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International Journal of Microbiology logoLink to International Journal of Microbiology
. 2023 Jun 2;2023:3727265. doi: 10.1155/2023/3727265

Urinary Tract Infection and Associated Factors among Pregnant Women Receiving Antenatal Care at a Primary Health Care Facility in the Northern Region of Ghana

Ezekiel K Vicar 1,✉, Samuel E K Acquah 2, Williams Wallana 1, Eugene D Kuugbee 3, Emmanuel K Osbutey 4, Abigail Aidoo 5, Emmanuel Acheampong 6,7, Gloria Ivy Mensah 8
PMCID: PMC10256441  PMID: 37303774

Abstract

Urinary tract infection (UTI) is frequently encountered during pregnancy and is associated with adverse maternal, fetal, and neonatal effects. However, very little information is available on the prevalence of UTI among pregnant women in the northern part of Ghana, a region with a high birth rate. This study employed a cross-sectional analysis of the prevalence, antimicrobial profile, and risk factors associated with UTI in 560 pregnant women attending primary care for antenatal check-ups. Sociodemographic obstetrical history and personal hygiene information were obtained using a well-structured questionnaire. Afterward, clean catch mid-stream urine samples were collected from all participants and subjected to routine microscopy examination and culture. Of 560 pregnant women, 223 cases (39.8%) were positive for UTI. There was a statistically significant association between sociodemographic, obstetric, and personal hygiene variables and UTI (p < 0.0001). Escherichia coli (27.8%) was the commonest bacterial isolate followed by CoNS (13.5%) and Proteus species (12.6%). These isolates exhibited greater resistance to ampicillin (70.1–97.3%) and cotrimoxazole (48.1–89.7%) but were fairly susceptible to gentamycin and ciprofloxacin. Gram-negative resistance to meropenem was up to 25.0%, and Gram positives resistance to cefoxitin and vancomycin was up to 33.3% and 71.4% respectively. The current findings extend our knowledge of the high frequency of UTIs and associated risk factors in pregnant women with E. Coli being the predominant and usual isolate. Variation existed in the resistance pattern of isolates to various drugs, underscoring the need to perform urine culture and susceptibility before treatment.

1. Introduction

Pregnancy causes several physical, hormonal, and functional changes in the urinary tract [1]. This increases urine stasis and the ascending of microbially contaminated urine from the bladder into the ureters, causing urinary tract infection (UTI) [1, 2]. The changes in the urinary tract and immunological changes associated with pregnancy, along with an already short urethra predispose women to UTI [3, 4]. Maternal UTI is the commonest nonintestinal infection in pregnant women globally, and it is a major health problem affecting up to 20% of expectant mothers [5, 6]. UTIs can either be symptomatic or asymptomatic and are linked with serious obstetric complications and poor maternal and neonatal outcomes such as preterm birth, low birth weight, stillbirth, sepsis, maternal anaemia, pyelonephritis, preeclampsia, amnionitis, and neonatal deaths [7–9]. Therefore, early diagnosis and treatment are timely and critical to prevent complications [10].

The prevalence of UTI among pregnant women varies among study populations. In Africa, it ranges from 11.6% to as high as 75% [11, 12]. In Ghana, the prevalence of UTI among pregnant women is represented by fragmented and small-size pocketed studies with a reported prevalence range of 42.8 to 56.5% [6, 13–16]. Approximately the most common reported pathogenic cause of UTI are members of the Enterobacteriaceae family which are responsible for 80% to 95% of all cases, of which Escherichia coli is the most frequently isolated bacteria [17, 18].

The severity of an UTI is usually influenced by the virulence of the bacteria and the susceptibility of the host. Antibiotics such as ceftazidime, amoxicillin, cefoxitin, penicillin, and norfloxacin have been widely used to empirically treat clinically examined individuals with UTI. However, over time, inappropriate prescriptions for the treatment of UTIs along with their widespread use have caused bacteria to mutate and develop drug resistance. A UTI can be caused by bacteria resistant to common antibiotics. This makes treating UTIs more difficult and raises the risk of complications, underscoring the need for using antibiotics correctly and identifying the best drug [6, 11, 19–23].

The most reliable tool for diagnosing UTI is urine culture, as it helps to detect and quantify the pathogen causing the infection [24]. In Ghana, as it is with most developing countries, routine culture tests are not done for persons receiving antenatal care. Instead, a urine dipstick analysis is done which is woefully inadequate to assess UTI in pregnant women [19]. Moreover, several factors, including parity, gravidity, gestational age, history of UTI, diabetes, anaemia, socio-economic status, educational status, sexual activity, and catheterization have been associated with an increased risk of UTI during pregnancy [25–27].

In cultured urine samples taken from pregnant women visiting the Kumbungu health center, we observed an unusually high occurrence of proteinuria, haematuria, and positive bacterial growth. These observations, along with the limited information on the prevalence of UTIs in the northern part of Ghana, raise serious concerns regarding the likelihood that pregnant in the Kumbungu district seeking antenatal care would contract UTIs. Thus, the aim of this study was to determine the prevalence of UTI in pregnant women receiving antenatal care in a primary health facility in Kumbungu, Northern Ghana, as well as the associated risk factors and the antibiotic susceptibility profile of the implicated aetiological agents.

2. Material and Methods

2.1. Study Design and Setting

We conducted a cross-sectional study at the Reproductive and Child Health (RCH) unit of the Kumbungu health centre between 21st January 2019 to 30th November 2019. This facility serves predominantly the rural dweller of the Kumbungu District. It is located in the Northern region of Ghana. The district has a population of 110,586 residents of which 55,295 being women and a population density of 73.75/km2 [28].

2.2. Study Population and Selection of Participants

The targeted study population was pregnant women attending an antenatal care clinic. By employing a random sampling technique, a total of 560 pregnant women who visited the antenatal clinic were recruited. Depending on the total number of clinic attendees per day, between 30 and 40 pregnant women were randomly recruited weekly until the sample size was achieved. We numbered 30 small pieces of cardboard and placed them in a box and pregnant women who met our selection criteria were asked to pick one. This was done till the number of pregnant women for the day was reached. Because antibiotic use can interfere with the antibiotic resistance profile of the isolated bacteria pregnant women who were on antibiotic treatment two weeks before their initial visit to the facility and those at 38 weeks or more gestational age were excluded from the study. Other obstetric information was extracted from the antenatal books of pregnant women. Sociodemographic information was obtained using a well-structured questionnaire. All the pregnant women who agreed to written consent were recruited for the study.

2.3. Bacteria Culture and Identification

Clean catch mid-stream urine samples were collected from all participants using a wide-mouthed sterile-capped container. The specimen was promptly transported to the microbiology laboratory and cultured within one hour of collection. We used a 0.001 ml calibrated wire loop to inoculate samples onto Cystine Lactose Electrolyte Deficient (CLED) agar, blood agar, and chocolate agar (plates (Oxoid Ltd., Hampshire, United Kingdom) and incubate at 37°C for 24–48 hours. Colony counts yielding bacterial growth of 105/ml of urine were regarded as significant for bacteriuria. Colony characteristics, Gram reaction, and biochemical reactions were used to identify bacterial isolates [29, 30]. For the identification of Gram-negative bacteria, oxidase test, lactose fermentation, and hydrogen sulfur (H2S) production in Kligler's iron agar (KIA) test, urease test, citrate test, and indole test were used. Gram positives were also identified using a type of haemolysis, a catalase test, and a coagulase test. Isolated bacteria were later confirmed using API 20E and API 20NE (bioMerieux) for Gram-negative bacteria and API-staph (bioMerieux) and API- Strep (bioMerieux) for Staphylococcus and Streptococcus species, respectively.

2.4. Antimicrobial Susceptibility Test

Antibiotics that are commonly prescribed and are mostly used for empirical treatment were selected for antibiotic susceptibility tests. The test was performed on all isolates according to the Clinical & Laboratory Standards Institute (CLSI) protocol [31]. Bacteria isolates were tested with the following drugs: amoxicillin-clavulanic acid (20 μg), ampicillin (30 μg), chloramphenicol (30 μg) and ceftriaxone (10 μg), cefoxitin (30 μg), ciprofloxacin (5 μg), erythromycin (15 μg), norfloxacin (10 μg), gentamicin (10 μg), nitrofurantoin (50 μg), tetracycline (30 μg), cotrimoxazole (25 μg), and vancomycin (30 μg).

2.5. Statistical Analysis

All data were entered into Microsoft office excel 2016 and exported into SPSS version 22 (SPSS Inc., Chicago, IL, USA) for analysis. Data were presented as frequencies and percentages and compared using the chi-square test for categorical values and with the student t-test for continuous variables. Univariate and multivariate logistic regression models were performed to determine the association between demographic characteristics and UTIs. A P value less than 0.05 was considered statistically significant.

3. Results

3.1. Participants' Demography and UTI Distribution

Table 1 shows the demographic characteristics and distribution of UTIs among 560 study participants. The overall prevalence of UTI among pregnant women receiving antenatal care was 39.8%, out of which 42/127 (33.1%) were symptomatic and 181/433(41.8%) asymptomatic. Among the 223 pregnant women who had UTIs, 181 (81.2%) had no known history of UTIs. Most of the participants (36.4%) were within 21–25 years of age, had an education to primary school level (46.3%), were unemployed mothers (46.3%), and more than half, 313 (55.9%) had been four to nine times pregnant. More than three-quarters (77.3%) of the participants were asymptomatic for UTI, and 409 (73.0%) had no known history of UTI. Regarding genital hygiene, 129 (23.0%) always wash or wipe their genital area after sex while 308 (54.5%) of the participants do that once in a while. We also observed from the study that a considerable proportion (55.0%) of the participants use public toilet facilities, and the use of paper is the commonest mode of cleaning after defecation. There were statistically significant differences between participants' background characteristics and UTIs except for symptomatic and asymptomatic UTIs (p=0.081).

Table 1.

Background characteristics and distribution of UTI among study participants.

Variables Numbers tested for UTI
Total N = 560 Positive (n = 223) Negative (n = 337) X 2, df P-value
n (%) n (%) n (%)
Age groups (years) 40.5, 4 <0.0001
<20 104 (18.6) 48 (46.2) 56 (53.8)
21–25 204 (36.4) 98 (48.0) 106 (52.0)
26–30 128 (22.9) 58 (45.3) 70 (54.7)
31–35 82 (14.6) 14 (17.1) 68 (82.9)
>36 42 (7.5) 5 (11.9) 37 (88.1)
Education 73.2, 4 <0.0001
None 122 (21.8) 87 (71.3) 35 (28.7)
Primary 259 (46.3) 72 (27.8) 187 (72.2)
JHS 126 (22.5) 52 (41.3) 74 (58.7)
SHS 51 (9.1) 12 (23.5) 39 (76.5)
Tertiary 2 (0.4) 0 (0.0) 2 (100.0)
Occupation 17.5, 4 0.0016
None 259 (46.3) 107.0 (41.3) 152 (58.7)
Trading 102 (18.2) 38.0 (37.3) 64 (62.7)
Apprenticeship 62 (11.1) 18.0 (29.0) 44 (71.0)
Farming 124 (22.1) 68.0 (54.8) 56 (45.2)
Formal 13 (2.3) 2.0 (15.4) 11 (84.6)
Gravidity 32.8, 3 <0.0001
1–3 151 (27.0) 38 (25.2) 113 (74.8)
4–6 185 (33.0) 89 (48.1) 96 (51.9)
6–9 128 (22.9) 68 (53.1) 60 (46.9)
>9 96 (17.1) 28 (29.2) 68 (70.8)
Parity 11.7, 2 0.0029
Nullipara 128 (22.9) 46 (35.9) 82 (64.1)
Primipara 154 (27.5) 79 (51.3) 75 (48.7)
Multipara 278 (49.6) 98 (35.3) 180 (64.7)
Trimester 21.4, 2 <0.0001
First 185 (33.0) 97 (52.4) 88 (47.6)
Second 255 (45.5) 78 (30.6) 177 (69.4)
Third 120 (21.4) 48 (40.0) 72 (60.0)
UTI   0.0806
Symptomatic 127 (22.7) 42 (33.1) 85 (66.9)
Asymptomatic 433 (77.3) 181 (41.8) 252 (58.2)
History of UTI   0.0004
Yes 151 (27.0) 42 (27.8) 109 (72.2)
No 409 (73.0) 181 (44.3) 228 (55.7)
Genital hygiene 123.5, 2 <0.0001
No 126 (22.5) 97 (77.0) 29 (23.0)
Once a while 305 (54.5) 114 (37.4) 191 (62.6)
Always 129 (23.0) 12 (9.3) 117 (90.7)
Defecation facility 51.8, 2 <0.0001
Private 113 (20.2) 14 (12.4) 99 (87.6)
Public 308 (55.0) 131 (42.5) 177 (57.5)
Open 139 (24.8) 78 (56.1) 61 (43.9)
Mode of cleaning after defecation 83.7, 3 <0.0001
Water from Buta 155 (27.7) 108 (69.7) 47 (30.3)
Tissue paper 112 (20.0) 31 (27.7) 81 (72.3)
Paper 235 (42.0) 63 (26.8) 172 (73.2)
Others 58 (10.4) 31 (53.4) 27 (46.6)
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UTI, urinary tract infection; X2, Chi-square value; df, degree of freedom; p < 0.001, statistically significant.

3.2. Bacterial Aetiologies Isolated from Urine Culture

As detailed in Figure 1, the commonest bacteria isolated from the urine cultures were Escherichia coli (27.80%) followed by CoNS (13.45%), Proteus species (12.6%), Enterococcus faecalis (11.2%), Klebsiella species (10.3%), Staphylococcus aureus (6.7%), Enterobacter species (5.4%), Citrobacter species (3.6%), Pseudomonas aeruginosa (3.6%), Streptococcus species (3.1%), and Serratia species (2.2%).

Figure 1.

Figure 1

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Distribution of bacterial aetiologies isolated from urine culture.

Figure 1 shows the frequency distribution of bacterial aetiologies isolated from urine culture among study participants.

3.3. Predictors of UTI among Pregnant Women

To identify the predictors of UTI among pregnant women, we performed a multivariate logistic regression analysis of participants' demography with the prevalence of UTI (Table 2). The regression model analysis reveals that pregnant women with gravidity of 4–6, and 6–9 were 2.89 (CI: 1.78–4.67; p <  0.0001) and 3.78 (CI: 2.43–5.78; p  < 0.0001) times likely to suffer UTI. Also, primiparous women were 1.97 times significantly likely to get a UTI (CI: 1.21–3.65; p=0.014). More significantly, those who use public defecation facilities and an individual who practice open defecation were 4.65 (CI: 2.90–9.87: p <  0.0001) and 9.45 (CI: 4.89- 17.80; p <  0.0001) time more likely to get a UTI. On the other hand, pregnant women within the age range 26–30, 31–35, and ≥36 years recorded a decreasing a significant likelihood of UTI positivity. Participants who frequently [OR = 0.10 (0.06–0.67), p < 0.001] practiced genital cleaning after sex were at lower odds of getting a UTI.

Table 2.

Logistic regression analysis of demographic characteristics with the prevalence of UTI.

Variables cOR 95% CI P value aOR 95% CI P value
Age groups (years)
<20 1     1    
21–25 1.08 0.68–1.73 0.809 1.28 0.67–1.76 0.814
26–30 0.97 0.57–1.64 0.999 0.90 0.61–1.72 0.878
31–35 0.24 0.12–0.48 <0.0001 0.19 0.14–0.54 <0.0001
>36 0.16 0.06–0.41 <0.0001 0.17 0.07–0.46 <0.0001
Education
None 1     1    
Primary 0.15 0.09–0.26 <0.0001 0.13 0.08–0.32 <0.0001
JHS 0.28 0.17–0.48 <0.0001 0.32 0.20–0.52 <0.0001
SHS 0.12 0.06–0.26 <0.0001 0.17 0.10–0.34 <0.0001
Occupation
None 1     1    
Trading 0.84 0.52–1.36 0.551 0.98 0.54–1.75 0.516
Apprenticeship 0.58 0.32–1.07 0.083 0.64 0.34–1.45 0.090
Farming 1.73 1.12–2.64 0.016 1.8 1.21–2.75 0.010
Formal 0.26 0.06–1.09 0.082 0.28 0.08–1.16 0.080
Gravidity
1–3 1     1    
4–6 2.76 1.73–4.44 <0.0001 2.89 1.78–4.67 <0.0001
6–9 3.37 2.01–5.66 <0.0001 3.78 2.43–5.78 <0.0001
>9 1.22 0.69–2.13 <0.0001 1.36 0.82–2.54 <0.0001
Parity
Nullipara 1     1    
Primipara 1.88 1.17–3.07 0.012 1.97 1.21–3.65 0.014
Multipara 0.97 0.63–1.50 0.911 0.98 0.78–1.89 0.914
Trimester
First 1     1    
Second 0.40 0.27–0.59 <0.0001 0.41 0.26–0.87 <0.0001
Third 0.60 0.38–0.97 0.035 0.63 0.37–0.94 0.036
UTI
Symptomatic 1     1    
Asymptomatic 1.45 0.96–2.23 0.081 1.54 0.97–2.65 0.087
History of UTI
Yes 1     1    
No 2.06 1.37–3.11 0.0004 2.54 1.65–3.15 0.0006
Genital hygiene (wash/wipe after sex)
No 1     1    
Once a while 0.18 0.11–0.28 <0.0001 0.20 0.15–0.20 <0.0001
Always 0.03 0.02–0.06 <0.0001 0.10 0.06–0.67 <0.0001
Defecation facility
Private 1     1    
Public 5.23 2.86–9.50 <0.0001 4.65 2.90–9.87 <0.0001
Open 9.04 4.76–17.10 <0.0001 9.45 4.89–17.34 <0.0001
Mode of cleaning after def.
Water from Buta 1     1    
Tissue paper 0.16 0.10–0.29 <0.0001 0.20 0.14–0.32 <0.0001
Paper 0.15 0.10–0.25 <0.0001 0.45 0.04–0.89 <0.0001
Others 0.5 0.27–0.92 0.035 0.64 0.20–0.98 0.067
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aOR = adjusted odds ratio; cOR = crude odds ratio; CI, confidence interval; UTI, urinary tract infections; p < 0.001, statistically significant.

3.4. Antibiogram Pattern of UTI-Associated Bacterial Isolates

We investigated the antimicrobial resistance pattern of isolates as shown in Figure 2. Gram-negatives were resistant to ampicillin in 144 (98.6%) of participants, followed by resistance to cotrimoxazole (131, 89.7%), ceftriaxone (123, 84.2%), tetracycline (114, 78.1%), erythromycin (107, 73.3%), nitrofurantoin (98, 67.1%), norfloxacin (61, 41.8%), chloramphenicol (58, 39.7%), and the least to amoxicillin-clavulanic acid (52, 35.6%), respectively. Low resistance was observed for antibiotics such as ciprofloxacin (32, 21.9%), meropenem (29, 19.9%), and gentamicin (29, 19.9%). Gram positives were resistant to ampicillin in 54 (70.1%) of the participants, followed by resistance to erythromycin (45, 58.4%), cotrimoxazole (37, 48.1%), vancomycin (37, 48.1%), chloramphenicol (35, 45.5%), and ceftriaxone (31, 40.3%) in that order. There was low resistance against gentamicin in 9 (11.7%) of the participants, amoxicillin-clavulanic acid in 10 (13.0%), ciprofloxacin in 19 (24.7%), and nitrofurantoin in 22 (28.6%) of the participants, respectively.

Figure 2.

Figure 2

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The antibiotic resistance pattern of bacterial isolates among study participants: (a) Antibiotic resistance pattern of Gram-negative isolates; (b) Antibiotic resistance pattern of Gram-positive isolates. AMClav: amoxicillin-clavulanic acid, AMP: ampicillin, SXT: cotrimoxazole, CEF: ceftriaxone, CHL: chloramphenicol, CIP: ciprofloxacin, GEN: gentamicin, ERY: erythromycin, NIT: nitrofurantoin, NOR: norfloxacin, MEM: meropenem and TET: tetracycline.

We also detected the multidrug resistance pattern of the bacteria isolated. Generally, 206 (92.4%) of the bacteria isolated were resistant to at least one antibiotic, however, 152 (68.2%) of the 223 bacteria isolated were multidrug resistant. Among the bacteria species, E. coli 35 (56.5%), Klebsiella sp. 18 (78.3%), and Proteus sp. 20 (71.4%) dominated the multidrug-resistant (MDR) Gram-negative bacteria, whereas Staphylococcus aureus 13 (86.7%) was also found to dominate the multidrug-resistant Gram-positive bacteria (Table 3).

Table 3.

Multidrug resistance profile of isolated bacteria.

Bacteria N R0 R1 R2 R3 R4 R5 R6 R7 MDR
n (%) n (%) n (%) n (%) n (%) n (%) n (%) n (%) n (%)
CoNS 30 4 (13.3) 4 (13.3) 2 (6.7) 5 (16.7) 8 (26.7) 5 (16.7) 2 (6.7) 0 (0.0) 20 (66.7)
Enterococcus Faecalis 25 2 (8.0) 0 (0.0) 0 (0.0) 3 (12.0) 4 (16.0) 4 (16.0) 2 (8.0) 1 (4.0) 14 (56.0)
Staphylococcus aureus 15 0 (0.0) 0 (0.0) 2 (13.3) 5 (33.3) 3 (20.0) 3 (20.0) 2 (13.3) 0 (0.0) 13 (86.7)
Streptococcus sp. 7 0 (0.0) 0 (0.0) 0 (0.0) 2 (28.6) 1 (14.3) 3 (42.9) 0 (0.0) 0 (0.0) 6 (85.7)
Citrobacter sp. 8 1 (12.5) 0 (0.0) 0 (0.0) 2 (25.0) 3 (37.5) 2 (25.0) 0 (0.0) 0 (0.0) 7 (87.5)
Enterobacter sp. 12 0 (0.0) 0 (0.0) 2 (16.7) 1 (8.3) 2 (16.7) 6 (50.0) 1 (8.3) 0 (0.0) 10 (83.3)
Escherichia coli 62 5 (8.1) 12 (19.4) 10 (16.1) 6 (9.7) 8 (12.9) 13 (21.0) 5 (8.1) 3 (4.8) 35 (56.5)
Klebsiella sp. 23 0 (0.0) 2 (8.7) 3 (13.0) 5 (21.7) 6 (26.1) 7 (30.4) 0 (0.0) 0 (0.0) 18 (78.3)
Proteus sp. 28 2 (7.1) 4 (14.3) 2 (7.1) 5 (17.9) 7 (25.0) 5 (17.9) 2 (7.1) 1 (3.6) 20 (71.4)
P. aeruginosa 8 2 (25.0) 0 (0.0) 0 (0.0) 4 (50.0) 2 (25.0) 1 (12.5) 0 (0.0) 0 (0.0) 7 (87.5)
Serratia sp. 5 1 (20.0) 0 (0.0) 2 (40.0) 2 (40.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (40.0)
  223 17 (7.6) 23 (10.3) 25 (11.2) 43 (19.3) 48 (21.5) 54 (24.2) 20 (9.0) 12 (5.4) 152 (68.2)
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Note. R0, no antibiotic resistance; R1, resistance to one; R2, resistance to two; R3, resistance to three; R4, resistance to four; R5, resistance to five; R6, resistance to six; R7, resistance to seven; MDR, multidrug-resistant.

4. Discussion

The overall prevalence of UTI among pregnant women in this study was 39.8% which is comparable to the rate of 42.7% reported in a previous study conducted in Ghana [16] and lower than the 56.5% reported in a study conducted in a different setting in southern Ghana [32]. Conversely, the observed UTI prevalence was higher than the earlier reported rate of 17.1% in the Ho Municipality of Ghana [33]. Our present result represents one of the highest UTI prevalences to date compared to previous findings in Africa and Asia. For instance, different studies from different parts of Ethiopia such as Gondar, Addis Ababa, and Dessie have revealed UTI prevalence ranges of 9.5%–15.5% [19, 34, 35]. In addition, lower reported prevalence rates have also been reported in Kenya (15.7%) [36] and Nigeria (15.8% and 25.3%) [37]. Among the other countries are Tanzania (16.8%) [38], Cameroon (23.5%) [39], Iran (13.1%) [37], Nepal (30.5%) [4], and India (20.1%–28.0%) [40, 41]. Nonetheless, the prevalence rate reported in a study conducted in Niger [12] is higher than our result. These findings highlight that UTI prevalence rates vary within a country, across countries and geographical areas, respectively, which can be attributed to factors such as varied personal hygiene practices, attitudes around UTIs, sexual behaviour, limited healthcare infrastructure, and diagnostic tools, as well as risk factors such as age and parity [35, 37, 42–44].

Asymptomatic UTI has been reported to be the commonest form of pregnancy-associated UTI [37]. We observed the same in this study, as the prevalence of UTI among symptomatic pregnant women was 33.0% whereas that of asymptomatic was 41.8%. The observed prevalence of asymptomatic UTI in this study is higher than in earlier studies among pregnant women in the Ghanaian community [24, 32, 45] and in other populations from developing countries like Ethiopia [34, 35, 46, 47], Tanzania [38], and Kenya [36]. These observed differences could be partially explained by the study population and sample sizes, and a lack of infrastructure, and the employment of different approaches for the diagnosis of UTI [34, 35].

Parity and gravidity play a vital role in conferring the infection during pregnancy [5, 44]. In this study, we found that women who have had four or more pregnancies were at increased risk of suffering UTIs. This finding concord with reports from studies conducted in Nigeria [48], Egypt [27], and Iran [49]. Conversely, no association was found between parity and UTI among pregnant women in cross-sectional studies from Sudan [50], Tanzania [23], Ghana [51], and West Ethiopia [52]. Poor hygiene practices during pregnancy have been associated with UTIs among pregnant women [53]. In this study, participants who frequently practice genital cleaning after sex had lower odds of getting a UTI. We also found out that those who use public defecation facilities and individuals who practice open defecation were five and nine times, respectively, more likely to get UTIs. A cross-sectional study by Parasuraman et al. [54] indicated that people who use public toilet facilities are at risk of various bacterial infections. Therefore, the use of the same sanitary facilities by strangers comes with related risks of faecal bacteria transmission [55].

Most of the bacterial isolates from the urine samples of pregnant women in this study were Gram-negative. E. coli was the commonest bacteria isolates. A similar trend has been reported in Ghana [13, 16, 24, 32], Nigeria [22], Sudan [50], Libya [56], and Ethiopia [34, 46]. The possible explanation for the predominance of Gram-negative bacteria among isolated UTI aetiological agents may be because they are common members of the vaginal and rectal flora [34, 47, 57]. On the other hand, CoNS dominated the Gram-positive isolates, followed by Enterococcus faecalis and Staphylococcus aureus. While some studies have detected CoNS as the most frequently isolated bacteria [11, 34], others detected S. aureus as the most frequently isolated Gram-positive bacteria [22, 23, 34, 58, 59]. Enterococcus faecalis has also been reported as the predominant Gram-positive bacterial isolate in other studies [45].

Antibiotic susceptibility test show that most isolates are susceptible to gentamycin. Like other studies, isolates' susceptibility to gentamycin was the highest [6, 11, 19, 20, 34]. High resistance was detected against ampicillin, cotrimoxazole, ceftriaxone, tetracycline, erythromycin, and nitrofurantoin. The irrational use and abuse of broad-spectrum antibiotics due to their affordability and easy access may be the reason for the high resistance to these drugs [13, 58]. The 29 (19.9%) Gram-negative bacteria resistant to meropenem may be a threat to antibiotic options available for the treatment of infections because carbapenems have the highest potency against bacteria. It is for this reason that they are reserved and used for more severe infections or as last-line drugs [60]. Another worrying result is the resistance of some Gram-positive bacteria to vancomycin, a glycopeptide whose emerging resistance is seen among enterococci and staphylococci which has led to restrictive use to only severe infections caused by Gram-positive bacteria for which no other alternative is acceptable [60].

The 68.2% of multidrug resistance detected among the bacteria isolated from the urine of pregnant women was higher than the 57.1% reported in northern Ethiopia [61]. However, this (68.2%) cannot be compared with the reported 77.5% in Uganda [62], 80.4% from Ethiopia by MA Belete [35], 85.5% in Somaliland [46], 96.0% from Kenya [36], and 100% in Nigeria [42].

A major issue worldwide is the rise in antibiotic resistance, especially in developing nations like Ghana. The MDR rates reported in this study and in the aforementioned countries threaten the effective treatment of UTI in pregnant women as there are greater incidences of antibiotic resistance to popular antimicrobial drugs used to treat urinary tract infections in pregnant women [63]. There will be a need for high-quality, expensive antibiotics. Additionally, this may result in a lengthier treatment period and hospitalisation which can take a toll on family or caregivers [64]. Untreated UTIs during pregnancy can lead to obstetric complications as well as poor maternal and neonatal outcomes [65]. Therefore, it is impossible to ignore the teratogenic effect of prolonged antibiotic exposure in pregnant women [66].

Nevertheless, the findings of this study are consistent with reports from numerous studies. This study's cross-sectional design limits its capacity to determine the cause-and-effect link between risk factors and UTI status, which is one of its limitations. Additionally, we did not assess the adverse effect and symptoms of pregnant women with UTIs and other coinfected conditions, underlying the need for further studies to address these limitations.

5. Conclusion

The current findings demonstrate that a high prevalence of UTIs exists among pregnant women in the northern part of Ghana. Escherichia coli was the most predominant bacteria isolated. UTI in pregnancy was associated with risk factors such as the use of public defecation facilities, open defecation, and a lack of good practice in genital hygiene after sex. The variation in the resistance pattern of isolates to various drugs observed in this study and the consequences of undiagnosed and untreated UTIs underpin the need to perform urine culture and antibiotic susceptibility before treatment.

Acknowledgments

The authors are grateful to the staff of the Reproductive and Child Health (RCH) unit of the Kumbungu health centre and all the study participants.

Data Availability

The data will be made available upon reasonable request through the corresponding author.

Ethical Approval

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Local IRB (Ref. No: IRB 021/19).

Consent

All the study participants who agreed to a written consent were recruited into the study.

Conflicts of Interest

The authors declare that they have no conflict of interest.

Authors' Contributions

EKV designed the study, participated in data collection and laboratory analysis, and drafted and revised the manuscript. EA, EO, and WW were involved in the design of the study, statistical analysis, and interpretation and revision of the manuscript. EDK and SEKA were involved in the laboratory analysis and revision of the manuscript. AA was involved in the data collection and revision of the manuscript. GIM was involved in the study design and revision of the manuscript. All authors read and approved the final manuscript.

References

  • 1.Hill J. B., Sheffield J. S., McIntire D. D., Wendel G. D. Acute pyelonephritis in pregnancy. Obstetrics & Gynecology . 2005;105(1):18–23. doi: 10.1097/01.aog.0000149154.96285.a0. [DOI] [PubMed] [Google Scholar]
  • 2.Matuszkiewicz-Rowińska J., Małyszko J., Wieliczko M. Urinary tract infections in pregnancy: old and new unresolved diagnostic and therapeutic problems. Archives of Medical Science: AMS . 2015;11(1) doi: 10.5114/aoms.2013.39202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Giraldo P. C., Araújo E. D., Junior J. E., Amaral R. L., Passos M. R., Gonçalves A. K. The prevalence of urogenital infections in pregnant women experiencing preterm and full-term labor. Infectious Diseases in Obstetrics and Gynecology . 2012;2012 doi: 10.1155/2012/878241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Raza S., Pandey S., Bhatt C. Microbiological analysis of the urine isolates in kathmandu medical college teaching hospital, kathmandu, Nepal. Kathmandu University Medical Journal . 2012;9(4):295–297. doi: 10.3126/kumj.v9i4.6348. [DOI] [PubMed] [Google Scholar]
  • 5.Tadesse E., Teshome M., Merid Y., Kibret B., Shimelis T. Asymptomatic urinary tract infection among pregnant women attending the antenatal clinic of Hawassa Referral Hospital, Southern Ethiopia. BMC Research Notes . 2014;7(1):p. 155. doi: 10.1186/1756-0500-7-155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Karikari A. B., Saba C. K. S., Yamik D. Y. Assessment of asymptomatic bacteriuria and sterile pyuria among antenatal attendants in hospitals in northern Ghana. BMC Pregnancy and Childbirth . 2020;20:239–247. doi: 10.1186/s12884-020-02936-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Hooton T. M. Uncomplicated urinary tract infection. New England Journal of Medicine . 2012;366(11):1028–1037. doi: 10.1056/nejmcp1104429. [DOI] [PubMed] [Google Scholar]
  • 8.Dimetry S. R., El-Tokhy H. M., Abdo N. M., Ebrahim M. A., Eissa M. Urinary tract infection and adverse outcome of pregnancy. Journal of the Egyptian Public Health Association . 2007;82(3-4):203–218. [PubMed] [Google Scholar]
  • 9.Gilbert N. M., O’brien V. P., Hultgren S., Macones G., Lewis W. G., Lewis A. L. Urinary tract infection as a preventable cause of pregnancy complications: opportunities, challenges, and a global call to action. Global Advances in Health and Medicine . 2013;2(5):59–69. doi: 10.7453/gahmj.2013.061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Smaill F. M., Vazquez J. C. Antibiotics for asymptomatic bacteriuria in pregnancy. Cochrane Database of Systematic Reviews . 2019;2019(11) doi: 10.1002/14651858.cd000490.pub4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Assefa A., Asrat D., Woldeamanuel Y., G/Hiwot Y., Abdella A., Melesse T. Bacterial profile and drug susceptibility pattern of urinary tract infection in pregnant women at Tikur Anbessa Specialized Hospital Addis Ababa, Ethiopia. Ethiopian Medical Journal . 2008;46(3):227–235. [PubMed] [Google Scholar]
  • 12.Adabara N., Momoh J., Bala J., Abdurrahman A., Abu-Bakr M. The prevalence of bacterial urinary tract infections (UTI) among women attending antenatal clinic in the general hospital, Minna in Niger state. International Journal of Biomedical Research . 2012;3(03):171–173. [Google Scholar]
  • 13.Afoakwa P., Domfeh S., Afranie B., et al. Asymptomatic bacteriuria and anti-microbial susceptibility patterns among women of reproductive age. A cross-sectional study in primary care, Ghana. Medical Science . 2018;6(4):p. 118. doi: 10.3390/medsci6040118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Adu-Poku M., Addo M. Antimicrobial susceptibility profile of urinary tract pathogenic infections in Diabetic patients attending a health facility in Kumasi, Ghana. International Journal of Pathogen Research . 2020;4(2):37–45. doi: 10.9734/ijpr/2020/v4i230109. [DOI] [Google Scholar]
  • 15.Fosu K., Quansah E., Dadzie I. J. M. R. J. I. Antimicrobial profile and asymptomatic urinary tract infections among pregnant women attending antenatal clinic in bolgatanga regional hospital, Ghana. Microbiology Research Journal International . 2019;28(3):1–8. doi: 10.9734/mrji/2019/v28i330132. [DOI] [Google Scholar]
  • 16.Forson A. O., Tsidi W. B., Nana-Adjei D., Quarchie M. N., Obeng-Nkrumah N. Escherichia coli bacteriuria in pregnant women in Ghana: antibiotic resistance patterns and virulence factors. BMC Research Notes . 2018;11(1):901–907. doi: 10.1186/s13104-018-3989-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Delzell J. E., Lefevre M. Urinary tract infections during pregnancy. American Family Physician . 2000;61(3):713–721. [PubMed] [Google Scholar]
  • 18.MacLean A. Urinary tract infection in pregnancy. International Journal of Antimicrobial Agents . 2001;17(4):273–277. doi: 10.1016/s0924-8579(00)00354-x. [DOI] [PubMed] [Google Scholar]
  • 19.Alemu A., Moges F., Shiferaw Y., et al. Bacterial profile and drug susceptibility pattern of urinary tract infection in pregnant women at University of Gondar Teaching Hospital, Northwest Ethiopia. BMC Research Notes . 2012;5(1):p. 197. doi: 10.1186/1756-0500-5-197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Demilie T., Beyene G., Melaku S., Tsegaye W. Urinary bacterial profile and antibiotic susceptibility pattern among pregnant women in North West Ethiopia. Ethiopian journal of health sciences . 2012;22(2):121–128. [PMC free article] [PubMed] [Google Scholar]
  • 21.Ferede G., Yismaw G., Wondimeneh Y., Sisay Z. The prevalence and antimicrobial susceptibility pattern of bacterial uropathogens isolated from pregnant women. European Journal of Experimental Biology . 2012;2(5):1497–1502. [Google Scholar]
  • 22.Oli A. N., Akabueze V. B., Ezeudu C. E., et al. Bacteriology and antibiogram of urinary tract infection among female patients in a tertiary health facility in south eastern Nigeria. The Open Microbiology Journal . 2017;11(1):292–300. doi: 10.2174/1874285801711010292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Masinde A., Gumodoka B., Kilonzo A., Mshana S. Prevalence of urinary tract infection among pregnant women at Bugando Medical Centre, Mwanza, Tanzania. Tanzania Journal of Health Research . 2009;11(3):154–159. doi: 10.4314/thrb.v11i3.47704. [DOI] [PubMed] [Google Scholar]
  • 24.Obirikorang C., Quaye L., Bio F., Amidu N., Acheampong I., Addo K. Asymptomatic bacteriuria among pregnant women attending antenatal clinic at the uni-versity hospital, kumasi, Ghana. Journal of Medicine and Biomedical Sciences . 2012;1(1):38–44. [Google Scholar]
  • 25.Amiri F., Rooshan M., Ahmady M., Soliamani M. Hygiene practices and sexual activity associated with urinary tract infection in pregnant women. Eastern Mediterranean Health Journal . 2009;15(1):104–110. doi: 10.26719/2009.15.1.104. [DOI] [PubMed] [Google Scholar]
  • 26.Ramzan M., Ba khsh S., Salam A., Khan G. M., Mustafa G. Risk factors in urinary tract infection. Gomal Journal of Medical Sciences . 2004;2 [Google Scholar]
  • 27.Enayat K., Fariba F., Bahram N. Asymptomatic bacteriuria among pregnant women referred to outpatient clinics in Sanandaj, Iran. International Braz J Urol . 2008;34(6):699–707. doi: 10.1590/s1677-55382008000600004. [DOI] [PubMed] [Google Scholar]
  • 28.Service G. S. Population & Housing Census: Demographic, Social, Economic & Housing Characteristics . Accra, Ghana: Ghana Statistical Service; 2021. [Google Scholar]
  • 29.Karah N., Rafei R., Elamin W., et al. Guideline for urine culture and biochemical identification of bacterial urinary pathogens in low-resource settings. Diagnostics . 2020;10(10):p. 832. doi: 10.3390/diagnostics10100832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Cheesbrough M. District Laboratory Practice in Tropical Countries . 2. Cambridge, UK: Cambridge University Press; 2005. [Google Scholar]
  • 31.Clsi. Performance Standards for Antimicrobial Susceptibility Testing: 25th Informational Supplement . Wayne, Pa, USA: Clinical and Laboratory Standards Institute; 2015. [Google Scholar]
  • 32.Boye A., Siakwa P. M., Boampong J. N., et al. Asymptomatic urinary tract infections in pregnant women attending antenatal clinic in Cape Coast, Ghana. E3 J Med Res . 2012;1(6):74–83. [Google Scholar]
  • 33.Adjato S. F. D., Amoako E. O., Abaka-Yawson A., Agbodzakey H., Tawiah P. Bacterial profile and antimicrobial sensitivity patterns in asymptomatic bacteriuria: a cross-sectional study of sickle cell disease patients in the Ho municipality. Asian Journal of Medicine and Health . 2019;15:1–7. [Google Scholar]
  • 34.Weldegebreal F., Derese B., Kedir H., Teklemariam Z., Balakrishnan S. Bacterial profile of urinary tract infection and antimicrobial susceptibility pattern among pregnant women attending at Antenatal Clinic in Dil Chora Referral Hospital, Dire Dawa, Eastern Ethiopia. Therapeutics and Clinical Risk Management . 2016;12:251–260. doi: 10.2147/tcrm.s99831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Belete M. A. <p>Bacterial profile and ESBL screening of urinary tract infection among asymptomatic and symptomatic pregnant women attending antenatal care of northeastern Ethiopia region<</p>. Infection and Drug Resistance . 2020;13:2579–2592. doi: 10.2147/idr.s258379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Onyango H. A., Ngugi C., Maina J., Kiiru J. Urinary tract infection among pregnant women at pumwani maternity hospital, nairobi, Kenya: bacterial etiologic agents, antimicrobial susceptibility profiles and associated risk factors. Advances in microbiology . 2018;8 [Google Scholar]
  • 37.Farazi A., Jabbariasl M. Asymptomatic bacteriuria in pregnancy in the central region of Iran: frequency, risk factors, and causative organisms. Clinical Epidemiology and Global Health . 2019;7(3):309–312. doi: 10.1016/j.cegh.2018.09.009. [DOI] [Google Scholar]
  • 38.Kaduma J., Seni J., Chuma C., et al. Urinary tract infections and preeclampsia among pregnant women attending two hospitals in Mwanza City, Tanzania: a 1: 2 matched case-control study. BioMed Research International . 2019;2019 doi: 10.1155/2019/3937812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Egbe T. O., Omarine N., Henri E., Francine W. W. C. D., Egbe D. N., Enow-Orock G. E. Uropathogens of urinary tract infection in pregnancy and maternal-fetal outcomes at the douala referral hospital, Cameroon: a case-control study. Open Journal of Obstetrics and Gynecology . 2020;10(07):914–929. doi: 10.4236/ojog.2020.1070087. [DOI] [Google Scholar]
  • 40.Thakre S., Dhakne S. N., Thakre S. B., Ughade S. N. Hygiene practices and sexual activity associated with urinary tract infection in rural pregnant women of nagpur, India. Indian Journal of Medical Microbiology . 2015;33(1):177–178. doi: 10.4103/0255-0857.148416. [DOI] [PubMed] [Google Scholar]
  • 41.Ranjan A., Sridhar S. T. K., Matta N., Chokkakula S., Ansari R. K. Prevalence of UTI among pregnant women and its complications in newborns. Indian Journal of Pharmacy Practice . 2017;10(1):45–49. doi: 10.5530/ijopp.10.1.10. [DOI] [Google Scholar]
  • 42.Akpan N. G., Umoyen A. J., Luka T. T., Esua I. S., Okon A. S., Antia U. Bacterial etiologic agents, prevalence and associated risk factors of asymptomatic bacteriuria among pregnant and non-pregnant women in primary health care centers in South-South Nigeria. International Journal of Medical and Health Research . 2019;5(6):66–76. [Google Scholar]
  • 43.Labib Al-Kashif M. M. Urinary tract infection among pregnant women and its associated risk factors: a cross-sectional study. Biomedical and Pharmacology Journal . 2019;12(4):2003–2010. doi: 10.13005/bpj/1832. [DOI] [Google Scholar]
  • 44.Vasudevan R. Urinary tract infection: an overview of the infection and the associated risk factors. Journal of Microbiology & Experimentation . 2014;1(2) doi: 10.15406/jmen.2014.01.00008.00008 [DOI] [Google Scholar]
  • 45.Labi A., Yawson A., Ganyaglo G., Newman M. J. G. Prevalence and associated risk factors of asymptomatic bacteriuria in ante-natal clients in a large teaching hospital in Ghana. Ghana Medical Journal . 2015;49(3):154–158. doi: 10.4314/gmj.v49i3.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Ali A. H., Reda D. Y., Ormago M. D. Prevalence and antimicrobial susceptibility pattern of urinary tract infection among pregnant women attending Hargeisa Group Hospital, Hargeisa, Somaliland. Scientific Reports . 2022;12(1):p. 1419. doi: 10.1038/s41598-022-05452-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Gebremariam G., Legese H., Woldu Y., Araya T., Hagos K., GebreyesusWasihun A. Bacteriological profile, risk factors and antimicrobial susceptibility patterns of symptomatic urinary tract infection among students of Mekelle University, northern Ethiopia. BMC Infectious Diseases . 2019;19(1):950–1011. doi: 10.1186/s12879-019-4610-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Ifeanyi Abraham O., Ekerenam U. E., Emmanuel E. A. Correlating urinary tract infection with patients’ presenting symptoms and bacterial isolation from urine in uyo, Nigeria. Science Journal of Clinical Medicine . 2019;8(3):21–27. doi: 10.11648/j.sjcm.20190803.11. [DOI] [Google Scholar]
  • 49.Amiri M., Lavasani Z., Norouzirad R., et al. Prevalence of urinary tract infection among pregnant women and its complications in their newborns during the birth in the hospitals of Dezful city, Iran. Iranian Red Crescent Medical Journal . 2015;17(8) doi: 10.5812/ircmj.26946.e26946 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Hamdan H. Z., Ziad A. H. M., Ali S. K. Adam I, antimicrobials, “Epidemiology of urinary tract infections and antibiotics sensitivity among pregnant women at Khartoum North Hospital. Annals of clinical microbiology . 2011;10(1):1–5. doi: 10.1186/1476-0711-10-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Turpin C., Minkah B., Danso K., Frimpong E. Asymptomatic bacteriuria in pregnant women attending antenatal clinic at komfo anokye teaching hospital, kumasi, Ghana. Ghana Medical Journal . 2007;41(1):26–29. [PMC free article] [PubMed] [Google Scholar]
  • 52.Emiru T., Beyene G., Tsegaye W., Melaku S. Associated risk factors of urinary tract infection among pregnant women at felege hiwot referral hospital, bahir dar, north west Ethiopia. BMC Research Notes . 2013;6(1):292–296. doi: 10.1186/1756-0500-6-292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Imade P. E., Izekor P. E., Eghafona N. O., Enabulele O. I., Ophori E. Asymptomatic bacteriuria among pregnant women. North American Journal of Medical Sciences . 2010;2(6):263–266. doi: 10.4297/najms.2010.2263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Parasuraman S., Wen L. E., Sam A. T., Christapher P. V., Kumar K. V. Analysis of correlation between defecation posture and risk of urinary tract infections among adolescent populations. Environmental Disease . 2016;1(2):p. 77. doi: 10.4103/2468-5690.185305. [DOI] [Google Scholar]
  • 55.Greed C. The role of the public toilet: pathogen transmitter or health facilitator? Building Services Engineering Research and Technology . 2006;27(2):127–139. doi: 10.1191/0143624406bt151oa. [DOI] [Google Scholar]
  • 56.Tamalli M., Bioprabhu S., Alghazal M. Urinary tract infection during pregnancy at Al-khoms, Libya. International Journal of Medicine and Medical Sciences . 2013;3(5):455–459. [Google Scholar]
  • 57.Minardi D., d’Anzeo G., Cantoro D., Conti A., Muzzonigro G. Urinary tract infections in women: etiology and treatment options. International Journal of General Medicine . 2011;4:333–343. doi: 10.2147/ijgm.s11767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Newman M. J., Frimpong E., Donkor E. S., Opintan J. A., Asamoah-Adu A. Resistance to antimicrobial drugs in Ghana. Infection and Drug Resistance . 2011;4:215–220. doi: 10.2147/IDR.S21769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Ugbogu O., Ogbonnaya R., Nworie O. Asymptomatic bacteriuria amongst pregnant women in Aba, Abia state, Nigeria. Niger J Microbiol . 2010;24:2024–2027. [Google Scholar]
  • 60.Van Bambeke F., Van Laethem Y., Courvalin P., Tulkens P. M. Glycopeptide antibiotics. Drugs . 2004;64(9):913–936. doi: 10.2165/00003495-200464090-00001. [DOI] [PubMed] [Google Scholar]
  • 61.Gontie G. B., Wolde H. F., Baraki A. G. Prevalence and associated factors of malaria among pregnant women in Sherkole district, Benishangul Gumuz regional state, West Ethiopia. BMC Infectious Diseases . 2020;20(1):p. 573. doi: 10.1186/s12879-020-05289-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Nteziyaremye J., Iramiot S. J., Nekaka R., et al. Asymptomatic bacteriuria among pregnant women attending antenatal care at Mbale Hospital, Eastern Uganda. PLoS One . 2020;15(3) doi: 10.1371/journal.pone.0230523.e0230523 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Asmat U., Mumtaz M. Z., Malik A. Rising prevalence of multidrug-resistant uropathogenic bacteria from urinary tract infections in pregnant women. Journal of Taibah University Medical Sciences . 2021;16(1):102–111. doi: 10.1016/j.jtumed.2020.10.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Yeta K. I., Michelo C., Jacobs C. Antimicrobial resistance among pregnant women with urinary tract infections attending antenatal clinic at levy mwanawasa university teaching hospital (LMUTH), lusaka, Zambia. International Journal of Microbiology . 2021;2021:9. doi: 10.1155/2021/8884297.8884297 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Kalinderi K., Delkos D., Kalinderis M., Athanasiadis A., Kalogiannidis I. Urinary tract infection during pregnancy: current concepts on a common multifaceted problem. Journal of Obstetrics and Gynaecology . 2018;38(4):448–453. doi: 10.1080/01443615.2017.1370579. [DOI] [PubMed] [Google Scholar]
  • 66.Mensah K. B., Opoku-Agyeman K., Ansah C. Antibiotic use during pregnancy: a retrospective study of prescription patterns and birth outcomes at an antenatal clinic in rural Ghana. Journal of Pharmaceutical Policy and Practice . 2017;10(1):24–27. doi: 10.1186/s40545-017-0111-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

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