{"id":63186,"date":"2024-12-30T10:10:57","date_gmt":"2024-12-30T10:10:57","guid":{"rendered":"https:\/\/biomedpharmajournal.org\/?p=63186"},"modified":"2025-01-07T04:21:55","modified_gmt":"2025-01-07T04:21:55","slug":"microbiological-and-antimicrobial-resistance-pattern-among-pregnant-women-in-the-sultanate-of-oman-comparison-between-symptomatic-and-asymptomatic-bacteriuria","status":"publish","type":"post","link":"https:\/\/biomedpharmajournal.org\/staging\/vol17no4\/microbiological-and-antimicrobial-resistance-pattern-among-pregnant-women-in-the-sultanate-of-oman-comparison-between-symptomatic-and-asymptomatic-bacteriuria\/","title":{"rendered":"Microbiological and Antimicrobial Resistance Pattern Among Pregnant Women in The Sultanate of Oman: Comparison Between Symptomatic and Asymptomatic Bacteriuria"},"content":{"rendered":"

Introduction<\/strong><\/p>\n

Bacteriuria is the manifestation of bacterial pathogens in the urine with and without causing apparent clinical manifestations1,2 <\/sup>Biologically, the urinary tract is sterile and designed to prevent infections3<\/sup>. The bladder and ureters are structured to stop urine from backing up toward the kidneys. The flow of urine during urination washes bacteria out of the urinary tract4<\/sup> However, infections can still occur because of some influencing factors, such as variations in the host\u2019s natural defense mechanisms, premenopausal and menopausal factors and age2<\/sup>. Urinary tract infection (UTIs) may result in serious complications such as cystitis, urethritis, and pyelonephritis5<\/sup>. \u00a0Symptomatic and asymptomatic UTIs result in adverse maternal and fetal outcomes2<\/sup>.<\/p>\n

Asymptomatic bacteriuria is a subclinical infection that is existing in cases where the urine culture shows a bacterial pathogen growth of higher than 105<\/sup> colony-forming units (CFU) per ml of urine and without apparent UTI clinical manifestations in the patient1<\/sup> . Proper management of asymptomatic bacteriuria can decrease its incidence by 80%\u201390% 6,7,8<\/sup><\/p>\n

The causative agent that accounts for more than 80% of all UTIs during pregnancy is Escherichia<\/em> coli<\/em>9<\/sup>. Other causes include Proteus mirabilis, , Staphylococcus epidermidis<\/em>, Staphylococcus<\/em> saprophyticus<\/em> and Klebsiella pneumoniae <\/em>3,8,9<\/sup>.<\/p>\n

A previous study in Nigeria on urine samples obtained randomly from 125 pregnant patients, showed that 40% of patients were positive for bacteriuria10<\/sup>. Another study in the United Arab Emirates showed that the highest rate of infection among symptomatic pregnant UTI patients was with E.Coli<\/em> followed by Group B streptococcus<\/em> 11<\/sup>. The percentage of bacteriuria is high in pregnant women due to many factors12<\/sup>. One factor is women\u2019s immune status during pregnancy. Pregnant women are considered immunocompromised UTI hosts8<\/sup>. . <\/sup>Other factors include the physical and hormonal changes1,8,12<\/sup>. For example, during pregnancy, there is a great increase in fluid discharges, which enhance bacterial growth. In addition, progesterone stimulates urethral smooth muscle resting, causing urinary stasis, which is significant in the etiology of cystitis9,13<\/sup>. During pregnancy, the urine pH reaches an appropriate level for E. coli <\/em>growth13<\/sup>.<\/p>\n

Undetected asymptomatic bacteriuria is linked to unfavorable obstetric and fetal outcomes, because of the increased chance of its progression to symptomatic bacteriuria 14,15<\/sup>. Therefore, screening and management of bacteriuria during pregnancy are essential to avoid UTI these adverse effects3<\/sup>.<\/p>\n

The aims of the present study were to investigate the prevalence of symptomatic and asymptomatic bacteriuria Omani among pregnant women and to identify the causative bacterial pathogens, and finally to determine the antibiotic resistance patterns of the bacterial pathogens isolated from this unique group of patients.<\/p>\n

Materials and Methods<\/strong><\/p>\n

Specimens<\/strong><\/p>\n

Detection of pathogenic bacteria in urine by routine culture<\/strong><\/p>\n

Microscopic examination of the urine samples was carried out by loading 60 \u03bcL of each urine sample into microtiter plate wells. Then, the urine specimens were examined under an inverted light microscope for the detection of epithelial cells, casts ,crystals,\u00a0 white and red blood cells. A UTI was diagnosed by bacterial culture. \u00a0All the urine specimens were inoculated aseptically using a bacteriological 3 mm loop on cysteine lactose electrolyte deficient agar (CLED).<\/p>\n

Following inoculation of the urine samples on CLED agar, the agar plates were incubated at 37\u02daC for 24 hours. The results were reported depending on the shape and number of colonies. The colonies were counted to determine the degree of significance, which depended on the loop size used. Only plates with more than 11 colonies were reported as significant. When three or more types of bacterial colonies were present, the sample was reported to have urogenital contamination. The CLED agar plates were examined for the presence of yellow or green colonies, which may indicate the presence of lactose-fermenting or non-lactose-fermenting bacteria.<\/p>\n

Pathogenic bacteria identification and antibiotic sensitivity tests<\/strong><\/p>\n

Biochemical identification of the pathogenic microorganisms in the urine samples and antibiotic sensitivity tests of the isolated bacterial pathogens were carried out for suspected colonies using the BD Phoenix\u2122 100 (Becton Dickinson, USA). The bacteria isolated from the urine samples were suspended in 0.85% NaCl and diluted to 0.5 McFarland. Then, they were loaded into specific panels and analyzed using the BD Phoenix\u2122 100.<\/p>\n

Detection of Streptococcus agalactiae<\/strong><\/p>\n

S. agalactiae<\/em> detection in the urine samples was conducted using the Alere BinaxNOW\u00ae Streptococcus agalactiae<\/em> Antigen Card (Abbott, USA), which is a rapid assay for the qualitative detection of S. <\/em>agalactiae (Group B Streptococci)<\/em> antigen in a patient\u2019s urine sample. The test was carried out by immersing a swab in the urine sample, and then the swab was inserted into the card. The reagent was added to the swab, and the result appeared after 15 minutes. If two lines appeared (control and test), a positive result was indicated. Positive samples by Alere BinaxNOW\u00ae Streptococcus agalactiae<\/em> Antigen Card were confirmed by the isolation of S. <\/em>agalactiae, <\/em>followed by antibiotic sensitivity testing.<\/p>\n

Data analysis<\/strong><\/p>\n

All patient data were collected and tabulated using the Excel program (Excel 2013). . \u00a0SPSS software.<\/p>\n

Results<\/strong><\/p>\n

Clinical features<\/strong><\/p>\n

Of the 230 urine samples analyzed, 216 (93.91%) samples were negative for bacteriuria, while 14 (6.03%) samples were positive. The 14 samples were categorized according to the patients\u2019 symptoms into symptomatic and asymptomatic bacteriuria. Table 1 shows the symptoms of the symptomatic bacteriuria patients; some symptomatic patients showed more than one clinical manifestation [Table 1]. The most common observed clinical manifestations \u00a0were dysuria followed by lower abdominal pain [Table 1]. Six symptomatic patients (2.06%) were positive for bacteriuria, while eight asymptomatic patients (3.47%) were positive for bacteriuria. [Figure 1], shows the rate of symptomatic and asymptomatic bacteriuria among the 230 isolated samples.<\/p>\n

Table 1:<\/strong> Symptoms that appeared in symptomatic bacteriuria patients (Total number of symptomatic bacteriuria patients<\/em> (14). Some patients showed more than one clinical manifestation<\/em>)<\/strong><\/p>\n\n\n\n\n\n\n\n\n
UTI Symptoms<\/strong><\/td>\nNumber of cases<\/strong><\/td>\n<\/tr>\n
Dysuria<\/td>\n5<\/td>\n<\/tr>\n
Lower abdominal pain<\/td>\n2<\/td>\n<\/tr>\n
Fever<\/td>\n1<\/td>\n<\/tr>\n
Urinary Frequency<\/td>\n1<\/td>\n<\/tr>\n
Flank pain<\/td>\n1<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n

Identity and prevalence of bacterial pathogens in symptomatic and asymptomatic bacteriuria<\/strong><\/p>\n

The most common bacterial pathogen isolated from the samples of the 14 pregnant patients with bacteriuria was E. coli.<\/em> Figure 2, shows the prevalence of the bacterial pathogens detected in the 14 positive urine samples obtained from both the symptomatic and the asymptomatic pregnant women. E. coli<\/em> was identified in 5 (35.71%) patients, followed by S. agalactiae (Group B Streptococci), <\/em>in 3 patients (21.43%) and Enterococcus faecalis<\/em> in 2 patients (14.29%). K. pneumoniae, Acintobacter baumannii, Staphylococcus aureus<\/em>, and Enterobacter aerogenes<\/em> were each detected in one patient (7.14%). The most common bacteria identified in the urine samples obtained from the symptomatic and asymptomatic pregnant women are shown in [Figures 3 & 4].<\/p>\n\n\n\n
\"\"<\/td>\nFigure 1: The prevalence of symptomatic and asymptomatic bacteriuria among 230 urine samples.<\/strong><\/p>\n

Click here to View Figure<\/a><\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n\n\n\n
\"\"<\/td>\nFigure 2: The prevalence of bacterial pathogens isolated from 14 positive urine samples<\/strong><\/p>\n

Click here to View Figure<\/a><\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n\n\n\n
\"\"<\/td>\nFigure 3: The most common bacteria among symptomatic bacteriuria in pregnancy samples.<\/strong><\/p>\n

Click here to View Figure<\/a><\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n\n\n\n
\"\"<\/td>\nFigure 4: The most common bacteria among asymptomatic bacteriuria in pregnancy samples.<\/strong><\/p>\n

Click here to View Figure<\/a><\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n

Antibiotic susceptibility<\/strong><\/p>\n

The results of the antibiotic sensitivity tests for E. coli,<\/em> K. pneumoniae, A. baumannii<\/em>, and E. aerogenes <\/em>are shown in [Table 2]. These bacteria were all sensitive to meropenem, while E. coli<\/em>, K. pneumoniae<\/em>, and A. baumannii<\/em> were resistant to ampicillin [Table 2]. Table 3 presents the antibiotic sensitivity test results for Group B streptococci (S. agalactiae)<\/em>, which was fully sensitive to linezolid, vancomycin, and penicillin [Table 3]. Table 4 shows the S. aureus <\/em>antibiotic sensitivity test results, indicating complete sensitivity to ciprofloxacin, erythromycin, tetracycline, linezolid, and trimethoprim\/sulfamethoxazole. Table 5 demonstrates the antibiotic sensitivity of the two samples with E. faecalis<\/em>, which were completely sensitive to ampicillin, linezolid, and vancomycin and completely resistant to tetracycline and erythromycin.<\/p>\n

Table 2: Antibiotics sensitivity test results for Escherichia coli, Klebsiella pneumoniae, Acintobacter baumannii <\/em>and Enterobacter aerogenes<\/em>.<\/strong><\/p>\n\n\n\n\n\n\n\n
Bacterial<\/strong><\/p>\n

Strains<\/strong><\/td>\n

N (%)<\/strong><\/td>\nAMP<\/strong><\/td>\n<\/td>\n<\/td>\n<\/td>\n<\/td>\n<\/td>\n<\/td>\n<\/td>\n<\/tr>\n
E.coli<\/em><\/td>\n5 (35.71%)<\/td>\n0<\/td>\n75%<\/td>\n80%<\/td>\n60%<\/td>\n100%<\/td>\n80%<\/td>\n60%<\/td>\n75%<\/td>\n<\/tr>\n
K.pneumoniae<\/em><\/td>\n1(7.14%)<\/td>\n0<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n0<\/td>\n0<\/td>\n100%<\/td>\n<\/tr>\n
A.baumannii<\/em><\/td>\n1(7.14%)<\/td>\n0<\/td>\n100%<\/td>\n100%<\/td>\n0<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n<\/tr>\n
E.aerogenes<\/em><\/td>\n1(7.14%)<\/td>\n100%<\/td>\n\u00a0\u00a0\u00a0 0<\/td>\n100%<\/td>\n0<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n[0: Resistant, 100% : Sensitive]\n

AMX = Ampicillin; CIP = Ciprofloxacin; ERY = Erythromycin; LZD = Linezolid; TNC = Tetracycline; TEI = Teicoplanin; VAN = Vancomycin; CRO = Ceftriaxone; CXM = Cefuroxime; SXT = trimethoprim\/sulfamethoxazole; AMK = amikacin; IMP = Imipenem; MEM = Metropenem<\/p>\n

Table 3:<\/strong> Antibiotics sensitivity test results for Streptococcus agalactiae<\/em><\/strong><\/p>\n\n\n\n\n
Bacterial<\/strong><\/p>\n

Strains<\/strong><\/td>\n

N(%)<\/strong><\/td>\nCLI<\/strong><\/td>\nERY<\/strong><\/td>\nLZD<\/strong><\/td>\nPNC<\/strong><\/td>\nTNC<\/strong><\/td>\nVAN<\/strong><\/td>\n<\/tr>\n
S. agalactiae<\/em><\/td>\n3(21.43%)<\/td>\n33.3%<\/td>\n33.3%<\/td>\n100%<\/td>\n100%<\/td>\n0<\/td>\n100%<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n[0: Resistant, 100% : Sensitive]\n

AMX = Ampicillin; CIP = Ciprofloxacin; ERY = Erythromycin; LZD = Linezolid; TNC = Tetracycline; TEI = Teicoplanin; VAN = Vancomycin; CRO = Ceftriaxone; CXM = Cefuroxime; SXT = trimethoprim\/sulfamethoxazole; AMK = amikacin; IMP = Imipenem; MEM = Metropenem<\/p>\n

Table 4: <\/strong>Antibiotics sensitivity test results for Staphylococcus aureus<\/em><\/strong><\/p>\n\n\n\n\n
Bacterial<\/strong><\/p>\n

Strains<\/strong><\/td>\n

N(%)<\/strong><\/td>\nAMP<\/strong><\/td>\nPNC<\/strong><\/td>\nCIP<\/strong><\/td>\nERY<\/strong><\/td>\nTNC<\/strong><\/td>\nTMP\/SMX<\/strong><\/td>\nLZD<\/strong><\/td>\nIMP<\/strong><\/td>\n<\/tr>\n
S. aureus<\/em><\/td>\n1(7.14%)<\/td>\n0<\/td>\n0<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n100%<\/td>\n0<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n[0: Resistant, 100% : Sensitive]\n

AMX = Ampicillin; CIP = Ciprofloxacin; ERY = Erythromycin; LZD = Linezolid; TNC = Tetracycline; TEI = Teicoplanin; VAN = Vancomycin; CRO = Ceftriaxone; CXM = Cefuroxime; SXT = trimethoprim\/sulfamethoxazole; AMK = amikacin; IMP = Imipenem; MEM = Metropenem<\/p>\n

Table 5: Antibiotics sensitivity test results for Enterococcus faecalis<\/em><\/strong><\/p>\n\n\n\n\n
Bacterial<\/strong><\/p>\n

Strains<\/strong><\/td>\n

N (%)<\/strong><\/td>\nAMP<\/strong><\/td>\nCIP<\/strong><\/td>\nERY<\/strong><\/td>\nLZD<\/strong><\/td>\nTNC<\/strong><\/td>\nTEI<\/strong><\/td>\nVAN<\/strong><\/td>\n<\/tr>\n
E.faecalis<\/em><\/td>\n2(14.29%)<\/td>\n100%<\/td>\n50%<\/td>\n0<\/td>\n100%<\/td>\n\u00a0 0<\/td>\n100%<\/td>\n100%<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n[0: Resistant, 100% : Sensitive]\n

AMX = Ampicillin; CIP = Ciprofloxacin; ERY = Erythromycin; LZD = Linezolid; TNC = Tetracycline; TEI = Teicoplanin; VAN = Vancomycin; CRO = Ceftriaxone; CXM = Cefuroxime; SXT = trimethoprim\/sulfamethoxazole; AMK = amikacin; IMP = Imipenem; MEM = Metropenem.<\/p>\n

Discussion<\/strong><\/p>\n

In this study, among the 230 urine samples collected from pregnant Omani female patients admitted to Sultan Qaboos University Hospital and screened for bacteriuria, only 14 (6.08%) cases were positive for the presence of bacteriuria. Among the 14 positive samples, 6 (2.06%) of the symptomatic pregnant patients were positive for bacteriuria, while 8 (3.47%) of the asymptomatic pregnant patients were positive for bacteriuria. These findings are comparable to a study conducted in Saudi Arabia, where 419 (15.8%) out of 2642 cases were positive for the presence of bacteriuria15<\/sup>. Of the 419 positive subjects, 188 (7.1%) subjects were asymptomatic for bacteriuria, and 231 (8.7%) were symptomatic15<\/sup>.<\/p>\n

In the present study the most common symptoms seen in symptomatic patients were dysuria followed lower abdominal pain. These findings were in contrast to previously published study in United Arab Emirates were lower abdominal pain was the most common followed by dysuria11<\/sup>.<\/p>\n

In the existing study, E. coli<\/em> (35.71%) was the most frequent cause of bacteriuria in both the asymptomatic and symptomatic pregnant patients. This finding is consistent with studies carried out in Saudi Arabia and UAE respectively, where E. coli<\/em> was the most common contributing agent to bacteriuria11,15<\/sup>. The detection of E. coli<\/em> can be explained by the difficulty in maintaining hygiene during pregnancy9<\/sup>. In addition, in pregnancy, urine pH reaches a level appropriate for E. coli<\/em> growth9<\/sup>. Conversely, the results are inconsistent with a study conducted in Brunei, where the leading cause of bacteriuria in pregnancy was Klebsiella spp. <\/em>(2.94%), followed by E. coli<\/em>16<\/sup>. In our study, the most common bacterial pathogens present in the symptomatic bacteriuria patients after E. coli <\/em>(35.71%) were S. agalactiae<\/em>, K. pneumoniae<\/em>, and A. baumannii<\/em> (all 16.66%). The most common bacterial pathogens present in the asymptomatic bacteriuia patients after E. coli <\/em>(25.00%) were S. agalactiae <\/em>(25.00%),<\/em> E. faecalis <\/em>(25.00%), S. aureus <\/em>(12.50%), and E. aerogenes <\/em>(12.50%).<\/p>\n

In the present study the isolated E. coli, S. aureus, K. pneumoniae<\/em>, and A. baumannii <\/em>were all completely resistant to ampicillin. This finding is coherent with a study performed in India, where most of their isolates were highly resistant to ampicillin17<\/sup>. This suggests that ampicillin should not be used as a first line of defense against UTIs in pregnancy in Oman. In the present study, Imipenem and meropenem were sensitive for most of the clinical isolates, so they might provide effective alternatives for treatment. In the present study Group B streptococci (S. agalactiae), <\/em>was fully sensitive to linezolid, vancomycin, and penicillin. This finding is constant with previously published studies 11,18,19,20 <\/sup>. Antibiotic over Prescribing for UTI results in the emerging of antibiotic resistant bacterial pathogens.21<\/sup> \u00a0Asymptomatic bacteriuria \u00a0caused by antibiotic resistant organisms is alarming and screening for asymptomatic bacteriuria \u00a0during pregnancy is of great importance to avoid \u00a0adverse maternal and fetal outcomes22<\/sup>.<\/p>\n

Conclusion<\/strong><\/p>\n

Our data suggest asymptomatic bacteriuria is more predominant than symptomatic bacteriuria in pregnant patients in Muscat, Oman.\u00a0E. coli,<\/em>\u00a0S. agalactiae<\/em>,\u00a0<\/em>and\u00a0E. faecalis\u00a0<\/em>were the\u00a0<\/em>most common contributors to bacteriuria in pregnant women in Muscat, Oman.\u00a0The outcomes of this investigation provide valuable understanding into the dynamics between symptomatic and asymptomatic bacteriuria in pregnancy. In addition, the present study shows the importance of frequent urine testing during pregnancy for early detection and treatment of UTI. Also, the present study shows the need for implementing new guidelines to prevent UTIs during pregnancy, with special reference to educating and encouraging pregnant women on the importance of personal hygiene in preventing UTIs during pregnancy and ultimately, preventing any adverse effect on the developing fetus.<\/p>\n

Acknowledgment<\/strong><\/p>\n

The authors would like to thank the staff of the Microbiology Department, SQUH for their support.<\/p>\n

Funding Sources<\/strong><\/p>\n

The author(s) received no financial support for the research, authorship, and\/or publication of this article.<\/p>\n

Conflict of Interest<\/strong><\/p>\n

The author(s) do not have any conflict of interest.<\/p>\n

Data Availability Statement<\/strong><\/p>\n

This statement does not apply to this article.<\/p>\n

Ethics statement<\/strong><\/p>\n

Informed Consent Statement<\/strong><\/p>\n

This study did not involve human participants, and therefore, informed consent was not required.<\/p>\n

Clinical Trial Registration<\/strong><\/p>\n

This research does not involve any clinical trials<\/p>\n

Author contributions<\/strong>\u00a0<\/strong><\/p>\n

Thikra Hilal Hamed Al dhuhli; Methodology, Analysis, Review;<\/p>\n

Ruwaida Nasser Abdulla AL-Lamki: Supervised-Methodology, Review;<\/p>\n

Mohamed Mabruk: Conceptualization, Design Supervision , Review-Editing.<\/p>\n

References<\/strong><\/p>\n

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    \n    CrossRef<\/a><\/li>\n<\/ol>\n","protected":false},"excerpt":{"rendered":"

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