How to Cite:

Hussein, M. N., Al-Saadi, Z. N., Al-Azzawi, J. A. T., & Hussein, D. N. (2022). Prevalence of bacterial co
infections among Covid 19 patients in wasit province. International Journal of Health Sciences, 6(S7),
6448-6461. https://doi.org/10.53730/ijhs.v6nS7.13709

Prevalence of bacterial co infections among

Covid 19 patients in wasit province

Mustafa N. Hussein
Department of Micobiology, College of Science, Wasit University, Iraq

Zainab N. Al-Saadi
Department of Micobiology, College of Science, Wasit University, Iraq

Jalal AbdulRazzaq Tofah Al-Azzawi

Department of Micobiology, College of Science, Wasit University, Iraq

Dhuha N. Hussein
Department of Micobiology, College of Science, Wasit University, Iraq

Abstract---Background: The pandemic of severe acute respiratory

syndrome coronavirus 2 raised the attention towards bacterial co-
infection and its role in coronavirus disease 2019 (COVID-19) disease.
This study aims to review and identify the prevalence of bacterial co-
infection in Iraqi patients as bacterial co-infection played an important
role in escalating the morbidity and mortality rate during previous
viral outbreaks and pandemics of COVID-19. Materials and Methods:
It was collected three hundred eighty clinical samples from covid-19
patients, in Iraqi patients from a period between November 2021 to
January 2021, in the bacteriology Unit. Patients samples were
included upper respiratory tract, 190 (50%) from Nasopharyngeal (NP)
and 190 (50%) from and Oropharyngeal (OP) specimen included 320
(84.2%) male and 60 (15.8%) female, in addition patients samples age
was ranged between 21-70 years old. Each specimen was cultured on
Blood agar, MacConkey agar, Mannitol Salt Agar and Chocolate Agar
plates to be isolated, then samples was identified using biochemical
test. Result: According to morphological and biochemical tests among
collected samples 80 (21.1%) were positive samples, while 300 (78.9%)
were negative samples, positive samples included 61(76.2%) gram
negative (Gr -ve) and 19 (23.8%) were gram positive (Gr +ve), positive
samples were distributed as following, 50 (62.5%) samples K.
pneumonia, 3 (3.8%) Pseudomonas aeruginosa, 5 (6.2%) Acinetobacter
baumanii, 4 (5%) Micrococcus, 12 (15%) Staphylococcus aureus, 3
(3.8%) Enterococcus cloacae and 3 (3.8%) were Aerococcus viridans.
negative samples distributed into 200 (66.6%) normal flora and 100
(33.4%) were contaminated samples. According to gender patients

International Journal of Health Sciences ISSN 2550-6978 E-ISSN 2550-696X © 2022.

Manuscript submitted: 9 May 2022, Manuscript revised: 18 July 2022, Accepted for publication: 27 August 2022
6448
 6449

samples included 320 (84.2%) male and 60 (15.8%) female, in

addition patients samples age was ranged between 21-70 years old
and mean of age was 40.9±2.0 standard deviation (SD). In positive
samples Klebsiella pneumonia represented 50 (62.5%) of 80(100%)
collected samples, while other bacteria were 3 (3.75%), 5 (6.25%), 4
(5%), 12 (15%), 3 (3.75%) and 3 (3.75%) for Pseudomonas aeruginosa,
Acinetobacter baumanii, Micrococcus, Staphylococcus aureus,
Enterococcus cloacae and Aerococcus viridans respectively. K.
pneumoniae according to age of patients age ranged between 21-70, it
was showed that 8(16%%) of patients were in age group (21-30),
9(18%%) of patients were in age group (31-40), 12(24%%) of patients
were in age group (41-50), 13(26%%) of patients were in age group
(51-60) and 8(16%%) of patients were in age group (61-70). In
distribution of K. pneumoniae according to gender of patients the vast
majority of patients were male as male represented 39 (78%) of the
patients while females were represented 11(22%). Conclusion: current
data revealed that there was high rate of bacterial coinfection in Wasit
province.

Keywords---Covid19, bacterial coinfection, Iraq

Introduction

Respiratory viral and bacterial infections contribute substantially to the global

burden of morbidity and mortality. Such simultaneous infections with the flu
virus or bacteria that cause pneumonia, tend to make the patient’s condition
critical (1). Although, critically ill patients rapidly develop acute respiratory
distress syndrome and sepsis, leading to death from multiple organ failure. The
main symptoms of COVID-19 are fever, fatigue, and dry cough. However, most
patients have a good prognosis (2). Bacterial co-infections associated with other
coronaviruses, such as SARS-CoV-1 and MERS-CoV, have been reported in
association with pandemic viruses at rates of 20–30%, respectively (3). Bacterial
co-infection is directly linked to increased morbidity and mor- tality from viral
respiratory infections. Hospital admissions increase the risk of healthcare-
associated infections (HCAI) which makes the disease more aggressive and
difficult to treat, as well as inducing life-threatening complications and increasing
the consumption of antibiotics, super infections and co-infections are commonly
found in many respiratory dis-eases; viral infectious diseases and bacterial co-
infections may be the cause of the increased mortality rate in patients infected
with any viral infection (4).

Coinfection associated with viral pneumonia is the main cause of mortality and
can considerably inhibit the host’s immune system, which decreases the
pharmacological response and makes the prognosis of the disease harmful (5).
SARS-CoV-2 is a newly emerged pathogen that causes pneumonia with the
possibility of worsening to hypoxic-type respiratory failure, organ failure, and
acute kidney injury followed by myocarditis and thromboembolism. SARS-Cov-2
(COVID-19) leaves the body vulnera-ble to bacterial infections; however, this co-
infection mechanism is not well understood but represents a threat to the
6450

respiratory epithelium favoring bacteremia (6). A study carried out with ICU
(Intensive Care Unit) patients in 88 countries showed that those patients who
received at least one antibiotic during acute hospitalization, of these, more than
half developed a secondary bacterial infection, requiring antibiotic
therapy, in China, 95% of patients and in the United Kingdom 80% of patients
received antibiotics (7). Antimicrobial resistance is seen as a major threat to
public health, as well as to the economy and health security at the local and
international levels. It is estimated that due to its spread across countries and
continents the bacterial resistance increase will cause 10 million deaths annually
by the year 2050, relevant advances have been achieved and determined by the
national AMR programme which is guided by the WHO Global Laboratory AMR
Surveillance System (GLASS) in Uganda. Using the WHONET software (8), ARM
data management was installed at the surveillance sites with trained personnel to
guarantee the quality of the data. Six major pathogens that cause resistance-
related deaths (Escherichia coli, followed by Staphylococcus aureus, Kleb- siella
pneumoniae, Streptococcus pneumoniae, Acinetobacter baumannii, and
Pseudomonas aeruginosa) were responsible for 929,000 deaths from ADR and
3.57 million (2.62–4.78) ADR-related deaths in 2019 (9). Secondary infections
predominantly involve a specific group of bacterial pathogens such as S. aureus,
Staphylococcus pneumoniae, Streptococcus pyogenes, and Haemophilus
influenza (10).

2-Materials and methods:

2-1-Samples Collection

It was collected 380 samples from COVID-19 patients, bacterial samples were
isolated and identified using different culture media in addition to various
biochemical test. Patient variables were assessed to be correlated with patients
age and sex, the percentage of positive isolates among collected samples also was
documented (11).

2-2 Isolation and identification of bacterial isolates

Each specimen was cultured on Blood agar, MacConkey agar, Mannitol Salt Agar
and Chocolate Agar plates. The resultant colonies in these media were
subcultured to be more tests for identification to the species level as described by
Bergey’s Manual for determinative Bacteriology. The isolates were identified on
the basis of typical morphology by gram staining, coagulase test, Triple Sugar
Iron Agar test (TSI) and the analytical profile index (API) system (12).

2-3 Data analyses

Patients variables were associated statistically using Statistical Package for the
Social Sciences (SPSS) software and analyzed with analysis of variance (ANOVA)
with the GEN STAT software package, and outcomes (screening and positivity for
secondary co-infection, death) using the Mann–Whitney test for continuous
variables and the Fisher exact test for categorical variables. A P-value of < 0.05
was considered statistically significant.
 6451

3-Results

3-1 Patients variables

A total of three hundred eighty clinical samples were collected from covid19
patients, according to Wasit University ethics committee, in Iraq from October
2021 to February 2021, in the bacteriology Unit. According to gender patients
samples included 320 (84.2%) male and 60 (15.8%) female, in addition patients
samples age was ranged between 21-70 years old and mean of age was 40.9±2.0
standard deviation (SD), table (1).

Table (1) Demographic of collected samples.

Collected samples
Samples type No (%)
Nasopharyngeal (NP) swab 190 (50%)
Source of samples Oropharyngeal (OP) swab 190 (50%)
Male 320 (84.2%)
Gender Female 60 (15.8%)
21-30 89 (23.4%)
31-40 121 (31.9%)
Age 41-50 93 (24.4%)
mean±SD 51-60 47 (12.4%)
(40.9±2.0) 61-70 30 (7.9%)

3-2 Identification of K. pneumonia

To identifying bacterial isolates, a variety of physiological, morphological,

and biochemical tests were used for K. pneumonia including colony morphology,
cultural and biochemical characteristics on the basis of typical morphology on
agar plates, catalase test, oxidase test, Triple Sugar Iron Agar test (TSI) and
the analytical profile index (API) system.

3-2-1 Colony morphology

Bacterial isolates were identified after 24-48 hours of aerobic incubation

on blood agar, Mannitol Salt Agar, Chocolate Agar and MacConkey medium agar
plates at 37°C. Klebsiella pneumonia colonies on MacConkey agar were Lactose
fermenting colonies that are pink in color, have a regular edge, and are spherical
and mucoid in texture, and big size (figure 1), concerning enrichment The
bacterial isolates were mucoid, big, white to grey, and nonhemolytic colony on a
blood-agar media, which was used to distinguish Klebsiella from other bacteria
that grow on MacConkey agar but heamolyses blood.
6452

Figure (1): Mucoid colonies of K. pneumoniae grown on MaConkey agar for 24 hrs
at 37°C.

3-2-2 Catalase and oxidase test

It have been grown K. pneumonia on blood agar, Mannitol Salt Agar, Chocolate
Agar and MacConkey medium agar plates at 37°C. Klebsiella pneumonia colonies
from MacConkey agar were tested for both catalase and oxidase test production,
results were positive for catalase as there was obvious bubbles formation and
negative for oxidase through there was no change of filter paper to blue color,
figure (2), (3).

Figure (2) catalase test of K. pneumonia

 6453

Figure (3) Oxidase test of K. pneumonia

3-2-3 Triple Sugar Iron Agar test (TSI)

It have been tested all 50 K. pneumonia isolate for Triple Sugar Iron Agar test
(TSI), results were that Alkaline slant/alkaline butt (K/K) as red/red represent
glucose, lactose, and sucrose non-fermenter, alkaline (K) slant, alkaline (K)
buttom, negative for gas production and negative for H2S production figure (4).

Figure (4): The TSI results of K. pneumonia.

6454

3-2-4 API 20E system identification of Klebsiella isolates

As indicated in figure (5) , the results of biochemical tests for Klebsiella (50
isolates) were confirmed using the API 20E system . The results of all bacterial
isolates were positive.

Figure (5): The analytic profile index 20E system for identifying K. pneumonia.

3-3 Percentage of positive isolates among collected samples

According to morphological and biochemical tests among collected samples 80

(21.1%) were positive samples, while 300 (78.9%) were negative samples, positive
samples included 61(76.2%) gram negative (Gr -ve) and 19 (23.8%) were gram
positive (Gr +ve), positive samples were distributed as following, 50 (62.5%)
samples K. pneumonia, 3 (3.8%) Pseudomonas aeruginosa, 5 (6.2%) Acinetobacter
baumanii, 4 (5%) Micrococcus, 12 (15%) Staphylococcus aureus, 3 (3.8%)
Enterococcus cloacae and 3 (3.8%) were Aerococcus viridans. negative samples
distributed into 200 (66.6%) normal flora and 100 (33.4%) were contaminated
samples, table (2).
Table 2 Distribution of bacterial.

Sample collection
Bacteri Gram -ve Gram +ve
No (%) No (%)
K. pneumonia 50 (62.5%) P. aeruginosa, 3 (3.8%)
S. aureus 12 (15%) A. viridans 3 (3.8%)
Positive samples A. baumanii 5 (6.2%) E. cloacae 3 (3.8)
Micrococcus 4 (5%)

Normal flora 200 (66.6%)

Negative samples Contaminated samples 100 (33.4%)
 6455

3-4 Percentage of Klebsiella pneumonia among positive samples

In positive samples Klebsiella pneumonia represented 50 (62.5%) of 80(100%)

collected samples, while other bacteria were 3 (3.75%), 5 (6.25%), 4 (5%), 12
(15%), 3 (3.75%) and 3 (3.75%) for Pseudomonas aeruginosa, Acinetobacter
baumanii, Micrococcus, Staphylococcus aureus, Enterococcus cloacae and
Aerococcus viridans respectively, table (3).

Table 3 Distribution of positive bacterial species.

Bacterial isolate No (%)

Klebsiella pneumoniae 50 (62.5%)
Pseudomonas aeruginosa 3 (3.75%)
Acinetobacter baumanii 5 (6.25%)
Micrococcus 4 (5%)
Staphylococcus aureus 12 (15%)
Enterococcus cloacae 3 (3.75%)
Aerococcus viridans 3 (3.75%)
Total 80 (100 %)

3-5 Distribution of K. pneumoniae according to age of patients

In this regard patients age ranged between 21-70, it was showed that 8(16%%) of
patients were in age group (21-30), 9(18%%) of patients were in age group (31-40),
12(24%%) of patients were in age group (41-50), 13(26%%) of patients were in age
group (51-60) and 8(16%%) of patients were in age group (61-70), table (4) below.
Table (4): Distribution of K. pneumoniae in age group of patients

Age group (year) Total No. of Isolates Percentage

21-30 8 16%

31-40 9 18%

41-50 12 24%

51-60 13 26%

61-70 8 16%

Total 50 100%
6456

3-6 Distribution of K. pneumoniae according to gender of patients

In this regard the vast majority of patients were male as male represented 39
(78%) of the patients while females were represented 11(22%), table (5).

Table (5): Distribution of K. pneumoniae in gender of patients

Gender of patients Total No. of Isolates Percentage

Male 39 78%

Female 11 22%

Total 50 100%

4-Discussion

A total of two hundred eighty clinical samples were collected from covid19
patients included upper respiratory tract, 140 (50%) from Nasopharyngeal (NP)
and 140 (50%) from and Oropharyngeal (OP) specimen, among collected samples
80 (28.5%) were bacterial growth or culture. Current data were disagreed with
Ahmed Hasan et al., (2021) (13) study aimed to determine the prevalence of
bacteria and investigate the antibiotic resistance profile among clinical specimens
of covid-19 at Azadi Teaching Hospital in Kirkuk, Iraq, in total, from clinical
specimens were collected, (7.6%) and (11.6%) respectively of isolates samples
were bacterial growth in culture, while our study agreed with other studies by
Kadum, (2020) (14), Namratha et al. (2015) (15) and Nirwati et al. (2019) (16)
reported such percentages as 4.03%, 17.36%, and 32.48%, these result is in line
with the findings of the studies conducted by Al-Rubaye et al., (2016) (17) in Iraq.
These differences in the mean prevalence rates among various studies could be
related to differences in geographical location and hygienic practices of the
population. Klebsiella pneumonia colonies on MacConkey agar were Lactose
fermenting colonies that are pink in color, have a regular edge, and are spherical
and mucoid in texture, and big size (18).

Klebsiella pneumonia colonies from MacConkey agar were tested for both catalase
and oxidase test production, results were positive for catalase as there was
obvious bubbles formation (19). It have been tested all 50 K. pneumonia isolate
for Triple Sugar Iron Agar test (TSI), results were that Alkaline slant/alkaline butt
(K/K) as red/red represent glucose, lactose, and sucrose non-fermenter, alkaline
(K) slant, alkaline (K) buttom, negative for gas production and negative for H2S
production (20). Results of Kligler Iron Agar (KIA) test according to H2S
 6457

production and carbohydrates fermentation pattern that differentiates

Enterobacteriaceae family from each other, this combination permits
differentiation of Gram-negative bacilli by their ability to ferment Dextrose or
Lactose, which produces color changes of the pH indicator in response to acid
production during fermentation of the sugars. Dextrose concentration is 10% of
the Lactose concentration. Ferric Ammonium Citrate and Sodium Thiosulfate
mare indicators of hydrogen sulfide production. Phenol Red is the pH indicator.
Sodium Chloride maintains the osmotic balance of the medium. Lactose
nonfermenters as pH indicator (phenol red) changed the medium color from
orange-red to yellow in the presence of acids. K. pneumoniae isolates able to
produc acidic yellow slant and acid yellow bottom with H2S and gas production,
indicating glucose and lactose fermentation (21). In citrate test positive outcomes
is an important phys-iological sign in order to diagnosing Enterobacteriaceae
family, K. pneumoniae had a positive reactions in this test. K. pneumoniae that
produced CO2, that reacting with medium components resulting in producing
alkaline compounds, bromthymol blue must be turned from green to blue color as
indicator of positive test (22). Indole negative in Klebsiella due to lacking of
tryptophanase, so Kovac's reagent when added to broth which is usually free of
indole, the red ring willnot formed (23). In urease test all isolates of K. pneumonia
were positive as it was able to produce urease enzyme converting the yellow color
to pink (20). It was showed that all K. pneumoniae isolates were positive for
catalase test indicating presence of catalase enzyme able to convert hydrogen
peroxide into H2O and O2 (24). In addition all K. pneumoniae isolates had been
given a negative results regarding oxidase test, this may due to that K. pneumonia
isolates lacking terminal receptor to O2 such as Cytochrome C enzyme (25).

According to morphological and biochemical tests among collected samples 80

(28.6%) were bacterial growth or culture , while 200 (71.4%) were negative
samples, bacterial growth or culture included 61(76.2%) gram negative (Gr -ve)
and 19 (23.8%) were gram positive (Gr +ve), bacterial growth or culture were
distributed as following, 50 (62.5%) samples K. pneumonia, 3 (3.8%)
Pseudomonas aeruginosa, 5 (6.2%) Acinetobacter baumanii, 4 (5%) Micrococcus, 12
(15%) Staphylococcus aureus, 3 (3.8%) Enterococcus cloacae and 3 (3.8%) were
Aerococcus viridans. negative samples distributed into 200 (66.6%) normal flora
and 100 (33.4%) were contaminated samples. These outcomes were agreed with
Guzek et al. (2022) (26) reported that during COVID-19 pandemic in Poland
included 103 patients, of whom 23 (73.9%) were positive for K. pneumonia, in
addition in the period of Arcari et al. (2021) (27) study, showed that
Carbapenemase-producing Klebsiella pneumoniae were detected in 14/41
patients (34%) only followed by P. aeruginosa, Micrococcus, Acinetobacter baumanii
and S. aureus. Overall, Alqahtani et al. (2022) (28) found that almost 70% of the
co-infected with gram-negative organisms, K. pneumonia was the most frequently
reported organism among all other bacterial isolates 57.69%.

While current data were non compatible with Stefanini et al. (2021) (29) showed
that a total of 100 species, distributed among 33 genera, the most abundant
species in covid-19 was Escherichia coli (420 isolates), followed by Klebsiella
pneumoniae (n = 192), Pseudomonas aeruginosa (n = 187), Enterococcus faecalis
(n = 184), Staphylococcus epidermidis (n = 175), and Staphylococcus aureus (n =
134). The observation of Acinetobacter baumannii/haemolyticus being more
6458

abundant among the COVID-19 isolates is not surprising, as this species is

known to cause ventilator-associated and bloodstream infections (30). This
difference in outcomes may due to sample sizes in each study because the sample
size increases, the confidence interval tends to become smaller, meaning that the
research can have greater confidence in the reliability of the findings, in addition
results possibly associated with the use of invasive devices widely used in the
treatment of COVID-19 (ventilator and urinary catheters), may support the
current dread of increase of nosocomial infections in COVID-19 pandemic and the
use steroid that directly affect results of bacterial culture. In spite of that, most
patients included in this study 200 ( 71.4%) of patients samples were negative in
bacterial cultures. This may due to recent antibiotic use, presence of fastidious
organisms such as nutritionally variant groups and inadequate samples in some
cases. Another reasons for negativity may be that the patients had non-
bacteremic illness or bacteria were present intermittently or at very low blood
density. However, an additional explanation is that the causative microorganisms
are delicate, fastidious, nonviable, slow growing at low densities, or uncultivable
in culture medium. or when antimicrobial treatment has been started before
blood collection, which may kill or inhibit pathogen growth. These diagnoses may
therefore be missed and may be referred to as “false negatives.”

In this study patients age ranged between (41-50) and (51-60) were more frequent
among all age groups, these information were in consistence with (Dergaa et al.
(2022) (31). In severe infections the respiratory and urinary tracts are the most
frequently involved systems which may be accompanied by severe sepsis.
Bacteremia and sepsis are also associated with indwelling vascular catheters in
the elderly who are admitted to the intensive care unit (ICU) (32, 33). While
present outcomes were not agreed with other mentioned that it was does not
suggest that the oldest individuals necessarily play the leading role in the spread
of SARS-CoV-2 in the community, suggest that younger adults, particularly those
aged under 35y often experience the highest cumulative rates of infection (34, 35).
The differences in results among studies may belongs to long or shortness in a
period of data collection in each study. Current results were in agreement with
Papadopoulos et al., (2021) who showed that aimed to provide a review of the
research literature, propose hypotheses, and therapies based on the potential link
to COVID-19 in elderly men compared to women, aging, inflammation, severe
acute respiratory syndrome (SARS) due to coronavirus infection, and COVID-19
disease state and outcomes was performed, the link between the immune system
and male aging is well-established, as is the progressive decline in T levels with
aging. In women, T levels drop before menopause and variably increase with
advanced age. Elevated IL-6 is a characteristic biomarker of patients infected with
COVID-19 and has been linked to the development of the acute respiratory
distress syndrome (ARDS), these data suggest that low T levels may exacerbate
the severity of COVID-19 infection in elderly men, T levels in aging hypogonadal
males create a permissive environment for severe responses to COVID-19
infection or if the virus inhibits androgen formation. Given the preponderance of
COVID-19 related mortality in elderly males, additional testing for gonadal
function and treatment with T may be merited (36). In addition reports from
China indicate that men accounted for 60% of COVID-19 patients (37). Moreover,
67% of patients admitted to the intensive care unit (ICU) were reported to be men
(38). These data seem to indicate that there might be a gender predisposition to
 6459

COVID-19, with men predisposed to being more severely affected and older men
accounting for most deaths (39). According to our knowledge all present research
indicated the prevalence of men in covid-19 in comparison to women.

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