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Rheumatology Advance Access originally published online on June 19, 2008
Rheumatology 2008 47(9):1352-1357; doi:10.1093/rheumatology/ken196
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© The Author 2008. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Long-term outcome and short-term survival of patients with systemic lupus erythematosus after bacteraemia episodes: 6-yr follow-up

M.-J. Chen1, H.-M. Tseng2, Y.-L. Huang1, W.-N. Hsu1, K.-W. Yeh1, T.-L. Wu3, L.-C. See4 and J.-L. Huang1

1Division of Allergy, Asthma and Rheumatology, Department of Pediatrics, Chang Gung Memorial Hospital, Chang Gung Children's Hospital and Chang Gung University, 2Department of Health Care Management, College of Management, Chang Gung University, 3Department of Clinical Pathology, Chang Gung Memorial Hospital, 4Biostatistics Consulting Center, Chang Gung University, Taoyuan, Taiwan.

Correspondence to: J.-L. Huang, Division of Allergy, Asthma and Rheumatology, Department of Pediatrics, Chang Gung Children's Hospital, Taoyuan, Taiwan 5, Fu-Hsin Street, Kweishan, Taoyuan, Taiwan. E-mail: long{at}adm.cgmh.org.tw


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Acknowledgement
 References
 
Objective. To describe the nature of bacteraemia in SLE patients and determine the short-term survival and long-term outcome of these patients.

Methods. Analysis of the medical records of 1442 SLE patients who were regularly followed up in a tertiary teaching medical centre from 2000 to 2005.

Results. Among 1442 SLE patients, 240 patients (17%) developed at least one episode of bacteraemia, corresponding to an incidence of 92.7 cases/1000 hospital admissions. Since SLE diagnosis, the overall survival of our patients was 92% at 5 yrs, 86% at 10 yrs and 79% at 15 yrs. However, after one episode of bacteraemia, the survival decreased to 76% at 30 days and 67% at 360 days. Of the 336 episodes of bacteraemia, 167 were community-acquired (49.7%) and 169 were nosocomial (50.3%). Staphylococcus aureus was the leading cause of Gram-positive bacteraemia. Among Gram-negative bacteria, non-typhoidal Salmonella and Escherichia coli were the most common species. Community-acquired Salmonella and Streptococcus bacteraemia were more common than nosocomial infections. Klebsiella and Acinetobacter spp. were significantly more responsible for nosocomial than community-acquired bacteraemia. Patients infected with Acinetobacter, Klebsiella or Pseudomonas had lower probabilities of 14-day survival (71.4, 55.6, 42.9%, respectively).

Conclusions. Among SLE patients, an episode of bacteraemia was associated with an unfavourable long-term outcome. The bacterial species significantly influenced short-term survival. Therefore, when empiric antibiotic therapy is initiated in SLE patients who are suspected of bacteraemia, we suggest use of antibiotics that are effective against Pseudomonas, Klebsiella, Acinetobacter, S. aureus, and E. coli.

KEY WORDS: Systemic lupus erythematosus, Infection, Bacteraemia, Mortality, Outcome measure


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Acknowledgement
 References
 
Systemic lupus erythematosus (SLE) is an autoimmune disease that typically affects multiple organs. The 5-yr survival rate of SLE patients was 50% in 1955 but is over 90% since 1990 [1–9]. Several studies have demonstrated that infection is the predominant cause of mortality in SLE patients [7, 10–15]. SLE patients are more susceptible to infection because they are immunocompromised and are typically given immunosuppressive drugs to control disease activity. Previous studies indicate that SLE patients with infections have poorer outcomes than uninfected patients [10–16]. Some reports also show that bacteraemia is common in SLE patients and that bacteraemia-related mortality is higher than mortality caused by other infections [13, 14, 17, 18]. Bacteraemia in SLE patients is typically caused by opportunistic pathogens and micro-organisms that are responsible for common infections in the general population. To date, few studies have provided detailed information regarding the nature of bacteraemia in SLE patients [11, 12, 19, 20] and there are no long-term studies of the outcomes of SLE patients following bacteraemia.

In this cohort study, we identify the species responsible for bacteraemia in SLE patients, determine the long-term outcomes of these patients and determine the short-term survival of these patients following infection with different species.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Acknowledgement
 References
 
Patients
All 1442 subjects were ethnic Chinese SLE patients [21] at the Chang Gung Memorial and Children's Hospital, a tertiary teaching medical centre in Taiwan where more than 4 million outpatients and 150 000 inpatients are treated annually. All enrolled patients were regularly followed up in the Rheumatology Clinic of this hospital between 1 January 2000 and 31 December 2005. Laboratory parameters and SLE disease activity were measured every 1–2 months regularly. Patients who were not regularly followed up in our hospital were excluded in this study. The Ethics Committee (Institution Review Board) of Chang Gung Memorial and Children's Hospital approved this study and informed consent was obtained from the subjects, parents or guardians.

Data collection
We searched the hospital database for all episodes of bacteraemia in the 1442 SLE patients and reviewed documentation of the organisms that were identified in the microbiology laboratory reports. For all patients, we recorded demographics (gender, age, etc.), dates of hospital admission, dates of positive blood cultures, length of hospital stays, outcomes, SLEDAI [22], use of immunosuppressive treatments and the levels of autoantibody and complements.

Definitions
Bacteraemia was deemed clinically significant when the patient had one or more positive blood cultures for bacteria and met two or more of the following criteria: (i) temperature >38°C or <36°C; (ii) heart rate >90 beats per minute; (iii) respiratory rate >20 breaths per minute or PaCO2 < 32 mmHg; and (iv) leucocyte count >12 000, <4000 or >10% band form counts [23, 24]. Some organisms were more likely to be skin contaminants (e.g. Bacillus spp., Corynebacterium spp. and Propionibacterium acnes), so we considered them clinically significant only if they were isolated from two or more separate blood cultures [24, 25]. We considered a patient to have polymicrobial bacteraemia if two or more species were isolated concomitantly (from the same blood culture or from two blood cultures that were obtained within 24 h). If a patient had repeated positive blood cultures with the same species during the same hospitalization period, we considered this an episode of bacteraemia. If a patient had repeated positive blood cultures with different microbial species during the same hospitalization period, we considered these as separate episodes [20, 26, 27]. Nosocomial infections were defined according to centres for disease control (CDC) criteria [28].

Juvenile-onset SLE was diagnosed if the patient was less than 16 yrs old at the time of diagnosis. Otherwise, the diagnosis was adult-onset SLE. We determined long-term outcomes from the date of SLE diagnosis and from the first episode of bacteraemia. We defined a survivor as a patient who was alive on 31 December 2005 or had ≥1 clinic visit after 31 December 2005. For short-term survival, the end-point was survival at 14 days following the first positive blood culture. Patients discharged from the hospital before 14 days were considered survivors [27].

We also compared the autoantibody, complements and disease activity ‘before’ (30–60 days prior to a positive blood culture) and ‘during’ (between 7 days before and 7 days after a positive blood culture) bacteraemia episodes.

Statistical analysis
We analysed data using the SPSS program 11.0 (SPSS Incorporated, Chicago, USA) and used descriptive statistics (means, S.D) for sex, age, number of admission episodes and length of hospital stay. We used paired t-tests to examine differences between laboratory data before and during a bacteraemia episode. We estimated survival rates using the Kaplan–Meier method and compared survival differences between groups by the log-rank test. The cumulative survival curves were fitted using SigmaPlot 9.0 (Systat Software Incorporated, CA, USA). A probability value (P) <0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Acknowledgement
 References
 
Incidence of bacteraemia
A total of 1442 SLE patients were admitted 3623 times for 46 957 days. During the 6-yr observation period, we identified a total of 336 episodes of bacteraemia, corresponding to an incidence of 92.7 cases/1000 hospital admissions.

Demographics and clinical characteristics
The demographic data and clinical characteristics of the patients are depicted in Table 1. A total of 1269 patients were females and 1264 patients were adult-onset SLE. Two hundred and forty patients (17%) developed at least one episode of bacteraemia, 207 of whom were females (86%) and 214 of whom were adult-onset SLE (89%). The sex distribution and age were not significantly different in the bacteraemic and non-bacteraemic groups.


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  		TABLE 1. Demographics, SLEDAI scores and treatment regimes of SLE patients with and without bacteraemia

 
Patients with bacteraemia had a mean age at diagnosis of 35.0 ± 17.3 yrs, significantly greater than patients without bacteraemia (31.8 ± 14.9 yrs, P = 0.008). However, there was no significant difference in the diagnosis age of bacteraemic and non-bacteraemic juvenile SLE patients (12.2 ± 3.2 vs 12.7 ± 2.5, P = 0.389). The mean duration of follow-up was 34.1 ± 24.0 months in the bacteraemia group and 34.9 ± 21.5 months in the non-bacteraemia group. In comparison with non-bacteraemic patients, bacteraemic patients had more frequent hospitalizations (4.0 vs 2.2, P < 0.001) and longer durations of hospitalization during the follow-up period (18.4 days vs 11.0 days, P < 0.001).

There was a significant difference in the SLEDAI scores between patients who developed bacteraemia infection and those who did not. Use of oral corticosteroids was more common in patients who developed bacteraemia. There were no significant differences of the two groups in the use of other immunosuppressants (methylprednisolone pulse therapy, AZA, cyclophosphamide).

Survival curves for SLE patients
Of the 1442 SLE patients, 161 (11.2%) died during the observation interval. The Kaplan–Meier survival curves show the survival probability for all patients following SLE diagnosis (Fig. 1) and for SLE patients following the first episode of bacteraemia (Fig. 2). Since SLE diagnosis, the overall survival of our cohort was 92% at 5 yrs, 86% at 10 yrs and 79% at 15 yrs. However, after the first episode of bacteraemia, the survival declined sharply and was 76% at 30 days and 67% at 360 days.


Figure 1
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  		FIG. 1. Survival curves for 1442 SLE patients.

 

Figure 2
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  		FIG. 2. Survival curves for 240 SLE patients after the first episode of bacteraemia.

 
Anti-dsDNA, complements and SLEDAI scores
Table 2 shows the levels of anti-dsDNA, complements and SLEDAI scores before and during bacteraemia episodes for all bacteraemic patients. We observed slightly higher anti-dsDNA during the bacteraemia episode (paired t-test, P = 0.069), but there were no differences in the levels of C3, C4 and SLEDAI scores (P = 0.449, 0.986, 0.324, respectively).


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  		TABLE 2. Autoantibody, SLEDAI scores and serum complements in bacteraemic SLE patients

 
Recurrent bacteraemia
Figure 3 is a flow diagram that shows the fate of each of 240 SLE patients following bacteraemia. One hundred and sixty-seven episodes of bacteraemia were community-acquired infections (49.7%) and 169 were nosocomial (50.3%). One hundred and seventy-seven patients had one bacteraemia episode and 63 (26.3%) had two or more episodes. Among all the micro-organisms isolated from patients with recurrent bacteraemia, 32.7% (38/110) were the same species as previously isolated. Staphylococcus aureus and Salmonella spp. were the most common pathogens which were the same as previous pathogens. For patients who had more than two episodes of bacteraemia, half were caused by the same species as previously.


Figure 3
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  		FIG. 3. Flow diagram showing the fate of each of the 240 SLE bacteraemic patients during the 6-yr observation period.

 
Distribution of micro-organisms
Table 3 shows the species of micro-organisms isolated from our bacteraemic SLE patients. Thirty-four (10.1%) episodes of bacteraemia were polymicrobial. We identified 378 micro-organisms, of which 179 (47.3%) were Gram-positive bacteria, 176 (46.6%) were Gram-negative bacteria, 11 (2.9%) were anaerobes and 12 (3.2%) were fungi. Among Gram-positive bacteria, S. aureus (31.0%) and Streptococcus spp. (6.6%) were the most common pathogens. Among Gram-negative bacteria, non-typhoidal Salmonella (11.6%), E. coli (11.1%), Klebsiella (6.0%), Pseudomonas (5.3%) and Acinetobacter spp. (3.4%) were the most common species. Community-acquired Salmonella and Streptococcus bacteraemia were more common than nosocomial bacteraemia (P = 0.003 and 0.001, respectively). Klebsiella and Acinetobacter species were significantly more responsible for nosocomial bacteraemia than community-acquired bacteraemia (P = 0.011 and 0.019, respectively).


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  		TABLE 3. Microbial species present in 336 blood cultures (including 34 polymicrobial culturesa) of SLE patients

 
Effect of bacteraemic species on 14-day survival rate
The survival rate of 240 bacteraemic patients at 14 days after the first blood culture was 80.8%. Of these 240 patients, 21 suffered from polymicrobial infection in the first episode. Excluding these 21 patients, the species responsible for the remaining 219 bacteraemia episodes were S. aureus (60 episodes), Streptococcus (18 episodes), non-typhoidal Salmonella (30 episodes), E. coli (30 episodes), Klebsiella (9 eisodes), Pseudomonas (7 episodes) and Acinetobacter (7 episodes). Fifty-eight other micro-organisms were responsible for fewer than four episodes.

The 14-day Kaplan–Meier survival curves of patients infected with the seven most common bacteraemic species are shown in Fig. 4. Patients infected with Salmonella had the best 14-day survival rates (93.3%). Patients infected with Acinetobacter, Klebsiella and Pseudomonas had 14-day survival rates of 71.4, 55.6 and 42.9%, respectively.


Figure 4
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  		FIG. 4. Fourteen-day survival curves of 161 SLE patients infected with different bacterial species after the first positive blood culture. Survival probabilities were estimated using the Kaplan–Meier method. Log-rank tests showed significant differences in 14-day survival between patients infected with Salmonella and Klebsiella (P = 0.005), Salmonella and Pseudomonas (P < 0.001), Streptococcus and Pseudomonas (P = 0.033), E. coli and Pseudomonas (P = 0.023), but no significant differences between infections by other species.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Acknowledgement
 References
 
This is the first large and detailed study of bacteraemia in SLE patients. The large number of patients allowed us reliably to characterize the variety of species that cause bacteraemia and to compare survival rates of patients following bacteraemia with different species.

Previous studies have shown that 16–47% of SLE patients suffered from bacteraemia [14, 16, 17]. In the present study, we detected bacteraemia in 17% of our SLE patients. Mok et al. [7] indicated that age was an important factor that affects the clinical manifestations and prognosis of SLE and that infection was the major cause of mortality in late-onset SLE. In our study, patients who developed bacteraemia were also associated with older diagnosis age.

The frequency of hospitalization among our bacteraemic patients was higher than that for non-bacteraemic patients (4.0 vs 2.2, P < 0.001). The average time in the hospital for bacteraemic patients was 18.4 days, longer than that for non-bacteraemic patients (11.0 days, P < 0.001). This is comparable with the results of a study in Toronto, which followed 81 SLE patients who were admitted over a 5-yr period. In the Toronto study, SLE patients who developed infections required longer hospitalization (28.5 vs 11.2 days, P < 0.001) and had higher SLEDAI scores (11.6 vs 7.1) [29]. A prospective study in the Hopkins Lupus Cohort also demonstrated that SLE activity (quantified by the SLEDAI) was a predictive factor for hospitalization because of infection [30]. For our SLE patients, bacteraemic patients may have experienced more frequent and longer hospitalizations because they had higher SLE disease activity, and therefore required more frequent dosing of corticosteroids. The greater frequency and longer duration of hospitalization of these patients presumably resulted in a higher incidence of bacteraemia due to nosocomial infections.

Multiple series have identified that active lupus is one of the risk factors for infection in SLE patients [15, 17, 29]. In our study, overall disease activity was evaluated using the SLEDAI score. Our results show that there is a significant difference in the SLEDAI score between patients who developed bacteraemia infection and those who did not. This suggests that active lupus in SLE patients may predispose SLE patients to bacteraemia.

Recent studies showed that the 5-yr survival rate of SLE patients is 90% and the 10-yr survival rate is 80% [3–6, 12]. In the present study, the cumulative survival rates were 92% at 5 yrs, 86% at 10 yrs and 79% at 15 yrs. This is similar to other recent studies [7–9]. However, after one episode of bacteraemia, our SLE patients had a 360-day cumulative survival rate of only 67%.

Previous studies indicated that patients with underlying immunodeficiency diseases, either primary or acquired, tend to have recurrent bacteraemia [31–33]. In the present study, the rate of recurrent bacteraemia in SLE patients was 26.3%. Around 32.7% of the pathogens responsible for recurrent bacteraemia were the same species that caused the previous episode. Furthermore, for patients who had more than two episodes of bacteraemia, half of the episodes were caused by the same species. In patients with recurrent bacteraemia, S. aureus and Salmonella spp. were the most common pathogens that were the same as previous pathogens. Therefore, when SLE patients are suspected of having an episode of recurrent bacteraemia, we suggest administration of an antibiotic(s) that covers the same pathogens as those identified in the previous episode.

SLE patients usually present with multiple organ dysfunction during bacteraemia, so it may be difficult to conclude that bacteraemia was the cause of death. We used a pre-determined, uniform end-point of survival (14 days) to determine short-term survival of bacteraemic SLE patients infected with different species. We believe that a 14-day survival rate more accurately reflects mortality from bacteraemia than criteria used in previous studies, which have used in-hospital mortality, 60-day mortality or 180-day mortality [20, 27]. Our method eliminates potential bias in assignment of cause of death and has been validated in previous prospective studies of bacteraemia [34–37]. In our study, the 14-day survival rate following bacteraemia was 80.8%, similar to the results of Stahl et al. [38].

A previous study showed that E. coli was the leading cause of Gram-negative bacteraemia in the general population, followed by Klebsiella spp. [39]. In the present study, non-typhoidal Salmonella was the leading cause of Gram-negative bacteraemia in SLE patients, similar to previous studies [2, 14, 16, 17, 19, 40]. In immunocompromised patients, such as those with SLE, the overall mortality of Salmonella bacteraemia has been reported as 26% [32]. In our study, the 14-day survival rate following non-typhoidal Salmonella bacteraemia was 93.3%, higher than that reported in a previous study of immunocompromised patients [32]. These differences may be due to differences in the methodology of the studies and/or to the increasing awareness of Salmonella infection and the corresponding use of more appropriate antibiotics.

Our study provides detailed information regarding the nature of bacteraemia in SLE patients. Gram-negative bacilli are the most common micro-organisms responsible for bacteraemia in Asian SLE patients [12], but Gram-positive cocci are more often encountered in Western SLE bacteraemic patients [10, 14, 15, 19]. In our study, Gram-positive cocci and Gram-negative bacilli bacteria were encountered equally. Among Gram-positive bacteria, S. aureus was the most common species. Among Gram-negative bacteria, non-typhoidal Salmonella, E. coli were the most common species.

We found that community-acquired Salmonella and Streptococcus bacteraemia were more common than nosocomial bacteraemia. On the other hand, Klebsiella and Acinetobacter species were significantly more responsible for nosocomial bacteraemia than community-acquired bacteraemia. Our results provide a basis for empirical selection of antibiotics for SLE patients who are suspected of having bacteraemia. The lowest 14-day survival rates were for Asian SLE patients infected with Pseudomonas, Klebsiella and Acinetobacter spp. Therefore, we suggest that empiric antibiotic therapy against Pseudomonas, Klebsiella, Acinetobacter, S. aureus and E. coli species be initiated in Asian SLE patients who are suspected of having bacteraemia.

In conclusion, bacteraemia episodes in SLE patients were associated with unfavourable long-term outcomes and the species that was responsible for the bacteraemia significantly influenced short-term patient survival.

Formula


   Acknowledgement
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgement
References
 
Funding: This study was partially supported by grants from the Chang Gung Medical Research Progress Grant (CMRPG 460031) and National Science Council Grant (NSC 95-2314-B-182A-172-MY3).

Disclosure statement: The authors have declared no conflicts of interest.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgement
 References
 

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Submitted 18 November 2007; revised version accepted 14 April 2008.
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