The importance of the bacterial spectrum in the clinical diagnostics and management of patients with spontaneous pyogenic spondylodiscitis and isolated spinal epidural empyema: a 20-year cohort study at a single spine center.

Bacterial spectrum Isolated spinal epidural empyema Osteomyelitis Spondylodiscitis Staphylococcus aureus

Journal

BMC infectious diseases
ISSN: 1471-2334
Titre abrégé: BMC Infect Dis
Pays: England
ID NLM: 100968551

Informations de publication

Date de publication:
02 Jan 2024
Historique:
received: 12 08 2023
accepted: 22 12 2023
medline: 4 1 2024
pubmed: 4 1 2024
entrez: 3 1 2024
Statut: epublish

Résumé

Personalized clinical management of spondylodiscitis (SD) and isolated spinal epidural empyema (ISEE) is challenging due to limited evidence of microbiologic findings and their clinical impact during the clinical course of the disease. We aimed to characterize clinico-microbiological and imaging phenotypes of SD and ISEE to provide useful insights that could improve outcomes and potentially modify guidelines. We performed chart review and collected data on the following parameters: bacterial antibiogram-resistogram, type of primary spinal infection, location of spinal infection, source of infection, method of detection, clinical complications (sepsis, septic embolism, and endocarditis), length of hospital and intensive care unit (ICU) stay, relapse rate, and disease-related mortality in patients with proven pyogenic SD and ISEE treated surgically in a university hospital in Germany between 2002 and 2022. We included data from 187 patients (125 SD, 66.8% and 62 ISEE, 33.2%). Gram-positive bacteria (GPB) were overall more frequently detected than gram-negative bacteria (GNB) (GPB: 162, 86.6% vs. GNB: 25, 13.4%, p < 0.001). Infective endocarditis was caused only by GPB (GPB: 23, 16.5% vs. GNB: 0, 0.0%, p = 0.046). Methicillin-susceptible Staphylococcus aureus was the most frequently isolated strain (MSSA: n = 100, 53.5%), occurred more frequently in the cervical spine compared to other bacteria (OB) (MSSA: 41, 41.0% vs. OB: 18, 20.7%, p = 0.004) and was most frequently detected in patients with skin infection as the primary source of infection (MSSA: 26, 40.6% vs. OB: 11, 16.7%, p = 0.002). Streptococcus spp. and Enterococcus spp. (SE: n = 31, 16.6%) were more often regarded as the cause of endocarditis (SE: 8, 27.6% vs. OB: 15, 11.4%, p = 0.037) and were less frequently detected in intraoperative specimens (SE: 19, 61.3% vs. OB: 138, 88.5%, p < 0.001). Enterobacterales (E: n = 20, 10.7%) were identified more frequently in urinary tract infections (E: 9, 50.0% vs. OB: 4, 3.6%, p < 0.001). Coagulase-negative Staphylococci (CoNS: n = 20, 10.7%) were characterized by a lower prevalence of sepsis (CoNS: 4, 20.0% vs. OB: 90, 53.9%, p = 0.004) and were more frequently detected in intraoperative specimens (CoNS: 20, 100. 0% vs. OB: 137, 82.0%, p = 0.048). Moreover, CoNS-associated cases showed a shorter length of ICU stay (CoNS: 2 [1-18] days vs. OB: 6 [1-53] days, median [interquartile range], p = 0.037), and occurred more frequently due to foreign body-associated infections (CoNS: 8, 61.5% vs. OB: 15, 12.8%, p = 0.008). The presence of methicillin-resistant Staphylococcus aureus (MRSA) prolonged hospital stay by 56 [24-58] days and ICU stay by 16 [1-44] days, whereas patients with Pseudomonas aeruginosa spent only 20 [18-29] days in the hospital and no day in the ICU 0 [0-5] days. Our retrospective cohort study identified distinct bacterial-specific manifestations in pyogenic SD and ISEE regarding clinical course, neuroanatomic targets, method of pathogen detection, and sources of infection. The clinico-microbiological patterns varied depending on the specific pathogens.

Sections du résumé

BACKGROUND BACKGROUND
Personalized clinical management of spondylodiscitis (SD) and isolated spinal epidural empyema (ISEE) is challenging due to limited evidence of microbiologic findings and their clinical impact during the clinical course of the disease. We aimed to characterize clinico-microbiological and imaging phenotypes of SD and ISEE to provide useful insights that could improve outcomes and potentially modify guidelines.
METHODS METHODS
We performed chart review and collected data on the following parameters: bacterial antibiogram-resistogram, type of primary spinal infection, location of spinal infection, source of infection, method of detection, clinical complications (sepsis, septic embolism, and endocarditis), length of hospital and intensive care unit (ICU) stay, relapse rate, and disease-related mortality in patients with proven pyogenic SD and ISEE treated surgically in a university hospital in Germany between 2002 and 2022.
RESULTS RESULTS
We included data from 187 patients (125 SD, 66.8% and 62 ISEE, 33.2%). Gram-positive bacteria (GPB) were overall more frequently detected than gram-negative bacteria (GNB) (GPB: 162, 86.6% vs. GNB: 25, 13.4%, p < 0.001). Infective endocarditis was caused only by GPB (GPB: 23, 16.5% vs. GNB: 0, 0.0%, p = 0.046). Methicillin-susceptible Staphylococcus aureus was the most frequently isolated strain (MSSA: n = 100, 53.5%), occurred more frequently in the cervical spine compared to other bacteria (OB) (MSSA: 41, 41.0% vs. OB: 18, 20.7%, p = 0.004) and was most frequently detected in patients with skin infection as the primary source of infection (MSSA: 26, 40.6% vs. OB: 11, 16.7%, p = 0.002). Streptococcus spp. and Enterococcus spp. (SE: n = 31, 16.6%) were more often regarded as the cause of endocarditis (SE: 8, 27.6% vs. OB: 15, 11.4%, p = 0.037) and were less frequently detected in intraoperative specimens (SE: 19, 61.3% vs. OB: 138, 88.5%, p < 0.001). Enterobacterales (E: n = 20, 10.7%) were identified more frequently in urinary tract infections (E: 9, 50.0% vs. OB: 4, 3.6%, p < 0.001). Coagulase-negative Staphylococci (CoNS: n = 20, 10.7%) were characterized by a lower prevalence of sepsis (CoNS: 4, 20.0% vs. OB: 90, 53.9%, p = 0.004) and were more frequently detected in intraoperative specimens (CoNS: 20, 100. 0% vs. OB: 137, 82.0%, p = 0.048). Moreover, CoNS-associated cases showed a shorter length of ICU stay (CoNS: 2 [1-18] days vs. OB: 6 [1-53] days, median [interquartile range], p = 0.037), and occurred more frequently due to foreign body-associated infections (CoNS: 8, 61.5% vs. OB: 15, 12.8%, p = 0.008). The presence of methicillin-resistant Staphylococcus aureus (MRSA) prolonged hospital stay by 56 [24-58] days and ICU stay by 16 [1-44] days, whereas patients with Pseudomonas aeruginosa spent only 20 [18-29] days in the hospital and no day in the ICU 0 [0-5] days.
CONCLUSIONS CONCLUSIONS
Our retrospective cohort study identified distinct bacterial-specific manifestations in pyogenic SD and ISEE regarding clinical course, neuroanatomic targets, method of pathogen detection, and sources of infection. The clinico-microbiological patterns varied depending on the specific pathogens.

Identifiants

pubmed: 38166791
doi: 10.1186/s12879-023-08946-x
pii: 10.1186/s12879-023-08946-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

39

Informations de copyright

© 2023. The Author(s).

Références

Jevtic V. Vertebral Infection. Eur Radiol. 2004;14(Suppl 3):E43–52.
pubmed: 14749956
Khan IA, Vaccaro AR, Zlotolow DA. Management of vertebral diskitis and osteomyelitis. Orthopedics. 1999;22(8):758–65.
doi: 10.3928/0147-7447-19990801-07 pubmed: 10465488
Tali ET. Spinal Infections. Eur J Radiol. 2004;50(2):120–33.
doi: 10.1016/j.ejrad.2003.10.022 pubmed: 15081128
Alerhand S, Wood S, Long B, Koyfman A. The time-sensitive challenge of diagnosing spinal epidural abscess in the emergency department. Intern Emerg Med. 2017;12(8):1179–83.
doi: 10.1007/s11739-017-1718-5 pubmed: 28779448
Babic M, Simpfendorfer CS. Infections of the spine. Infect Dis Clin North Am. 2017;31(2):279–97.
doi: 10.1016/j.idc.2017.01.003 pubmed: 28366222
Davis DP, Wold RM, Patel RJ, Tran AJ, Tokhi RN, Chan TC, Vilke GM. The clinical presentation and impact of diagnostic delays on emergency department patients with spinal epidural abscess. J Emerg Med. 2004;26(3):285–91.
doi: 10.1016/j.jemermed.2003.11.013 pubmed: 15028325
Shroyer SR, Davis WT, April MD, Long B, Boys G, Mehta SG, Mercaldo SF. A clinical Prediction Tool for MRI in Emergency Department patients with spinal Infection. West J Emerg Med. 2021;22(5):1156–66.
doi: 10.5811/westjem.2021.5.52007 pubmed: 34546893 pmcid: 8463051
Grammatico L, Baron S, Rusch E, Lepage B, Surer N, Desenclos JC, Besnier JM. Epidemiology of vertebral osteomyelitis (VO) in France: analysis of hospital-discharge data 2002–2003. Epidemiol Infect. 2008;136(5):653–60.
doi: 10.1017/S0950268807008850 pubmed: 17568478
Krogsgaard MR, Wagn P, Bengtsson J. Epidemiology of acute vertebral osteomyelitis in Denmark: 137 cases in Denmark 1978–1982, compared to cases reported to the National Patient Register 1991–1993. Acta Orthop Scand. 1998;69(5):513–7.
doi: 10.3109/17453679808997789 pubmed: 9855235
Sapico FL, Montgomerie JZ. Pyogenic vertebral osteomyelitis: report of nine cases and review of the literature. Rev Infect Dis. 1979;1(5):754–76.
doi: 10.1093/clinids/1.5.754 pubmed: 542761
Herren C, Jung N, Pishnamaz M, Breuninger M, Siewe J, Sobottke R. Spondylodiscitis: diagnosis and treatment options. Dtsch Arztebl Int. 2017;114(51–52):875–82.
pubmed: 29321098 pmcid: 5769318
Stangenberg M, Mende KC, Mohme M, Kratzig T, Viezens L, Both A, Rohde H, Dreimann M. Influence of microbiological diagnosis on the clinical course of spondylodiscitis. Infection. 2021;49(5):1017–27.
doi: 10.1007/s15010-021-01642-5 pubmed: 34254283 pmcid: 8476479
Gouliouris T, Aliyu SH, Brown NM. Spondylodiscitis: update on diagnosis and management. J Antimicrob Chemother. 2010;65(Suppl 3):iii11–24.
pubmed: 20876624
Berbari EF, Kanj SS, Kowalski TJ, Darouiche RO, Widmer AF, Schmitt SK, Hendershot EF, Holtom PD, Huddleston PM 3rd, Petermann GW, et al. Executive Summary: 2015 Infectious Diseases Society of America (IDSA) Clinical Practice guidelines for the diagnosis and treatment of native vertebral osteomyelitis in adults. Clin Infect Dis. 2015;61(6):859–63.
doi: 10.1093/cid/civ633 pubmed: 26316526
Pola E, Taccari F, Autore G, Giovannenze F, Pambianco V, Cauda R, Maccauro G, Fantoni M. Multidisciplinary management of pyogenic spondylodiscitis: epidemiological and clinical features, prognostic factors and long-term outcomes in 207 patients. Eur Spine J. 2018;27(Suppl 2):229–36.
doi: 10.1007/s00586-018-5598-9 pubmed: 29667140
Sobottke R, Seifert H, Fatkenheuer G, Schmidt M, Gossmann A, Eysel P. Current diagnosis and treatment of spondylodiscitis. Dtsch Arztebl Int. 2008;105(10):181–7.
pubmed: 19629222 pmcid: 2696793
Appalanaidu N, Shafafy R, Gee C, Brogan K, Karmani S, Morassi G, Elsayed S. Predicting the need for surgical intervention in patients with spondylodiscitis: the Brighton Spondylodiscitis score (BSDS). Eur Spine J. 2019;28(4):751–61.
doi: 10.1007/s00586-018-5775-x pubmed: 30317386
Gentile L, Benazzo F, De Rosa F, Boriani S, Dallagiacoma G, Franceschetti G, Gaeta M, Cuzzocrea F. A systematic review: characteristics, Complications and treatment of spondylodiscitis. Eur Rev Med Pharmacol Sci. 2019;23(2 Suppl):117–28.
pubmed: 30977878
Loibl M, Stoyanov L, Doenitz C, Brawanski A, Wiggermann P, Krutsch W, Nerlich M, Oszwald M, Neumann C, Salzberger B, et al. Outcome-related co-factors in 105 cases of vertebral osteomyelitis in a tertiary care hospital. Infection. 2014;42(3):503–10.
doi: 10.1007/s15010-013-0582-0 pubmed: 24446233
Pola E, Autore G, Formica VM, Pambianco V, Colangelo D, Cauda R, Fantoni M. New classification for the treatment of pyogenic spondylodiscitis: validation study on a population of 250 patients with a follow-up of 2 years. Eur Spine J. 2017;26(Suppl 4):479–88.
doi: 10.1007/s00586-017-5043-5 pubmed: 28324216
Valancius K, Hansen ES, Hoy K, Helmig P, Niedermann B, Bunger C. Failure modes in Conservative and surgical management of infectious spondylodiscitis. Eur Spine J. 2013;22(8):1837–44.
doi: 10.1007/s00586-012-2614-3 pubmed: 23247861
Adogwa O, Karikari IO, Carr KR, Krucoff M, Ajay D, Fatemi P, Perez EL, Cheng JS, Bagley CA, Isaacs RE. Spontaneous spinal epidural abscess in patients 50 years of age and older: a 15-year institutional perspective and review of the literature: clinical article. J Neurosurg Spine. 2014;20(3):344–9.
doi: 10.3171/2013.11.SPINE13527 pubmed: 24359002
Donovan J, Skittrall JP, Moore T, Sargent C, Agranoff D, Llewelyn M. An ageing population and changing UK bacteraemia profile may affect the characteristics and microbiology of infective spondylodiscitis. J Infect. 2016;73(1):91–3.
doi: 10.1016/j.jinf.2016.04.005 pubmed: 27066877
Ghobrial GM, Franco D, Theofanis T, Margiotta PJ, Andrews E, Wilson JR, Harrop JS, Heller JE. Cervical spondylodiscitis: presentation, timing, and Surgical Management in 59 patients. World Neurosurg. 2017;103:664–70.
doi: 10.1016/j.wneu.2017.04.119 pubmed: 28457929
Shousha M, Heyde C, Boehm H. Cervical spondylodiscitis: change in clinical picture and operative management during the last two decades. A series of 50 patients and review of literature. Eur Spine J. 2015;24(3):571–6.
doi: 10.1007/s00586-014-3672-5 pubmed: 25432097
Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12(1):547–69.
doi: 10.1080/21505594.2021.1878688 pubmed: 33522395 pmcid: 7872022
Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, et al. Invasive methicillin-resistant Staphylococcus aureus Infections in the United States. JAMA. 2007;298(15):1763–71.
doi: 10.1001/jama.298.15.1763 pubmed: 17940231
Rasigade JP, Dumitrescu O, Lina G. New epidemiology of Staphylococcus aureus Infections. Clin Microbiol Infect. 2014;20(7):587–8.
doi: 10.1111/1469-0691.12718 pubmed: 24930666
Courjon J, Lemaignen A, Ghout I, Therby A, Belmatoug N, Dinh A, Gras G, Bernard L. Group DTSs: pyogenic vertebral osteomyelitis of the elderly: characteristics and outcomes. PLoS ONE. 2017;12(12):e0188470.
doi: 10.1371/journal.pone.0188470 pubmed: 29206837 pmcid: 5716588
Nolla JM, Ariza J, Gomez-Vaquero C, Fiter J, Bermejo J, Valverde J, Escofet DR, Gudiol F. Spontaneous pyogenic vertebral osteomyelitis in nondrug users. Semin Arthritis Rheum. 2002;31(4):271–8.
doi: 10.1053/sarh.2002.29492 pubmed: 11836660
Pigrau C, Almirante B, Flores X, Falco V, Rodriguez D, Gasser I, Villanueva C, Pahissa A. Spontaneous pyogenic vertebral osteomyelitis and endocarditis: incidence, risk factors, and outcome. Am J Med. 2005;118(11):1287.
doi: 10.1016/j.amjmed.2005.02.027 pubmed: 16271915
Namvar AE, Bastarahang S, Abbasi N, Ghehi GS, Farhadbakhtiarian S, Arezi P, Hosseini M, Baravati SZ, Jokar Z, Chermahin SG. Clinical characteristics of Staphylococcus epidermidis: a systematic review. GMS Hyg Infect Control. 2014;9(3):Doc23.
pubmed: 25285267 pmcid: 4184040
Jimenez-Mejias ME, de Dios Colmenero J, Sanchez-Lora FJ, Palomino-Nicas J, Reguera JM, de la Garcia J, Garcia-Ordonez MA, Pachon J. Postoperative spondylodiskitis: etiology, clinical findings, prognosis, and comparison with nonoperative pyogenic spondylodiskitis. Clin Infect Dis. 1999;29(2):339–45.
doi: 10.1086/520212 pubmed: 10476739
Legrand E, Flipo RM, Guggenbuhl P, Masson C, Maillefert JF, Soubrier M, Noel E, Saraux A, Di Fazano CS, Sibilia J, et al. Management of nontuberculous infectious discitis. Treatments used in 110 patients admitted to 12 teaching hospitals in France. Joint Bone Spine. 2001;68(6):504–9.
doi: 10.1016/S1297-319X(01)00315-3 pubmed: 11808988
Saeed K, Esposito S, Ascione T, Bassetti M, Bonnet E, Carnelutti A, Chan M, Lye DC, Cortes N, Dryden M, et al. Hot topics on vertebral osteomyelitis from the International Society of Antimicrobial Chemotherapy. Int J Antimicrob Agents. 2019;54(2):125–33.
doi: 10.1016/j.ijantimicag.2019.06.013 pubmed: 31202920
Bernard L, Dinh A, Ghout I, Simo D, Zeller V, Issartel B, Le Moing V, Belmatoug N, Lesprit P, Bru JP, et al. Antibiotic treatment for 6 weeks versus 12 weeks in patients with pyogenic vertebral osteomyelitis: an open-label, non-inferiority, randomised, controlled trial. Lancet. 2015;385(9971):875–82.
doi: 10.1016/S0140-6736(14)61233-2 pubmed: 25468170

Auteurs

Mido Max Hijazi (MM)

Department of Neurosurgery, Division of Spine Surgery, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany. mido.hijazi@ukdd.de.

Timo Siepmann (T)

Department of Neurology, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Ibrahim El-Battrawy (I)

Department of Cardiology, Bergmannsheil University Hospital, Ruhr University Bochum, Bürkle de la Camp-Platz 1, 44789, Bochum, Germany.

Percy Schröttner (P)

Institute for Clinical Chemistry and Laboratory Medicine, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.
Institute for Microbiology and Virology, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Dino Podlesek (D)

Department of Neurosurgery, Division of Spine Surgery, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Gabriele Schackert (G)

Department of Neurosurgery, Division of Spine Surgery, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Tareq A Juratli (TA)

Department of Neurosurgery, Division of Spine Surgery, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Ilker Y Eyüpoglu (IY)

Department of Neurosurgery, Division of Spine Surgery, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Andreas Filis (A)

Department of Neurosurgery, Division of Spine Surgery, Technische Universität Dresden, Faculty of Medicine, and University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany.

Classifications MeSH