|Year : 2014 | Volume
| Issue : 2 | Page : 79-85
Asymptomatic bacteriuria among antenatal care women in a tertiary hospital in Benin, Nigeria
Chiedozie Kingsley Ojide1, Victoria Ade Wagbatsoma2, Eziyi Iche Kalu3, Victor Ugochukwu Nwadike4
1 Department of Medical Microbiology, Ebonyi State University, Abakaliki, Nigeria
2 Department of Community Health, University of Benin, Benin, Nigeria
3 Department of Medical Microbiology, Federal Medical Centre, Umuahia, Abia, Nigeria
4 Department of Medical Microbiology, Federal Medical Centre, Abeokuta, Nigeria
|Date of Web Publication||17-Nov-2014|
Chiedozie Kingsley Ojide
Department of Medical Microbiology, Ebonyi State University, Abakaliki
Source of Support: None, Conflict of Interest: None
Introduction: Asymptomatic bacteriuria (ASB) in pregnancy is associated with acute pyelonephritis, premature deliveries, low birth weight, still birth, pre-eclampsia, hypertension, anaemia, and postpartum endometritis. Early detection and treatment of this condition reduces the incidence of these complications. Objective: To determine the prevalence, associated bacteria agents and susceptibility, and risk factors of ASB among pregnant women at the University of Benin Teaching Hospital. Materials and Methods: Two hundred and sixty five respondents were selected using systematic sampling method, between November 2011 and October 2012. These subjects provided clean catch midstream urine samples that were cultured, significant bacteriuric isolates were identified through biochemical tests and sensitivity against regular antimicrobial agents carried out. Data were analysed using SPSS version 16. Results: Of the 265 urine samples cultured, 28 (10.6%) had asymptomatic bacteriuria. Isolates were predominantly Escherichia coli (46.4%), Proteus species (14.3%), Enterococcus faecalis (10.7%), and Staphylococcus aureus (10.7%). These organisms were generally susceptible to tested antibiotics at different degrees. Risk factors included maternal age, parity, and level of education of the woman, as well as spouse's level of education. Occupation of the woman and that of the spouse, gestational age, religion, and ethnicity were not risk factors. Conclusion: Prevalence of ASB among pregnant women in University of Benin Teaching Hospital was 10.6%. Age, parity, and levels of education of both the women and the spouses were risk factors. Periodic surveillance of prevalence, etiology and antibiotics susceptibility is recommended.
Keywords: Asymptomatic bacteriuria, antenatal women, benin
|How to cite this article:|
Ojide CK, Wagbatsoma VA, Kalu EI, Nwadike VU. Asymptomatic bacteriuria among antenatal care women in a tertiary hospital in Benin, Nigeria
. Niger J Exp Clin Biosci 2014;2:79-85
|How to cite this URL:|
Ojide CK, Wagbatsoma VA, Kalu EI, Nwadike VU. Asymptomatic bacteriuria among antenatal care women in a tertiary hospital in Benin, Nigeria
. Niger J Exp Clin Biosci [serial online] 2014 [cited 2019 Jul 18];2:79-85. Available from: http://www.njecbonline.org/text.asp?2014/2/2/79/144841
| Background|| |
Asymptomatic bacteriuria (ASB) refers to the presence of a positive urine culture in the absence of specific symptoms of acute urinary tract infection (UTI). , This condition occurs more often in women due to the short nature of their urethra which is colonized by normal flora that are easily pushed into the bladder during sexual activity.  Although ASB is not more common in the pregnant women than in nonpregnant women,  it is associated in the former with complications, both for the mother and the fetus. The complications include; acute pyelonephritis, premature deliveries, low birth weight, still birth, pre-eclampsia, hypertension, anemia, and postpartum endometritis. , Studies have shown that treatment of ASB in pregnancy reduces the incidence of these complications. ,
Globally, prevalence of ASB in pregnancy varies from 2-7%.  In Nigeria prevalence is a bit higher, ranging from 15-21%. ,, However very unusual high rates of 86.6% was reported a decade ago in Benin city  and 78.7% reported in Abakiliki.  Eschericia coli is the most commonly isolated organism, accounting for 30-50% in most studies.  Other isolates include members of enterobacteriaceae family, Pseudomonas aeruginosa, Enterococcus species, group B streptococcus, and Candida albicans.,, Occasionally, rare organisms like Staphylococcus aureus and Staphylococcus saprophyticus are also incriminated. 
In Nigeria and many other developing countries, routine urine culture for detecting ASB is not carried out for antenatal women probably due to cost and delay in obtaining culture result.  Strip urinalysis is often preferred by most clinicians to culture in accessing urine in pregnant women because of speed and simplicity. Though this method can detect presence of protein, nitrite, and leucocytes esterase enzyme which may suggest bacteriuria, its sensitivity is low.  Moreover, unlike culture, strip urinalysis fails to identify the etiologic agents and the antibiotic sensitivity pattern. This practice will not allow for proper management of ASB in antenatal woman, thus increasing her risk of coming down with complications. Due to the above reasons, the burden of ASB in pregnant women and its associated complications in this environment may still be highly underestimated. It is against this background that this study aimed at investigating ASB amongst pregnant women attending antenatal care at University of Benin Teaching Hospital is made.
| Materials and methods|| |
The study design was descriptive cross-sectional and the study was carried out at the University of Benin Teaching Hospital, Benin, Edo state. This is a 650 bed tertiary hospital located along the old Lagos-Benin express way, serving as a referral centre to Edo and other neighbouring states in the south-south region of Nigeria. This study spanned through November 2011 to October 2012, and was backed by ethical approval obtained from the institution's ethics and research committee.
Study population consisted of pregnant women attending antenatal care in University of Benin Teaching Hospital, Benin, city, Edo state. Inclusion criteria were pregnancy, registration for antenatal care at University of Benin Teaching hospital and participants consent. Pregnant women who were having symptoms suggestive of urinary tract infection (dysuria, frequency, and urgency) and those who had received antibiotics within the previous 7 days were excluded.
The minimum sample size was calculated to 265. This was calculated using the formula below:
N = The desired population size.
The standard normal deviate, usually set at 1.96, which corresponds to the 95% confidence level.
P = The proportion in the targeted population that have a particular characteristic = 19.5% (0.195) being the prevalence of ASB among pregnant women in Oshogbo, south-west, Nigeria. 
q = 1.0 - p
d = degree of accuracy desired, usually set at 0.05
Therefore the minimum sample size will be 241 + 24 = 265
Candidates were chosen using systematic sampling method. Previous antenatal care records showed that an average of 428 pregnant women was seen weekly. This figure was divided by the minimum sample size to get a sapling fraction of 1.6, approximated to 2. Therefore every other woman was selected. The first person was selected using simple random method.
The tool for data collection was an interviewer administered questionnaire administered by trained assistants (House Officers). Information sought in the questionnaire included; age, marital status, highest educational attainment, husband's highest educational attainment, gestational age, number of children, history suggestive of urinary tract infection (dysuria, frequency, fever, suprapubic and loin pain), and history of antibiotics use.
After obtaining verbal consent and administering the questionnaire, each participant was instructed on how to collect clean catch mid-stream urine and given a pre-labelled sterile universal bottle, containing 0.5 g of boric acid crystals to obtain her urine specimen. The urine specimens were taken to the medical microbiology laboratory department by the trained assistants for processing. Each specimen was processed within 2 hours of arriving the laboratory following standard methods. Quantitative culture method using a calibrated wire loop (0.02 ml) was done on Cystine Lactose Electrolyte deficient (CLED) culture media and incubated aerobically at 37C for 18-24 hours. With the help of a magnifying glass colonies were counted for each plate with growth and number of colonies per ml of urine determined by dividing the number of colonies counted by the volume of urine delivered by the calibrated wire loop (0.02 ml). Significant bacteriuria was set at10 5 CFU/ml of urine.
Isolates were identified using standard biochemical tests. The antibiotics susceptibility patterns of the isolates were determined according to modified Kirby Bauer [Clinical and Laboratory Standard Institute (CLSI)] disc diffusion technique.
Data collected and the results from the laboratory analysis of specimens were subjected to statistical computations by a computer using the SPSS software, version 16. Results were presented as mean, percentages and frequency tables. Cross-tabulations were used to examine the relationship between variables. Chi square or Fisher's exact tests were used to test for associations. Significant association was presumed if P < 0.05.
| Results|| |
Of the 265 pregnant women that took part in the study 137 (51.7%) were between 21-30 years of age, only 24 (9.0%) fell above 40 years. Their mean age was 29.7 6.5, with a range of 15-48 years. Majority of the women (95.8%) were of the Christian faith, while only 4.2% were Muslims. Furthermore, 176 (66.4%) of the pregnant women were from the different ethnic groups in Edo state, while the remaining 89 (33.6%) were from ethnic groups outside Edo state. The study population were relatively educated as 42.3% had tertiary education and another 50.9% completing secondary education. Spouses seem more educated as 163 (61.5%) had tertiary education [Table 1]. A hundred and 10 (38.1%) of participants were traders, 53 (20.0%) professionals, and 45 (17.0%) civil servants.
|Table 1: General Characteristics of all participants (UBTH Antenatal women, November 2011 and October 2012)|
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About half of the women studied (50.9%) were in their second trimester, 36.2% were in their third trimester, while only 12.8% were in their first trimester, as shown in [Table 2] One hundred and twenty one (45.6%) of the women studied were carrying their first pregnancy (nullipara) while only 12 (4.5%) had delivered more than four times before the index pregnancy (grandmultipara), as shown in [Table 2]. Those who had delivered once (primipara) and two to four times (multipara) before the index pregnancy respectively make up a quarter of the study population.
|Table 2: Obstetrics Characteristics of all participants (UBTH Antenatal women, November 2011 and October 2012)|
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Out of 265 antenatal women studied, only 28 had significant bacteriuria. Thus the prevalence of ASB among the studied antenatal women was 10.6%. Escherichia coli was responsible for majority (46.4%) of identified cases, followed by Proteus species (14.3%), Enterococcus faecalis (10.7%), and Staphyloccus aureus (10.7%). The rest were Group B streptococcus (7.1%), Staphylococcs saprophyticus (7.1%) and Candida albicans (3.6%) [Table 3].
|Table 3: Isolated Organisms associated with Asymptomatic bacteriuria (n = 28)|
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The antibiotics susceptibility patterns of the causative organisms are illustrated in [Table 4]. Imepenem, gentamicin, cotrimoxazole and nitrofurantoin had excellent effectiveness against isolates of asymptomatic baceriuria, as their sensitivity to isolates were 100.0%, 83.5%, 81.0%, and 79.5% respectively. Amoxicillin/clavulanate (72.6%), ampicillin (67.5%), ciprofloxacin (62.9%), and ceftazidime (62.8%) were comparably not as effective. Group B streptococcus was the most sensitive isolate as it showed 100% sensitivity to all tested antibiotics, while Proteus species were the least sensitive isolates (53.1%). Escherichia coli, the most prevalent organism, were more sensitivite to imipenem (100%), gentamicin (84.6%), ceftazidime (76.9%) and nitrofurantoin (76.9%); than cotrimoxazole (69.2%), amoxicillin/clavulanate (69.2%), and ampicillin (38.4%).
[Table 5] showed that prevalence of ASB increased with age among the study population. This relationship though is not statistically significant (P = 0.136). All the 28 cases of ASB were among women of the Christian faith while none was detected among women of Islamic faith. This association was similarly not found to be significant (P = 0.244). There is also non-significant higher prevalence among antenatal women who are Edo indigene compared to their counterpart who are non-Edos (13.1% versus 5.6%), (χ² = 3.472, df = 1, P = 0.062).
|Table 5: Prevalence of asymptomatic bacteriuria by age, religion, ethnicity, parity, trimester and levels|
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A steady increase in prevalence with parity was observed, from 7.4% in nulliparous to 41.7% in grandmultiparous women, and the association was found to be statistically significant (P = 0.005). There was however no relationship between gestational age and prevalence. An inverse relationship was observed between prevalence of ASB and level of education, as [Table 5] shows a steady decline in prevalence from 50.0% among women with completed primary education to 8.0% among women with tertiary level of education. This relationship was however not statistically significant (P = 0.124).
Similarly, prevalence of ASB was observed to decrease with increasing level of education of the spouses, from 14.7% among spouses with completed secondary education to 9.2 among spouses with tertiary level of education as indicated in [Table 5]. Again this observation was not statistically significant (P = 0.668).
| Discussions|| |
From our survey literacy level of the women studied was high, as up to 93.2% had at least their secondary education completed. This is in line with other studies carried out among pregnant women attending antenatal clinic. , The spouses also had a high literacy level as 98.5% of the respondents had spouses that had secondary level of education completed and above. This is higher than 79.0% reported in Ibadan  , Nigeria. The high literacy level for both respondents and spouses, as observed in this study, could be explained by the fact that higher educational attainment of both partners is one of the factors that have a positive influence on the utilization of antenatal service in Nigeria, as also reported in previous studies. ,
The women were also mainly of low parity as 45.6% were carrying their first pregnancy (nulliparous), in keeping with other studies conducted among pregnant women attending antenatal clinics. , Only 12.8% of the women studied were in their first trimester and this could be explained by the fact that pregnant women in this environment tend to book for antenatal care late. This finding is similar to a study in Enugu, Nigeria that reported that 92.2% of women booked for antenatal care after the first trimester.  Most pregnant women view antenatal care as curative rather than preventive and therefore do not understand why they should book early when they feel they do not have problems.
The prevalence of ASB among pregnant women in this study was 10.6%. This figure is by far lower than the 86.6% reported in an earlier study in Benin city  , and 78.7% reported in Abakiliki  , both in Nigeria. It is however slightly higher than 7.0% and 7.3% reported in Ethiopia  and Ghana  respectively. This study shows that the problem of ASB may not be as alarming as these previous Nigerian studies cited above had portrayed. Perhaps training of the participants on how to collect clean catch urine, appropriate storage and/or immediate processing of samples and avoiding contaminated culture plates, as were strictly observed in this study, may have contributed to the difference. Lower prevalence as seen in this study compared to earlier study may also be due to high literacy level of participants and spouses. Prevalence as low as 4.0% was reported in Lagos  , Nigeria and most other studies from the western countries had reported prevalence that ranged from 2-7%. 
As observed from this study Escherichia coli was the major causative agent of ASB among pregnant women, constituting 46.6% of all isolated pathogens. This is in line with most previous studies , , but at variance with others that reported Staphylococcus aureus as the most prevalent causative agent. , The proximity of anal opening to the genital region and the multiple virulent factors expressed by Escherichia coli such as P fimbriae, S fimbriae, hemolysin, aerobactin, and serum resistance, may contribute to this organism well-suited to colonize the urinary tract. ,,
The next most prevalent organism implicated in this study after Escherichia coli is Proteus species which accounted for 14.3% of the cases found. Most of the previous studies have equally isolated Proteus species, although their position in terms of prevalence varied. ,,, Being a coliform, proteus species are usually found in the gut and may have been introduced into the urethral orifice due to poor personal hygiene. Urease production by proteus species, together with the presence of bacterial motility and fimbriae, contributes most significantly to their ability to colonize the urinary tract. ,
Isolation of Group B streptococcus as in this study is of unique importance. Beyond the complications of pyelonephritis, low birth weight and preterm labour generally associated with untreated ASB among pregnant women, intrapartum transmission of this organism can lead to neonatal Group B streptococcal infection which could present as pneumonia, meningitis, sepsis, and may result in death of the baby if not aggressively managed. 
Isolates from this study were generally sensitive to the antibiotics tested, especially imipenem (100%) and gentamicin (83.5%). This is in line with a similar study in Minna, Nigeria  and may be attributed to their potent activity to gram negative rods, gram positive organisms and anaerobes. Moreover their intravenous or intramuscular route of administration makes them less subject to abuse unlike oral antibiotics. Escherichia coli the most prevalent isolate show good sensitivity to imipenem (100%), gentamicin (84.6%), nitrofurantoin (76.9%), and ceftazidime (76.9%). Similar sensitivity patterns have been reported from a study in Tanzania  and Ethiopia.  These drugs are comparatively less frequently used in the study area, thus explaining their good sensitivity.
Maternal age as observed in this study increased with prevalence of bacteriuria. This is in agreement with some studies which implicated maternal age as a significant risk factor for ASB among pregnant women ,, , but at variance with a study in Iran that found lower maternal age significantly associated with bacteriuria in pregnancy.  The reason often given for the direct relationship between maternal age and bacteriuria, as in this study, is that increasing maternal age is naturally associated with increasing parity, the latter having been reported as a risk factor for ASB. 
Parity was a risk factor for ASB in pregnancy from this study. This finding agrees with some previous studies that reported multiparity to be significantly associated with increased bacteriuria in pregnancy. , Changes in the urinary tract, such as ureteral dilatation and decrease in bladder tone resulting in increased urinary stasis, occurring during each pregnancy and often not perfectly returning to normal even after delivery, perhaps makes multiparous women more prone to ASB. In Ghana, however, though women with four or more children had a prevalence of 16.1% as against 3.7% in the nulliparous women, there was no statistically significant association between multiparity and bacteriuria.  Also in Saudi Arabia, there was no meaningful trend between prevalence and parity observed. 
The trimester of the pregnancy is not a risk factor for ASB from this study. While the frequency of ASB were almost same in the first and second trimester (11.8% and 11.9% respectively), it dropped in third trimester (8.3%). Reports of the relationship between trimester and ASB from previous work are conflicting. One study reported a direct relationship, with prevalence of 0.9%, 1.83%, and 5.6% in the first, second and third trimesters respectively  ; while another reported an inverse relationship, with an observed prevalence of 5.3%, 4.1%, and 2.8% for first, second and third respectively.  However a Nigerian study suggests no particular trend as there was high incidence of bacteriuria during the third trimester of pregnancy (21.9%) compared with that in the first trimester (7.7%), while the level in the second trimester was 22.5%. 
Prevalence of ASB, in this study, decreased as the level of education of respondents increased, indicating that level of education is a risk factor. Same conclusion was also arrived at in a similar study in Pakistan  and in Nnewi, south eastern Nigeria, where the least educated women had higher incidence of bacteriuria.  In Iran, however, no particular trend was followed as prevalence of 2.6%, 7.1%, 6.1%, 6.5%, and 2.3% were reported for illiterates, primary education, secondary education, high school degree and higher education respectively.  It is believed that improved hygiene that goes with higher level of education is responsible for the drop in prevalence of bacteriuria observed in this study.
Also prevalence of ASB decreased with increasing level of education of spouses. This may be due to the fact that a well-educated man is more likely to marry an educated woman, level of education in pregnant women having been reported as a risk factor for ASB.  Moreover, higher education most of the time translates to better job and higher income for the family; all these will ultimately improve health status of the woman.
This study also suggests that Christian pregnant women are more prone to ASB than their Muslim counterparts as all the cases were found among the former. It is important to note that Muslim women recruited in this study were very few (4.2%) and further studies where they are adequately represented to prove the authenticity or otherwise of this observation is advocated. However, in a study at Ilorin where Muslims women were in the majority, a lower prevalence of 33% among the Muslim women was reported compared to 51% among their Christian counterparts. 
It is not clear from the literatures whether ethnicity is a risk factor for ASB or not because most work on this subject did not evaluate it. In this study, it appears that pregnant women from Edo state are more prone to ASB (13.1%) than those not from the state (5.6%). This observation is however not statistically significant (P = 0.062). In Jeddah, Al Sibiani reported a prevalence of 2.3% for Saudi and 0.7% for the non-Saudi pregnant women and concluded that nationality had significant relationship with prevalence of ASB among pregnant women (P = 0.0005).  People of the same nationality living in different environment have also been shown to have varying prevalence. , More work in this area is advocated in other to determine the role of ethnicity or nationality on prevalence of ASB among pregnant women.
| Conclusion|| |
This study has demonstrated that the prevalence of ASB among pregnant women in University of Benin Teaching Hospital, Benin city is 10.6%. Escherichia coli (46.6%) followed by Proteus spp (14.3%) and Enterococcus (10.7%) were the most commonly isolated bacterial aetiologic agents. Isolates were generally susceptible to antibiotic tested especially imipenem, gentamicin, nitrofurantoin and ceftazidime. Maternal age, parity, and levels of education of both partners were associated risk factors. Periodic laboratory based surveillance of ASM among pregnant women, targeted screening of multiparous women, limited family size and continuous education of both partners are recommended to reduce prevalence. However being a tertiary hospital based study, finding may not apply to general population.
| References|| |
Maclean AB. Urinary tract infection in pregnancy. Br J Urol 1997;80:10-3.
Norden CW, Kass EH. Bacteriuria of pregnancy-A critical appraisal. Annu Rev Med 1968;19:431-70.
Ugbogu OC, Ogbonnaya R, Nworie O. Asymptomatic bacteriuria amongst pregnant women in Aba, Abia state, Nigeria. Niger J Microbiol 2010;24:2024-7.
Al Sibiani SA. Asymptomatic bacteriuria in pregnant women in Jeddah, Western region of Saudi Arabia: Call for assessment. JKAU 2010;17:29-42.
Cunningham FG, Lucas MJ. Urinary tract infections complicating pregnancy. Baillieres Clin Obstet Gynaecol 1994;8:353-73.
Smaill F, Vazquez JC. Antibiotics for asymptomatic bacteriuria in pregnancy. Cochrane Database Syst Rev 2007;2:CD000490.
Mittendorf R, Williams MA, Kass EH. Prevention of preterm delivery and low birth weight associated with asymptomatic bacteriuria. Clin Infect Dis 1992;14:927-32.
Whalley P. Bacteriuria of pregnancy. Am J Obstet Gynecol 1967;97:723-38.
Abbey SD. Asymptomatic bacteriuria in the Port Harcourt metropolis of Nigeria. Microbios 1987;49:73-7.
Akinloye O, Ogbolu DO, Akinloye OM, Terry Alli OA. Asymptomatic bacteriuria of pregnancy in Ibadan: A re-accessment. Br J Biomed 2006;63:109-12.
Taiwo SS, Adegbite II, Adofioye OA. Asymptomatic bacteriuria in Osogbo with special reference to Staphylococcus saprophyticus. Afr J Infect Dis 2009;3:8-10.
Akerele J, Abhulimen P, Okonufa F. Prevalence of asymptomatic bacteriuria among pregnant women in Benin city. Niger J Obstet Gynaecol 2001;21:141-4.
Amadi ES, Enemuo OB, Uneke CJ, Nwosu OK, Onyeagba RA, Ugbogu OC. Asymptomatic bacteriuria among pregnant women in Abakaliki, Ebonyi State, Nigeria. J Med Sci 2007;7:698-700.
Daniyan SY, Dangana A, Abalaka ME. Incidence of asymptomatic bacteriuria in antenatal patients attending General Hospital Minna, Niger State. Libyan Agric Res Cen J Intl 2010;1:100-2.
Nnatu S, Essien EE, Akinkugbe A, Odum CU. Asymptomatic bacteriuria in pregnant Nigerian patients. Clin Exp Obstet Gynecol 1989;16:126-9.
Imade PE, Izekor PE, Eghafona NO, Enabulele OI, Ophori E. Asymptomatic bacteriuria among pregnant women. N Am J Med Sci 2010;2:263-6.
Colgan R, Nicolle LE, McGlone A, Hooton TM. Asymptomatic bacteriuria in adults. Am Fam Physician 2006;74:985-90.
Ajayi AB, Nwabuisi C, Aboyeji AP, Ajayi NS, Fowotade A, Fakeye OO. Asymptomatic bacteriuria in antenatal patients in Ilorin, Nigeria. Oman Med J 2012;27:31-5.
Jimoh AA. Utilisation of antenatal services at the Provincial Hospital, Mongomo, Guinea Equatoria. Afr J Reprod Health 2003;7:49-54.
Dairo MD, Owoyokun KE. Factors affecting the utilization of antenatal care services in Ibadan, Nigeria. Benin J Postgrad Med 2010;12:3-13.
Awusi VO, Anyanwu EB, Okeleke V. Determinants of antenatal care services utilization in emevor village, Nigeria. Benin J Postgrad Med 2009;11:21-6.
Ezeome IV, Ikeme AC, Okezie OA, Onyebueke EA. Asymptomatic bacteriuria in pregnant women in Enugu, Nigeria. Trop J Obstet Gynaecol 2006;23:12-3.
Gabre-Selassie S. Asymptomatic bacteriuria in pregnancy: Epidemiological clinical and microbiological approach. Ethiop Med J 1998;36:185-92.
Turpin CA, Minkah B, Danso KA, Frimpong EH. Asymptomatic bacteriuria in pregnant women attending antenatal clinic at Komfo Anokye Teaching Hospital, Kumasi, Ghana. Ghana Med J 2007;41:26-9.
Oli AN, Okafor CI, Ibezim EC, Akujiobi CN, Onwunzo MC. The prevalence and bacteriology of asymptomatic bacteriuria among antenatal patients in Nnamdi Azikiwe University Teaching Hospital Nnewi; South Eastern Nigeria. Niger J Clin Pract 2010;13:409-12.
Johnson JR. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 1991;4:80-128.
Mobley HL, Island MD, Massad G. Virulence determinants of uropathogenic Escherichia coli and Proteus mirabilis. Kidney Int Suppl 1994;47:S129-36.
Masinde A, Gumodoka B, Kilonzo A, Mshana SE. Prevalence of urinary tract infection among pregnant women at Bugando Medical Centre, Mwanza, Tanzania. Tanzan J Health Res 2009;11:154-9.
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. Ethiop Med J 2008;46:227-35.
Samad H. Asymptomatic bacteriuria in pregnant women. Urol J (Tehran) 2007;4:24-7.
Nawal Salim Al Senani. Asymptomatic bacteriuria in pregnant women. Bahrain Med Bull 2011;33:10-3.
Tugrul S, Oral O, Kumru P, Köse D, Alkan A, Yildirim G. Evaluation and importance of asymptomatic bacteriuria in pregnancy. Clin Exp Obstet Gynecol 2005;32:237-40.
Haider G, Zehra N, Munir AA, Haider A. Risk factors of urinary tract infection in pregnancy. J Pak Med Assoc 2010;60:213-6.
al-Sibai MH, Saha A, Rasheed P. Socio-biological correlates of bacteriuria in Saudi pregnant women. Public Health 1989;103:113-21.
Ullah MA, Barman A, Siddique MA, Haque AK. Prevalence of asymptomatic bacteriuria and its consequences in pregnancy in a rural community of Bangladesh. Bangladesh Med Res Counc Bull 2007;33:60-4.
Versi E, Chia P, Griffiths DJ, Harlow BL. Bacteriuria in pregnancy: A comparison of Bangladeshi and Caucasian women. Int Urogynecol J Pelvic Floor Dysfunct 1997;8:8-12.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]