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Bloodstream infection by Acinetobacter radioresistens: the first case report in Brazil

ABSTRACT

This report is the description of the first case in Brazil of community-acquired bloodstream infection caused byAcinetobacter radioresistens. A 73-year-old male patient with Alzheimer’s and Parkinson’s disease was hospitalized and diagnosed with pneumonia at a general hospital. MacConkey agar pure culture was obtained from blood cultures. Conventional tests identified the isolate as Acinetobacter baumannii complex. However, the matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) technique identified it as Acinetobacter radioresistens. The isolate was sensitive to all antibiotics tested by the disk diffusion method, including carbapenem. However, blaoxa-23 gene was detected by the polymerase chain reaction (PCR) assay. Acinetobacter radioresistens can be considered an important agent of opportunistic infections in immunocompromised patients, a potential disseminator of resistance genes.

Key words:
Acinetobacter; bacteremia; Alzheimer disease

RESUMEN

Este reporte es la descripción del primer caso en Brasil de bacteriemia por Acinetobacter radioresistens adquirida en la comunidad. Paciente masculino de 73 anos de edad, portador de las enfermedades de Alzheimer y de Parkinson, fue atendido en un hospital general y diagnosticado con cuadro de neumonía. Cultivo puro en agar MacConkey fue obtenido de hemocultivos. Pruebas convencionales identificaron el aislado como complejo Acinetobacter baumannii, pero el sistema desorción/ionización láser asistida por matriz-tiempo de vuelo (MALDI-TOF) lo identificó como Acinetobacter radioresistens. El aislado se presentó sensible a todos antibióticosprobados mediante el método de difusión en disco, incluyendo los carbapenemas. Sin embargo, el gen blaoxa-23 fue detectadopor la técnica de reacción en cadena de lapolimerasa (RCP). Acinetobacter radioresistenspuedeser considerado un agente importante de infecciones oportunistas en pacientes inmunocomprometidos, un potencial diseminador de genes de resistencia.

Palabras clave:
Acinetobacter; bacteriemia; enfermedad de Alzheimer

RESUMO

Este relato éa descrição do primeiro caso no Brasil de bacteremia adquirida na comunidade causada por Acinetobacter radioresistens. Paciente do sexo masculino, 73 anos de idade, portador da doença de Alzheimer e de Parkinson, foi assistido em um hospital geral e diagnosticado quadro de pneumonia. Cultura pura em ágar MacConkey foi obtida a partir de hemoculturas. Testes convencionais identificaram o isolado como complexo Acinetobacter baumannii, porém o sistema matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) identificou como Acinetobacter radioresistens. O isolado apresentou-se sensível a todos os antibióticos testados por meio da técnica do disco difusão, incluindo os carbapenens. Contudo, foi detectado o gene blaOXA23 pela técnica da reação em cadeia da polimerase (PCR). Acinetobacter radioresistens pode ser considerado um agente importante de infecções oportunistas em pacientes imunocomprometidos, um potencial disseminador de genes de resistência.

Unitermos:
Acinetobacter; bacteremia; doença de Alzheimer

INTRODUCTION

Acinetobacter spp. has shown to be a potential opportunistic pathogen, which mainly affects patients with some comorbidity(11 Falagas ME, Karveli EA, Kelesidis I, Kelesidis T. Community-acquired Acinetobacter infections. Eur J Clin Microbiol Infect Dis. 2007; 26(12): 857-68.). The Acinetobacter baumannii species, in particular, is in the first place of the “critical state” list of bacteria requiring special attention, according to the World Health Organization(22 Harbarth S, Kahlmeter G, Kluytmans J, et al. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. 2017. Available at: http://www.who.int/medicines/publications/WHO-PPL Short_Summary_25Feb-ET_NM_WHO.
http://www.who.int/medicines/publication...
). However, the special attention given to this species should also be directed towards other emerging members of this genus, such as Acinetobacter radioresistens. This species shows great adaptability to an environment with low relative humidity, and great persistence and survival in hospital environments, under such conditions(33 Jawad A, Snelling AM, Heritage J, Hawkey PM. Exceptional desiccation tolerance of Acinetobacter radioresistens. J Hosp Infect [Internet]. 1998 Jul [cited 2016 Sep 1]; 39(3): 235-40. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0195670198902638.
http://linkinghub.elsevier.com/retrieve/...
). It is also considered a possible reservoir and disseminator of genes that confer resistance to carbapenem(44 Poirel L, Figueiredo S, Cattoir V, Carattoli A, Nordmann P. Acinetobacter radioresistens as a silent source of carbapenem resistance for Acinetobacter spp. Antimicrob Agents Chemother. 2008; 52(4): 1252-6.). To date, there are a few clinical case reports involving A. radioresistens(55 Brady AC, Lewis JS, Pfeiffer CD. Rapid detection of blaOXA in carbapenem-susceptible Acinetobacter radioresistens bacteremia leading to unnecessary antimicrobial administration. Diagn Microbiol Infect Dis. 2016; 85(4): 488-9.

6 Savov E, Pfeifer Y, Wilharm G, et al. Isolation of Acinetobacter radioresistens from a clinical sample in Bulgaria. J Glob Antimicrob Resist. 2016; 4: 57-9. Available at: http://linkinghub.elsevier.com/retrieve/pii/S2213716515001228.
http://linkinghub.elsevier.com/retrieve/...
-77 Visca P, Petrucca A, De Mori P, et al. Community-acquired acinetobacter radioresistens bacteremia in an HIV-positive patient Paolo. Emerg Infect Dis. 2001; 7(6): 1032-5.) , of which only one describes a community-acquired bloodstream infection, from a human immunodeficiency virus (HlV)-positive patient(77 Visca P, Petrucca A, De Mori P, et al. Community-acquired acinetobacter radioresistens bacteremia in an HIV-positive patient Paolo. Emerg Infect Dis. 2001; 7(6): 1032-5.).

CASE REPORT

A 73-year-old male patient was hospitalized at a general hospital localized in Natal, Brazil Northeast, presenting fever, respiratory secretions and wheezing on chest auscultation. The patient was diagnosed with pneumonia and was breathing with the aid of a 50% ventilation mask. He was hypertensive and presented Alzheimer’s and Parkinson’s disease. Urine, sputum and blood samples were collected for cultures in three different sites upon hospital admission. The urine culture on cystine-, lactose-, and electrolyte-deficient (CLED) agar (HiMedia, India) was negative, and the sputum culture on chocolate agar (HiMedia, India) showed growth (50,000 cfu/ml) with Gram-negative features (i.e. small and non-pigmented), however, this was considered a non-significant growth by the microbiology laboratory. Three blood samples were later inoculated on chocolate agar (HiMedia, India) and incubated at 37°C on microaerophilic environment for 18 h, and all of them yielded significant monomicrobial growth. After Gram staining performance, Gram-negative coccobacilli isolate was observed. Biochemical tests results revealed a non-fermenting isolate. In addition, the strain presented oxidase-negative, catalase-positive, immobile properties and growth at 44°C, which was suggestive of Acinetobacter baumannii complex. Still, the matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) technique (VITEK-MS® - bioMerieux, Rio de Janeiro, Brazil) identified the strain as Acinetobacter radioresistens (NT5476 strain). Antimicrobial susceptibility was evaluated by the Clinical and Laboratory Standards Institute (CLSI) disk-diffusion technique assays(88 CLSI. M100 Performance standards for antimicrobial susceptibility testing. 27th edition. 2017. 224 p.). According to CLSI breakpoints the NT5476 strain was susceptible to all antimicrobials in vitro tested: ciprofloxacin (5 pg), amikacin (30 pg), gentamicin (10 pg), ceftriaxone (30 pg), ampicillin + sulbactam (20 pg), meropenem (10 pg), imipenem (10 pg), sulphamethoxazole + trimethoprim (25 pg), piperacillin + tazobactam (30 pg), and cefotaxime (30 pg).

Polymerase chain reaction (PCR) assays screening for carbapenem-hydrolyzing class D β-lactamases encoding genes were performed, as previously published(99 Woodford N, Ellington MJ, Coelho JM, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents [Internet]. 2006 Dec 3; 27(4): 351-3. Available at: http://dx.doi.org/10.1016/j.ijantimicag.2006.01.004
http://dx.doi.org/10.1016/j.ijantimicag....
). The strain showed positive results for blaoxa23 gene. The amplicon was observed in an agarose gel electrophoresis at 2%, stained with ethidium bromide, visualized under ultra-violet (UV) transilluminator, and photographed. After blaoxa23 gene was confirmed, NT 5376 strain was also screening for the insertion sequence ISabal by PCR assay, as previously described by Segal et al. (2005)(1010 Segal H, Garny S, Elisha BG. Is ISABA-1 customized for Acinetobacter? FEMS Microbiol Lett. 2005; 243(2): 425-9.). The strain presented negative results for this insertion sequence.

DISCUSSION

This is the first report of bloodstream infection by A. radioresistens in Brazil. Antimicrobial therapy was performed with ceftriaxone and the patient received hospital discharge in good clinical condition. This infection can be considered as a community-acquired infection since it was detected upon patient’s hospital admission and was not related to any previous hospitalization(1111 Van Duin D, Paterson DL. Multidrug-resistant bacteria in the community: trends and lessons learned. Infect Dis Clin North Am. 2016; 30(2): 377-90.). Community infections associated to Acinetobacter spp. mainly affect patients with some morbidity(11 Falagas ME, Karveli EA, Kelesidis I, Kelesidis T. Community-acquired Acinetobacter infections. Eur J Clin Microbiol Infect Dis. 2007; 26(12): 857-68.). The patient from this report presented Alzheimer and Parkinson’s disease. In addition, diseases such as Alzheimer and Parkinson increase the risk of saliva aspiration, more prone to respiratory infections. The infection occurred, possibly, through the upper airways with subsequent dissemination through the bloodstream.

The respiratory systems are a gateway for Acinetobacter spp. bloodstream infection(1212 Wisplinghoff H, Edmond MB, Pfaller MA, Jones RN, Wenzel RP, Seifert H. Nosocomial bloodstream infections caused by Acinetobacter species in United States hospitals: clinical features, molecular epidemiology, and antimicrobial susceptibility. Clin Infect Dis [Internet]. 2000; 31(3): 690-7. Available at: https://academic.oup.com/cid/articlelookup/doi/10.1086/314040.
https://academic.oup.com/cid/articlelook...
), which is in agreement with the initial diagnosis of the case, which was pneumonia. The development of aspiration pneumonia with Alzheimer’s disease is related to the reduced level of consciousness, dysphagia, and loss of reflexes, favoring the aspiration of commensal microorganisms from the environment to the airways, causing pneumonia with subsequent dissemination through the bloodstream(1313 Wada H, Nakajoh K, Satoh-Nakagawa T, et al. Risk factors of aspiration pneumonia in Alzheimer’s disease patients. Gerontology. 2001; 47: 271-6.). Although the strain harbored blaoxa-23 gene, it was susceptible to the carbapenems tested and it showed absence of ISabal by PCR screening. Our findings agree with some other studies, which also detected blaoxa-23gene and absence of ISabal in A. radioresistens sensitive to carbapenems. This phenomenon has been explained by relating this sensitivity to the absence of genetic elements in the genome, particularly the ISabal insertion sequences(55 Brady AC, Lewis JS, Pfeiffer CD. Rapid detection of blaOXA in carbapenem-susceptible Acinetobacter radioresistens bacteremia leading to unnecessary antimicrobial administration. Diagn Microbiol Infect Dis. 2016; 85(4): 488-9.).

Therefore, further studies will be needed to better understand the pathogenic potential of the Acinetobacter radioresistens species, since it may play a significant role as an infectious agent, especially in immunocompromised patients. Furthermore, additional experiments are required to understand the importance of harboring resistance genes in their genome, which show no expression, and their ability to disseminate them to other species.

ACKNOWLEDGMENTS

The authors thank to Dra. Beatriz Meurer Moreira for helping them identifying the A. radioresistens isolate and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ) for the financial support.

REFERENCES

  • 1
    Falagas ME, Karveli EA, Kelesidis I, Kelesidis T. Community-acquired Acinetobacter infections. Eur J Clin Microbiol Infect Dis. 2007; 26(12): 857-68.
  • 2
    Harbarth S, Kahlmeter G, Kluytmans J, et al. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. 2017. Available at: http://www.who.int/medicines/publications/WHO-PPL Short_Summary_25Feb-ET_NM_WHO
    » http://www.who.int/medicines/publications/WHO-PPL Short_Summary_25Feb-ET_NM_WHO
  • 3
    Jawad A, Snelling AM, Heritage J, Hawkey PM. Exceptional desiccation tolerance of Acinetobacter radioresistens. J Hosp Infect [Internet]. 1998 Jul [cited 2016 Sep 1]; 39(3): 235-40. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0195670198902638
    » http://linkinghub.elsevier.com/retrieve/pii/S0195670198902638
  • 4
    Poirel L, Figueiredo S, Cattoir V, Carattoli A, Nordmann P. Acinetobacter radioresistens as a silent source of carbapenem resistance for Acinetobacter spp. Antimicrob Agents Chemother. 2008; 52(4): 1252-6.
  • 5
    Brady AC, Lewis JS, Pfeiffer CD. Rapid detection of blaOXA in carbapenem-susceptible Acinetobacter radioresistens bacteremia leading to unnecessary antimicrobial administration. Diagn Microbiol Infect Dis. 2016; 85(4): 488-9.
  • 6
    Savov E, Pfeifer Y, Wilharm G, et al. Isolation of Acinetobacter radioresistens from a clinical sample in Bulgaria. J Glob Antimicrob Resist. 2016; 4: 57-9. Available at: http://linkinghub.elsevier.com/retrieve/pii/S2213716515001228
    » http://linkinghub.elsevier.com/retrieve/pii/S2213716515001228
  • 7
    Visca P, Petrucca A, De Mori P, et al. Community-acquired acinetobacter radioresistens bacteremia in an HIV-positive patient Paolo. Emerg Infect Dis. 2001; 7(6): 1032-5.
  • 8
    CLSI. M100 Performance standards for antimicrobial susceptibility testing. 27th edition. 2017. 224 p.
  • 9
    Woodford N, Ellington MJ, Coelho JM, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents [Internet]. 2006 Dec 3; 27(4): 351-3. Available at: http://dx.doi.org/10.1016/j.ijantimicag.2006.01.004
    » http://dx.doi.org/10.1016/j.ijantimicag.2006.01.004
  • 10
    Segal H, Garny S, Elisha BG. Is ISABA-1 customized for Acinetobacter? FEMS Microbiol Lett. 2005; 243(2): 425-9.
  • 11
    Van Duin D, Paterson DL. Multidrug-resistant bacteria in the community: trends and lessons learned. Infect Dis Clin North Am. 2016; 30(2): 377-90.
  • 12
    Wisplinghoff H, Edmond MB, Pfaller MA, Jones RN, Wenzel RP, Seifert H. Nosocomial bloodstream infections caused by Acinetobacter species in United States hospitals: clinical features, molecular epidemiology, and antimicrobial susceptibility. Clin Infect Dis [Internet]. 2000; 31(3): 690-7. Available at: https://academic.oup.com/cid/articlelookup/doi/10.1086/314040
    » https://academic.oup.com/cid/articlelookup/doi/10.1086/314040
  • 13
    Wada H, Nakajoh K, Satoh-Nakagawa T, et al. Risk factors of aspiration pneumonia in Alzheimer’s disease patients. Gerontology. 2001; 47: 271-6.

Publication Dates

  • Publication in this collection
    02 Mar 2020
  • Date of issue
    Nov-Dec 2019

History

  • Received
    19 Oct 2018
  • Reviewed
    22 Oct 2018
  • Accepted
    15 May 2019
  • Published
    20 Dec 2019
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