The 29 LICs included in the World Bank classification are distributed over six geographical regions; Sub-Saharan Africa (n = 23), the Middle East and North Africa (n = 2), South Asia (n = 1), Latin America and The Caribbean (n = 1), Europe and Central Asia (n = 1), and East Asia and Pacific (n = 1). Accordingly, this review will address the studies that originated from each of these six regions. In particular, an overview of the incidences of A. baumannii infections, the MDR phenotype spread, the presence of carbapenem-resistance, the associated genetic resistance determinants if available, and any phenotypic or genotypic characterization performed.
3.1. Sub-Saharan Africa
The Sub-Saharan Africa region included a total of 23 countries of the LICs. The reports about A. baumannii in these countries in the searched databases are summarized below. They are arranged in a descending order according to the number of reports related to each country.
Ethiopia is ranked the first among this group in the number of reports about
A. baumannii infections with a total of 10 studies. The first report of the detection of
A. baumannii in this country came in 2012, and it was isolated from human head and body lice collected from healthy individuals [
10]. The genotypic analysis of these isolates showed that these particularly sensitive strains harbored several hundred insertion sequence elements that served in their genome reduction (disruptions of genes and simple loss of DNA). Additionally, it was pointed out that they have low catabolic capacities compared to the human MDR
A. baumannii isolates. This signifies the adaptation of this bacterium to the louse environment [
10]. In the same year,
A. baumannii was reported in human infections for the first time from the ulcers of leprosy patients [
11]. Yet, only 20% of these isolates showed MDR phenotype. It took almost five years to detect MDR
A. baumannii that are carbapenem-resistant harboring the
blaNDM-1 resistance determinant. However, susceptibility testing indicated that they remain susceptible to both polymyxin and amikacin [
12]. Genome sequencing confirmed that the isolates carried the
blaNDM-1; however, they are distinct from the outbreak strains reported from neighboring countries like Kenya. This argued against the regional spread of the
blaNDM-1-positive organism but rather implied the independent environmental dependent generation of the resistance [
12]. Moreover, MDR
A. baumannii was isolated from a hospital’s air setup implicating this troublesome pathogen in the widespread colonization of the hospital’s setting [
13]. The prevalence of MDR and Extended Spectrum Beta-Lactamase (ESBL) producers are reaching alarming rates from the isolated specimens in Ethiopian hospitals [
14,
15,
16]. In another study, 33% of the isolates from nosocomial infections were meropenem-resistant [
17]. The situation got more complicated in other instances where the isolates turned out to be extensively drug resistant (XDR); resistant to at least one agent in all but two or fewer antimicrobial categories, pan-drug-resistant (PDR); resistant to all antibiotic classes [
18,
19].
With only five studies dealing with
A. baumannii infections,
Madagascar came next in the list of LIC nations in this geographical sub-region. The first reports about
A. baumannii outbreaks in Madagascar hospitals came in 2010 [
20,
21]. The isolated strains showed up to 44% carbapenem-resistance, and harboring genes encoding the β-lactamases AmpC, OXA23, and OXA51 [
21]. Interestingly, the emergence of these strains in Madagascar preceded the availability of carbapenems in this country’s hospitals. Nosocomial infections between 2006 and 2013 were caused by carbapenem-resistant
A. baumannii carrying only the
blaOXA23 and
blaOXA51 genes as the only carbapenemase-producing genes [
21]. During the period between 2011 and 2013, MDR
A. baumannii started to show up as one of the causative agents of urinary tract infections (UTI) in Madagascar; however, they were still carbapenem-sensitive [
22]. On the other hand, reports about clinical samples collected between 2013 and 2016 indicated the predominance of Sequence Type 2 (ST2) and the acquisition of carbapenemases
blaOXA24 and
blaOXA58 for the first time since the first outbreak of
A. baumannii in Madagascar [
23]. In 2019,
A. baumannii were detected in human head lice, yet they were negative for
blaOXA23,
blaOXA24,
blaIMP, and
blaVIM [
24].
Four reports have come from
Uganda in the last 21 years reporting the detection of
A. baumannii in the hospitals of this country. A recent report regarded
A. baumannii as a minor cause of sepsis (~1%) in a multisite study [
25]. An earlier report, examining the prevalence of
A. baumannii and its rates of resistance between 2007 and 2009, showed that it was responsible for about 3% of the infections with 31% of these isolates carbapenem-resistant [
26]. What was alarming in this report is that
A. baumannii represented 14% of the environmental samples in the hospital and 55% were carbapenem-resistant. The β-lactamases encoding genes detected in this study included;
blaOXA23-like,
blaOXA24-like,
blaOXA58-like, and
blaVIM-like [
26]. Focusing on the isolates from the same hospital, cluster analysis using repetitive element sequence-based polymerase chain reaction (Rep-PCR) fingerprinting indicated a high level of genetic diversity among the isolates [
27]. Yet, certain MDR isolates from the environment and patients were clustered, indicating possible environmental transmission of these strains to the patients in the hospital. Ten years later and in a follow-up study published in 2019, the same hospital reported a significant decrease in carbapenem resistance prevalence in the isolated
Acinetobacter reaching only 2.7% [
28]. However, all the carbapenemase-producing isolates were MDR and the
blaVIM was the most prevalent carbapenemase-encoding gene. An explanation for this decrease was not discussed by the authors, however a possible one could be the very limited number of the
A. baumannii strains investigated in the earlier study as compared to the very large number of isolates in the later study (more than 1000). Accordingly, the high rates in the earlier study could be an over-estimation of the situation then.
Only two reports about
A. baumannii infections in each of Burkina Faso, Democratic Republic of the Congo, Malawi, Mozambique, and Sudan were published in the last 21 years. For
Burkina Faso, the first report came in 2016 about oral infections and they detected 3
A. baumannii strains out of 125 clinical samples [
29]. All three were MDR and ESBL-positive and the β-lactamases encoding genes identified were
blaTEM and
blaCTX-M. In a more recent study, few
A. baumannii strains were isolated from a hospital there and they belonged to sequence type 2, or what is known as international clone II which has a high distribution worldwide [
30,
31]. On the other hand, in the
Democratic Republic of the Congo (formally known as Zaire), a single report about nosocomial infections caused by
A. baumannii came out in 2017 [
32]. The isolates were not MDR and remained sensitive to both cefotaxime and gentamycin. Another report came from the same country in 2019; however, this time
A. baumannii was isolated from human body lice but without determination of their antibiotic susceptibility patterns [
33]. Regarding
Malawi, a study published in 2012 reported the isolation of only one
A. baumannii strain from a blood-stream infection of an HIV patient [
34]. Following the incidence of bloodstream infections in children ≤5 years in a central hospital in Malawi in 20 years from 1998 to 2017,
A. baumannii increased 10-fold from 0.2% (2003–2007) to 2.2% (2013–2017), and the isolates showed MDR phenotypes [
35]. In
Mozambique, a case of a hospitalized fatal pneumonia caused by an MDR
A. baumannii strain belonging to the international clone II took place in 2014, yet it was not reported until 2018 as a case study [
36]. The same case was reported earlier by another study in 2016 dealing with evaluating minimally invasive autopsy procedures to identify the infectious cause of death in the same hospital [
37]. Finally, for
Sudan, which has moved recently to the LIC group, the first report of
A. baumannii was published in 2019 about the whole genome sequencing of an
A. baumannii strain isolated from a hospitalized patient in the capital, Khartoum [
38]. The sequence analyses indicated that the strain belonged to sequence type 164. In 2020, a survey of antimicrobial resistance in a hospital in Khartoum indicated that
A. baumannii was the most frequent carbapenemase-producing organism (89% of the isolates) and they demonstrated higher resistance rates (100%) for cephalosporins and trimethoprim/sulfamethoxazole [
39].
Only two studies about
A. baumannii in
Rwanda were published with the first one in 2004 and reported ten strains, from three different genotypes, detected in human body louse [
40]. However, a very recent report came in 2020 and indicated the detection of
A. baumannii in flies from a tertiary hospital [
41]. Only one strain of
A. baumannii was detected in this setting, yet its genome carried genes encoding virulence factors that are known to be associated with serum survival and invasion [
41]. Only one study about
A. baumannii in
Burundi was published in 2004, which is the same report as the one mentioned above from the neighboring Rwanda. However, it only reported three strains detected in human body louse from the same genotype [
40]. On the other hand, only one study reported
A. baumannii infection in
Mali, where it represented only 10% of the studied cases of pregnant women with cervicofacial cellulitis [
42]. The isolated strain remained sensitive to amoxicillin/clavulanic acid. While in
Sierra Leone,
A. baumannii was responsible for 14 out of 164 nosocomial infections in an urban tertiary hospital [
43]. The isolated strains were MDR and positive for ESBL, yet the carbapenem-resistance was as low as 10%.
There is only one report that originated from Somalia and was published online in November 2020 that describes the detection of
A. baumannii in a hospital in
Somalia [
44]. In this report,
A. baumannii was the most prevalent pathogen that belonged to MDR and XDR patterns in 69.1% of the samples with isolates showing 100% resistance rates against beta-lactam, cephalosporins, fluoroquinolones, and carbapenems. Finally, only one report about
A. baumannii in head lice and
Niger was published in 2018 [
45]. In this case,
A. baumannii were not detected in head lice from people residing in Niger; however, they were refugees from this country in neighboring Algeria.
No reports were published in the searched three databases for A. baumannii infections in the following countries since the beginning of the 21st century; Central African Republic, Chad, Eritrea, Gambia, Guinea, Guinea-Bissau, Liberia, South Sudan, and Togo. A graphical representation of the distribution of the included studies in the LICs in the Sub-Saharan region is presented in Figure 2.
Figure 2. Reports of
A. baumannii infections in LICs in Sub-Saharan Africa from 2000 to 2020. A geographical map of the Sub-Saharan Africa region highlighting the numbers of reports about
A. baumannii infections in the 21 first years of the 21st century. The map was generated using the MapChart web tool (
https://mapchart.net/, accessed on 21 June 2021).
3.2. Middle East and North Africa
Only two countries belonging to the LIC group are located within this geographical region: Syria and Yemen. Despite being ravaged by wars for many years within the last two decades, the linkage between
Syria and
A. baumannii infections has a very good share in the reports covered in this review; 10 studies. However, most of these reports were including Syrian patients who were treated in hospitals outside Syria especially in neighboring countries. The first report of
A. baumannii in Syria was in 2012 and the study was conducted in a Syrian city showing high rates of MDR strains and the carbapenem-resistance was around 65% among them [
46]. Yet, these strains remained susceptible to colistin. All the later reports dealt with Syrians treated in other countries. Wounded Syrians treated in Jordan showed up to 80% carbapenem-resistance among MDR
A. baumannii infections between August 2011 and March 2013 [
47]. Syrian bone-wounded civilians treated in Jordan and infected with
A. baumannii were also among those reported in another study in 2017 together with wounded civilians from two other wars [
48]. In another study analyzing data in Jordanian hospitals over a decade (2006–2016), 140 Syrians who had bone war wounds were included. This study showed that MDR
A. baumannii was among the causative agents of these infections and the carbapenem-resistance level among these isolates was as high as 66.7% [
49]. Moreover, Syrians treated in Israeli hospitals showed carriage of MDR
A. baumannii [
50]. Concerns about the exporting of NDM-1-producing
A. baumannii strains and/or their genetic determinants from Syria was highlighted in a report from Turkey, where a Syrian refugee was linked to the introduction of the MDR and carbapenem-resistant strains to Turkey, and the strain belonged to sequence type 85 [
51]. More recently in 2019, a Turkish study reported the detection of
A. baumannii (~5%) among the causative agents of infection in Syrian war-injured patients [
52]. As in Turkey, Lebanon too linked the introduction of MDR NDM-1 producing
A. baumannii strains to Syrians injured in the war and transferred to Lebanese hospitals for treatment [
53]. Similar to the Turkish case, the isolates belonged to sequence type 85 showing that Syria could constitute a reservoir for these strains. Two more studies from Lebanon reported the detection of MDR
A. baumannii strains originating in Syria with carbapenem-resistance rates ranging from 74% to 100% [
54,
55].
The second country of the LIC group in the Middle East and North Africa is
Yemen, where the situation is not greatly different from Syria as the country was inflicted with war for many years during the last 21 years. Only one study was reported from inside a hospital in Yemen, where three MDR carbapenem-resistant isolates were investigated [
56]. Genetic analyses indicated that they harbor the
blaOXA23-like, 16S rRNA methylase
armA, and the acetyltransferase
aac(6′)-Ib genes. The three strains belonged to sequence type 2 (ST2) and they were still susceptible to colistin. Yemen was linked to
A. baumannii infections in another study but not for people receiving healthcare inside the country. In these cases, they were bones war-wounded patients hospitalized in Jordan and when detected,
A. baumannii was carbapenem-resistant [
49].