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R. Tariq, D. Pardi, P. Tosh, R. Walker, R. Razonable, S. Khanna (2017)
Fecal Microbiota Transplantation for Recurrent Clostridium difficile Infection Reduces Recurrent Urinary Tract Infection FrequencyClinical Infectious Diseases, 65
Kelly (2016)
Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection: a randomized trialAnn Intern Med, 165
J. Stalenhoef, E. Terveer, C. Knetsch, P. Hof, I. Vlasveld, J. Keller, L. Visser, E. Kuijper (2017)
Fecal Microbiota Transfer for Multidrug-Resistant Gram-Negatives: A Clinical Success Combined With Microbiological FailureOpen Forum Infectious Diseases, 4
N. Crum‐Cianflone, Eva Sullivan, G. Ballon-Landa (2015)
Fecal Microbiota Transplantation and Successful Resolution of Multidrug-Resistant-Organism ColonizationJournal of Clinical Microbiology, 53
A. Freedman, S. Eppes (2014)
1805Use of Stool Transplant to Clear Fecal Colonization with Carbapenem-Resistant Enterobacteraciae (CRE): Proof of ConceptOpen Forum Infectious Diseases, 1
Bilinski (2017)
Fecal microbiota transplantation in patients with blood disorders inhibits gut colonization with antibiotic-resistant bacteria: results of a prospective, single-center studyClin Inect Dis, 65
A. Halpin, L. McDonald (2016)
Editorial Commentary: The Dawning of Microbiome Remediation for Addressing Antibiotic Resistance.Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 62 12
Joshua Stripling, Ranjit Kumar, J. Baddley, A. Nellore, P. Dixon, Donna Howard, T. Ptacek, E. Lefkowitz, Jose Tallaj, William Benjamin, Casey Morrow, J. Rodriguez (2015)
Loss of Vancomycin-Resistant Enterococcus Fecal Dominance in an Organ Transplant Patient With Clostridium difficile Colitis After Fecal Microbiota TransplantOpen Forum Infectious Diseases, 2
J. Grainger (2018)
Faculty Opinions recommendation of Effect of Fecal Microbiota Transplantation on Recurrence in Multiply Recurrent Clostridium difficile Infection: A Randomized Trial.Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature
J. Biliński, P. Grzesiowski, N. Sørensen, K. Mądry, J. Muszyński, Katarzyna Robak, M. Wróblewska, T. Dzieciątkowski, G. Dulny, J. Dwilewicz-Trojaczek, W. Wiktor-Jedrzejczak, G. Basak (2017)
Fecal Microbiota Transplantation in Patients With Blood Disorders Inhibits Gut Colonization With Antibiotic-Resistant Bacteria: Results of a Prospective, Single-Center StudyClinical Infectious Diseases, 65
S. García-Fernández, M. Morosini, M. Cobo, J. Foruny, A. López-Sanromán, J. Cobo, J. Romero, R. Cantón, R. Campo (2016)
Gut eradication of VIM-1 producing ST9 Klebsiella oxytoca after fecal microbiota transplantation for diarrhea caused by a Clostridium difficile hypervirulent R027 strain.Diagnostic microbiology and infectious disease, 86 4
Ramandeep Singh, E. Nood, Max Nieuwdorp, B. Dam, I. Berge, S. Geerlings, F. Bemelman (2014)
Donor feces infusion for eradication of Extended Spectrum beta-Lactamase producing Escherichia coli in a patient with end stage renal disease.Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases, 20 11
Open Forum Infectious Diseases ID CASE increasing antimicrobial resistance (Figure 1, Table 1). Cultures Fecal Microbiota Transplant for grew E. coli, Enterobacter cloacae, Citrobacter amalonaticus, Refractory Clostridium dic ffi ile Proteus vulgaris, Enterococcus faecium, Providencia rettgeri, Infection Interrupts 25-Year History of Morganella morganii, ESBL K. pneumoniae, and ESBL K. oxy- toca. Antibiotics used to treat these isolates included nitro- Recurrent Urinary Tract Infections furantoin, cephalexin, cefuroxime, ceftriaxone, levofloxacin, 1 2,3 2 4 Tiffany Wang, Colleen S. Kraft, Michael H. Woodworth, Tanvi Dhere, and 2 doxycycline, trimethoprim-sulfamethoxazole, vancomycin, fos- Molly E. Eaton 2 4 fomycin, piperacillin-tazobactam, meropenem, and ertapenem. Division of Infectious Diseases and Division of Digestive Diseases, Department of Medicine, 1 3 Emory University School of Medicine, Atlanta, Georgia; Department of Pathology and Across 20 presentations from November 2013 to October Laboratory Medicine, Emory University Hospital, Atlanta, Georgia 2015, symptoms included urinary urgency and worsened in- continence 11 times, generalized fatigue (without urgency or Keywords. Clostridium difficile infection; fecal micro- incontinence) 5 times, both sets of symptoms 3 times, and dys- biota transplant; multidrug resistant organisms; urinary tract uria with suprapubic tenderness once. Though her symptoms infection. were somewhat atypical of cystitis, she was treated for urinary infection given significant pyuria on urinalyses, neurologic changes, and limited ability to review systems with her comor- CASE bidities. Symptoms prompted each urinalysis and urine culture, An 83-year-old female with history of cerebral meningioma, and all antibiotics were prescribed according to susceptibility multiple spinal hemangiomas with postresection lower ex- results. No antibiotics were prescribed without symptoms and a tremity weakness, urinary incontinence, and 25-year history positive urine culture. Except for 2 doses of fosfomycin, which of recurrent urinary tract infections (UTIs) presented to our she could not obtain, and 1 course of levofloxacin interrupted infectious disease clinic in December 2010 with 5 UTIs over for rash, all antibiotic courses were completed. Extensive non- 4 months. Symptoms abated for only a week between antibiotic antibiotic UTI prevention was attempted from 2010 to 2014, courses. Allergies to ciprofloxacin, nitrofurantoin, and sulfa including solifenacin succinate, vaginal estrogen, increased drugs limited treatment options. Prophylactic cephalexin gave uid in fl take, scheduled voiding, stool soen ft ers, methenamine temporary relief only. From October 2013 to February 2014, she hippurate, and vitamin C. was treated with 5 antibiotic courses for UTIs. Two urine cul- In March 2015, she developed diarrhea, tested positive for tures grew extended-spectrum β-lactamase (ESBL)-producing C. difficile, and completed 16 days of metronidazole. The fol- multidrug-resistant (MDR) Escherichia coli. Another culture in lowing 6 months, her symptomatic UTIs (with bacteriuria and September grew a different MDR E. coli. pyuria) continued but with decreased symptom-free intervals In October and November 2014, she had 3 ED presentations between infections from weeks to days. Aer ep ft isodes with with MDR E. coli UTIs, with signs of sepsis on her third presen- MDR K. oxytoca and K. pneumoniae were treated with intra- tation. Cystoscopy with pyelograms revealed no fistula or nidus venous ertapenem, a surgical port was placed in anticipation of of infection. Subsequently, multiple symptomatic episodes further parenteral therapy. of cystitis yielded 16 positive urine cultures demonstrating In May 2015, a C. difficile relapse was treated with oral vanco- mycin with prolonged taper. Aer a ft nother C. difficile relapse in October, fecal microbiota transplantation (FMT) was planned. Antibiotics were discontinued 48 hours prior. Stool from an un- Received 20 November 2017; editorial decision 5 January 2018; accepted 12 January 2018. related donor who underwent routine serological and stool test- Correspondence: C. S. Kraft, MD, MSc, Emory University Hospital, 1364 Clifton Rd, NE, Suite ing was delivered via colonoscopy without complications. Nine F145, Atlanta, GA 30322 (colleen.kraft@emory.edu). days post-FMT, she had complete resolution of all UTI and Open Forum Infectious Diseases © The Author(s) 2018. Published by Oxford University Press on behalf of Infectious Diseases Clostridium difficile infection (CDI) symptoms. At 25 months Society of America. This is an Open Access article distributed under the terms of the Creative post-FMT, there have been no recurrences. Of 2 urinalyses Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/ by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any obtained since FMT for symptoms of increased fatigue, neither medium, provided the original work is not altered or transformed in any way, and that the work has indicated bacteriuria or pyuria, and she has not been pre- is properly cited. For commercial re-use, please contact journals.permissions@oup.com DOI: 10.1093/ofid/ofy016 scribed antibiotics. ID CASE • OFID • 1 Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofy016/4808593 by Ed 'DeepDyve' Gillespie user on 16 March 2018 FMT PRESENT MDR K. PNEUMONIAE M. MORGANII M. MORGANII MDR. K. OXYTOCA P. RETTGERI P. VULGARIS K. PNEUMONIAE 4 5 K. PNEUMONIAE , E. CLOACAE 1 2 MDR E. COLI MDR E. COLI 1 3 MDR E. COLI E. COLI C. AMALONATICUS 12/18/2013 9/1/2017 C. AMALONATICUS E. FAECIUM 11 12 P. VULGARIS , P. VULGARIS K. PNEUMONIAE MDR. K. OXYTOCA MDR. K. PNEUMONIAE 16 17 K. PNEUMONIAE , M. MORGANII Figure 1. (1) Extended-spectrum β-lactamase (ESBL) Escherichia coli, resistant to ampicillin, ampicillin/sulbactam, aztreonam, cefazolin, cefepime, ceftazidime, ceftriax- one, cefuroxime, gentamicin, levofloxacin, piperacillin/tazobactam, tobramycin, and trimethoprim/sulfa. (2) ESBL Escherichia coli, resistant to ampicillin, ampicillin/sulbac- tam, aztreonam, cefazolin, cefepime, ceftazidime, ceftriaxone, cefuroxime, levofloxacin, piperacillin/tazobactam, tetracycline, and trimethoprim/sulfa. (3) ESBL Escherichia coli, resistant to ampicillin. (4) Klebsiella pneumoniae, resistant to ampicillin; intermediate resistance to cefoxitin. (5) Enterobacter cloacae, resistant to ampicillin, ampicillin/ sulbactam, cefazolin, cefoxitin, and nitrofurantoin; intermediate resistance to cefuroxime. (6) Citrobacter amalonaticus, resistant to ampicillin, ampicillin/sulbactam, cefa- zolin, ceftriaxone, cefuroxime, levofloxacin, tetracycline, and trimethoprim/sulfa; intermediate resistance to aztreonam. (7) Klebsiella pneumoniae, resistant to ampicillin. (8) Proteus vulgaris, resistant to ampicillin, ampicillin/sulbactam, cefazolin, ceftriaxone, cefuroxime, nitrofurantoin, and tetracycline. (9) Enterococcus faecium, resistant to ampicillin and penicillin. (10) Providencia rettgeri, resistant to ampicillin, ampicillin/sulbactam, cefazolin, and nitrofurantoin; intermediate resistance to tetracycline. (11) Proteus vulgaris, resistant to ampicillin, ampicillin/sulbactam, cefazolin, cefuroxime, nitrofurantoin, tetracycline; intermediate resistance to aztreonam and ceftriaxone. (12) Proteus vulgaris, resistant to ampicillin, ampicillin/sulbactam, cefazolin, cefuroxime, nitrofurantoin, and tetracycline. (13) ESBL Klebsiella oxytoca, resistant to ampicillin, ampicillin/sulbactam, aztreonam, cefazolin, cefepime, ceftazidime, ceftriaxone, cefuroxime, gentamicin, piperacillin/tazobactam, tetracycline, tobramycin, and trimethoprim/ sulfa; intermediate resistance to levofloxacin. (14) Morganella morganii, resistant to ampicillin, ampicillin/sulbactam, cefazolin, cefuroxime, nitrofurantoin, and tetracycline; intermediate resistance to cefoxitin. (15) ESBL Klebsiella pneumoniae, resistant to ampicillin, ampicillin/sulbactam, aztreonam, cefazolin, cefepime, ceftazidime, ceftriax- one, cefuroxime, nitrofurantoin, piperacillin/tazobactam, tetracycline, tobramycin, and trimethoprim/sulfa. (16) Klebsiella pneumoniae, resistant to ampicillin, ampicillin/ sulbactam, nitrofurantoin, tetracycline, tobramycin, and trimethoprim/sulfa. (17) Morganella morganii, resistant to ampicillin, ampicillin/sulbactam, cefazolin, ceftazidime, cefuroxime, and tetracycline; intermediate resistance to cefoxitin and nitrofurantoin. Abbreviations: FMT, fecal microbiota transplantation; MDR, multidrug-resistant. DISCUSSION MDR P. aeruginosa, recurrent renal allograft pyelonephritis with ESBL E. coli, and carbapenemase-producing K. pneumo- FMT is safe and effective for recurrent CDI [1]. It has also niae osteomyelitis and sepsis [8–10]. emerged as potential therapy for decolonization of MDR Here, we describe resolution of recurrent symptomatic UTI organisms (MDROs), offering a safe and possibly cost-effective aer FMT f ft or RCDI in a woman who had been treated with strategy for tackling antibiotic resistance beyond current nearly continuous antibiotics in the preceding 2 years. As com- efforts to improve antibiotic stewardship and prevent infec- mon sources of morbidity, UTIs make significant contributions tion [2]. toward antibiotic resistance and antibiotic-associated infec- Intestinal MDRO decolonization aer FMT h ft as been tions. Though FMT may have changed provider behavior, post- described in case reports, retrospective studies, and a pro- FMT urine cultures were not indicated in the absence of further spective single-center study [3–5]. However, MDRO eradica- symptoms. Pre- or post-FMT stool cultures were not obtained tion from nongastrointestinal body sites is not as well described for microbiota analysis. However, our case adds evidence for [6]. A recent review found that FMT for recurrent Clostridium FMT as a safe and potentially efficacious intervention for the difficile infection (RCDI) was associated with decreased UTI prevention and treatment of infections outside of C. difficile, frequency and improved antibiotic susceptibility profiles [7]. suggesting a possible role for FMT in combatting antimicrobial Case reports have also described interruption of recurrent UTIs resistance. with a Verona integron-encoded metallo-β-lactamase-positive 2 • OFID • ID CASE Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofy016/4808593 by Ed 'DeepDyve' Gillespie user on 16 March 2018 ID CASE • OFID • 3 Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofy016/4808593 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Table 1. Antimicrobial Susceptibility Patterns of Urine Isolates 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 MDR ESBL ESBL Klebsiella Klebsiella MDR Klebsiella Klebsiella Escherichia Escherichia Escherichia pneumo- Enterobacter Citrobacter pneumo- Proteus Enterococcus Providencia Proteus Proteus Klebsiella Morganella pneumo- pneumo- Morganella Antibiotic coli coli coli niae cloacae amalonaticus niae vulgaris faecium rettgeri vulgaris vulgaris oxytoca morganii niae niae morganii Amikacin S S S S S S S S S S S S S S S S Ampicillin R R R R R R R R R R R R R R R R R Amp/Sul R R S S R R S R R R R R R R R R Aztreonam R R S S S I S S S I S R S R S S Cefazolin R R S S R R S R R R R R R R S R Cefepime R R S S S S S S S S S R S R S S Cefoxitin S I R S S S S S S I R S I Ceftazidime R R S S S S S S S S S R S R S R Ceftriaxone R R S S S R S R S I S R S R S S Cefuroxime R R S S I R S R S R R R R R S R Colistin a a Fosfomycin S Gentamicin R S S S S S S S S S S R S S S S Levofloxacin R R S S S R S S S S S I S S S S Meropenem S S S S S S S S S S S Nitrofurantoin S S S S R S S R S R R R S R R R I Penicillin R Pip/Tazo R R S S S S S S S S S R S R S S Tetracycline S R S S S R S R S I R R R R R R R Tigecycline S Tobramycin R S S S S S S S S S S R S R R S Trim/Sulfa R R S S S R S S S S S R S R R S Vancomycin S Abbreviations: Amp/Sul, ampicillin/sulbactam; Pip/Tazo, piperacillin/tazobactam; Trim/Sulfa, trimethoprim/sulfamethoxazole. Minimum inhibitory concentration (MIC) >1024 ug/mL. MIC 0.125 ug/mL. Acknowledgements 5. Stripling J, Kumar R, Baddley JW, et al. Loss of vancomycin-resistant entero- coccus fecal dominance in an organ transplant patient with Clostridium difficile Potential coni fl cts of interest. The authors have no conflicts of interest. colitis after fecal microbiota transplant. Open Forum Infect Dis 2015; 2:ofv078. 6. Crum-Cianflone NF, Sullivan E, Ballon-Landa G. Fecal microbiota transplanta- References tion and successful resolution of multidrug-resistant-organism colonization. J 1. Halpin AL, McDonald LC. Editorial commentary: the dawning of microbiome Clin Microbiol 2015; 53:1986–9. remediation for addressing antibiotic resistance. Clin Infect Dis 2016; 62:1487–8. 7. Tariq R, Pardi DS, Tosh PK, et al. Fecal microbiota transplantation for recurrent 2. Kelly CR, Khoruts A, Staley C, et al. Effect of fecal microbiota transplantation Clostridium difficile infection reduces recurrent urinary tract infection frequency. on recurrence in multiply recurrent Clostridium difficile infection: a randomized Clin Infect Dis 2017; 65:1745–7. trial. Ann Intern Med 2016; 165:609–16. 8. Stalenhoef JE, Terveer EM, Knetsch CW, et al. Fecal microbiota transfer for mul- 3. García-Fernández S, Morosini MI, Cobo M, et al. Gut eradication of VIM-1 tidrug-resistant gram-negatives: a clinical success combined with microbiological producing ST9 Klebsiella oxytoca after fecal microbiota transplantation for diar- failure. Open Forum Infect Dis 2017; 4:ofx047. rhea caused by a Clostridium difficile hypervirulent R027 strain. Diagn Microbiol 9. Singh R, van Nood E, Nieuwdorp M, et al. Donor feces infusion for eradication Infect Dis 2016; 86:470–1. of extended spectrum beta-lactamase producing Escherichia coli in a patient with 4. Bilinski J, Grzesiowski P, Sorensen N, et al. Fecal microbiota transplantation in end stage renal disease. Clin Microbiol Infect 2014; 20:O977–8. patients with blood disorders inhibits gut colonization with antibiotic-resist- 10. Freedman A, Eppes S. Use of stool transplant to clear fecal colonization with ant bacteria: results of a prospective, single-center study. Clin Infect Dis 2017; carbapenem-resistant enterobacteriaceae (CRE): proof of concept. Open Forum 65:364–70. Infect Dis 2017; 1:ofu051. 4 • OFID • ID CASE Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofy016/4808593 by Ed 'DeepDyve' Gillespie user on 16 March 2018
Open Forum Infectious Diseases – Oxford University Press
Published: Feb 1, 2018
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