Open access peer-reviewed chapter

Antibiotic Resistance among Iraqi Local E. coli Isolates

Written By

Hussein O.M. Al-Dahmoshi, Noor S.K. Al-Khafaji and Mohammed H.O. Al-Allak

Submitted: 18 December 2019 Reviewed: 13 March 2020 Published: 20 April 2020

DOI: 10.5772/intechopen.92107

From the Edited Volume

E. Coli Infections - Importance of Early Diagnosis and Efficient Treatment

Edited by Luis Rodrigo

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Abstract

Escherichia coli is a famous Gram-negative bacillary bacterium that belongs to Enterobacteriaceae. It is either micro-biota innocent for human or pathogenic with arrays of diseases. The pathogenic E. coli can be assigned to intestinal (InPEC) or extraintestinal (ExPEC) with disease ranging from watery diarrhea to pulmonary distress. The most prevalent form of InPEC is enteropathogenic E. coli (EPEC), while the most prevalent ExPEC is uropathogenic E. coli (UPEC). The other InPEC includes Shiga toxin–producing (STEC), enteroaggregative (EAEC), enterotoxigenic (ETEC), enteroinvasive (EIEC), diffusely adherent (DAEC) and adherent invasive E. coli (AIEC). ExPEC was implicated in cystitis, pyelonephritis, sepsis, respiratory tract infection, cervicovaginal infection (CVEC), meningitis (NMEC), otitis media, cholecystitis and wound infection. Antibiotic resistance is the challenging in world nowadays. Multidrug-resistant (MDR) Escherichia coli has become challenging with existing antibiotic options. E. coli pathogens have various virulence factors that determine their pathogenesis and antimicrobial resistance mechanisms. The rapid and ongoing spread of antimicrobial-resistant organisms threatens our ability to successfully treat a growing number of infectious diseases. It is well established that antibiotic use is a significant, and modifiable, driver of antibiotic resistance. The most commonly used antibiotic classes for InPEC and ExPEC were third-generation cephalosporin, carbapenem, fluoroquinolone and aminoglycosides. Actually, the most effective prescribed medication is one of the following: cefotaxime, ceftriaxone, ciprofloxacin, amikacin, gentamycin, levofloxacin and imipenem. Generally, according to our review for more than 100 local Iraqi studies among Iraqi provinces, the results revealed the resistance rate from highest to lowest as follows: cefotaxime (76.5%), ceftriaxone (75.9%), gentamycin (41.65%), ciprofloxacin (32.13%), amikacin (17.3%), levofloxacin (15%) and imipenem (5.14%). The resistance mechanisms may include genes encoding antibiotic-modifying enzymes like those of extended-spectrum beta-lactamases gene comprising: blaCTX-M, blaTEM, blaSHV, blaOXA, blaPER, blaVIM, blaIMP, blaNDM and blaAMPc. Efflux pumping includes AcrAB, while resistance to quinolone may be mediated by mutation among qnrA, qnrB, qnrD and qnrS. Resistance to aminoglycosides includes encoding to aminoglycoside-modifying enzymes like aac(6)-Ib, aph(3)-I, aph(3)-IIa, aph(3)-Ib, ant(3)-I, aac(3)-II and aac(3)-IV.

Keywords

  • InPEC
  • ExPEC
  • CVEC
  • NMEC
  • DEC
  • blaCTX-M
  • blaTEM
  • blaSHV

1. Introduction

Escherichia coli is prominent Gammaproteobacteria, Gram-negative bacilli live facultatively. It is the principal non-pathogenic facultative flora of the human intestine with harmless effect in healthy individuals. The virulent pathotypes of E. coli strains have the capability to cause a collection of intestinal and extraintestinal diseases, especially in immune-compromised persons [1]. Intestinal disease includes diarrhea or dysentery caused by six pathotypes, while extraintestinal diseases consists of vaginosis, urinary tract infections, respiratory tract infection, otitis media and meningitis [2, 3]. The enteropathogenic or diarrheagenic E. coli is an imperative cause of diarrhea in the newborn, immunocompromised and travelers. It can be assigned to one of the seven pathotypes: enteropathogenic (EPEC), Shiga toxin–producing (STEC), enteroaggregative (EAEC), enterotoxigenic (ETEC), enteroinvasive (EIEC), diffusely adherent (DAEC) and adherent invasive E. coli (AIEC) [4, 5, 6].

Uropathogenic Escherichia coli (UPEC) strains are the most significant causative agents of UTIs in humans. The total prevalence of UTIs caused by the UPEC strains is about 30–70% [7]. UPEC is the most common cause of community- and hospital-acquired urinary tract infections (UTIs). Isolates from uncomplicated community-acquired UTIs express a variety of virulence traits that promote the efficient colonization of the urinary tract. In contrast, nosocomial UTIs can be caused by E. coli strains that differ in their virulence traits from the community-acquired UTI isolates. UPEC virulence markers are used to distinguish these facultative extraintestinal pathogens, which belong to the intestinal flora of many healthy individuals, from intestinal pathogenic E. coli (IPEC) [8, 9].

One of the important extraintestinal E. coli (ExPEC) infections is nosocomial ventilator-associated pneumonia (VAP) with the mortality rate reaching 13%. Until the early 2000s, the ExPEC was not considered as a major pathogen responsible for ventilator-assisted pneumonia that may be due to focusing on other bacteria like Staphylococcus aureus, Acinetobacter baumannii and Pseudomonas aeruginosa [10, 11, 12]. Many studies stated the high frequency of ExPEC among VAP even more than Staphylococcus aureus and Pseudomonas aeruginosa. In developing countries, both hospital- and community-acquired respiratory tract infections (RTIs) are linked with emerging MDR E. coli [13, 14, 15].

Escherichia coli is most commonly associated with bloodstream infections and death due to sepsis. Sepsis is a life-threatening clinical condition affecting more than 40 million worldwide with mortality rate more than 15%. The incidence of sepsis caused by Gram-negative bacteria, such as Escherichia coli (E. coli), has been steadily increasing since the late 1990s. It ranks as the leading cause of death in intensive care units. E. coli accounts for approximately 14.1% of early onset neonatal sepsis and it is the second most common pathogen, along with coagulase negative Staphylococcus, after group B Streptococcus (GBS)2 [16, 17, 18].

Escherichia coli (especially K1) is one of the most common causative pathogens of neonatal meningitis, but the presence of E coli in an immunocompetent adult, causing meningitis, is rare with an annual incidence of less than one case per year. The penetration of E. coli through the blood-brain barrier is a key step of the meningitis pathogenesis. Diabetes mellitus, alcoholism, cirrhosis, HIV infection and malignancies are some of the risk factors to develop E coli meningitis. A distant source is usually identified, either from the urinary or the digestive tract [19, 20, 21, 22].

According to the World Health Organization, Enterobacteriaceae, including Escherichia coli, are among the critical priority antibiotic-resistant bacteria. Multidrug-resistant (MDR) Escherichia coli has been listed as a priority pathogen by the World Health Organization (WHO) due to emerging antimicrobial resistance (AMR) [23, 24].

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2. Escherichia coli diseases and antibiotic resistance

E. coli causes a wide range of diseases that can be assigned to either intestinal caused by intestinal E. coli (InPEC) or extraintestinal caused by extraintestinal E. coli (ExPEC) [25]. The most important diseases are as follows:

2.1 ExPEC-associated cystitis and antibiotic resistance

Cystitis is a common and expensive condition that impacts humans of different age groups from the neonate till geriatric age group. It is a pathogenic inflammation of the lower urinary tract. Women are more commonly afflicted with UTIs, and they are caused by common pathogens such as Escherichia coli (86%) [26]. Uropathogenic Escherichia coli (UPEC) is significantly associated with cystitis via sets of virulence factors (adhesins, siderophores, toxins, capsule production and protease) that assist its colonization, invasion, and survival within the host urinary system [27, 28]. High recurrence rates and increasing antimicrobial resistance among UPEC threaten to greatly increase the economic burden of these UTIs [5]. The resistance rate of Iraqi local UPEC to different antibiotic classes is summarized in Table 1. The resistance genes are listed in Table 2.

AntibioticNo. of isolate/studyResistance %ProvinceReference
Cefotaxime24685.13Babylon[34, 40, 41, 42, 43]
7688.9Najaf[30]
6276.9Karbala[44]
9175.8Wasit[36]
5082.5Saladin[45]
9089.15Erbil[46]
10652Zakho[47]
23470Kirkuk[48]
38170.8Duhok[49, 50]
5078Sulemania[51]
Ceftriaxone17681.21Babylon[34, 40, 41, 43]
62100Karbala[44]
8175Missan[31]
9174.7Wasit[36]
773.15Anbar[33]
9052Erbil[46]
10670Zakho[47]
23467Kirkuk[48]
38171.3Duhok[49, 50]
5034.5Sulemania[51]
Ciprofloxacin25841.73Babylon[9, 34, 40, 41, 43, 52]
6068.3Baghdad[53]
5072.5Saladin[45]
1425Tikrit[54]
38153.25Duhok[49, 50]
11324.8Anbar[55]
5052.6Sulemania[51]
5052.6Erbil[39]
8123.4Missan[31]
9140.6Wasit[36]
Levofloxacin10238.5Babylon[42, 50]
140Tikrit[54]
Amikacin32225.1Babylon[29, 34, 40, 41, 43, 51, 52]
6224Sulemania[44]
5095Karbala[45]
9025.15Saladin[46, 51]
145Erbil[54]
2345.9Tikrit[48]
3310.85Kirkuk[48]
5046Duhok[49, 50]
1139.8Anbar[55]
8111.1Missan[31]
919.8Wasit[36]
Gentamycin28637.48Babylon[29, 34, 40, 41, 42, 43, 52]
10674.35Sulemania[30]
7622.2Najaf[45]
5075Saladin[46]
9064.5Erbil[54]
1425Tikrit[48]
38151.2Duhok[49, 50]
11350Anbar[55]
8111.1Missan[31]
9146.1Wasit[36]
Imipenem4211.9Babylon[41]
725Anbar[33]
910Wasit[36]
1060Zakho[47]
2341.5Kirkuk[48]
3812.25Duhok[49, 50]
1134.5Anbar[55]
504.7Sulemania[51]
504.7Erbil[54]

Table 1.

Distribution of antibiotic resistance among Iraqi local UPEC.

Antibiotic classGenesProvinceReference
QuinolonesqnrA, qnrB, qnrD, qnrSBabylon[9]
Beta-lactamblaTEM, blaCTX-MSulemania[29]
Beta-lactamblaTEM, blaCTX-M, blaSHVNajaf[30, 31, 32]
Beta-lactamblaSHVAnbar[33]
Beta-lactamblaTEM, blaCTX-M, blaSHV, blaOXA, AmpCBabylon[34]
Beta-lactamblaCTX-M14, blaCTX-M15
blaCTX-M24, blaCTX-M27
Duhok[35]
Beta-lactamsblaTEM, blaCTX-M, blaSHV
blaOXA
Wasit[36]
Beta-lactamsblaCTX-MKarbala[37]
Beta-lactamsblaTEM, blaPER, blaVIM and blaCTX-M-2, blaTEM,Baghdad[38]
Aminoglycosidesaac(6)-Ib, aph(3)-I, aph(3)-IIa
aph(3)-Ib, ant(3)-I, aac(3)-II
aac(3)-IV
Najaf[31, 39]

Table 2.

Antibiotic resistance genes among Iraqi local UPEC.

The average resistance rate is as follows: cefotaxime (77%), ceftriaxone (70%), ciprofloxacin (45.47%), amikacin (23.42%), gentamycin (45.69%) and imipenem (6.06%). Resistance to beta-lactams was attributed to many mechanisms, and one of them is to the modifying enzymes especially blaTEM, blaSHV, blaCTX-M, blaOXA, blaPER and blaVIM, while resistance to ciprofloxacin was interpreted due to the presence of qnrA, qnrB, qnrD and qnrS genes [9, 29, 30, 31, 32, 33, 34, 35, 36, 37]. Resistance to aminoglycosides among UPEC may be mediated by aac(6)-Ib, aph(3)-I, aph(3)-IIa, aph(3)-Ib, ant(3)-I, aac(3)-II and aac(3)-IV [31, 39].

2.2 ExPEC-associated sepsis and RTIs antibiotic resistance

Lower respiratory tract infections are a leading cause of morbidity and death worldwide. Optimizing the treatment of respiratory tract infections (RTIs) caused by multidrug-resistant (MDR) Escherichia coli has become challenging with existing antibiotic options. E. coli pathogens have various virulence factors that determine their pathogenesis and antimicrobial resistance (AMR) mechanisms [38]. The rapid and ongoing spread of antimicrobial-resistant organisms threatens our ability to successfully treat a growing number of infectious diseases. It is well established that antibiotic use is a significant, and modifiable, driver of antibiotic resistance [56, 57]. Physician visits for respiratory tract infections (RTI) commonly result in an antibiotic prescription, despite the fact that most upper RTIs are viral in nature. In these cases, antibiotics provide no benefit; thus, guidelines limit their recommended use to certain situations where the etiology is likely bacterial [58, 59, 60].

Over- and inappropriate prescribing of antibiotics is highly prevalent in the primary care setting, especially for upper respiratory tract infections (URTIs). In the outpatient setting, URTIs account for approximately 50–70% of total antibiotic prescriptions, even though most cases are of viral origin [61, 62]. The overuse of broad-spectrum antibiotics, such as third-generation cephalosporins, amoxicillin-clavulanate and fluoroquinolones, is strongly associated with the emergence of resistant strains, does not provide better clinical outcomes, and may lead to adverse events as well as unnecessary costs. Reducing unnecessary antibiotic prescriptions and the overuse of broad-spectrum agents may contain antimicrobial resistance and preserve the efficacy of existing antibiotics [63, 64, 65].

The Iraqi studies dealing with antibiotic resistance among sepsis-associated E. coli are summarized in Table 3. Most E. coli strains isolated from bloodstream were resistant to most antimicrobials particularly β-lactam antibiotics and third-generation cephalosporins. It might be that long-term exposure to these antimicrobials by patients infected with bacteremia leads to horizontal transfer of plasmid-resistant antimicrobial genes between different strains of bacteria [66].

AntibioticNo. of isolate/studyResistance %ProvinceReference
Cefotaxime792Najaf[66]
19, 42, 294.8, 95.2, 100Duhok[67, 68, 69]
941Karbala[70]
4151.1Baghdad[71]
Ceftriaxone790Najaf[66]
19, 4294.8, 93Duhok[67, 68]
929Karbala[70]
Ciprofloxacin746Najaf[66]
190.0Duhok[67, 68]
Amikacin744Najaf[66]
19, 42, 20.0, 35.7, 0.0Duhok[67, 68, 69]
930Karbala[70]
4122Baghdad[71]
Gentamycin746Najaf[66]
19, 42, 278.5, 52.4, 40Duhok[67, 68, 69]
938Karbala[70]
41, 1722, 29.4Baghdad[71, 72]
Imipenem76Najaf[66]
19, 42, 20.0, 9.5, 0.0Duhok[67, 68, 69]
92Karbala[70]

Table 3.

Distribution of antibiotic resistance among Iraqi local sepsis-associated E. coli.

The average resistance rate is as follows: cefotaxime (79%), ceftriaxone (76.7%), ciprofloxacin (23%), amikacin (21.95%), gentamycin (43.7%) and imipenem (3.5%). The third-generation cephalosporins were the most commonly prescribed antibiotics compiling 54.3% followed by quinolones 7.5% of all prescribed antibiotics. Cefotaxime and ceftriaxone seem to be the preferred prescribed antibiotic for both surgical and medical wards [32].

2.3 InPEC-associated diarrheagenic infection and antibiotic resistance

Diarrhea is one of the major causes of serious issues among children in the developing world. More than 4 million children die annually from diarrhea in developing world. Diarrheagenic E. coli (DEC) is the most common cause of bacterial diarrhea in children worldwide and responsible for about 600,000 deaths per year [73, 74]. Diarrheagenic E. coli infection manifests as watery or bloody diarrhea accompanied by mild-to-severe dehydration. Βeta-lactamases are a big problem when produced by DEC rendering the infection hard to be treated or untreatable. The arising of resistance toward extended-spectrum cephalosporins is most often due to hydrolyzing them by extended-spectrum β-lactamases (ESBLs) or due to AmpC. AmpC β-lactamases can prompt resistance to cephalothin, cefoxitin, cefazolin, most penicillins and beta-lactamase inhibitor-beta-lactam combinations. Escherichia coli isolates with CTX-M ESBLs are spreading multiresistance in the community and in hospitals [75, 76]. The resistance rate of Iraqi local diarrheagenic E. coli to different antibiotic classes is summarized in Table 4. The resistance genes are listed in Table 5.

AntibioticNo. of isolate/studyResistance %ProvinceReference
Cefotaxime1892Najaf[66]
89, 39, 11482.9, 89.7, 100Babylon[76, 77, 78]
100, 14571.4, 96.4Wasit[79, 80]
51, 374, 54Baghdad[81, 82]
3096.7Tikrit[83]
Ceftriaxone1890Najaf[66]
89, 39, 11474.6, 79.5, 100Babylon[76, 77, 78]
10081Wasit[79]
3740.5Baghdad[82]
16376.66Basra[84]
3096.7Tikrit[83]
Ciprofloxacin1846Najaf[66]
89, 39, 1140.0, 15.8, 72.7Babylon[76, 77, 78]
24, 51, 370.0, 8, 45.9Baghdad[81, 82, 85]
14525Wasit[80]
3023.3Tikrit[83]
Amikacin18, 53544, 0.0Najaf[66, 86]
89, 39, 11422.6, 12.8, 36.4Babylon[76, 77, 78]
100, 1457.1, 50Wasit[79, 85]
24, 51, 3716.6, 59, 67.5Baghdad[81, 82, 85]
3040Tikrit[83]
Gentamycin18, 53546, 9.1Najaf[66, 86]
89, 39, 1142.8, 51.3, 54.5Babylon[76, 77, 78]
24, 51, 370.0, 16, 100Baghdad[81, 82, 85]
14557.14Wasit[80]
3020Tikrit[83]
Imipenem18, 5356, 0.0Najaf[66, 86]
89, 1149.5, 36.4Babylon[76, 77, 78]
100, 1450.0, 0.0Wasit[79, 80]
3713.5Baghdad[82]
1630.0Basra[84]

Table 4.

Distribution of antibiotic resistance among Iraqi local diarrheagenic E. coli.

Antibiotic classGenesProvinceReference
Beta-lactamsblaTEM, blaCTX-M, blaSHV, blaOXA, AmpCNajaf[86]

Table 5.

Antibiotic resistance genes among Iraqi local diarrheagenic E. coli.

The average resistance rate is as follows: cefotaxime (76.34%), ceftriaxone (79.87%), ciprofloxacin (26.3%), amikacin (31.21%), gentamycin (35.68%) and imipenem (8.18%).

The possible explanation to high level of resistance to this drug may be as a result of it being the most commonly available antibiotic used as a routine therapy among gastrointestinal infections and people readily purchasing it across the counter for self-medication in last years. This could be a reflection of use and misuse of these antibiotics in the society. This finding is a result of the fact that outside the hospital environment the general population has easy access to various antibiotics from any pharmacy without prescription from a doctor [82].

2.4 ExPEC-associated vaginosis and antibiotic resistance

Bacterial vaginosis (BV) is the most common vaginal infections among women in reproductive age. It is a condition of vaginal flora imbalance, in which the typically plentiful H2O2-producing lactobacilli are scarce and other bacteria such as E. coli are abundant [87, 88]. Multi-drug resistant cervicovaginal Escherichia coli (CVEC) infections are a serious health problem. Bacteria use several strategies to avoid the effects of antimicrobial agents and have evolved a highly efficient means for clonal spread and for the dissemination of resistance traits [4]. Extended-spectrum β-lactamases (ESBLs) are capable of hydrolyzing broad-spectrum cephalosporins and monobactams. In addition, ESBL-producing organisms exhibit co-resistance to many other classes of antibiotics resulting in limitation of therapeutic options. Vaginal E. coli represents a real threat especially to neonates; however, little information is available regarding its antibiotic resistance [89, 90]. The resistance rate of Iraqi local cervicovaginal E. coli to different antibiotic classes is summarized in Table 6. The resistance genes are listed in Table 7.

AntibioticNo. of isolate/studyResistance %ProvinceReference
Cefotaxime3262.5Babylon[88]
5186.2Wasit[91]
Ceftriaxone3250Babylon[88]
5145Wasit[91]
Ciprofloxacin5129.4Wasit[91]
Gentamycin5125.4Wasit[91]
Imipenem3215.6Babylon[88]
510.0Wasit[91]

Table 6.

Distribution of antibiotic resistance among Iraqi local cervicovaginal E. coli.

Antibiotic classGenesProvinceReference
Beta-lactamasesblaCTX-M, blaSHV, blaOXAWasit[91]

Table 7.

Antibiotic resistance genes among Iraqi local cervicovaginal E. coli.

The average resistance rate is as follows: cefotaxime (75%), ceftriaxone (47.5%), ciprofloxacin (29.4%), gentamycin (25.4%) and imipenem (7.8%).

2.5 ExPEC-associated otitis media, meningitis and cholecystitis infection and antibiotic resistance

Ear infection is a common clinical problem throughout the world and the major cause of preventable hearing loss in the developing world [92]. Its chronic form is a serious problem in all age groups with less chance of recovery. In certain cases, this condition can lead to serious life-threatening complications, such as hearing impairment, brain abscesses or meningitis, mostly in childhood and late in life [93]. E. coli is one of the major causative agents of ear infection. The burden and prevalence of ear infection are more intense in developing countries due to the poor living standard and hygienic conditions along with a lack of proper nutrition. Increased antimicrobial resistance is one of the greatest global public health challenges, which has been accelerated by overprescription of antibiotics worldwide. Infection with antibiotic-resistant bacteria may cause severe illness, increased mortality rates and an increased risk of complications and admission to hospital and longer stay. E. coli was the most prevalent multi-antibiotic-resistant pathogenic bacteria isolated from suspected patient ear discharges with otitis media [94, 95, 96].

Gram-negative bacillary meningitis continues to be an important cause of mortality and morbidity (15% and 50%, respectively) throughout the world despite advances in antimicrobial chemotherapy and supportive care [97]. E. coli is the most common Gram-negative bacillary organism causing meningitis. Recent reports of E. coli strains producing CTX-M-type or TEM-type extended-spectrum β-lactamases create a challenge. E. coli meningitis follows a high degree of bacteremia and invasion of the blood-brain barrier [21, 98].

Cholecystitis is most often caused by gall stones. Gall stones are one of the most common disorders of the gastrointestinal tract. Bacterial infection accounts for 50–85% of the disease’s onset. Escherichia coli was the main biliary pathogenic microorganism [99]. It is strongly associated with retrograde bacterial infection and is an inflammatory disease that can be fatal if inappropriately treated [100]. The resistance rate of Iraqi local E. coli isolated from otitis media, meningitis and cholecystitis to different antibiotic classes is summarized in Table 8. The resistance genes are listed in Table 9.

AntibioticNo. of isolate/studyResistance %ProvinceReference
Cefotaxime93100Anbar[101]
2276Najaf[102]
2100Baghdad[103]
714.29Babylon[104]
Ceftriaxone9390.57Anbar[101]
2276Najaf[102]
250Baghdad[103]
757Babylon[104]
Ciprofloxacin1020Basra[105]
9398.11Anbar[101]
2276Najaf[102]
50.0Tikrit[106]
714.29Babylon[104]
Levofloxacin2262Najaf[102]
Amikacin1020Basra[105]
2214Najaf[102]
20.0Baghdad[103]
50.0Tikrit[106]
Gentamycin1020Basra[105]
4100Thi-Qar[107]
2244.8Najaf[102]
250Baghdad[103]
70.0Babylon[104]
Imipenem220Najaf[102]

Table 8.

Distribution of antibiotic resistance among Iraqi local E. coli associated with otitis media, meningitis and cholecystitis.

Antibiotic classGenesProvinceReference
Beta-lactamasesacrABAnbar[101]
QuinolonegyrA, parCAnbar[101]
Beta-lactamasesblaCTX-M, blaSHV, blaOXA, blaTEMNajaf[102]
Beta-lactamasesblaCTX-M, blaSHV, blaOXA, blaTEMAl-Qadisiyah[108]

Table 9.

Antibiotic resistance genes among Iraqi local E. coli associated with otitis media, meningitis and cholecystitis.

The average resistance rate is as follows: cefotaxime (72.57%), ceftriaxone (68.39%), ciprofloxacin (8.5%), gentamycin (42.46%) and imipenem (0%).

2.6 ExPEC-associated wound infection and antibiotic resistance

A wound can represent a simple or a severe disorder to an organ (such as the skin) or a tissue and can spread to other tissues and anatomical structures (e.g., subcutaneous tissue, muscles, tendons, nerves, vessels and even to the bone). Among all human body (HB) organs, the skin is without doubt the most exposed to impairment and injury, scratches and burns. By damaging the epithelium and connective structures, the HB’s capability to provide protection from the outer environment is weakened [109]. An improper repair process can cause severe damage, like the loss of skin, initiation of an infection, with consequent harms to the subjacent tissues and even systemic ones. The most common and inevitable impediment to wound healing is the installation of an infection [110].

Skin and soft tissue infections (SSTIs) are one of the most common infections in patients of all age groups. The most common causative agents are Staphylococcus aureus and aerobic streptococci. However, several reports associating the Escherichia coli with SSTI have been published: E. coli was found to be the causative agent of neonatal omphalitis, cellulitis localized to lower or upper limbs, necrotizing fasciitis, surgical site infections, infections after burn injuries and others [111, 112]. Cellulitis due to Escherichia coli is rare and usually secondary to a cutaneous portal of entry. Skin and soft tissue infections (SSTIs) secondary to E. coli bacteremia have been reported exclusively in immunodeficient patients. The resistance rate of Iraqi local E. coli isolated from wound infection to different antibiotic classes is summarized in Table 10. The resistance genes are listed in Table 11.

AntibioticNo. of isolate/studyResistance %ProvinceReference
Cefotaximes785Karbala[113]
165100Baghdad[101]
290Anbar[114]
933.33Karbala[115]
4100Baghdad[116]
1688.09Baghdad[117]
5174.5Najaf[118]
Ceftriaxone777Karbala[113]
16590.57Baghdad[101]
290Anbar[114]
4100Baghdad[116]
7100Erbil[119]
1983.8Erbil[120]
1575Erbil[121]
5168.6Najaf[118]
Ciprofloxacin742Karbala[113]
16598.11Baghdad[101]
220Anbar[114]
9100Karbala[115]
450Baghdad[116]
785.8Erbil[119]
1673.8Baghdad[117]
1954.4Erbil[120]
1516.66Erbil[121]
5135.2Najaf[118]
2885.7Diyala[122]
Levofloxacin220Anbar[114]
40.0Baghdad[116]
785.8Erbil[119]
1673.8Baghdad[117]
1517.7Erbil[121]
Amikacin220Anbar[114]
922.22Karbala[115]
475Baghdad[116]
714.2Erbil[119]
191.9Erbil[120]
1518.33Erbil[121]
5139.2Najaf[118]
Gentamycin755Karbala[113]
290Anbar[114]
966.67Karbala[115]
757.1Erbil[119]
1635.71Baghdad[117]
1940.6Erbil[120]
1525Erbil[121]
5178.4Najaf[118]
2864.3Diyala[122]
Imipenem210Anbar[114]
922.2Karbala[115]
40.0Baghdad[116]
70.0Erbil[119]
164.76Baghdad[117]
191.25Erbil[120]
155Erbil[121]
510.0Najaf[118]

Table 10.

Distribution of antibiotic resistance among Iraqi local E. coli associated with wound infections.

Antibiotic classGenesProvinceReference
Beta-lactamasesblaNDM-1Baghdad[123]
CarbapenemblaIMPBaghdad[124]
Beta-lactamasesblaNDM-1Basra[125]
Beta-lactamasesblaCTX-MErbil[121]
Beta-lactamasesblaTEM, blaSHV, blaOXA51Babylon[126]

Table 11.

Antibiotic resistance genes among Iraqi local E. coli associated with wound infections.

The average resistance rate is as follows: cefotaximes (81.56%), ceftriaxone (85.62%), ciprofloxacin (60.15%), levofloxacin (39.54%), amikacin (27.26%), gentamycin (56.97%) and imipenem (5.4%).

References

  1. 1. Gomes TA, Elias WP, Scaletsky IC, Guth BE, Rodrigues JF, Piazza RM, et al. Diarrheagenic Escherichia coli. Brazilian Journal of Microbiology. 2016;47:3-30. DOI: 10.1016/j.bjm.2016.10.015
  2. 2. Foxman B. The epidemiology of urinary tract infection. Nature Reviews Urology. 2010;7(12):653. DOI: 10.1038/nrurol.2010.190
  3. 3. Foxman B, Wu J, Farrer EC, Goldberg DE, Younger JG, Xi C. Early development of bacterial community diversity in emergently placed urinary catheters. BMC Research Notes. 2012;5(1):332. DOI: 10.1186/1756-0500-5-332
  4. 4. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nature Reviews Microbiology. 2004;2(2):123-140. DOI: 10.1038/nrmicro818
  5. 5. Cabrera-Sosa L, Ochoa TJ. Escherichia coli diarrhea. In: Hunter’s Tropical Medicine and Emerging Infectious Diseases. 10th ed. Elsevier. 2020. pp. 481-485. DOI: 10.1016/B978-0-323-55512-8.00046-6
  6. 6. Zhang J, Xu Y, Ling X, Zhou Y, Lin Z, Huang Z, et al. Identification of diarrheagenic Escherichia coli by a new multiplex PCR assay and capillary electrophoresis. Molecular and Cellular Probes. 2020;49:101477. DOI: 10.1016/j.mcp.2019.101477
  7. 7. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: Epidemiology, mechanisms of infection and treatment options. Nature Reviews Microbiology. 2015;13(5):269-284. DOI: 10.1038/nrmicro3432
  8. 8. Toval F, Köhler CD, Vogel U, Wagenlehner F, Mellmann A, Fruth A, et al. Characterization of Escherichia coli isolates from hospital inpatients or outpatients with urinary tract infection. Journal of Clinical Microbiology. 2014;52(2):407-418. DOI: 10.1128/JCM.02069-13
  9. 9. Al-Hasnawy HH, Jodi MR, Hamza HJ. Molecular characterization and sequence analysis of plasmid-mediated quinolone resistance genes in extended-spectrum beta-lactamases producing uropathogenic Escherichia coli in Babylon Province, Iraq. Reviews in Medical Microbiology. 2018;29(3):129-135. DOI: 10.1097/MRM.0000000000000136
  10. 10. Melsen WG, Rovers MM, Groenwold RH, Bergmans DC, Camus C, Bauer TT, et al. Attributable mortality of ventilator-associated pneumonia: A meta-analysis of individual patient data from randomised prevention studies. The Lancet Infectious Diseases. 2013;13(8):665-671. DOI: 10.1016/S1473-3099(13)70081-1
  11. 11. Chastre J, Fagon JY. Ventilator-associated pneumonia. American Journal of Respiratory and Critical Care Medicine. 2002;165(7):867-903. DOI: 10.1164/ajrccm.165.7.2105078
  12. 12. Russo TA, Johnson JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: Focus on an increasingly important endemic problem. Microbes and Infection. 2003;5(5):449-456. DOI: 10.1016/S1286-4579(03)00049-2
  13. 13. Fihman V, Messika J, Hajage D, Tournier V, Gaudry S, Magdoud F, et al. Five-year trends for ventilator-associated pneumonia: Correlation between microbiological findings and antimicrobial drug consumption. International Journal of Antimicrobial Agents. 2015;46(5):518-525. DOI: 10.1016/j.ijantimicag.2015.07.010
  14. 14. Kollef MH, Ricard JD, Roux D, Francois B, Ischaki E, Rozgonyi Z, et al. A randomized trial of the amikacin fosfomycin inhalation system for the adjunctive therapy of Gram-negative ventilator-associated pneumonia: IASIS Trial. Chest. 2017;151(6):1239-1246. DOI: 10.1016/j.chest.2016.11.026
  15. 15. Atia A, Elyounsi N, Abired A, Wanis A, Ashour A. Antibiotic resistance pattern of bacteria isolated from patients with upper respiratory tract infections; a four year study in Tripoli city. Preprint. 20182018080435. DOI: 10.20944/preprints201808.0435.v1
  16. 16. Zhang K, Schneider D, Biswas R, Espriella MG, Rao J, Baffoe-Bonnie A. 2603. Biofilm formation as a predictive marker of prognosis for Escherichia coli sepsis. InOpen Forum Infectious Diseases. 2019;6:S904-S905. DOI: 10.1093/ofid/ofz360.2281
  17. 17. Gallardo L, Bauer M, Pannullo N, Michel LV. Determining the role of pal in Escherichia coli sepsis. The FASEB Journal. 2019;33(1_supplement):648-643. DOI: 10.1096/fasebj.2019.33.1_supplement.648.3
  18. 18. Pierpaoli E, Cirioni O, Simonetti O, Orlando F, Giacometti A, Lombardi P, et al. Potential application of berberine in the treatment of Escherichia coli sepsis. Natural Product Research. 2020;31:1-6. DOI: 10.1080/14786419.2020.1721729
  19. 19. Xu X, Zhang L, Cai Y, Liu D, Shang Z, Ren Q , et al. Inhibitor discovery for the E. coli meningitis virulence factor IbeA from homology modeling and virtual screening. Journal of Computer-Aided Molecular Design. 2020;34(1):11-25. DOI: 10.1007/s10822-019-00250-8
  20. 20. Kim M, Simon J, Mirza K, Swong K, Johans S, Riedy L, et al. Spinal Intradural Escherichia coli abscess masquerading as a neoplasm in a pediatric patient with history of neonatal E. coli meningitis: A case report and literature review. World Neurosurgery. 2019;126:619-623. DOI: 10.1016/j.wneu.2019.02.243
  21. 21. Kasimahanti R, Satish SK, Anand M. Community-acquired Escherichia coli meningitis with ventriculitis in an adult—A rare case report. Journal of Intensive Care. 2018;6(1):1-5. DOI: 10.1186/s40560-018-0332-6
  22. 22. Bichon A, Aubry C, Dubourg G, Drouet H, Lagier JC, Raoult D, et al. Escherichia coli spontaneous community-acquired meningitis in adults: A case report and literature review. International Journal of Infectious Diseases. 2018;67:70-74. DOI: 10.1016/j.ijid.2017.12.003
  23. 23. Shrivastava SR, Shrivastava PS, Ramasamy J. World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. Journal of Medical Society. 2018;32:76-77. DOI: 10.4103/jms.jms_25_17
  24. 24. Rodrigo-Troyano A, Sibila O. The respiratory threat posed by multidrug resistant gram-negative bacteria. Respirology. 2017;22(7):1288-1299. DOI: 10.1111/resp.13115
  25. 25. Masters N, Wiegand A, Ahmed W, Katouli M. Escherichia coli virulence genes profile of surface waters as an indicator of water quality. Water Research. 2011;45(19):6321-6333. DOI: 10.1016/j.watres.2011.09.018
  26. 26. Markowitz MA, Wood LN, Raz S, Miller LG, Haake DA, Kim JH. Lack of uniformity among United States recommendations for diagnosis and management of acute, uncomplicated cystitis. International Urogynecology Journal. 2019;30(7):1187-1194. DOI: 10.1007/s00192-018-3750-z
  27. 27. Zude I, Leimbach A, Dobrindt U. Prevalence of autotransporters in Escherichia coli: What is the impact of phylogeny and pathotype? International Journal of Medical Microbiology. 2014;304(3-4):243-256. DOI: 10.1016/j.ijmm.2013.10.006
  28. 28. Behzadi P, Najafi A, Behzadi E, Ranjbar R. Microarray long oligo probe designing for Escherichia coli: An in-silico DNA marker extraction. Central European Journal of Urology. 2016;69(1):105. DOI: 10.1016/j.ijmm.2013.10.006
  29. 29. Saeed NM. Detection of extended spectrum beta-lactamase gene production by E. coli isolated from human and broiler in Sulemania province/Iraq. Journal of Zankoy Sulaimani-Part A. 2014;16:2. DOI: 10.17656/jzs.10296
  30. 30. Alkhudhairy MK, Alshammari MM. Extended spectrum β-lactamase-producing Escherichia coli isolated from pregnant women with asymptomatic UTI in Iraq. EurAsian Journal of BioSciences. 2019;13(2):1881-1889
  31. 31. Alquraishi ZH, Alabbasy AJ, Alsadawi AA. Genotype and phenotype detection of E. coli isolated from children suffering from urinary tract infection. Journal of Global Pharmacy Technology. 2018;10(1):38-45
  32. 32. Majeed HT, Aljanaby AA. Antibiotic susceptibility patterns and prevalence of some extended spectrum beta-lactamases genes in gram-negative bacteria isolated from patients infected with urinary tract infections in Al-Najaf City, Iraq. Avicenna Journal of Medical Biotechnology. 2019;11(2):192
  33. 33. Al-Ouqaili MT. Molecular detection and sequencing of SHV gene encoding for extended-spectrum β-lactamases produced by multidrug resistance some of the gram-negative bacteria. International Journal of Green Pharmacy (IJGP). 2019;12(04):S910-S918. DOI: 10.22377/ijgp.v12i04.2274
  34. 34. Al-Charrakh AH, AL-Tememy AZ. Phenotypic and genotypic characterization of IRS-producing Escherichia coli isolated from patients with UTI in Iraq. Medical Journal of Babylon. 2015;12(1):80-95
  35. 35. Michael NS, Saadi AT. Detection of bla CTX-M, bla TEM-01 and bla SHV genes in multidrug resistant uropathogenic E. coli isolated from patients with recurrent urinary tract infections. International Journal of Medical Research & Health Sciences. 2018;7(9):81-89
  36. 36. Al-Mayahie S, Al Kuriashy JJ. Distribution of ESBLs among Escherichia coli isolates from outpatients with recurrent UTIs and their antimicrobial resistance. The Journal of Infection in Developing Countries. 2016;10(06):575-583. DOI: 10.3855/jidc 6661
  37. 37. Zirjawi AM, Hussein NH, Taha BM, Hussein JD. Molecular detection of Ctx-M-Β-lactamases in Pseudomonas aerogenosa strains isolated from corneal infections. European Journal of Biomedical. 2017;4(4):70-74
  38. 38. Promite S, Saha SK. Escherichia coli in respiratory tract infections: Evaluating antimicrobial resistance and prevalence of fimA, neuC and iutA virulence genes. Gene Reports. 2020;18:100576. DOI: 10.1016/j.genrep.2019.100576
  39. 39. Alm’amoori KO, Hadi ZJ, Almohana AM. Molecular investigation of aminoglycoside modifying enzyme among aminoglycoside-resistant uropathogenic Escherichia coli isolates from Najaf Hospitals, Iraq. Indian Journal of Public Health Research & Development. 2019;10(10):2298-2303. DOI: 10.5958/0976-5506.2019.03199.1
  40. 40. Alhamdany MH. Antibiotic susceptibility of bacteria isolated from patients with diabetes mellitus and recurrent urinary tract infections in Babylon Province, Iraq. Medical Journal of Babylon. 2018;15(1):63-68. DOI: 10.4103/MJBL.MJBL_16_18
  41. 41. Al-Hasnawy HH, Judi MR, Hamza HJ. The dissemination of multidrug resistance (MDR) and extensively drug resistant (XDR) among uropathogenic E. coli (UPEC) isolates from urinary tract infection patients in Babylon Province, Iraq. Baghdad Science Journal. 2019;16(4 Supplement):986-922. DOI: 10.21123/bsj.2019.16.4(Suppl.).0000
  42. 42. AL-Sa’ady AT, Al-Mawla YH. Comparison of effects antibiotics and natural honey and extracts of plants on Escherichia coli growth isolated from different pathogenic cases. Journal of University of Babylon for Pure and Applied Sciences. 2019;27(3):420-434
  43. 43. Abed ZH, Jarallah EM. Antibiotics susceptibility pattern of clinical and environmental Escherichia coli isolates from Babylon hospitals. In Journal of Physics: Conference Series. 2019;1294(6):062105. DOI: 0.1088/1742-6596/1294/6/062105
  44. 44. Mohammed S, Ahmed M, Karem K. Incidence of multi-drug resistant Escherichia coli isolates from blood and urine in Kerbala, Iraq. Journal of Kerbala University. 2014;12(4):222-227
  45. 45. AL-Samarraie MQ , Omar MK, Yaseen AH, Mahmood MI. The wide spread of the gene haeomolysin (Hly) and the adhesion factor (Sfa) in the E. coli isolated from UTI. Journal of Pharmaceutical Sciences and Research. 2019;11(4):1298-1303
  46. 46. Mansoor IY, AL-Otraqchi KI, Saeed CH. Prevalence of urinary tract infections and antibiotics susceptibility pattern among infants and young children in Erbil city. Zanco Journal of Medical Sciences. 2015;19(1):915-922. DOI: 10.15218/zjms.2015.0012
  47. 47. Polse R, Yousif S, Assafi M. Prevalence and antimicrobial susceptibility patterns of uropathogenic E. coli among people in Zakho, Iraq. International Journal of Research in Medical Sciences. 2016;4(4):1219-1223. DOI: 10.18203/2320-6012.ijrms20160813
  48. 48. Alsamarai AG, Ali S. Urinary Tract Infection in Female in Kirkuk City, Iraq: Causative Agents and Antibiogram. Vol. 5. WJPPS; 2016. pp. 261-273. DOI: 10.20959/wjpps20166-6807
  49. 49. Assafi MS, Ibrahim NM, Hussein NR, Taha AA, Balatay AA. Urinary bacterial profile and antibiotic susceptibility pattern among patients with urinary tract infection in Duhok city, Kurdistan region, Iraq. International Journal of Pure and Applied Sciences and Technology. 2015;30(2):54
  50. 50. Hussein NR, Daniel S, Salim K, Assafi MS. Urinary tract infections and antibiotic sensitivity patterns among women referred to Azadi Teaching Hospital, Duhok, Iraq. Avicenna Journal of Clinical Microbiology and Infection. 2017;5(2):27-30. DOI: 10.34172/ajcmi.2018.05
  51. 51. Merza NS, Jubrael JM. The prevalence of virulence factors among uropathogenic Escherichia coli strains isolated from different hospitals in Kurdistan Region-Iraq. International Journal of Bioinformatics and Biomedical Engineering. 2015;1(4):338-343
  52. 52. Hindi NK, Hasson SO, Hindi SK. Bacteriological study of urinary tract infections with antibiotics susceptibility to bacterial isolates among honeymoon women in Al Qassim Hospital, Babylon Province, Iraq. Biotechnology Journal International. 2013;3:332-340. DOI: 10.9734/BBJ/2013/3573
  53. 53. Ibrahim AA. Identification of iha and kpsMT virulence genes in Escherichia coli isolates with urinary tract infection in Iraqi patients. Indian Journal of Natural Sciences. 2019;52(9):16675-16682
  54. 54. Al-Jebouri MM, Mdish SA. Antibiotic resistance pattern of bacteria isolated from patients of urinary tract infections in Iraq. Open Journal of Urology. 2013;3(2):124-131. DOI: 10.4236/oju.2013.32024
  55. 55. Lafi SA, Alkarboly AA, Lafi MS. Bacterial urinary tract infection in adults, hit district Anbar governorate, west of Iraq. Egyptian Academic Journal of Biological Sciences, G. Microbiology. 2012;4(1):21-26, 10.21608/EAJBSG.2012.16656
  56. 56. Spellberg B, Guidos R, Gilbert D, Bradley J, Boucher HW, Scheld WM, et al. Infectious Diseases Society of America. The epidemic of antibiotic-resistant infections: A call to action for the medical community from the Infectious Diseases Society of America. Clinical Infectious Diseases. 2008;46(2):155-164. DOI: 10.1086/524891
  57. 57. Bell BG, Schellevis F, Stobberingh E, Goossens H, Pringle M. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infectious Diseases. 2014;14(1):13. DOI: 10.1186/1471-2334-14-13
  58. 58. Hersh AL, Shapiro DJ, Pavia AT, Shah SS. Antibiotic prescribing in ambulatory pediatrics in the United States. Pediatrics. 2011;128(6):1053-1061. DOI: 10.1542/peds.2011-1337
  59. 59. Lee GC, Reveles KR, Attridge RT, Lawson KA, Mansi IA, Lewis JS, et al. Outpatient antibiotic prescribing in the United States: 2000 to 2010. BMC Medicine. 2014;12(1):96. DOI: 10.1186/1741-7015-12-96
  60. 60. Hersh AL, Jackson MA, Hicks LA. Committee on infectious diseases. Principles of judicious antibiotic prescribing for upper respiratory tract infections in pediatrics. Pediatrics. 2013;132(6):1146-1154. DOI: 10.1542/peds.2013-3260
  61. 61. Fleming-Dutra KE, Hersh AL, Shapiro DJ, Bartoces M, Enns EA, File TM, et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. Journal of the American Medical Association. 2016;315(17):1864-1873. DOI: 10.1001/jama.2016.4151
  62. 62. Smieszek T, Pouwels KB, Dolk FC, Smith DR, Hopkins S, Sharland M, et al. Potential for reducing inappropriate antibiotic prescribing in English primary care. Journal of Antimicrobial Chemotherapy. 2018;73(suppl_2):ii36-ii43. DOI: 10.1093/jac/dkx500
  63. 63. Gerber JS, Ross RK, Bryan M, Localio AR, Szymczak JE, Wasserman R, et al. Association of broad-vs narrow-spectrum antibiotics with treatment failure, adverse events, and quality of life in children with acute respiratory tract infections. Journal of the American Medical Association. 2017;318(23):2325-2336. DOI: 10.1001/jama.2017.18715
  64. 64. Kreitmeyr K, von Both U, Pecar A, Borde JP, Mikolajczyk R, Huebner J. Pediatric antibiotic stewardship: Successful interventions to reduce broad-spectrum antibiotic use on general pediatric wards. Infection. 2017;45(4):493-504. DOI: 10.1007/s15010-017-1009-0
  65. 65. Poole NM, Shapiro DJ, Fleming-Dutra KE, Hicks LA, Hersh AL, Kronman MP. Antibiotic prescribing for children in United States emergency departments: 2009-2014. Pediatrics. 2019;143(2):e20181056. DOI: 10.1542/peds.2018-1056
  66. 66. Aljanaby AA, Alfaham QM. Phenotypic and molecular characterization of some virulence factors in multidrug resistance Escherichia coli isolated from different clinical infections in Iraq. American Journal of Biochemistry and Molecular Biology. 2017;7:65-78. DOI: 10.3923/ajbmb.2017.65.78
  67. 67. Al-Delaimi MS, Nabeel M. Early onset neonatal sepsis: Bacteriological antimicrobial susceptibility study in Duhok Province, Iraq. Journal of University of Babylon for Pure and Applied Sciences. 2019;27(3):196-212
  68. 68. ABDULRAHMAN IS, SAADI AT. Bacterial isolates and their antimicrobial resistance patterns in neonatal sepsis recorded at Hevi Teaching Hospital in Duhok City/Kurdistan Region of Iraq. Duhok Medical Journal. 2019;13(2):84-95
  69. 69. Saadi AT, Garjees NA, Rasool AH. Antibiogram profile of septic meningitis among children in Duhok, Iraq. Saudi Medical Journal. 2017;38(5):517
  70. 70. Al-mousawi MR. Bacterial profile and antibiogram of bacteremic children in Karbala city, Iraq. Karbala Journal of Pharmaceutical Sciences. 2016;11:131-139
  71. 71. Raham TF, Abood AM. Bacterial profile and antimicrobial susceptibility in neonatal sepses, Al-Alwyia Pediatric Teaching Hospital in Baghdad. Al-Kindy College Medical Journal. 2017;13(2):21-25
  72. 72. Ibrahim SA, Rahma S. Microbiological profile of neonatal septicemia. Iraqi Postgraduate Medical Journal. 2012;11:13-18
  73. 73. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the Global Burden of Disease Study 2010. The Lancet. 2012;380(9859):2095-2128. DOI: 10.1016/S0140-6736(12)61728-0
  74. 74. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): A prospective, case-control study. The Lancet. 2013;382(9888):209-222. DOI: 10.1016/S0140-6736(13)60844-2
  75. 75. Livermore DM, Woodford N. The β-lactamase threat in Enterobacteriaceae. Pseudomonas and Acinetobacter. Trends in Microbiology. 2006;14(9):413-420. DOI: 10.1016/j.tim.2006.07.008
  76. 76. Al-Marzoqi AH, Aziz HW, Dulaimi TH. Genotype, phenotype and virulence genes markers in Escherichia coli: Molecular characterization and antimicrobial susceptibility associated with Diarrhoea among children in Babil province, Iraq. International Journal of Biochemistry, Bioinformatics a nd Biotechnology Studies. 2019;4(1):11-20
  77. 77. Al-Dahmoshi HO, Al-Yassari AK, Al-Saad NF, Al-Dabagh NN, Al-Khafaji NS, Mahdi RK, et al. Occurrence of AmpC, MBL, CRE and ESBLs among diarrheagenic Escherichia coli recovered from Infantile Diarrhea, Iraq. Journal of Pharmaceutical and Biomedical Sciences. 2015;5:189-195
  78. 78. Al-Saadi ZH, Tarish AH, Saeed EA. Phenotypic detection and antibiotics resistance pattern of local serotype of E. coli O157: H7 from children with acute diarrhea in Hilla city/Iraq. Journal of Pharmaceutical Sciences and Research. 2018;10(3):604-609
  79. 79. Abdul-hussein ZK, Raheema RH, Inssaf AI. Molecular diagnosis of diarrheagenic E. coli infections among the pediatric patients in Wasit Province, Iraq. Journal of Pure and Applied Microbiology. 2018;12(4):2229-2241
  80. 80. Shamki JA, Al-Charrakh AH, Al-Khafaji JK. Detection of ESBLs in enteropathogenic E. coli (EPEC) isolates associated with infantile diarrhea in Kut City. Medical Journal of Babylon. 2012;9(2):403-412
  81. 81. Khalil ZK. Isolation and identification of different diarrheagenic (DEC) Escherichia coli pathotypes from children under five years old in Baghdad. Iraqi Journalof Community Medicine. 2015;28(3):126-132
  82. 82. Hassan JS. Antimicrobial resistance patterns of Escherichia coli O157: H7 isolated from stool sample of children. Iraqi Journal of Medical Sciences. 2015;13(3):259-264
  83. 83. Jameel ZJ, Al-Assie AH, Badawy AS. Isolation and characterization of enteroaggregative Escherichia coli among the causes of bacterial diarrhea in children. Tikrit Journal of Pure Science. 2018;20(4):30-37
  84. 84. Yaqoob MM, Mahdi KH, Al-Hmudi HA, Mohammed-Ali MN. Detection of rotavirus a and Escherichia coli from diarrhea cases in children and Coliphage characterization. International Journal of Current Microbiology and Applied Sciences. 2016;5(4):68-83. DOI: 10.20546/ijcmas.2016.504.011
  85. 85. AL-Shuwaikh AM, Ibrahim IA, Shwaikh RM. Detection of E. coli and rotavirus in diarrhea among children under five years old. Iraqi Journal of Biotechnology. 2015;14(1):85-92
  86. 86. Alsherees HA, Ali SN. A preliminary occurrence of extended-spectrum and AmpC Beta-lactamases in clinical isolates of enteropathogenic Escherichia coli in Najaf, Iraq. bioRxiv. 2019;1:512731. DOI: 10.1101/512731
  87. 87. Hemalatha R, Ramalaxmi BA, Swetha E, Balakrishna N, Mastromarino P. Evaluation of vaginal pH for detection of bacterial vaginosis. The Indian Journal of Medical Research. 2013;138(3):354
  88. 88. Al-Khaqani MM, Alwash MS, Al-Dahmoshi HO. Investigation of phylogroups and some virulence traits among cervico-vaginal Escherichia coli (CVEC) isolated for female in Hilla City, Iraq. Malaysian Journal of Microbiology. 2017;13(2):132-138
  89. 89. Paniagua-Contreras GL, Monroy-Pérez E, Solis RR, Cerón AB, Cortés LR, Alonso NN, et al. O-serogroups of multi-drug resistant cervicovaginal Escherichia coli harboring a battery of virulence genes. Journal of Infection and Chemotherapy. 2019;25(7):494-497. DOI: 10.1016/j.jiac.2019.02.004
  90. 90. Chen LF, Chopra T, Kaye KS. Pathogens resistant to antibacterial agents. Infectious Disease Clinics. 2009;23(4):817-845. DOI: 10.1016/j.idc.2009.06.002
  91. 91. Al-Mayahie SM. Phenotypic and genotypic comparison of ESBL production by vaginal Escherichia coli isolates from pregnant and non-pregnant women. Annals of Clinical Microbiology and Antimicrobials. 2013;12(1):7. DOI: 10.1186/1476-0711-12-7
  92. 92. Ullauri A, Smith A, Espinel M, Jimenez C, Salazar C, Castrillon R. WHO ear and hearing disorders survey: Ecuador national study 2008-2009. Conference Papers in Science. 2014;2014:13. DOI: 10.1155/2014/847526.847526
  93. 93. Fauci AS, Kasper DL, Longo DL, et al. Harrison’s Principles of Internal Medicine. 17th ed. New York, NY, USA: McGraw-Hill; 2008
  94. 94. Yiengprugsawan V, Hogan A. Ear infection and its associated risk factors, comorbidity, and health service use in Australian children. International Journal of Pediatrics. 2013;2013:7. DOI: 10.1155/2013/963132.963132
  95. 95. Llor C, Bjerrum L. Antimicrobial resistance: Risk associated with antibiotic overuse and initiatives to reduce the problem. Therapeutic Advances in Drug Safety. 2014;5(6):229-241. DOI: 10.1177/2042098614554919
  96. 96. Afolabi OA, Salaudeen AG, Ologe FE, Nwabuisi C, Nwawolo CC. Pattern of bacterial isolates in the middle ear discharge of patients with chronic suppurative otitis media in a tertiary hospital in North central Nigeria. African Health Sciences. 2012;12(3):362-367. DOI: 10.4314/ahs.v12i3.18
  97. 97. Okike IO, Johnson AP, Henderson KL, Blackburn RM, Muller-Pebody B, Ladhani SN, et al. Incidence, etiology, and outcome of bacterial meningitis in infants aged< 90 days in the United Kingdom and Republic of Ireland: Prospective, enhanced, national population-based surveillance. Clinical Infectious Diseases. 2014;59(10):e150-e157. DOI: 10.1093/cid/ciu514
  98. 98. Kim KS. Human meningitis-associated Escherichia coli. EcoSal Plus. 2016;7(1):1-25. DOI: 10.1128/ecosalplus.ESP-0015-2015
  99. 99. Liu J, Yan Q , Luo F, Shang D, Wu D, Zhang H, et al. Acute cholecystitis associated with infection of Enterobacteriaceae from gut microbiota. Clinical Microbiology and Infection. 2015;21(9):851-8e1. DOI: 10.1016/j.cmi.2015.05.017
  100. 100. Kujiraoka M, Kuroda M, Asai K, Sekizuka T, Kato K, Watanabe M, et al. Comprehensive diagnosis of bacterial infection associated with acute cholecystitis using metagenomic approach. Frontiers in Microbiology. 2017;8:685. DOI: 10.3389/fmicb.2017.00685
  101. 101. Al-Fayyadh ZH, Turkie AM, Al-Mathkhury HJ. New mutations in GyrA gene of Escherichia coli isolated form Iraqi patients. Iraqi Journal of Science. 2017;58(2B):778-788. DOI: 10.24996.ijs.2017.58.2B.1
  102. 102. Alfatlawi AS, Alsaidi MA, Almaliky NK, Alsherees HA. Molecular characterization of extended spectrum â-lactamases (ESBLs) producing Escherichia coli isolated from Cholecystitis. EurAsian Journal of BioSciences. 2019;13(1):113-120
  103. 103. Al-Rawazq HS, Mohammed AK, Hussein AA. Etiology and antibiotic sensitivity for otitis media in a central pediatric teaching hospital. Iraqi Medical Journal. 2013;59(2):84-90
  104. 104. Kumar A, Jayachandran L, Kumar S. Antimicrobial susceptibility pattern in chronic suppurative otitis media patient in a tertiary care hospital. Value in Health. 2016;19(7):A845-A846
  105. 105. Alsaimary IE, Alabbasi AM, Najim JM. Impact of multi drugs resistant bacteria on the pathogenesis of chronic suppurative otitis media. African Journal of Microbiology Research. 2010;4(13):1373-1382
  106. 106. Ibrahim II. Bacteriological study of chronic suppurative otitis media among patients attending Tikrit Teaching Hospital for the year 2013. The Medical Journal of Tikrit. 2015;20(2):15-28
  107. 107. Neamah AS. Detection of bacterial pathogens causing a chronic suppurative otits media and study of antibiotic susceptibility in Iraqi patients. International Journal of Research in Pharmaceutical Sciences. 2019;10(3):2567-2571. DOI: 10.26452/ijrps.v10i3.1511
  108. 108. Wajid AR, Alwan SK. Bacteriological and genetic study on Escherichia coli causing acute calculus cholecystitis for diabetes patients in AL-Diwanyia City. International Journal. 2015;3(6):1374-1382
  109. 109. van Koppen CJ, Hartmann RW. Advances in the treatment of chronic wounds: A patent review. Expert Opinion on Therapeutic Patents. 2015;25(8):931-937. DOI: 10.1517/13543776.2015.1045879
  110. 110. Sorg H, Tilkorn DJ, Hager S, Hauser J, Mirastschijski U. Skin wound healing: An update on the current knowledge and concepts. European Surgical Research. 2017;58(1-2):81-94. DOI: 10.1159/000454919
  111. 111. Moet GJ, Jones RN, Biedenbach DJ, Stilwell MG, Fritsche TR. Contemporary causes of skin and soft tissue infections in North America, Latin America, and Europe: Report from the SENTRY Antimicrobial Surveillance Program (1998-2004). Diagnostic Microbiology and Infectious Disease. 2007;57(1):7-13. DOI: 10.1016/j.diagmicrobio.2006.05.009
  112. 112. Tourmousoglou CE, Yiannakopoulou EC, Kalapothaki V, Bramis J, Papadopoulos JS. Surgical-site infection surveillance in general surgery: A critical issue. Journal of Chemotherapy. 2008;20(3):312-318. DOI: 10.1179/joc.2008.20.3.312
  113. 113. Al-Abbas AK. Aerobic bacteria isolation from post-caesarean surgical site and their antimicrobial sensitivity pattern in Karbala city, Iraq. Iraq Medical Journal. 2017;1(4):94-98
  114. 114. Lafi SA, Al-Shamarry M, Ahmed MS, Ahmed WI. Bacterial profile of infected traumatic wound and the antibiogram of predominant bacterial isolates using Viteck automated system in Ramadi Teaching Hospital, Iraq. Egyptian Academic Journal of Biological Sciences, G. Microbiology. 2018;10(1):69-76
  115. 115. Abboud ZH, Al-Ghanimi NH, Ahmed MM. An insight into bacterial profile and antimicrobial susceptibility of burn wound infections in Kerbala, Iraq. Karbala Journal of Medicine. 2014;7(2):2023-2032
  116. 116. Alkaabi SA. Bacterial isolates and their antibiograms of burn wound infections in Burns Specialist Hospital in Baghdad. Baghdad Science Journal. 2013;10(2):331-340
  117. 117. Ali MR, Al-Taai HR, Al-Nuaeyme HA, Khudhair AM. Molecular study of genetic diversity in Escherichia coli isolated from different clinical sources. Biochemical and Cellular Archives. 2018;18(2):2553-2560
  118. 118. Aljanaby AA, Aljanaby IA. Prevalence of aerobic pathogenic bacteria isolated from patients with burn infection and their antimicrobial susceptibility patterns in Al-Najaf City. Iraq-a three-year cross-sectional study. F1000Research. 2018;7(1157):1157-10.12688/f1000research.15088.1
  119. 119. Abdulqader HH, AT S. The distribution of pathogens, risk factors and their antimicrobial susceptibility patterns among post-surgical site infection in Rizgari Teaching Hospital in Erbil/Kurdistan Region/Iraq. Journal of Duhok University. 2019;22(1):1-0. DOI: 10.26682/sjuod.2019.22.1.1
  120. 120. Ali FA, Merza EM, Aula TS. Antibiotic resistance among Escherichia coli isolated from different clinical samples in Erbil City. International Journal of Research Studies in Science, Engineering and Technology. 2017;4(10):12-21
  121. 121. Ali FA. Distribution of CTX-M gene among Escherichia coli strains isolated from different clinical samples in Erbil City. Iraqi Journal of Biotechnology. 2018;17(1):78-90
  122. 122. Al-Azawi ZH. Antimicrobial susceptibility patterns of aerobic bacterial species of wound infections in Baquba General Teaching Hospital-Diyala. Diyala Journal of Medicine. 2013;4(1):94-100
  123. 123. Hussein NH. Genotypic detection of carbapenem-resistant Escherichia coli producing NDM-1 gene for the first time in Baghdad/Iraq. Journal of Global Pharma Technology. 2017;9(9):106-111
  124. 124. ASK A-K, Albaayit A, Ibraheem OS, Abdul-Ilah HH. Molecular investigation of metallo-β-lactamase encoding gene in nosocomial carbapenem-resistant Enterobacteriaceae in Iraqi Hospitals. The Eurasia Proceedings of Science, Technology, Engineering & Mathematics. 2018;2:239-243
  125. 125. Abas IJ, Al-Hamdani MA. New Delhi metallo-Β-lactamase 1 (Ndm-1) producing Escherichia coli in Basrah Hospitals, Iraq. European Journal of Biomedical. 2017;4(02):102-107
  126. 126. Al-Hasnawy HH, Saleh RH, Hadi BH. Existence of a ESBL genes in Escherichia coli and Acinetobacter baumannii isolated from different clinical specimens. Journal of Pharmaceutical Sciences and Research. 2018;10(5):1112-1117

Written By

Hussein O.M. Al-Dahmoshi, Noor S.K. Al-Khafaji and Mohammed H.O. Al-Allak

Submitted: 18 December 2019 Reviewed: 13 March 2020 Published: 20 April 2020