the presence of fluconazole, no fungal organisms were isolated, whereas fungi accounted for 13% of isolates in the absence of fluconazole (OR = 0.87; 95% CI = 0.74 to 1.0; P = NS). Similarly, no Gram negatives were isolated in patients who were receiving clarithromycin, whereas Gram negatives accounted for 19% of isolates in the absence of clarithromycin (OR = 0.71; 95% CI = 0.64 to 0.95; P = NS). Isolates did not differ in the other antibiotic groups. None of the demographic or laboratory variables were associated with the presence of a fungal isolate. Patient mortality did not differ according to microbiologic isolates: Gram negative, two deaths; Gram positive, seven deaths; fungal, zero deaths.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Infection Rates between HIV+ and Controls
In TCC used for hemodialysis, Marr et al. (5) reported a higher risk of bacteremia in immunocompromised patients (RR = 1.6, 95% CI = 1.0 to 2.5); however, only 5 of the 23 immunocompromised patients were infected with HIV, 3 had a malignancy, and 15 were receiving long-term steroids. In the present study, HIV infection was not associated with higher TCC infection rates. A possible explanation for the differences in the results of Marr's study and the present study may be qualitative differences in various immunocompromised states (HIV+ versus corticosteroid use).

The percentage of patients with DM and hepatitis C in the control group was representative of the chronic hemodialysis population in the Bronx, and the hepatitis C prevalence is comparable to that at other North American centers (8 to 36%) (4,5,8,9). Although DM has been reported to be a risk factor for bacteremia in dialysis patients, more recent large series did not find higher bacteremia rates in patients with DM (5,10,11,12). In the present study, diabetic and nondiabetic controls had similar TCC infection rates. The mean TCC infection rates in the control group in the present study were comparable to that reported in previously published studies (3,4,5,8,13).

Higher catheter infection rates have been reported in the non-ESRD HIV population relative to controls consisting of cancer patients (14,15,16,17). Reasons for these findings may be due to the selection of control groups. The catheter infection rates reported in the controls are lower than those published in the existing literature, possibly as a result of concurrent antibiotic administration. In fact, in one study, 77% of catheters were used for antibiotic infusion, none of which developed an infection (17).

Multivariate Analysis of Risk for TCC Infection
Factors shown to be associated with higher rates of TCC infection in HIV+ patients were black race, hepatitis C, and IDU. Data regarding the association with hepatitis B surface antigenemia were conflicting in this study and were dependent on the IDU status. These preliminary findings require further investigation in a larger population. Black race has been associated with septicemia in the general population; however, data in the dialysis population are conflicting. Powe et al. (18) did not find a significant association between black race and septicemia in hemodialysis patients, when adjusted for socioeconomic and demographic factors. However, black race was associated with a significantly lower risk of septicemia in peritoneal dialysis patients (12). The analysis of race and TCC exit site infection was not adjusted for socioeconomic factors, such as insurance status and education, which may explain these findings. Hepatitis C had not been previously reported to be an independent risk factor for infections in the general dialysis population, although IDU has been reported to be a risk factor for TCC bacteremia (RR = 1.7, 95% CI = 0.9 to 3.2) (5).

The use of prophylactic antibiotics for AIDS-related illnesses and the CD4 count were inversely associated with the TCC exit site infection rate. Lower infection rates have been reported in central vein catheters used for antibiotic administration in nondialysis patients (17). The high prevalence of antibiotic use in the HIV population may explain why this group did not have higher TCC infection rates, as has been described in other immunosuppressed groups. In addition, an inverse correlation of CD4 count and catheter infection rates has been described in HIV+ patients (19). An association between antiretroviral therapy and lower catheter infection rates in HIV patients has been reported in the literature but was not observed in this study (19,20).

Differences in Microbiologic Isolates
Gram-positive species were significantly less prevalent in the HIV+ group. HIV+ patients had a significantly higher risk (fivefold) of having a Gram-negative isolate. HIV+ patients were also at higher risk (sevenfold) of having a fungal isolate, although this was not significant. These findings are similar to results observed in nondialysis HIV+ patients with central venous catheters and in HIV+ peritoneal dialysis patients with peritonitis, in whom a higher prevalence of Gram-negative and fungal organisms was reported (17,19,21).

In the low-risk control group, Gram-negative organisms accounted for only 5% of isolates, whereas previous series report a prevalence of 24 to 33% of Gram-negative isolates (5,8,21,22). One explanation for the differences in the control group in the present study and those reported in the literature may be that the populations studies by other investigators included a subpopulation of immunosuppressed patients, possibly including those with HIV. In a study by Marr et al. (5), which evaluated TCC-related bacteremia in 102 patients, 23 patients (23%) were immunocompromised. In the other studies, data regarding immune status were not provided (8,22,23).

In conclusion, HIV was not found to be an independent risk factor for TCC infection in this study. When adjusted for IDU, black race was a significant risk factor for TCC exit site infections, whereas the use of prophylactic antibiotics for AIDS-related infections and a high CD4 count were associated with a significantly lower risk of TCC exit site infections. Data regarding hepatitis B surface antigenemia as a risk factor for TCC exit site infection were conflicting and require further investigation. TCC infection rate was associated with both hepatitis C and IDU; however, they were not statistically significant. Gram-negative and fungal isolates were more prevalent in the HIV+ population. The results of this study support the use of broad-spectrum antibiotic coverage (with an anti-Pseudomonal agent) for empiric initial antimicrobial therapy in TCC infections in HIV+ patients.

	Acknowledgments

 
The authors thank Dr. Joel Neugarten for reviewing this manuscript.

	References

Top Abstract Introduction Materials and Methods Results Discussion References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by MOKRZYCKI, M. H. Articles by FEINGOLD, R. Search for Related Content PubMed PubMed Citation Articles by MOKRZYCKI, M. H. Articles by FEINGOLD, R.