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Carbapenem-Resistant Acinetobacter baumannii in Latin America

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Thiago Pavoni Gomes Chagas, Karyne Rangel and Salvatore Giovanni De-Simone

Submitted: 29 September 2023 Reviewed: 23 October 2023 Published: 07 February 2024

DOI: 10.5772/intechopen.1003713

<em>Acinetobacter baumannii</em> IntechOpen
Acinetobacter baumannii The Rise of a Resistant Pathogen Edited by Karyne Rangel

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Acinetobacter baumannii - The Rise of a Resistant Pathogen

Karyne Rangel and Salvatore Giovanni De-Simone

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Abstract

Acinetobacter baumannii is an important bacterial pathogen associated with healthcare-associated infections (HAIs), especially in critically ill patients admitted to Intensive Care Units (ICU). Its ability to acquire antibiotic resistance determinants has propelled its clinical relevance. The rise in Acinetobacter infections and hospital outbreaks have been extensively described worldwide and are usually caused by carbapenem-resistant isolates. To compound the problem, Carbapenem-resistant A. baumannii (CRAb) isolates are also resistant to a wide range of other antibiotics, representing a serious threat to public health. Since 2017, A. baumannii has been listed as a critical priority pathogen that poses a great threat to human health, according to the World Health Organization (WHO). The carbapenem-resistant rates in A. baumannii are notorious around the world. However, Latin America has one of the highest in the world. Carbapenem resistance in A. baumannii is due mainly to the presence of horizontally acquired OXA-type carbapenem resistance genes, including blaOXA-23, in most regions. Thus, this review aims to summarize the distribution of CRAb and its major carbapenem resistance mechanisms in Latin America.

Keywords

  • Acinetobacter baumannii
  • carbapenems
  • antimicrobial resistance
  • carbapenemases
  • oxacillinases

1. Introduction

Acinetobacter baumannii is Gram-negative, nonfermenting, aerobic coccobacilli, catalase-positive, oxidase-negative, and non-motile [1, 2]. It has also been considered the most serious among the ‘ESKAPE’ (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, A. baumannii, Pseudomonas aeruginosa, and Enterobacter species), a group of six pathogens with multidrug resistance and virulence factors [3].

In the Acinetobacter genus, A.baumannii is a more relevant species grouped as the Acinetobacter calcoaceticus–Acinetobacter baumannii (ACB) complex [4]. Clinical samples frequently recover this microorganism. It has been responsible for many nosocomial infection outbreaks in Intensive Care Units (ICU) [5]. A. baumannii can also be associated with community-acquired infections such as pneumonia and bacteremia. However, these community infections are less common and have been associated with comorbidities (e.g., alcoholism, smoking, diabetes mellitus, chronic obstructive pulmonary disease, and renal disease) [6, 7].

A. baumannii has been recognized as causing severe healthcare-associated infections (HAIs) [6]. This Gram-negative pathogen has been associated with pneumonia, endocarditis, bacteremia, wound infections, urinary tract infections, and meningitis in hospital settings. However, ventilator-associated pneumonia and bloodstream infections are the most important infections, accompanied by the highest mortality rates [3, 5, 6, 8]. Risk factors associated with colonization or infection include intensive care unit admission, invasive medical procedures, prolonged hospitalization, antimicrobial agent exposure, prior hospitalization, and local colonization pressure on susceptible patients [8].

The ability to resist the vast majority of available antimicrobial agents is an important determinant in clinical outcomes of A. baumannii infections and spread in the hospital setting [7, 9, 10]. Multidrug-resistant isolates of A. baumannii have been reported increasingly during the last decade [11, 12]. Previous studies indicated that the estimated global incidence of A. baumannii infections is approximately 1,000,000 cases annually, of which 50% are resistant to multiple antibiotics, including carbapenems [13, 14]. Carbapenem-resistant A. baumannii (CRAb) isolates have been increasingly observed worldwide, constituting a serious threat to public health [12], especially in Latin America [15], being significantly associated with increased mortality.

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2. Carbapenem-resistance A. baumannii

Antimicrobial resistance (AMR) has emerged as one of the global healthcare threats of the twenty-first century [16]. Projections estimated 10 million deaths per year attributable to bacterial AMR by 2050 [17, 18]. A. baumannii strains can develop resistance to all the antibiotics available, and outbreaks caused by multidrug-resistant (MDR), extensively drug-resistant (XDR) and even pan-drug-resistant (PDR) strains have been reported around the world [19].

Different global health authorities, including the European Centre for Disease Prevention and Control (ECDC), Infectious Diseases Society of America (IDSA), and Center for Disease Control and Prevention (CDC) have appointed MDR A. baumannii a critical threat to global health [20, 21, 22, 23]. 2017, the World Health Organization (WHO) listed CRAb as a crucial priority due to its high AMR rates [24]. The rise of CRAb strains as an opportunistic pathogen poses a significant threat to global health.

2.1 Carbapenems

Carbapenems, such as the most popular imipenem and meropenem, play a critically important role as a therapeutic option for serious infections caused by MDR A. baumannii [8] due to their effective activity and their safety [25, 26]. This β-lactam subclass demonstrates a wider range of antimicrobial activity than penicillins, cephalosporins, or β-lactam/ β-lactamase inhibitor combinations [27].

Generally, they have excellent bactericidal activity and stability toward a range of β-lactamases, except the emerging carbapenemases [8, 28, 29]. Carbapenems (except ertapenem that is inactive against Pseudomonas and A. baumannii) displayed activity against both Gram-negatives (except Stenotrophomonas maltophilia) and Gram-positive bacteria (except methicillin-resistant S. aureus, E. faecium and Enterococcus fecalis apart from imipenem) [30].

Like other β-lactams, carbapenems are bactericidal agents that bind to the penicillin-binding proteins (PBPs), inhibiting bacterial cell wall synthesis [31]. Specifically, they prevent transpeptidation [32]. Conventionally, that β-lactam class enters Gram-negative bacteria through outer membrane proteins (OMPs), also known as porins [28].

A classification system for carbapenems was proposed based on their antimicrobial activity, dividing them into three groups. Carbapenems group 1, which included ertapenem, are inefficient against non-fermentative Gram-negative bacilli and may be more suitable for community-acquired infections. Carbapenems from group 2, such as meropenem, imipenem, and doripenem, have broad-spectrum actions, are active against non-fermentative Gram-negative bacilli, and are effective against nosocomial infections. Group 3 carbapenems are potent against non-fermentative Gram-negative bacilli and S. aureus, which are resistant to methicillin [33, 34, 35].

Carbapenems have low oral bioavailability and must be administered intravenously because they cannot cross the gastrointestinal membranes readily. Additionally, imipenem-cilastatin and ertapenem can also be administered intramuscularly. All these carbapenem antibiotics are excreted via the kidneys [28].

These agents have a role as empirical and definitive therapy options in a range of serious infections. In ICU, carbapenems are especially valuable in units with known third-generation cephalosporin resistance problems, in patients with disease who have received previous antibiotic courses, and in polymicrobial infections [36]. Carbapenems are appropriate for use in the lower respiratory tract, skin and soft tissue, central nervous system, urinary tract, joint, muscle, gynecologic, obstetric, and abdominal infections or in the management of febrile neutropenia and problems due to cystic fibrosis [27].

Since the first CRAb was identified in 1991, there has been a considerable increase in the amount of A. baumannii strains that have acquired resistance to this β-lactam class [37]. This problem is critical, especially considering that most CRAb strains resist other antibiotic classes.

2.2 Treatment options

When carbapenem resistance is suspected and/or determined, some agents can be used in therapeutic combinations to treat CRAb infections, for example, β-lactamase inhibitors such as sulbactam; polymyxins, tetracyclines, such as minocycline and doxycycline; fosfomycin, rifamycin, and carbapenem therapy combined with other antibiotics [38].

2.3 Global rates of CRAb

Carbapenem resistance rates can vary according to the geographic Region around the world. Among 2.674 A. baumannii isolates collected from 13 countries in the Asia-Pacific region by Antimicrobial Testing Leadership and Surveillance (ATLAS) program between 2012 and 2019, carbapenem resistance rates ranged from the lowest in Japan (2.8%) and Australia (6.5%) to the highest in South Korea (88%). According to the previous review, CRAb is critically problematic across Asia and the Americas, except in Japan (3.5%) and Canada (4.7%). Oceania, Western Europe, the Nordic Region, and part of central Europe have the lowest rates (<10%). However, in areas surrounding the Mediterranean, including southern Europe, the Middle East, and North Africa, up to 90% of strains are resistant to carbapenems [39].

The latest Surveillance of AMR in Europe 2022 reports the total carbapenem resistance rate ranged from 31.9 to 38% among Acinetobacter spp. Isolates from 2016 to 2020. The percentages of carbapenem-resistant Acinetobacter spp. Varied within the Region in 2020, from below 1% in three (8%) of 38 countries/areas (Ireland, the Netherlands, and Norway) to percentages equal to or above 50% in 21 (55%) countries/areas, mostly in Southern and Eastern Europe [40]. The number of European countries with 50% or higher carbapenem resistance rates increased from 12 in 2015–2018 to 21 countries in 2018–2020 [40, 41].

From 2012 to 2017, the incidence of CRAb from clinical cultures decreased in the United States. The Centers for Disease Control and Prevention (CDC) estimated 8500 cases among U.S. hospitalized patients in 2017, resulting in 700 deaths [42]. Between 2013 and 2016, the SENTRY Antimicrobial Surveillance Program reported, among ACB complex Isolates, a susceptibility rate for meropenem of 54.9% in North America [43]. For imipenem, the susceptibility rate was 57.7%. Comparing the intervals 1997–2000 and 2013–2016, the susceptibility rate for meropenem significantly decreased from 88.8 to 54.9% [43].

Among 4.320 A. baumannii isolates collected across different regions of the world between 2016 and 2018 by Seifert et al. [44], the global resistance rate for meropenem was 64.4%. The highest meropenem resistance rates observed were in Africa/Middle East (81.1%), Latin America (78.4%), Asian/South Pacific (67.5%), and Europe (63%) [44].

2.4 CRAb in Latin America

Rates of carbapenem resistance among A. baumannii in Latin America appear to be one of the highest in the world. These rates up to 90% for A. baumannii isolates can be found across the different countries of Latin America, with the resistance rate of A. baumannii isolates greater than 50% in many countries [15]. In a review by Ma and McClean [39], Carbapenem resistance rates ranged from 0 to 97.5% among Latin American isolates [39].

ACB complex Isolates were collected from 17 Latin America centers (7 countries) from January 1997 to December 2016 through the SENTRY Program. Data of this Surveillance program appointed a susceptibility rate for meropenem of 13.7%. For imipenem, this resistance rate was 14.4%. The susceptibility rates declined continuously in Latin America’s 2009–2012 and 2013–2016 periods [43].

The global dissemination of CRAb is associated with clonal lineages, illustrating this organism’s success in acquiring carbapenem resistance [45]. Initially, three disseminated lineages of A. baumannii called European clones I, II, and III were characterized in European countries. Posteriorly, complementary studies showed that these lineages had already spread worldwide, and thus, European clones were renamed international clonal (IC) lines I, II, and III [7, 45, 46]. At the moment, molecular epidemiological studies have recognized nine major International Clones (1–9) of A. baumannii, the most widespread of which is IC 2 (II) [47]. However, CRAb isolates in Latin America are not associated with the most pervasive IC2 [48, 49].

In Latin countries such as Brazil, Argentina, Chile, and Paraguay, the major CRAb clones were found to belong to IC 4 and IC 5 [49, 50]. These IC 4 and IC 5 correspond to clonal complexes CC15Past/CC103OXF and CC79Past/CC227OXF defined by Pasteur (Past) and Oxford (OXF) Multilocus Sequence Type (MLST) schemes [49, 50, 51]. Other ICs have been observed in Latin regions, such as IC 1 (CC1Past/CC109OXF), IC 2 (CC2Past/CC92OXF), IC 6 (CC78Past/CC944OXF) and IC7 (CC25Past/CC110OXF) [50, 52, 53, 54, 55].

2.5 CRAb in COVID-19 pandemic

Latin America has faced critical moments during the COVID-19 pandemic and was considered one of the world epicenters [56]. Hospitalization of COVID-19 patients predisposed to severe consequences such as HAIs and secondary or coinfections associated with MDR bacteria such as A. baumannii [57, 58, 59]. Since the beginning of COVID-19, the emergence of resistant microorganisms causing HAIs has been documented [60].

An increased risk of CRAb infections in patients with an increased risk of mortality due to COVID-19 infections was reported. This increased incidences of A. baumannii infections during the COVID-19 pandemic were related to various reasons such as prolonged hospital stay, mechanical ventilation, and immunosuppression [61].

In a retrospective analysis of two prospective observational cohort studies of COVID-19 patients in 10 countries, including Colombia, Chile, Ecuador, Mexico, Argentina, Uruguay, and Brazil, A. baumannii was Latin America’s fourth most prevalent bacteria (10.6%). However, this bacteria was less predominant in Europe [62].

A recent study reported the occurrence of CRAb belonging to IC 2 caused a large outbreak among COVID-19 patients at a public hospital in Brazil [63]. At an Argentinian hospital, an experience with carbapenem-resistant isolates such as CRAb during the period with active cases of COVID-19 was reported [64]. Loyola-Cruz et al. described A. baumannii involved in outbreaks non-detected in COVID-19 patients at a Mexican hospital. Among 14 A. baumannii isolates, meropenem and imipenem resistance rates were 100% [65]. Another Mexican study conducted by Alcántar-Curiel et al. [66] reported 34% (n = 39) of CRAb isolates linked to nosocomial bacteremias in COVID-19 patients [66].

Brazilian studies can be examples of increased carbapenem resistance in A. baumannii isolates trends in Latin American territories in Pandemic times. A recent report described that CRAb was notified in 7.9% (373/4734) of device-associated infections notifications in 2019 and 12.4% (805/6514) in 2020 in 99 hospitals from Paraná state, south of Brazil. The monthly incidence density of CRAB per 1000 patient days increased significantly after April 2020, having a strong positive correlation with the incidence density of COVID-19 [67].

Polly et al. reported a retrospective observational study that compared the incidence density of HAIs caused by MDR bacteria (including CRAb) pre-COVID (2017–2019) and during the COVID-19 pandemic (2020) in hospitalized patients at a tertiary care public teaching hospital (São Paulo, Brazil). CRAb incidence density in the Pre-pandemic period (2017–2019) was 0.53. That increase can also be expressed by 108% in HAI infection by CRAB in all hospital units and 42% in ICU [68].

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3. Mechanisms of carbapenem-resistance in A. baumannii

Several mechanisms of carbapenem resistance have been described in A. baumannii [1, 12, 48, 69]. Considering intrinsic cellular mechanisms, carbapenem resistance might be attributed to loss or decrease in outer membrane porins (OMPs), decreased drug affinity due to the downregulation of PBPs, and over-expression of efflux pumps [70, 71, 72, 73].

However, inactivation or enzymatic degradation of carbapenems has been considered the major key associated with the development of carbapenem resistance in A. baumannii [12, 74, 75]. Different classes of carbapenem-hydrolyzing enzymes (carbapenemases) are based on molecular Ambler classification: Class A, B, and D [1, 12]. These enzymes are found frequently on plasmids and are transmissible [76]. Class A carbapenemases consist mainly of six members (SME, IMI, NMC, GES, SFC, and KPC), and GES class A carbapenemases seem the most prevalent in A. baumannii. Metallo-lactamases (MBLs), also called Class B enzymes, are potent carbapenemases, and four families (IMP, VIM, SIM, and NDM) have also been described in A. baumannii [77].

Instead of Class A and B, which are commonly identified in other bacterial pathogens, the carbapenem-hydrolyzing-class-D β-lactamases (CHDLs), also called oxacillinases/OXA-type β-lactamases, are referred as the most common carbapenemases in A. baumannii [12, 69]. β-lactamases of Ambler class D, OXA enzymes, possess an active serine site similar to class A and C β-lactamases. These β-lactamases show cloxacillin- and oxacillin-hydrolyzing activity and are classified into Bush-Jacoby functional group 2d. Those OXA enzymes that hydrolyze carbapenems belong to the Bush-Jacoby active subgroup 2df. Originally, OXA-type carbapenemases have mainly been found on the chromosomes of A. baumannii strains. However, several types of β-lactamases are also encoded on plasmids, allowing for their wide dissemination [78, 79].

There are six main groups in /OXA-type β-lactamases known to be harbored by A. baumannii: the intrinsic OXA-51-like and the acquired OXA-23-like, OXA-58-like, OXA-24/40-like, OXA-143-like and OXA-235-like [1, 12, 48, 80, 81]. Among them, OXA-23-like is the most prevalent worldwide. Clonal outbreaks of carbapenem-resistant and OXA–23–23-producing A. baumannii have been reported in many countries [82]. Analysis of the genetic environment of OXA-carbapenemases genes has shown that the genes are associated with various mobile elements [83].

A major expression of OXA genes might be facilitated by insertion sequences (ISs) because these genetic elements have strong promoters that enable the expression of OXA genes [74, 84]. For example, ISAba1, ISAba2, ISAba3, ISAba4, and IS18 are commonly associated with the presentation of carbapenemase genes in A. baumannii [85]. Transposons are another important genetic element responsible for the rapid spread of resistance genes worldwide [84]. The dissemination of blaOXA–23, for example, has been strongly associated with transposons such as Tn2006, Tn2007, and Tn2008 that were identified as genetic structures harboring this gene [82, 85].

3.1 CRAb and carbapenemases in Latin America

More than 50% of Acinetobacter spp. Isolates in Latin America expressed carbapenem resistance. Additionally, the high prevalence of OXAs in CRAB isolates in Latin America is notorious [86]. Other carbapenemases have been reported in some Latin American countries but less frequently (Table 1). The spread of OXA-23 is also observed in Latin America and other parts of the world. And this dissemination has been commonly associated with CC113/CC79 and CC104/CC15 [132, 133].

CountriesOXa-type carbapenemasesOther carbapenemasesReferences
ArgentinaOXA-23-like, OXA-58-likeNDM[87, 88, 89, 90, 91, 92]
BoliviaOXA-23-like, OXA-58-like—[93, 94, 95, 96]
BrazilOXA-23-like, OXA-24-like, OXA-58-like, OXA-143-likeKPC, NDM, IMP, VIM[97, 98, 99, 100, 101, 102, 103, 104, 105]
ColombiaOXA-23-like, OXA-24-like, OXA-143-likeNDM, VIM[52, 106, 107, 108, 109, 110, 111, 112]
CubaOXA-23-like, OXA-24-like, OXA-58-likeNDM[113, 114]
ChileOXA-23-like, OXA-58-like—[94, 115, 116]
EcuadorOXA-23-like, OXA-24-likeNDM[94, 117]
Honduras—NDM[94, 118]
MéxicoOXA-24-like, OXA-58-like, OXA-235-ilkeVIM[80, 119, 120, 121]
ParaguayOXA-23-like—[94]
PeruOXA-23-like, OXA-24-like, OXA-143-likeNDM[19, 122, 123, 124, 125]
Puerto Rico—KPC[97, 126, 127]
UruguayOXA-23-like, OXA-58-like—[94, 128]
VenezuelaOXA-23-like, OXA-58-likeNDM[129, 130, 131]

Table 1.

Reports of the carbapenemase distribution in A. baumannii isolates in Latin America.

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4. Conclusion

In summary, this chapter presents a comprehensive review of the distribution of CRAb in Latin America. The chapter begins by highlighting the current significance of CRAb as a relevant pathogen associated with healthcare-acquired infections globally. Carbapenems have played a critical role as a therapeutic option for infections caused by MDR A. baumannii. However, the world has faced increased A. baumannii strains that have acquired carbapenem resistance. The spread of CRAb is associated with two international clones, IC 4 and IC 5 in the Latin countries. As observed in other parts of the world, carbapenem resistance is mediated mainly by OXA-type β-lactamases in Latin America. That dissemination illustrates these OXA-23-CRAb strains’ success in Latin territory. Knowing the Latin American real scenario of CRAb is the first step in adopting measures to combat and control this challenging pathogen.

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Acknowledgments

This research was funded by the Carlos Chagas Filho Foundation for Research Support of the State of Rio de Janeiro/FAPERJ (#110.198-13) and the Brazilian Council for Scientific Research (CNPq, #467.488/2014-2 and 301744/2019-0). Funding was also provided by FAPERJ (#210.003/2018) through the National Institutes of Science and Technology Program (INCT) to Carlos M. Morel (INCT-IDPN).

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Conflict of interest

The authors declare no conflict of interest.

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Author contributions

Conceived and designed the experiments: T.P.G.C., K.R.; writing—original draft: T.P.G.C.; review and editing: K.R., S.G.D.-S.; funding: S.G.D.-S. All authors have read and agreed to the published version of the manuscript.

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Written By

Thiago Pavoni Gomes Chagas, Karyne Rangel and Salvatore Giovanni De-Simone

Submitted: 29 September 2023 Reviewed: 23 October 2023 Published: 07 February 2024

© The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.0 License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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