1Department of Microbiology, Government Medical College, Nirmal, Telangana state, India. 2*Department of Obstetrics and Gynecology, GITAM Institute of Medical Sciences and Research, GITAM Deemed to be University, Visakhapatnam-530045, AP, India. 3Department of Microbiology, Kamineni Institute of Medical Sciences, Sreepuram, Narketpally, Dist. Nalgonda-508254, Telangana State, India
*Corresponding author: Sailaja Pidugu; Email: spidugu@gitam.edu
Received: 08 Jun 2023, Revised and Accepted: 26 Jul 2023
ABSTRACT
Objective: The study's main objective was to isolate and characterize the bacteria that cause asymptomatic UTIs in pregnant and nonpregnant women attending a tertiary care teaching hospital.
Methods: It is a comparative cross-sectional study that was carried out from January 2021 to January 2022. A structured questionnaire was used to gather clinical information (such as parity and the history of UTIs) and sociodemographic data (such as age, marital status, educational level, place of residence, occupation, and income) from eligible participants. A total of 200 urine samples were collected (100 pregnant and 100 nonpregnant) and analyzed using standard microbiological methods for the detection of isolates and their antibiotic sensitivity using the Kirby-Bauer method.
Results: Most patients who participated were aged 21-30 y (50.5%). E. coli incidence was more in UTI of pregnant women (42.3%) and nonpregnant women (34.2%). Among the 33 isolates of E. coli from pregnant and nonpregnant women, most strains were resistant to amoxicillin+clavulanic acid (57.6%) and cotrimoxazole (54.5%). They were sensitive to other tested antibiotics like norfloxacin, nitrofurantoin, gentamicin, and cefuroxime.
Conclusion: Pregnant women were more likely to get UTIs than nonpregnant women, and the frequency of UTIs among women was more significant. It is recommended that women, especially pregnant women, undergo routine UTI screenings to identify infected cases and receive prompt treatment to prevent urinary problems.
Keywords: Urinary tract infection, Pregnant, Non-pregnant, Prevalence, Antibiotics
© 2023 The Authors. Published by Innovare Academic Sciences Pvt Ltd. This is an open access article under the CC BY license (https://creativecommons.org/licenses/by/4.0/)
DOI: https://dx.doi.org/10.22159/ijcpr.2023v15i5.3054. Journal homepage: https://innovareacademics.in/journals/index.php/ijcpr
Any urinary system infection is referred to as a urinary tract infection. It involves bladder, ureters, kidneys, and urethra. The lower urinary system, including the bladder and urethra, is where most infections occur [1]. When microorganisms invade the urinary tract, they result in a UTI. While fungi can sporadically infect the urinary system, bacteria are the most frequent cause of UTIs. The most common cause of UTIs is when bacteria enter the urinary tract via the urethra and start to colonize the bladder. The urinary system's architecture keeps bacteria out. But occasionally, the defenses give way, allowing the bacteria to settle in and spread throughout the urinary system, leading to a full-blown infection [1]. The likelihood of developing a urinary tract infection may be boosted by several illnesses, including diabetes, hormonal changes, kidney stones, and spinal cord injuries [2]. Compared to nonpregnant women, pregnant women are more prone to UTIs with uropathogenic bacteria, which can adversely affect the mother and fetus [3]. In nonpregnant women, the uterus is located directly behind and partially above the bladder; however, in pregnant women, the larger uterus affects all the tissues of the urinary system to varying degrees. Growing uteruses gain weight, which prevents urine from draining from the bladder and causes urinary stasis, which in turn causes urinary tract infections [4, 5]. Sexual activity also makes it easier for bacteria to enter the bladder. Asymptomatic bacteriuria (AB) is the presence of bacteria that are actively proliferating in the urinary tract, excluding the distal urethra, in a patient who has no overt symptoms of the urinary system. To diagnose asymptomatic bacteriuria, finding 100,000 or more colony-forming units of a single bacteria per milliliter in two consecutive clean catch urine specimens or a single catheter specimen in the absence of urinary symptoms and signs is necessary. Asymptomatic bacteriuria, which affects 2% to 10% of all pregnancies, is commonly characterized as true bacteriuria without characteristic acute urinary tract infection symptoms [6]. Asymptomatic bacteriuria has been linked to preterm birth and low birth weight. Pregnant and nonpregnant women have similar infection prevalence levels, most strongly correlated with socioeconomic status [7]. A history of recurrent urinary tract infections, urinary tract blockages brought on by kidney stones, diabetes, and anatomical abnormalities of the urinary tract are all recognized as additional risk factors for bacteriuria. At least 80% of isolates with asymptomatic bacteriuria are E. coli, making it the most prevalent pathogen. For around 80% of community-acquired UTIs, Escherichia coli and Staphylococcus saprophyticus are responsible [8]. Other Gram-negative pathogens, including Pseudomonas spp, Enterobacter spp, Citrobacter spp, and Klebsiella spp, are also incriminated in urinary tract infection [6]. Gram-positive bacteria, including Enterococcus spp and Staphylococcus spp [9], can cause nosocomial UTIs due to selective pressure from the antimicrobial agents used in hospitalized patients. Pregnant women should be screened for UTIs due to the relatively high prevalence of these infections, their severe effects on women, and the probable result of the pregnancy [10]. Pregnant women with bacteria in their urine, even if they don't have symptoms, should be treated to lower their risk since they have a 25 to 30% chance of developing acute pyelonephritis. Usually, a brief course of oral antibiotics is adequate. Pyelonephritis was less common in women with asymptomatic bacteriuria who received antibiotic therapy. Typical antibiotics used for treatment include sulfisoxazole, ampicillin, amoxicillin, cephalexin, nitrofurantoin, and trimethoprim/sulfamethoxazole. This study aimed to isolate and identify the bacterial agents causing asymptomatic UTIs in pregnant and nonpregnant women attending a tertiary care teaching hospital.
It is a comparative cross-sectional study conducted over one year in a Tertiary care teaching hospital from Jan 2021 to Jan 2022 involving 100 pregnant and 100 nonpregnant women. Samples were collected from all pregnant and nonpregnant women who gave their consent without obvious clinical signs of UTI and/or kidney malfunction. The study excluded women who had received any form of antibiotic treatment 15 d before and during the study period. A structured questionnaire was used to gather clinical information (such as parity and the history of UTIs) and sociodemographic data (such as age, marital status, educational level, place of residence, occupation, and income) from eligible participants. Clean-catch midstream urine was collected from each patient into a sterile universal container. Blood agar, Mac Conkey agar, and cysteine lactose electrolyte deficient agar (CLED) were used to culture the samples. For 24 h, plates were incubated aerobically at 37 °C. In order to calculate the number of bacteria per milliliter in the original urine specimen and check for significant bacteriuria, which denotes the existence of UTIs, the colonies were counted, multiplied by 1000, and analyzed. Pure isolates of bacteria 105cfu/ml or more were considered significant for infection. The Gram staining procedure was used to identify the isolated organisms from culture plates. The biochemical tests include carbohydrate fermentation tests with glucose, lactose, sucrose, xylose, mannitol, and maltose, etc., tests for the detection of indole, coagulase, urease, oxidase, and catalase production, methyl red test, Voges-Proskauer test, citrate utilization, nitrate reduction test, triple sugar iron agar test, etc. Antibiotic susceptibility patterns of isolates used in the empiric treatment of UTI were studied. Antimicrobial susceptibility tests were performed on bacterial isolates from midstream urine using antimicrobial discs, according to the Clinical and Laboratory Standards Institute (CLSI) on Muller Hinton agar. The antimicrobial disks used to test against Gram-negative bacteria include amoxicillin+clavulanic acid, norfloxacin, nitrofurantoin, gentamicin, cotrimoxazole, and cefuroxime. Disks for Gram-positive bacteria contain the following antimicrobials: penicillin G, cefoxitin, gentamycin, amoxicillin+clavulanic acid, nitrofurantoin, and Cotrimoxazole. After incubation at 37 °C for 18 to 24 h, the zone diameter of inhibition was measured to the nearest milliliter and interpreted as sensitive (S), intermediate (I), or resistance (R) per the Clinical and Laboratory Standards Institute (CLSI) guideline.
200 women (100 pregnant and 100 nonpregnant) participated in this study, with a response rate of 100%. Table 1 depicts the sociodemographic variables of the study. Most of the patients who participated were aged 21-30 (50.5%). Most of them completed school and high school studies (37%). Most of the patients reported were belonged to low-middle income (61.5%). Rural patients (67.5%) were reported more than the urban population. Most of the patients reported were daily laborers (45.5%). Table 2 shows the prevalence of microorganisms isolated from the urine samples of both pregnant and nonpregnant women. E. coli incidence was more in UTI of pregnant women (42.3%) and nonpregnant women (34.2%). This was followed by S. aureus in both pregnant (26.7%) and nonpregnant women (22.1%). Table 3 depicts the antimicrobial susceptibility pattern of Gram-negative bacteria isolated from pregnant and nonpregnant women. Among the 33 isolates of E. coli from pregnant and nonpregnant women, most strains were resistant to amoxicillin+clavulanic acid (57.6%) and cotrimoxazole (54.5%). They were sensitive to other tested antibiotics like norfloxacin, nitrofurantoin, gentamicin, and cefuroxime. Similarly, Klebsiella strains and Proteus species were also resistant to amoxicillin+clavulanic acid and co-trimoxazole. Pseudomonas aeruginosa showed equal susceptibility to nitrofurantoin and cefuroxime (42.8%) and resistance to amoxicillin+clavulanic acid and cotrimoxazole. Table 4 shows the antimicrobial susceptibility pattern of Gram-positive bacteria isolated from pregnant and nonpregnant women. Among the Gram-positive microorganisms isolated, S. aureus and CONS showed maximum susceptibility to nitrofurantoin, gentamicin, cotrimoxazole, and cefoxitin and resistant to amoxicillin+clavulanic acid (52.3%), (62.5%) and penicillin-G (85.8%), (62.5%). In contrast, Enterococci strains showed equal susceptibility to amoxicillin+clavulanic acid (50%), more resistance to penicillin-G and 100% sensitivity to nitrofurantoin, gentamicin, cotrimaxazole, and cefoxitin.
Table 1: Sociodemographic variables of the study
Variables | Pregnant number | Nonpregnant number | Total number |
Age (years) | |||
>40 | 2 | 8 | 10 |
31-40 | 35 | 39 | 74 |
21-30 | 59 | 42 | 101 |
<21 | 4 | 11 | 15 |
Educational status | |||
No education | 10 | 19 | 29 |
Graduation | 14 | 12 | 26 |
High school | 37 | 34 | 71 |
School | 39 | 35 | 74 |
Economic status | |||
Lower middle-income | 62 | 61 | 123 |
Upper middle-income | 38 | 39 | 77 |
Residence | |||
Urban | 29 | 36 | 65 |
Rural | 71 | 64 | 135 |
Occupation | |||
House-wife | 25 | 15 | 40 |
Employee | 35 | 34 | 69 |
Daily labor | 40 | 51 | 91 |
Table 2: Microorganisms isolated
Microorganism | Pregnant n (%) | Nonpregnant n (%) | Total |
E. coli | 19 (42.3%) | 14 (34.2%) | 33 |
S. aureus | 12 (26.7%) | 9 (22.1%) | 21 |
Klebsiella species | 1 (2.2%) | 2 (4.9%) | 3 |
Pseudomonas aeruginosa | 3 (6.6%) | 4 (9.7%) | 7 |
Proteus species | 5 (11.2%) | 5 (12.1%) | 10 |
CONS | 4 (8.8%) | 4 (9.7%) | 8 |
Enterococci | 1 (2.2%) | 3 (7.3%) | 4 |
Total | 45 (100%) | 41 (100%) | 86 |
Table 3: Antimicrobial susceptibility pattern of gram-negative bacteria isolated from pregnant and nonpregnant women
Bacterial isolates | Number | Pattern | Amoxicillin+clavulanic acid | Norfloxacin | Nitrofurantoin | Gentamicin | Cotrimoxazole | Cefuroxime |
E. coli | 33 | S | 12 (36.3%) | 19 (57.6%) | 20(60.6%) | 18(54.5%) | 14 (42.4%) | 21(63.6%) |
I | 2 (6.06%) | 0 | 2 (6.06%) | 2(6.06%) | 1(3.03%) | 1(3.03%) | ||
R | 19 (57.6%) | 14 (42.4%) | 11(33.3% | 13(39.4%) | 18(54.5%) | 11(33.3%) | ||
Klebsiella species | 3 | S | 1 (33.3%) | 2(66.6%) | 2(66.6%) | 2(66.6%) | 1(33.3%) | 3(100%) |
I | 0 | 0 | 0 | 0 | 0 | 0 | ||
R | 2 (66.6%) | 1(33.3%) | 1(33.3%) | 1(33.3%) | 2(66.6%) | 0 | ||
Pseudomonas aeruginosa | 7 | S | 2 (28.6%) | 5(71.4%) | 3(42.8%) | 4(57.2%) | 3(42.8%) | 3(42.8%) |
I | 1 (14.2%) | 1(14.2%) | 1(14.2%) | 0 | 0 | 1(14.2%) | ||
R | 4 (57.2%) | 1(14.2%) | 3(42.8%) | 3(42.8%) | 4(57.2%) | 3(42.8%) | ||
Proteus species | 10 | S | 4 (40%) | 7 (70%) | 7 (70%) | 5(50%) | 4(40%) | 7(70%) |
I | 0 | 0 | 1 (10%) | 2(20%) | 1(10%) | 0 | ||
R | 6 (60%) | 3 (30%) | 2(20%) | 3(30%) | 5(50%) | 3(30%) |
Table 4: Antimicrobial susceptibility pattern of gram-positive bacteria isolated from pregnant and nonpregnant women
Bacterial isolates | Number | Pattern | Amoxicillin+clavulanic acid | Penicillin-G | Nitrofurantoin | Gentamicin | Cotrimoxazole | Cefoxitin |
S. aureus | 21 | S | 9(42.8%) | 3 (14.2%) | 18(85.8%) | 17 (80.9%) | 15 (71.4%) | 17(80.9%) |
I | 1 (4.76%) | 0 | 0 | 0 | 1 (4.76%) | 0 | ||
R | 11(52.3%) | 18(85.8%) | 3(14.2%) | 4(9.1%) | 5 (23.8%) | 4(9.1%) | ||
CONS | 8 | S | 3(37.5%) | 3(37.5%) | 7(87.5%) | 6(75%) | 7(87.5%) | 7(87.5%) |
I | 0 | 0 | 0 | 1(12.5%) | 0 | 0 | ||
R | 5(62.5%) | 5(62.5%) | 1(12.5%) | 1(12.5%) | 1(12.5%) | 1(12.5%) | ||
Enterococci | 4 | S | 2 (50%) | 1 (25%) | 4 (100%) | 4(100%) | 4(100%) | 4(100%) |
I | 0 | 0 | 0 | 0 | 0 | 0 | ||
R | 2 (50%) | 3 (75%) | 0 | 0 | 0 | 0 |
In the present study, the prevalence of UTIs among pregnant and nonpregnant women was 45% and 41%. The fact that the prevalence of UTIs was lower in nonpregnant women than in pregnant women indicates that this condition is more prevalent during pregnancy and highlights the need for adequate care. Similar findings were reported by Bachchan and Sen Ramanujan (2016) [12] and Degu Abate et al. (2020) [13]. The environment, low socioeconomic position, poor personal cleanliness, hormonal and physiological changes, and urethral dilatation may cause an increased risk of UTIs during pregnancy [14, 15]. In the current investigation, Gram-negative bacteria (61.6%) outnumbered Gram-positive bacteria (38.4%) in frequency. Similar reports were shown by Lone et al. [16] and Degu Abate et al. [13]. The predominance of Gram-negative bacteria may be caused by adhesions, which aid in the attachment of bacteria to uroepithelial cells and prevent them from flushing in the urine, allowing for bacterial proliferation and tissue penetration that results in pyelonephritis in pregnancy [14]. The most predominant causative agent of UTIs in this study was E. coli (38.3%), followed by S. aureus (24.4%), which was similar in etiology but different in magnitude from previous findings of Degu Abate et al. [13]. The increased frequency of E. coli isolations could be explained by various virulence factors, including P-fimbriae and S-fimbriae adhesions for invasion and colonization of the urinary epithelium and persistence in the vagina [17]. E. coli was highly sensitive to cefuroxime in the present study and can be recommended for treating UTI.
Similarly, Degu Abate et al. reported the same results, and Niranjan and Malini (2014) [17] showed contradictory results compared to the current study and showed higher resistance to cefuroxime by the E. coli strains. Degu Abati showed S. aureus high sensitivity to the antibiotics like cefoxitin (85.7%), ciprofloxacin (85.7), and gentamicin (71.4%) which was in accordance with the current study 80.9% sensitivity to cefoxitin and gentamicin. The frequent use of broad-spectrum antibiotics in human and animal feeds, the inappropriate and incorrect administration of antibiotics during empiric therapies, and a lack of effective infection control measures may all contribute to the development of bacterial resistance. These factors can result in the spread of resistant organisms in both the hospital and the community.
Pregnant women were more likely to get UTIs than nonpregnant women, and the frequency of UTIs among women was more significant. E. coli and S. aureus were the two most typical bacteria responsible for UTIs. It is advised that women, especially pregnant women, undergo routine UTI screenings to identify infected cases and receive prompt treatment to prevent urinary problems. The management of UTIs requires the development of local guidelines that consider local factors, such as the susceptibility patterns of the bacteria that cause UTIs in the local population and the necessity to monitor antimicrobial usage to encourage responsible drug use.
Nil
All the authors have contributed equally.
All authors declared No conflict of interest
Tan CW, Chlebicki MP. Urinary tract infections in adults. Singapore Med J. 2016 Sep;57(9):485-90. doi: 10.11622/smedj.2016153, PMID 27662890, PMCID PMC5027397.
Storme O, Tiran Saucedo J, Garcia Mora A, Dehesa Davila M, Naber KG. Risk factors and predisposing conditions for urinary tract infection. Ther Adv Urol. 2019 May 2;11:1756287218814382. doi: 10.1177/1756287218814382, PMID 31105772, PMCID PMC6502981.
Habak PJ, Griggs, Jr RP. Urinary tract infection in pregnancy. Stat Pearls. Available from: https://www.ncbi.nlm.nih.gov/books/NBK537047/. [Last accessed on 05 Jul 2022]
Demilie T, Beyene G, Melaku S, Tsegaye W. Urinary bacterial profile and antibiotic susceptibility pattern among pregnant women in northwest Ethiopia. J Health Sci. 2012;22(2):121-8.
Jalali M, Shamsi M, Roozbehani N, Kabir K. Prevalence of urinary tract infection and some factors affected in pregnant women in Iran Karaj city. Middle East J Sci Res. 2014;20(7):781-5.
Givler DN, Givler A. Asymptomatic bacteriuria. Stat Pearls. Available from: https://www.ncbi.nlm.nih.gov/ books/NBK441848/. [Last accessed on 19 Jan 2023]
Abdullah AA, Al-Moslih MI. Prevalence of asymptomatic bacteriuria in pregnant women in Sharjah, United Arab Emirates. East Mediterr Health J. 2005;11(5-6):1045-52. PMID 16761676.
Cheesbrough M. District laboratory practice in tropical countries. 2nd ed. Cambridge, UK: Cambridge University Press; 2006.
Moyo SJ, Aboud S, Kasubi M, Maselle SY. Bacterial isolates and drug susceptibility patterns of urinary tract infection among pregnant women at Muhimbili National Hospital in Tanzania. Tanzan J Health Res. 2010;12(4):236-40. doi: 10.4314/thrb.v12i4.52997, PMID 24409630.
Habte TM, Dube S, Ismail N, Hoosen AA. Hospital and community isolates of uropathogens at a tertiary hospital in South Africa. S Afr Med J. 2009;99(8):584-7. PMID 19908617.
Okorondu SI, Akujobi CO, Nnadi CB. Prevalence and antibiotic sensitivity profile of urinary tract infection pathogens among pregnant and nonpregnant women in Owerri, Imo State, Nigeria. Int J Biol Chem Sci. 2013;7(4):1668-77.
Bachchan KT, Sen Ramanujan S. Prevalence of multidrug resistant asymptomatic bacteriuria from pregnant and nonpregnant women in the Erode district. Int J Biochem Biotechnol. 2016;5(3):665-9.
Abate D, Marami D, Letta S. Prevalence, antimicrobial susceptibility pattern, and associated factors of urinary tract infections among pregnant and nonpregnant women at public health facilities, Harar, Eastern Ethiopia: A comparative cross-sectional study. Can J Infect Dis Med Microbiol. 2020 Aug 7;2020:9356865. doi: 10.1155/2020/9356865, PMID 32831981, PMCID PMC7428927.
Hamdan HZ, Ziad AHM, Ali SK, Adam I. Epidemiology of urinary tract infections and antibiotics sensitivity among pregnant women at Khartoum North Hospital. Ann Clin Microbiol Antimicrob. 2011;10(1):2. doi: 10.1186/1476-0711-10-2, PMID 21244660.
Glover M, Moreira CG, Sperandio V, Zimmern P. Recurrent urinary tract infections in healthy and nonpregnant women. Urol Sci. 2014;25(1):1-8. doi: 10.1016/j.urols.2013.11.007, PMID 27499825.
Lone TA, Lone RA. The pervasiveness of multi-drug resistance asymptomatic bacteriuria from pregnant and nonpregnant women in Erode district. Int J Biotechnol Res. 2014;2:65-9.
Niranjan V, Malini A. Antimicrobial resistance pattern in Escherichia coli causing urinary tract infection among inpatients. Indian J Med Res. 2014 Jun;139(6):945-8. PMID 25109731, PMCID PMC4165009.