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Retrospective analysis of nosocomial urinary tract infections with spinal cord injury patients in a rehabilitation setting/Bir rehabilitasyon merkezindeki spinal kord yarali hastalarda gorulen nozokomiyal uriner sistem infeksiyonlarinin retrospektif analizi.

Introduction

Nosocomial infections are common among patients with spinal cord injury (SCI) admitted to rehabilitation centers (1). A high prevalence rate of nosocomial infections, especially nosocomial acquired urinary tract infections (NAUTIs), has been determined in rehabilitation units. They cause a vicious circle, by prolonging the length of hospital stay and rehabilitation procedure, increasing the potential for a new nosocomial infection (2). Therefore, they are associated with negative physical and psychological effects and socio-economic costs (3,4).

The literature that is focused on nosocomial infections has recorded high urinary tract infection (UTI) rates in patients with SCI (1). About one-half of all nosocomial infections are reported to originate from the urinary tract in association with urinary catheters and other drainage devices. On the other hand, a high frequency of antibiotic use also increases the risk of infection with antibiotic-resistant organisms, further complicating the treatment of NAUTI (5).

Despite the fact that a UTI is a common complication, what exactly constitutes a UTI in catheterized patients is controversial. Symptoms of fever associated with cloudy or foul-smelling urine strongly suggest the presence of a UTI and the need for treatment (6). Spinal cord injury patients with neurogenic bladder often have bacteriuria without signs and symptoms of infection due to catheterization. These asymptomatic cases generally do not require any treatment (7).

In this retrospective study, we reviewed the records of spinal cord injury patients and described the 2-year data of NAUTIs in our rehabilitation center. We aimed to report the distribution of NAUTIs and the spectrum of antibiotic resistance in patients with SCI.

Material and Methods

In this retrospective study, 2-year data (2008-2010) of NAUTIs recorded by the Infection Control Committee were retrieved. NAUTI was defined as an infection occurring in a patient during the process of care in a hospital or other health care facility that was not present or incubating at the time of admission according to the Centers for Disease Control and Prevention (CDC, Atlanta, USA) (8). Inpatient records from 276 spinal cord injured patients diagnosed with NAUTI were included in the current study. Since the isolation of more than one organism from a single specimen of urine must always be interpreted with caution, and considering contamination, the patients whose culture results had polymicrobic bacteriuria samples were excluded from the study. Ethics committee approval was obtained from the local hospital ethics committee of Gulhane Military Medical Academy.

The data gathered for each patient were as follows: definition of UTI (symptomatic UTI [SUTI] or asymptomatic bacteriuria [ASB]), time of injury, hospitalization date, date of UTI diagnosis, length of hospital stay, method of bladder emptying, isolated pathogens, and their susceptibility to antimicrobial agents. Antimicrobial susceptibility of the following pathogens was recorded: Escherichia coli (E. coli), extended spectrum beta-lactamase (ESBL) (+) E. coli, Klebsiella species pluralis (spp), Proteus spp., Enterobacter spp., Pseudomonas aeruginosa (P aeruginosa), Enterococcus spp., and Acinetobacter spp. The resistance rates against the following antibiotics were analyzed: amoxicillin, ampicillin in combination with sulbactam, amikacin, gentamicin, imipenem, levofloxacin, norfloxacin, ciprofloxacin, doxycycline, and trimethoprim in combination with sulfamethoxazole (TMP-SMX).

The isolated pathogens and the resistance rates against antibiotics were compared between acute (first 6 months after injury) and chronic (6 months-2 years after injury) spinal cord injury patients.

The incidence density rate of nosocomial infections was calculated by dividing the total number of nosocomial infections by the total patient-days (x1000) during the defined period of time. The total patient-days were calculated by summing the days of all patients hospitalized in the SCI unit.

Statistical analysis

Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL, USA) software, version 10.0. The qualitative variables were described as proportion and percentage. One-way ANOVA was used to compare mean differences between the subgroups. Any differences between the two groups were compared using the independent samples t-test. The level of statistical significance was set at p<0.05.

Results

A total of 276 spinal cord injury patients diagnosed with NAUTI were included; 159 of them were chronic spinal cord injury patients, and 117 of them were acute spinal cord injury patients. The frequency rate of ASB and SUTIs was 166 (61%) and 110 (39%), respectively. The demographic and clinical characteristics of the patients are documented in Table 1.

E. coli, Klebsiella spp., and ESBL(+) E. coli were the most common pathogens for NAUTIs in patients with spinal cord injury. In patients with acute spinal cord injury, E. coli was the most frequently isolated pathogen, accounting for more than half of the pathogenic population of SUTIs, followed by Pseudomonas. The most frequently isolated pathogen in ASBs of acute spinal cord injury patients was Klebsiella spp. On the other hand, in patients with chronic spinal cord injury, E. coli was the most frequently isolated pathogen in ASBs and SUTIs (Table 2).

The comparison of the microorganisms' resistance rates against antibiotics between acute and chronic spinal cord injury patients is documented in Table 3. More than half of the E. coli and Klebsiella spp. isolates were sensitive to amikacin and gentamicin in patients with acute SCI. No imipenem resistance was detected for E. coli and Klebsiella spp. isolates in the acute period. More than half of the Pseudomonas isolates were sensitive to amikacin and imipenem in patients with acute SCI.

Most of the E. coli and ESBL(+) E. coli isolates had the lowest rates of resistance to amikacin and gentamicin in patients with chronic SCI. No imipenem resistance was detected for E. coli and ESBL(+) E. coli isolates in chronic spinal cord injury patients. Klebsiella spp. isolates generally had the lowest rates of resistance to amikacin, gentamicin, imipenem, levofloxacin, norfloxacin, ciprofloxacin, and trimethoprim/sulfamethoxazole (TMP/ SMX) in patients with chronic SCI. The difference in resistance rates of all uropathogens between acute and chronic spinal cord injury patients was statistically significant (p<0.05).

We investigated the bladder drainage method among 117 acute spinal cord injury patients; 88 of them were using clean intermittent catheterization (CIC), 17 patients were using an indwelling Foley catheter, and 12 patients had catheter-free voiding function. Among 159 chronic spinal cord injury patients, 119 patients were using clean intermittent catheterization (CIC), 24 patients were using an indwelling Foley catheter, and 16 patients had catheter-free voiding function. We also analyzed the infection rates among the patients, and we found that the infection rate was significantly higher in patients with SCI using an indwelling Foley catheter (52%) than those who were using CIC (37%) and those who had catheter-free voiding function (25%) (p<0.05) (Table 4). There was no statistically significant difference in the rates of NAUTI (ASB and SUTI) between acute and chronic spinal cord injury patients (p>0.05) (Table 5).

The mean length of stay (LOS) for hospitalizations in spinal cord injury patients with NAUTIs was 37.8 [+ or -] 9.8 days. The mean time from admission to the onset of UTIs was 21.5 [+ or -] 11.1 days (median, 17.0 days; range, 10-60 days). A total of 416 hospital-acquired infections (HAIs) occurred during 57,104 patient-days in the spinal cord injury unit (incidence rate, 7.2 HAIs per 1000 patient-days). The most common HAIs were UTIs (276 [66.3%] of the 416 HAIs; incidence rate, 4.8 cases per 1000 patient-days).

Discussion

The results of this study revealed that the most frequent type of NAUTI is asymptomatic bacteriuria, and the most frequently isolated nosocomial pathogen is E. coli in patients with spinal cord injury. These findings are consistent with previous studies and indicate that NAUTIs are often associated with the use of invasive devices (9-11).

E. coli and Klebsiella spp., members of gram-negative enteric bacilli, have been reported as almost the most common causes of catheter-associated UTIs (12). Two-thirds of all urinary infections are caused by organisms ascending from the perineum along the surface of the catheter, such as gram-negative enteric bacilli, which are common commensals of the perineum. However, Pseudomonas, Enterobacter, or Acinetobacter may use the intraluminal route from the collection bag.

Esclarin de Ruz et al. (13) found that SCI patients had more risk factors, but the only independent significant factor was indwelling catheterization. In this study, the risk factors were age, injury level, hyper-reflexic bladder with detrusor-sphincter dyssynergia, dependency level, and bladder catheterization. In our study, we could not assess the risk factors, since only patients who had NAUTIs were included. However, we found that infection rates were higher in patients with SCI using an indwelling Foley catheter. Therefore, in order to reduce the rate of NAUTIs, the use of an indwelling catheter should be removed as soon as possible with CIC.

There are limited data concerning the epidemiology of nosocomial infections among patients admitted for acute rehabilitation after medical stabilization of spinal cord injury patients. Studies have reported that the most common nosocomial infections are urinary tract infections (14). However, none of these studies provided specific data on the organisms causing nosocomial infections. In the present study, we detailed our data on nosocomial NAUTIs according to uropathogen, method of bladder emptying, and resistance testing of isolated pathogens.

According to our study's results, the most common cause of SUTI in acute spinal cord injury patients was E. coli, followed by Pseudomonas. The most frequently isolated pathogen in ASB with acute spinal cord injury patients was Klebsiella spp. In patients with chronic spinal cord injury, E. coli was the most frequently isolated pathogen in ASB and SUTIs. The most commonly used method for bladder emptying was intermittent bladder catheterization (75%) in patients with SCI. The rest of the SCI patients used indwelling catheters (14.9%) and the reflex voiding (10.1%) method for bladder emptying.

On the other hand, the patients who have been evaluated in the literature have varied, from those who were just beginning acute rehabilitation to those who have had chronic disabilities for many years. This variation in the characteristics of the patients makes comparisons difficult. Thus, we compared the results of acutely injured and chronic spinal cord injury patients. In patients with acute SCI, E. coli and Klebsiella spp. isolates had the lowest rates of resistance to amikacin and gentamicin, and no imipenem resistance was determined. All other remaining antibiotics had a much higher overall resistance rate. Pseudomonas isolates also showed the lowest rate of resistance to amikacin and imipenem in patients with acute SCI. The resistance rate of P aeruginosa against fluoroquinolone was the highest. In patients with chronic SCI, E. coli and ESBL(+) E. coli isolates had the lowest rates of resistance to amikacin and gentamicin, and no imipenem resistance was determined. Therefore, the options for adequate empiric antibiotic therapy in hospitalized SCI patients with NAUTI are limited.

The results of our study revealed that the difference in resistance rates of all uropathogens between acute and chronic spinal cord injury patients was statistically significant (p<0.05). In general, the lowest resistance rates were seen in chronic spinal cord injury patients, while the highest resistance rates against most of the antibiotics tested were seen in acute spinal cord injury patients. We think that this finding might be caused by resistant flora in our acute care unit.

The resistance rates were lower for amikacin, gentamicin, and imipenem in common uropathogens in both acute and chronic SCI patients. Amikacin and gentamicin are not commonly used antibiotics because of their potential nephrotoxicity, which might be a cause for this result.

Previous studies have focused on the antibiotic resistance of P. aeruginosa (15-19) or K. pneumoniae in patients with SCI (16,19-22). Although Klebsiella was the second most common uropathogen seen in our SCI patients, its distribution was not significantly different between acute and chronic patients. We could not be sure that this was because of the colonization described in the studies above.

The increase in fluoroquinolone-resistant E. coli infections in patients with SCI is frightening. It was first pointed out by Canavati et al. (23) in a rehabilitation setting in the late 1990s. The resistance rate reported was 5.9% at that time, and it reached 70% in our findings. We believe that this increase in fluoroquinolone-resistant E. coli infections might be because of their common use in general practice.

In the present study, the incidence rate of HAIs was 7.2 per 1000 patient-days. The most common HAIs were UTIs, and the incidence rate of UTIs was 4.8 per 1000 patient-days. According to the data on the incidence rate, our study showed consistent results with the literature. When the results of this study were assessed in terms of the method of bladder emptying, we found out that the susceptibility rates for E. coli were very low in both acute and chronic SCI patients using Foley catheters. Fortunately, the number of patients using indwelling catheters was lower. Although the resistance rates for E. coli were not so bad in SCI patients using CIC, the resistance rates were higher than 50% for most of the uropathogens.

Conclusion

The results that we obtained from this study reveal a blunt truth-that the treatment of NAUTIs will be a great challenge in near future. Although this study has some limitations because of its retrospective nature, such as the lack of data on risk factors, the picture presented here may give rehabilitation specialists important clues for future studies.

DOI: 10.5152/tftrd.2014.31032

Ethics Committee Approval: Ethics committee approval was received for this study from the ethics committee of Gulhane Military Medical Academy.

Informed Consent: Informed consent was not obtained because of the retrospective design of the study.

Peer-review: Externally peer-reviewed.

Author Contributions: Concept--B.Y.; Design--B.Y., F.Y.; Supervision--B.Y.; Funding--F.Y., E.A.; Materials--F.Y.; Data Collection and/or Processing--F.Y., B.Y., E.A.; Analysis and/or Interpretation--F.Y., B.Y.; Literature Review--F.Y., B.Y., E.A.; Writer--F.Y., B.Y.; Critical Review--B.Y.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study has received no financial support.

Hasta Onami: Arastirma retrospektif oldugundan onam alinmamistir.

Hakem degerlendirmesi: Dis bagimsiz.

Yazar Katkilari: Fikir--B.Y.; Tasarim--B.Y., F.Y.; Denetleme--B.Y.; Kaynaklar F.Y., E.A.; Malzemeler--F.Y.; Veri toplanmasi ve/veya islemesi--F.Y., B.Y., E.A.; Analiz ve/veya yorum--F.Y., B.Y.; Literatur taramasi--F.Y., B.Y., E.A.; Yaziyi yazan--F.Y., B.Y.; Elestirel Inceleme--B.Y.

Cikar Catismasi: Yazarlar cikar catismasi bildirmemislerdir.

Finansal Destek: Yazarlar bu calisma icin finansal destek almadiklarini beyan etmislerdir.

Etik Komite Onayi: Bu calisma icin etik komite onayi Gulhane Askeri Tip Akademisi'nden alinmistir.

References

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(2.) Myolette JM, Graham R, Kahler L, Young L, Goodnough S. Impact of nosocomial infection on length of stay and functional improvement among patients admitted to an acute rehabilitation unit. Infect Control Hosp Epidemiol 2011;22:83-7. [CrossRef]

(3.) Hill TC, Baverstock R, Carlson KV, Estey EP, Gray GJ, Hill DC, et al. Best practices for the treatment and prevention of urinary tract infection in the spinal cord injured population: The Alberta context. Can Urol Assoc J 2013;7:122-30.

(4.) Girard R, Mazoyer MA, Plauchu MM, Rode G. High prevalence of nosocomial infections in rehabilitation units accounted for by urinary tract infections in patients with spinal cord injury. J Hosp Infect 2006;62:473-9. [CrossRef]

(5.) Cardenas DD, Mayo ME. Management of Bladder Dysfunction. In: Braddom RL, editor. Physical medicine and rehabilitation. 3rd ed. Philadelphia, CN: Saunder & Elsevier; 2007.p.617-37.

(6.) Deresinski SC, Perkash I. Urinary tract infections in male spinal cord injured patients. Part two: diagnostic value of symptoms and of quantitative urinalysis. J Am Paraplegia Soc 1985;8:7-10.

(7.) Bryce TN, Ragnarsson KT, Stein AB. Spinal Cord Injury. In: Braddom RL, editor. Physical medicine and rehabilitation. 3rd ed. Philadelphia, CN: Saunder&Elsevier; 2007.p.1285-351.

(8.) Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309-32. [CrossRef]

(9.) National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004;32:470-85. [CrossRef]

(10.) Rosenthal VD, Guzman S, Orellano PW. Nosocomial infections in medical-surgical intensive care units in Argentina: attributable mortality and length of stay. Am J Infect Control 2003;31:291-5. [CrossRef]

(11.) Edwards JR, Peterson KD, Andrus ML, Tolson J, Goulding J, Dudeck M, et al. National Healthcare Safety Network (NHSN) Report, data summary for 2006, issued June 2007. Am J Infect Control 2006;35:290-301. [CrossRef]

(12.) Tambyah PA. Catheter-associated urinary tract infections: diagnosis and prophylaxis. Int J Antimicrob Agents 2004;24:44-8. [CrossRef]

(13.) Esclarin de Ruz A, Garcia Leoniu E, Herruzo Cabrera R. Epidemiology and risk factors for urinary tract infection in patients with spinal cord injury. J Urol 2000;164:1285-9. [CrossRef]

(14.) Tambyah PA, Oon J. Catheter-associated urinary tract infection. Curr Opin Infect Dis 2012;25:365-70. [CrossRef]

(15.) Montgomerie JZ, Morrow JW. Long-term pseudomonas colonization in spinal cord injury patients. Am J Epidemiol 1980;112:50817.

(16.) Gilmore DS, Aeilts GD, Alldis BA, Bruce SK, Jimenez EM, Schick DG, et al. Effects of bathing on Pseudomonas and Klebsiella colonization in patients with spinal cord injuries. J Clin Microbiol 1981;14:404-7.

(17.) Gilmore DS, Bruce SK, Jimenez EM, Schick DG, Morrow JW, Montgomerie JZ. Pseudomonas aeruginosa colonization in patients with spinal cord injury. J Clin Microbiol 1982;16:856-60.

(18.) Shlaes DM, Currie CA, Rotter G, Eanes M, Floyd R. Epidemiology of gentamicin-resistant, gram-negative bacillary colonization in a spinal cord injury unit. J Clin Microbiol 1983;18:227-35.

(19.) Montgomerie JZ, Madorsky JGB, Gilmore DS, Graham IE. Colonization of patients with spinal cord injury with Pseudomonas aeruginosa and Klebsiella pneumoniae at different institutions. J Hosp Infect 1987;10:198-203. [CrossRef]

(20.) Montgomerie JZ, Gilmore DS, Ashley MA, Schick DG, Jimenez EM. Longterm colonization of spinal cord injury patients with Klebsiella pneumoniae. J Clin Microbiol 1989;27:1613-6.

(21.) Montgomerie JZ, John JF, Atkins LM, Gilmore DS, Ashley AS. Increased frequency of large R-plasmids in Klebsiella pneumoniae colonizing patients with spinal cord injury. Diagn Microbiol Infect Dis 1993;16:25-9. [CrossRef]

(22.) Thompson W, Romance L, Bialkowska-Hobrazanska H, Rennie RP, Ashton F, Nicolle LE. Klebsiella pneumoniae infection on a rehabilitation unit:comparison of epidemiologic typing methods. Infect Control Hosp Epidemiol 1993;14:203-10. [CrossRef]

(23.) Canawati HN, el-Farra R, Seymour J, Shimashita J, Dunn D, Montgomerie JZ. Ciprofloxacin-resistant Escherichia coli emerging in a rehabilitation medical center. Diagn Microbiol Infect Dis 1997;29:133-8. [CrossRef]

Bilge YILMAZ, Ferdi YAVUZ, Emre ADIGUZEL Department of Physical Medicine and Rehabilitation, Turkish Armed Forces Rehabilitation Center, Gulhane Military Medical Academy, Ankara, Turkey

Address for Correspondence / Yazisma Adresi: Bilge Yilmaz, MD, Department of Physical Medicine and Rehabilitation, Turkish Armed Forces

Rehabilitation Center, Gulhane Military Medical Academy, Ankara, Turkey. Phone: +90 312 291 16 00 E-mail: bilgeyilmaztr@hotmail.com

Received/Gelis Tarihi: April/Nisan 2013 Accepted/Kabul Tarihi: February/Subat 2014
Table 1. The demographic and clinical characteristics of the
patients

Age, mean [+ or -] SD             35.47 [+ or -] 18.59 years
LOS for hospitalization            37.8 [+ or -] 9.8 days
HAI rate per 1000 patient-days            7.2

                                      n            %
Time of injury
  Acute SCI                          117          42.4
  Chronic SCI                        159          57.6
Male                                 195          70.6
Tetraplegia                           94          34.1
ASIA-A                               151          54.7
ASIA-B                                42          15.2
ASIA-C                                38          13.8
ASIA-D                                39          14.1
ASIA-E                                6           2.2
CIC                                  207           75
IC                                    41          14.9
CF                                    28          10.1

SD: standard deviation; CIC: clean intermittent catheterization; IC:
indwelling catheterization; CF: catheter-free; LOS: length of stay;
HAI: hospital-acquired infection

Table 2. The distribution of NAUTIs

Pathogens                          Spinal Cord Injury Patients

                         Acute period               Chronic period
                     (6 months after injury)   (6 months-2 years after
                                                       injury)

                    ASB      SUTI    Total     ASB      SUTI    Total

Acinetobacter        3        2        5        7        4        11
E. coli              18       22       40       32       31       63
E. coli ESBL(+)      12       --       12       11       5        16
Enterococ            2        5        7        6        5        11
Enterobacter         --       --       --       10       1        11
Klebsiella           25       2        27       20       7        27
Proteus              3        5        8        6        6        12
Pseudomonas          9        9        18       2        6        8
Total                72       45      117       94       65      159

ASB: asymptomatic bacteriuria; SUTI: symptomatic urinary tract
infection; ESBL: extended spectrum beta-lactamase; NAUTIs: nosocomial
urinary tract infections

Table 3. The comparison of the microorganisms' resistance rates
against antibiotics between acute and chronic spinal cord injury
patients

                    Amp+Sulbac    Amoxicillin    Amikacin

E. coli                100%           64%           34%
Klebsiella sp.         100%           72%           20%
Pseudomonas            100%           93%           8%
E. coli                72%            55%           15%
Klebsiella sp.         91%            55%           14%
ESBL(+) E. coli        100%           100%          50%

                    Amp+Sulbac     Gentamicin    Imipenem

E. coli                100%           24%          NR *
Klebsiella sp.         100%           34%           NR
Pseudomonas            100%           58%           36%
E. coli                72%            30%           NR
Klebsiella sp.         91%            22%           5%
ESBL(+) E. coli        100%           33%           NR

                    Amp+Sulbac    Levofloxacin   Norfloxacin

E. coli                100%           67%            64%
Klebsiella sp.         100%           67%            72%
Pseudomonas            100%           58%            72%
E. coli                72%            55%            60%
Klebsiella sp.         91%            40%            45%
ESBL(+) E. coli        100%           92%            100%

                    Amp+Sulbac    Ciprofloxacin    Doxycycline

E. coli                100%            67%             87%
Klebsiella sp.         100%            67%             62%
Pseudomonas            100%            65%             80%
E. coli                72%             58%             72%
Klebsiella sp.         91%             45%             55%
ESBL(+) E. coli        100%            100%            92%

                    Amp+Sulbac    TMP-SMX

E. coli                100%         64%
Klebsiella sp.         100%         72%
Pseudomonas            100%          NR
E. coli                72%          54%
Klebsiella sp.         91%          25%
ESBL(+) E. coli        100%         60%

* NR: No resistance

Table 4. Relationship between the drainage methods and NAUTI

          Indwelling     Clean intermittent    Catheter-free     p *
           catheter        catheterization        voiding

SUTI     21/41 (52%)        76/207 (37%)         7/28 (25%)     0.036
ASB      20/41 (48%)        131/207 (63%)       21/28 (75%)     0.028

*: a One-way ANOVA test was used. ASB: asymptomatic bacteriuria; SUTI:
symptomatic urinary tract infection; NAUTI: nosocomial urinary tract
infection

Table 5. Comparison of the rates of NAUTI between acute and
chronic spinal cord injury patients

         Acute Spinal     Chronic Spinal
          Cord Injury       Cord Injury
           Patients          Patients        p *

ASB      72/117 (61%)      94/159 (59%)     0.45
SUTI     45/117 (39%)      65/159 (41%)     0.75

*: independent-samples t-test was used. ASB: asymptomatic bacteriuria;
SUTI: symptomatic urinary tract infection; NAUTI: nosocomial urinary
tract infection
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Title Annotation:Original Article/Orijinal Makale
Author:Yilmaz, Bilge; Yavuz, Ferdi; Adiguzel, Emre
Publication:Turkish Journal of Physical Medicine and Rehabilitation
Article Type:Report
Geographic Code:7TURK
Date:Dec 1, 2014
Words:3704
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