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Prevalence and antimicrobial susceptibility pattern of urinary tract infection among pregnant women attending Hargeisa Group Hospital, Hargeisa, Somaliland

The aim of this study was to determine the prevalence, antimicrobial susceptibility pattern and associated factors of urinary tract infection (UTI) among pregnant women attending Hargeisa Group Hospital (HGH), Hargeisa, Somaliland. A cross-sectional study was conducted at HGH, Hargeisa, Somaliland and participants were selected by systematic random sampling technique. Clean catch midstream urine samples were collected from 422 participants and cultured and antimicrobial susceptibility pattern was determined for the isolates. Univariable and multivariable logistic regression analyses were utilized to identify the independent risk factors for UTI. The prevalence of UTI was 16.4% (95% CI 13.3–19.9). The predominant bacteria isolate was E. coli (43.5%) followed by Coagulase negative staphylococcus (CoNS) 11(16%), S. aureus 9(13%), K. pneumonia 6(8.7%), Pseudomonas aeruginosa 5(7.2%), Proteus mirabilis 4(5.8%), Citrobacter spp 3(4.4%) and M. morganii 1(1.5%) Gram negative bacilli were resistant to ampicillin (96%) and tetracycline (71.4%) and Gram-positive cocci were also resistant to ampicillin (90%), tetracycline (55%). Multidrug resistance was observed in 85.5% of bacterial isolated. No formal education participants, previous history of catheterization and previous history of UTI had 3.18, 3.22 and 3.73 times respectively more likely to develop UTI than their counterparts. Culture and susceptibility test is vital for appropriate management of UTI in the study area.

Ethics approval and consent to participate. Ethical approval was obtained from the institutional review board of Hawassa University, College of medicine and health sciences (Ref No: IRB/231/11). Informed written consent was obtained from all participants. All methods were carried out in accordance with relevant guidelines and regulations. Clinicians were communicated the findings of culture and sensitivity tests.

Consent for publication.
Individual data such as images and videos did not accompany this particular manuscript and hence consent for publication is not applicable.

Results
A total of 422 pregnant women were participated during the study period. In this study the mean age of study participants was 30.9 (± 5.6 SD) years within the age range of 18-44 (Table 1).
Obstetrics and clinical characteristics are indicated in Table 2.

Discussion
The overall prevalence of UTI in pregnant women in this study was 16.4%. This is comparable to the prevalence of UTI reported in in Mwanza City, Tanzania 16.8% 10 23 . This variation in prevalence might be due to across different studies from one country to another and among regions of the same country might be attributed to the difference in associated factors, sample size, social habits of the community, the standard of personal hygiene and education 24 .
The prevalence of UTI among symptomatic and asymptomatic pregnant women in this study was 9.5% and 6.9% respectively. The occurrence of UTI case among asymptomatic was in line with the previous study done in Cameroon 7.8% 25 , in Kanpur, India 7.3% 26 and in Makkah, Saudi Arabia 8% 27 , On the other hand, a low prevalence of 0.13% In meta-analysis in Iran 28 , in Colombo, Sri Lanka 3.6% 29 and in Ghana 5.5% 30 was reported asymptomatic UTI. While higher prevalence was recorded in Hawassa, Southern 21.2% 31 , in Bangladesh 10.2% 32 and in Nairobi, Kenya 21.5% 33 .
In this study the symptomatic study was 9.5%, These result of symptomatic UTI were agree with a study conducted from in Khartoum Sudan 12.1% 23 14 , in Tanzania also Gram negative bacteria and Gram positive bacteria were reported 61.9% and 38.1% 39 respectively. This could be due to the presence of unique structure in Gram negative bacteria which help for attachment to the uroepithelial cells and prevent bacteria from urinary lavage, allowing for multiplication and tissue invasion-resulting in invasive infection and pyelonephritis in pregnancy 40 .
Among isolated pathogens, were E. coli was the most predominant bacteria 43.5%, which is similar with previous studies in Ambo town, Central Ethiopia 46.4% of isolated cases 14 , in Bangalore, India 43.9% 41 and in Nairobi, Kenya 40.0% was reported 42 . However, it was lower than reported in the previous studies conducted in different countries, which was India 53.8%, Italy 57.1% and Iran 57.25% 22,43,44 . E. coli is the most common microorganism in the vaginal and rectal area. Because of anatomical and functional changes and difficulty of maintaining personal hygiene during pregnancy, may increase the risk of acquiring UTI from E. coli 45 48 .
In this study the other drugs also showed highly resistance to Gram-negative were tetracycline (71.4%), trimethoprim-sulfamethoxazole (57.1%), amoxicillin clavulanic acid (55.1%) and nalidixic acid (51%) and this agree the other study done in Dil Chora Referral Hospital, Dire Dawa, Eastern Ethiopia AMP (89.5%), amoxicillin (73.7%), and TTC (73.7%), NA (52.6%), except nitrofurantoin (57.9%) 48 and in Mbarara Regional Referral Hospital, South-western Uganda were highly resistant to Amoxicillin, Ampicillin, and Amoxicillin/Clavulanic acid at 95.7%, 95.0%, and 72.9% 38 . The findings of this study is not in line with the reports from Kenya 42 . These differences could be due to variations in antibiotic prescription patterns across various countries.
In this current study, the Gram-negatives, the predominant isolate was E. coli, which is resistant to ampicillin (93.3%), TTC (73.3%), SXT (60%), nalidixic acid (53.3%) and AMC (46.7%). Similar findings have been reported from previous studies in Dire Dawa, Eastern Ethiopia, South-western Uganda and Addis Ababa, Ethiopia 38,47,48 . The other isolated Gram negative bacteria include K. pneumonia showed more than 65% sensitive to meropenem, gentamicin, ceftriaxone, ciprofloxacin and nitrofurantoin this agreed with the study done in South-western Uganda 38 , K. pneumoniae was 100% resistant to ampicillin, Similar findings were done in Adigrat General Hospital, Northern Ethiopia and Karamara Hospital Jigjiga, Eastern Ethiopia 46,51 . In this study, the Gram positive bacterial isolates were relatively sensitive to erythromycin, cefoxitin, ceftriaxone, nitrofurantoin, gentamicin, ciprofloxacin and each accounted 85%, 85%, 75%, 75%, 70% and 65%. This was comparable with the finding from Ivory Coast, Dire Dawa, Eastern Ethiopia and Gonder Ethiopia 48,52,53 However, in contrast with study report from Southern Ethiopia, which ceftriaxone was 100% resistant to grampositive bacteria 54 . Table 5. Multi drug resistance pattern of bacterial isolates from pregnant women with UTI attended antenatal care at HGH, Hargeisa, Somaliland, 2020 (n = 69). R2 = resistance to two drugs, R3 = resistance to three drugs, R4 = resistance to four drugs, R5 = resistance to five drugs, R6 = resistance to six drugs and ≥ R7 = resistance to seven and more drugs, MDR = resistance for three or more antibiotics. www.nature.com/scientificreports/ In this study, Gram positive bacteria showed highly resistance to ampicillin 90% and tetracycline 55%. This could be due to the infrequent use of the drug in the study area. Comparable result was reported in Gonder Ethiopia 53 , in Lagos, Nigeria, and Benishangul Gumuz Region, Western Ethiopia 55 . Coagulase negative staphylococci, which were the predominant isolates from Gram-positives 55% and was found 63% to 81% sensitive to erythromycin, cefoxitin, ceftriaxone, nitrofurantoin gentamicin and ciprofloxacin. However, in contrast was shown nitrofurantoin to 26.7% resistance in study done in Ethiopia 56 , while comparable studies done in Hawassa, Ethiopia 50 . Table 6. Bivariate and multivariate analysis for the assessment of factors associated with UTI among pregnant women attending antenatal care at HGH, Hargeisa, Somaliland, 2020 (n = 422). I reference, AOD adjusted odds ratio, COR crude odds ratio, N number, UTI Urinary tract infection. www.nature.com/scientificreports/ In this study, S. aureus which constituted for 45% of the Gram positive bacteria showed 66.7-88.9% were sensitive to erythromycin, cefoxitin, ceftriaxone, nitrofurantoin, ciprofloxacin and gentamicin, this agree with study done in Hawassa, Ethiopia, Benishangul Gumuz Region, Western Ethiopia and Nairobi, Kenya 42,50,55 . In contrast to research done in Addis Ababa, Ethiopia, which erythromycin was highly resistant 60% 47 . However, this study showed 100% ampicillin to S. aureus, similar study done in Jigjiga, Ethiopia, Dire Dawa, Eastern Ethiopia and Addis Ababa, Ethiopia 46,48,57 . This is caused by use of empirical treatment against bacterial infections of the urinary tract infection in the study area. This implies that ampicillin cannot be used as empirical therapy for urinary tract infection particularly in the study area.
In this study, MDR was seen in 85.5% of all bacteria isolated. Our finding is higher than studies done in same regions of Ethiopia like 57.1% in Addis Ababa, and 73% in Mekelle 35,47 , in Tanzania 77% 39 and in Eastern Uganda 77.5 58 . Our finding is lower than studies done in South-South Nigeria 100% 49 , in Kenya 96% 11 and same regions in Ethiopia like in Dire Dawa 100%, Gondar 95% and Jigjiga 96% 21,46,48 . This indicates that multi drug resistance was found to be very high to the commonly used antibiotics. Antibiotic resistance has been recognized as the consequence of antibiotic use and abuse 59 . Therefore, the reasons for this alarming phenomenon might be inappropriate and incorrect administration of antimicrobial agents in empiric therapies and lack of appropriate infection control strategies, which can cause a shift to increase prevalence of resistant organisms in the community.
In the present study, the result of multivariable logistic regression models revealed that socio-demographic factors among pregnant women were statistically significance with no formal education and low level of family income (≤ $100) [P = 0.045, AOR = 3.183 (1.027, 9. In the study, obstetrics and clinical characteristics were shown that, highly significant proportion of UTI was recorded among those study subjects with prior history of UTI. The multivariate logistic regression analysis of current study showed that 3.7 more likely to occur the UTI compared with pregnant women that have not the previous history of UTI [P = 0.000 AOR = 3.734 (1.855, 7.515)]. This finding is similar with report from Uganda (P = 0.002), Libya (P = 0.00), Egypt (P = 0.001), India (P = 0.0423), and same regions of Ethiopia like Gondar, (P-value = 0.001), Dire Dewa (P-value = 0.006) and Addis Ababa (P = 0.004) 15,21,22,38,47,48,61 . The possible explanation for this association could be due to the existence of antibiotic-resistant strains from the previous infection.
In the current study, participants with the previous history of indwelling catheterization had about 3.2 times chance of developing UTI [P = 0.012 AOR = 3.216 (1.287, 8.038)] among pregnant women. This finding agrees with similar reports from Northeastern Ethiopia, Addis Ababa, Ethiopia and Gonder Ethiopia 21,34,47 . This could be due to long duration of catheterization, frequent catheterization or contamination during inserting catheters. However other studies done in Dire Dawa, Eastern Ethiopia and Jigjiga Eastern Ethiopia disagreed of this study 46,48 . In the present study, there was no statistical significant association between prevalence of UTI among pregnant women and maternal age, residence, marital status, occupation, gestational period, gravidity, History of diabetes mellitus, History of abortion History of obstetric and gynecologic surgery and History of premature labor. this results were agreed the report from Bangladesh 36 , Nairobi, Kenya except the maternal age 33 , Nigeria 49 , Goba and Sinana Ethiopia 37 , Dire Dawa, Eastern Ethiopia 48 and Addis Ababa, Ethiopia except history of abortion 47 .
. Majority of the isolates were resistant to the commonly prescribed antibiotics, therefore culture and antibiotic susceptibility testing was recommended before giving treatment to prevent antimicrobial resistance at least at Referral Hospital Setup and health information dissemination to the patients recommended to avoid self-medication practice.

Data availability
The datasets used and analyzed in the current study are available from the corresponding author on reasonable request.