Skip to main content

Advertisement

SpringerLink
Log in

Performance of two methods of carbapenem-resistant Enterobacterales surveillance on a kidney transplant ward: selective culture of and real-time PCR directly from rectal swabs

  • Original Paper
  • Published:
Infection Aims and scope Submit manuscript

Abstract

Background

Infection with carbapenem-resistant Enterobacterales (CRE) is associated with a high mortality rate in kidney transplant recipients, and colonization with CRE is one of the major risk factors for CRE infection. There is, therefore, a need to improve the capacity to detect colonization with CRE among inpatients.

Methods

In this prospective study, we compared the performance of real-time PCR for carbapenemase directly from rectal swabs with that of conventional CRE surveillance culture in all patients admitted to a kidney transplant ward between February 2019 and March 2020. Surveillance culture and real-time PCR were performed at admission and weekly until hospital discharge. Two perineum-rectal swabs were collected: one for culture and one for PCR.

Results

We collected 905 paired samples for CRE surveillance from 399 patients, of whom 347 (87.0%) were kidney transplant recipients and 52 were waiting list patients. CRE was detected by culture and/or PCR in 75 patients (18.8%). Positivity for CRE was identified by PCR in 62 (15.5%) of the 399 patients and by culture in 55 (13.8%); 20 (5.0%) of the patients tested positive only on PCR, and 13 (3.3%) tested positive only on culture. The most common carbapenemase and species were, respectively, blaKPC (in 85.5%) and Klebsiella pneumoniae (in 80.0%). Infection with CRE occurred in 21.6% of the colonized patients, those cases occurred only among kidney transplant recipients. None of the patients who tested negative on culture developed CRE infection.

Conclusion

In conclusion, the two methods are complementary and could be useful in a scenario of high CRE prevalence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2
Fig 3

Similar content being viewed by others

References

  1. Bartoletti M, Giannella M, Tedeschi S, Viale P. Multidrug-resistant bacterial infections in solid organ transplant candidates and recipients. Infect Dis Clin North Am. 2018;32:551–80.

    Article  PubMed  Google Scholar 

  2. Aguado JM, Silva JT, Fernández-Ruiz M, Cordero E, Fortún J, Gudiol C, Martínez-Martínez L, Vidal E, Almenar L, Almirante B, Cantón R, Carratalá J, Caston JJ, Cercenado E, Cervera C, Cisneros JM, Crespo-Leiro MG, Cuervas-Mons V, Elizalde-Fernández J, Fariñas MC, Gavaldà J, Goyanes MJ, Gutiérrez-Gutiérrez B, Hernández D, Len O, López-Andujar R, López-Medrano F, Martín-Dávila P, Montejo M, Moreno A, Oliver A, Pascual A, Pérez-Nadales E, Román-Broto A, San-Juan R, Serón D, Solé-Jover A, Valerio M, Muñoz P, Torre-Cisneros J. Management of multidrug resistant gram-negative bacilli infections in solid organ transplant recipients: SET/GESITRA-SEIMC/REIPI recommendations. Transplant Rev. 2018;32:36–57.

    Article  CAS  Google Scholar 

  3. Taimur S, Pouch SM, Zubizarreta N, Mazumdar M, Rana M, Patel G, Freire MP, Pellett Madan R, Kwak EJ, Blumberg E, Satlin MJ, Pisney L, Clemente WT, Zervos MJ, La Hoz RM, Huprikar S. Impact of pre-transplant carbapenem-resistant Enterobacterales colonization and/or infection on solid organ transplant outcomes. Clin Transplant. 2021;35:e14239.

    Article  CAS  PubMed  Google Scholar 

  4. Nguyen MH, Shields RK, Chen L, Pasculle AW, Hao B, Cheng S, Sun J, Kline EG, Kreiswirth BN, Clancy CJ. Molecular epidemiology, natural history and long-term outcomes of multi-drug resistant Enterobacterales colonization and infections among solid organ transplant recipients. Clin Infect Dis. 2021;15261:1–12.

    Google Scholar 

  5. Saliba R, Aho-Glélé LS, Karam-Sarkis D, Zahar JR. Evaluation of polymerase chain reaction assays for direct screening of carbapenemase-producing Enterobacteriaceae from rectal swabs: a diagnostic meta-analysis. J Hosp Infect. 2020;104:381–9.

    Article  CAS  PubMed  Google Scholar 

  6. Cury AP, Almeida Junior JN, Costa SF, Salomão MC, Boszczowski Í, Duarte AJS, Rossi F. Diagnostic performance of the Xpert Carba-R™ assay directly from rectal swabs for active surveillance of carbapenemase-producing organisms in the largest Brazilian University Hospital. J Microbiol Methods. 2020;171: 105884.

    Article  CAS  PubMed  Google Scholar 

  7. Otter JA, Dyakova E, Bisnauthsing KN, Querol-Rubiera A, Patel A, Ahanonu C, Auguet OT, Edgeworth JD, Goldenberg SD. Universal hospital admission screening for carbapenemase-producing organisms in a low-prevalence setting. J Antimicrob Chemother. 2016;71:3556–61.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Freire MP, Villela Soares Oshiro IC, Bonazzi PR, Pierrotti LC, de Oliveira LM, Machado AS, Van Der Heijdenn IM, Rossi F, Costa SF, Carneiro D’Albuquerque LA, Abdala E. Surveillance culture for multidrug-resistant gram-negative bacteria: performance in liver transplant recipients. Am J Infect Control. 2017;45:e40–4.

    Article  PubMed  Google Scholar 

  9. Fernández-Martínez M, González-Rico C, Gozalo-Margüello M, Marco F, Gracia-Ahufinger I, Aranzamendi M, Sánchez-Díaz AM, Vicente-Rangel T, Chaves F, Calvo Montes J, Martínez-Martínez L, Fariñas MC, Salas C, Armiñanzas C, de las Revillas FA, Casafont-Morencos F, Lavín AC, Fábrega E, Fariñas-Álvarez C, Morales VF, Rodrigo E, Millán JCRS, Bodro M, Moreno A, Linares L, Navasa M, Cofan F, Rodríguez F, Torre-Cisneros J, Vega AP, Montejo JM, Blanco MJ, Arana JN, Fortún J, Sánchez RE, Dávila PM, Garbajosa PR, Martínez A, Graus J, Fernández A, Muñoz P, Valerio M, Machado M, Olmedo M, Bento CA, Sanz CR, Ferrero MLR, Cámara LAS, Aguado JM, Resino E. Molecular characterization of multidrug resistant Enterobacterales strains isolated from liver and kidney transplant recipients in Spain. Sci Rep. 2021;11:1–9.

    Article  Google Scholar 

  10. Freire MP, Camargo CH, Yamada AY, Nagamori FO, Reusing Junior JO, Spadão F, Cury AP, Rossi F, Nahas WC, David-Neto E, Pierrotti LC. Critical points and potential pitfalls of outbreak of IMP-1-producing carbapenem-resistant Pseudomonas aeruginosa among kidney transplant recipients: a case–control study. J Hosp Infect. 2021;115:83–92.

    Article  CAS  PubMed  Google Scholar 

  11. Freire MP, Carvalho LB, Reusing JO, Spadão F, Lopes MIBF, Nahas WC, David-Neto E, Pierrotti LC. Carbapenem-resistant Enterobacteriaceae among kidney transplant recipients—insights on the risk of acquisition and CRE infection. Infect Dis (Auckl). 2021;53:430–9.

    Article  CAS  Google Scholar 

  12. Cepheid. Xpert Carb-R; 2015. https://csvlab.com.br/Carba-R-Bula-Cepheid.pdf

  13. EUCAST. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters 0–77; 2018.

  14. CLSI. Performance standards for antimicrobial susceptibility testing, 27th edn. CLSI supplement M100. Wayne: Clinical and Laboratory Standards Institute; 2017.

  15. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis. 2011;70:119–23.

    Article  CAS  PubMed  Google Scholar 

  16. CDC/NHSN Surveillance Definitions for Specific Types of Infections; 2017.

  17. Jin S, Lee JY, Park JY, Jeon MJ. Xpert Carba-R assay for detection of carbapenemase-producing organisms in patients admitted to emergency rooms. Medicine (Baltimore). 2020;99: e23410.

    Article  PubMed  Google Scholar 

  18. Giannella M, Freire M, Rinaldi M, Abdala E, Rubin A, Mularoni A, Gruttadauria S, Grossi P, Shbaklo N, Tandoi F, Ferrarese A, Burra P, Fernandes R, Aranha Camargo LF, Asensio A, Alagna L, Bandera A, Simkins J, Abbo L, Halpern M, Santana Girao E, Valerio M, Muñoz P, Fernandez Yunquera A, Statlender L, Yahav D, Franceschini E, Graziano E, Morelli MC, Cescon M, Viale P, Lewis R, Bartoletti M, Pascale R, Campoli C, Coladonato S, Cristini F, Tumietto F, Siniscalchi A, Laici C, Ambretti S, Romagnoli R, De Rosa FG, Muscatello A, Mangioni D, Gori A, Antonelli B, Dondossola D, Rossi G, Invernizzi F, Peghin M, Cillo U, Mussini C, Di BF, Terrabuio DRB, Bittante CD, do Toniolo AR, Balbi E, Garcia JHP, Morrás I, Ramos A, Cruz AF, Salcedo M. Development of a risk prediction model for carbapenem-resistant enterobacteriaceae infection after liver transplantation: a multinational cohort study. Clin Infect Dis. 2021;73:e955–66.

    Article  PubMed  Google Scholar 

  19. Pérez-Nadales E, Gutiérrez-Gutiérrez B, Natera AM, Abdala E, Reina Magalhães M, Mularoni A, Monaco F, Camera Pierrotti L, Pinheiro Freire M, Iyer RN, Mehta Steinke S, Grazia Calvi E, Tumbarello M, Falcone M, Fernández-Ruiz M, María Costa-Mateo J, Rana MM, Mara Varejão Strabelli T, Paul M, Carmen Fariñas M, Trindade Clemente W, Roilides E, Muñoz P, Dewispelaere L, Loeches B, Lowman W, Hock Tan B, Escudero-Sánchez R, Bodro M, Antonio Grossi P, Soldani F, Gunseren F, Nestorova N, Pascual Á, Martínez-Martínez L, María Aguado J, Rodríguez-Baño J, Torre-Cisneros J, Wan Song AT, Andraus W, Carneiro D’Albuquerque LA, David-Neto E, Jota de Paula F, Rossi F, Ostrander D, Avery R, Rizzi M, Losito AR, Raffaelli F, Del Giacomo P, Tiseo G, Lora-Tamayo J, San-Juan R, Gracia-Ahufinger I, Castón J, Ruiz YA, Altman DR, Campos S V., Bar-Sinai N, Koppel F, Arnaiz de las Revillas Almajano F, González Rico C, Fernández Martínez M, Mourão PHO, Neves FA, Ferreira J, Pyrpasopoulou A, Iosifidis E, Romiopoulos I, Minero M V., Sánchez-Carrillo C, Lardo S, Coussement J, Dodémont M, Jiayun K, Martín-Dávila P, Fortún J, Almela M, Moreno A, Linares L, Gasperina DD, Balsamo ML, Rovelli C, Concia E, Chiesi S, Salerno DN, Ogunc D, Pilmis B, Seminari EM, Carratalá J, Domínguez A, Cordero E, Lepe JA, Montejo M, Merino de Lucas E, Eriksson BM, van Delden C, Manuel O, Arslan H, Koçak Tufan Z, Kazak E, David M, Lease E, Nestorova N, Cornaglia G, Akova M. Predictors of mortality in solid organ transplant recipients with bloodstream infections due to carbapenemase-producing Enterobacterales: the impact of cytomegalovirus disease and lymphopenia. Am J Transplant. 2019; 20:1629–1641.

  20. Antonelli A, Arena F, Giani T, Colavecchio OL, Valeva SV, Paule S, Boleij P, Rossolini GM. Performance of the BD MAX™ instrument with check-direct CPE real-time PCR for the detection of carbapenemase genes from rectal swabs, in a setting with endemic dissemination of carbapenemase-producing Enterobacteriaceae. Diagn Microbiol Infect Dis. 2016;86:30–4.

    Article  CAS  PubMed  Google Scholar 

  21. Nadji S, Gaillot O, Hallaert C, Messaadi S, Loukili N, Naas T, Lemaître N. Prospective evaluation of the Amplidiag® CarbaR+VRE assay for direct screening of carbapenemase producing gram-negative bacilli from rectal swabs. Diagn Microbiol Infect Dis. 2019;95: 114890.

    Article  CAS  PubMed  Google Scholar 

  22. Falcone M, Tiseo G, Galfo V, Giordano C, Leonildi A, Marciano E, De Simone P, Biancofiore G, Boggi U, Barnini S, Menichetti F. Bloodstream infections in patients with rectal colonization by Klebsiella pneumoniae producing different type of carbapenemases: a prospective, cohort study (CHIMERA study). Clin Microbiol Infect. 2021;28:298.

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, National Council for Scientific and Technological Development; Grant no. 402470/2018-4 from Call for Projects no. 01/2018—Line 2—Development and innovation in new diagnostic methods to control and combat antimicrobial resistance). The funder had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Author information

Authors and Affiliations

  1. Working Committee for Hospital Epidemiology and Infection Control, School of Medicine, Hospital 18 das Clínicas da Faculdade de Medicina da Universidade de São Paulo, Rua Dr Eneas de 19 Carvalho Aguiar, 255, São Paulo, SP, 05403-900, Brazil

    Maristela P. Freire & Fernanda Spadão

  2. Centro de Laboratório Regional de Marília, Instituto Adolfo Lutz, São Paulo, Brazil

    Doroti de Oliveira Garcia, Stephanie Garcia Lima & Cláudia Regina Delafiori Pea

  3. Department of Urology, Renal Transplantation Unit, University of São Paulo School of Medicine Hospital das Clínicas, São Paulo, Brazil

    Jose Otto Reusing Junior, William C. Nahas & Elias David-Neto

  4. Microbiology Laboratory, Central Laboratory, University of São Paulo School of Medicine Hospital das Clínicas, São Paulo, Brazil

    Ana Paula Cury & Flavia Rossi

  5. Department of Infectious Diseases, University of São Paulo School of Medicine Hospital das Clínicas, São Paulo, Brazil

    Ligia C. Pierrotti

Authors
  1. Maristela P. Freire
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doroti de Oliveira Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephanie Garcia Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cláudia Regina Delafiori Pea
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jose Otto Reusing Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fernanda Spadão
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ana Paula Cury
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Flavia Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. William C. Nahas
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elias David-Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ligia C. Pierrotti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maristela P. Freire.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests. The authors have approved the final article.

Ethical standards

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the University of São Paulo Human Research Ethics Committee (Reference no. 82685818.0.0000.0068) and Adolfo Lutz Institute (CTC 70-L/2019). The requirement for informed consent was waived.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 29 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Freire, M.P., de Oliveira Garcia, D., Lima, S.G. et al. Performance of two methods of carbapenem-resistant Enterobacterales surveillance on a kidney transplant ward: selective culture of and real-time PCR directly from rectal swabs. Infection 50, 1525–1533 (2022). https://doi.org/10.1007/s15010-022-01839-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s15010-022-01839-2

Keywords

Search

Navigation