This article was downloaded by: [New York University] On: 02 September 2015, At: 04:15 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: 5 Howick Place, London, SW1P 1WG
Journal of Obstetrics and Gynaecology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ijog20
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting a
a
b
c
J. O. Awoleke , A. I. Adanikin , D. D. Ajayi & O. S. Ayosanmi a
Department of Obstetrics and Gynaecology, Ekiti State University Teaching Hospital, AdoEkiti, Ekiti State, Nigeria b
Department of Microbiology and Parasitology, Ekiti State University Teaching Hospital, AdoEkiti, Ekiti State, Nigeria c
Department of Family Medicine, Ekiti State University Teaching Hospital, Ado-Ekiti, Ekiti State, Nigeria Published online: 16 Jul 2014.
Click for updates To cite this article: J. O. Awoleke, A. I. Adanikin, D. D. Ajayi & O. S. Ayosanmi (2015) Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting, Journal of Obstetrics and Gynaecology, 35:1, 25-29, DOI: 10.3109/01443615.2014.935724 To link to this article: http://dx.doi.org/10.3109/01443615.2014.935724
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Obstetrics and Gynaecology, January 2015; 35: 25–29 © 2014 Informa UK, Ltd. ISSN 0144-3615 print/ISSN 1364-6893 online DOI: 10.3109/01443615.2014.935724
OBSTETRICS
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting J. O. Awoleke1, A. I. Adanikin1, D. D. Ajayi2 & O. S. Ayosanmi3
Downloaded by [New York University] at 04:15 02 September 2015
Departments of 1Obstetrics and Gynaecology, 2Microbiology and Parasitology and 3Family Medicine, Ekiti State University Teaching Hospital, Ado-Ekiti, Ekiti State, Nigeria
This study aims at identifying predictors of asymptomatic bacteriuria (AB) among pregnant women in a low-resource setting, with the intent of recommending a guideline for screening during antenatal care. A total of 266 healthy pregnant women were antenatally recruited after informed consent. They had routine antenatal investigations, a 1 h 50-g oral glucose tolerance test and quantitative urine culture and sensitivity. The data collected were analysed using statistical software package SPSS v. 17. Prevalence of AB was 23 (8.6%). Escherichia coli was the commonest isolate (6, 26.1%), closely followed by Staphylococcus aureus (5, 21.7%). AB was commoner among patients aged 25–34 years, of low parity and higher education. Blood group B- rhesus-positive significantly predicts the likelihood of developing AB in pregnancy (adjusted OR: 0.36; 95% CI: 0.14–0.96). We conclude that blood group B-rhesuspositive in association with other patients’ characteristics, such as age 25–34 years, low parity and higher education could form guidelines for a screening algorithm in our environment.
likely to be at increased risk of the condition; this group may then benefit from routine prenatal screening and treatment. To this effect, some studies have reported higher prevalence of AB in pregnant women with sickle cell traits, diabetes mellitus, anaemia, HIV infection and low socioeconomic status (Smaill 2007; Enayat et al. 2008; Awolude et al. 2010). The body of research however still continues to grow, with varying screening guidelines promulgated by different nations and professional bodies, based on the peculiarity of identifiable risk factors and settings of clinical practice. To date, in our environment, AB is not routinely screened during pregnancy and no guideline exists. This study aims to identify predictors of the condition among our pregnant women with the intent of recommending an acceptable guideline for screening during antenatal care.
Keywords: Asymptomatic bacteriuria, pregnancy, screening
This cross-sectional study was conducted at the Ekiti State University Teaching Hospital, Ado-Ekiti between February and April, 2011. The health institution is located in a State capital within the South-west zone of Nigeria. The hospital has an average delivery rate of 2,500 births per year. All healthy pregnant women who came for the antenatal booking visit at the health facility during the study period were eligible. Using AB prevalence of 10.7% among pregnant women (Awonuga et al. 2010), we calculated that a minimum sample size of 147 participants was required for a precision of 0.05 at a 95% confidence interval. However, 266 pregnant women were recruited to increase the power of the study. The women were adequately counselled about AB and those who gave informed consent to participate were recruited. Women with symptoms of urinary tract infection (frequency, dysuria, urgency, etc.), antibiotic use in the index pregnancy or known underlying renal disease were excluded. Sociodemographic and obstetrics characteristics of respondents were entered into the study proforma. A 1-h, 50-g oral glucose challenge test was given to participants with a cut-off value set at ⬎ 130 mg/dl (7.2 mmol/l), which identifies 90% of women with GDM (American Diabetes Association 2009). Samples of routine antenatal investigations (blood group, genotype, HIV test, hepatitis B surface antigen status, etc.) were also collected.
Introduction Asymptomatic bacteriuria (AB) is defined as the quantitative growth of the same bacteria organism, ⱖ 105 colony forming units/ml of an aseptically collected midstream urine specimen, in the absence of symptoms of urinary tract infection (Awolude et al. 2010). Its prevalence in pregnancy varies from 2% to 10% (Schnarr and Smaill 2008). Interest in AB has grown over the years owing to the propensity for adverse medical and obstetrics outcomes if left unchecked in some patients. Documented evidence has shown that if AB is not treated, as many as 30% of pregnant women develop overt acute pyelonephritis (Whalley 1967; Abdullah and Al-Moslih 2005). AB has also been associated with preterm delivery, fetal loss and pre-eclampsia (Romero et al. 1989). Based on the impact that the condition could have on pregnancy outcome, a recommendation for universal screening of all parturients was made (Naber et al. 2001; US Preventative Services Task Force 2008); however the logistic feasibility and financial implications made the recommendation unpopular, especially in low-resource settings (Awonuga et al. 2010). Thus, attention is shifting to identifying the subset of pregnant women that are
Methodology
Correspondence: A. I. Adanikin, Department of Obstetrics and Gynaecology, Ekiti State University Teaching Hospital, Ado-Ekiti, Nigeria. E-mail: [email protected]
Downloaded by [New York University] at 04:15 02 September 2015
26
J. O. Awoleke et al.
In addition, while at the booking clinic, these patients were instructed to obtain a midstream urine specimen as follows: after an initial cleaning of the perineum with water, a portion of the urine is voided before about 10 ml of urine is collected into sterile universal bottles which had earlier been correctly labelled and distributed to them. Any other urine in the bladder is then voided into the toilet. The urine samples in the sterile universal bottles were transported to the laboratory for processing within 1 h of voiding. Where immediate processing was not possible, the samples were promptly refrigerated at 4°C to avoid multiplication of bacteria at room temperature. Samples were subjected to routine microscopy, culture and sensitivity according to standard practice. Suspected pathogens were identified using standard biochemical and sugar utilisation tests. Bacteriuria was diagnosed as the quantitative growth of the same bacteria organism, ⱖ 105 colony forming units/ml of aseptically collected midstream urine specimen. Based on antibiotic sensitivity of the isolated organisms, those with AB were treated. Data entry and analysis were done with SPSS v. 17. Statistical analysis was performed with the χ2-test, Fisher’s exact test and Student’s t-test as appropriate and, level of confidence was set at 95%. Ethical clearance for the study was obtained from the ethics committee of Ekiti State University Teaching Hospital.
Results The mean age of respondents was 30.66 ⫾ 4.96 years; most of them, 189 (69.2%), were between the age of 25–34 years. A total of 86 (32.3%) women were ⬍ 20 weeks pregnant, while 25 (9.4%) were ⬎ 34 weeks pregnant. The majority had blood group O-rhesus-positive followed by A-rhesus-positive and then B-rhesus-positive. Only three (1.2%) participants had sickle cell disease; nine (3.4%) had HIV infection and 41 (15.4%) were positive on the 1-h oral glucose challenge test (Table I). Table II shows the prevalence of asymptomatic bacteriuria and isolated organisms on culture. In total, 23 (8.6%) respondents had asymptomatic bacteriuria. Among these, Escherichia coli, Staphylococcus aureus, Enterococcus faecalis and Klebsiella were isolated in six (26.1%), five (21.7%), four (17.4%) and three (13.1%) urine specimens, respectively. Table III highlights the antibiotics sensitivity patterns of the isolated organisms. Escherichia coli, the most common isolate, showed sensitivity to cotrimoxazole, streptomycin, amoxicillin, augmentin and cefuroxime. The next prominent isolate, Staphylococcus aureus, was sensitive to nalidixic acid, augmentin, cloxacillin and cefuroxime. In general, all the organisms were sensitive to augmentin and cefuroxime. Amoxicillin and cotrimoxazole equally showed a promising therapeutic efficacy, except partial sensitivity of Staphylococcus aureus to them. Table IV is a display of the multiple logistic regression analysis of association between the respondents’ sociodemographic features and presence of asymptomatic bacteriuria. Blood group B-rhesus-positive predicts the likelihood of having asymptomatic bacteriuria (adjusted OR: 0.36; 95% CI: 0.14–0.96).
Discussion This study found the prevalence of AB to be 8.6% among pregnant women presenting for antenatal booking at the Ekiti State University Teaching Hospital. Escherichia coli was the commonest isolate. Analysis of the sociodemographic and obstetrics characteristics of the respondents showed that blood group
Table I. Sociodemographic features of respondents. Variable Age (years) ⱕ 24 25–34 35–44 ⱖ 45 Parity ⱕ1 2–3 ⱖ4 Gestational age (weeks) ⱕ 20 20–27 28–34 ⬎ 34 Body mass index (kg/m2) ⬍20 20–30 ⬎ 30 Educational level No formal Primary Secondary Tertiary Occupation Skilled Semi-skilled Unskilled Blood group A⫹ B⫹ AB⫹ O⫹ A– B– AB– O– Genotype AA AS AC SC SS HIV status Positive Negative HBsAg status Positive Negative GDM screening Positive
n
(%)
25 184 54 3
9.4 69.2 20.3 1.1
183 74 9
68.8 27.8 3.4
86 96 59 25
32.3 36.1 22.2 9.4
8 183 75
3.0 68.8 28.2
9 15 47 195
3.4 5.6 17.7 73.3
55 99 112
20.7 37.2 42.1
56 41 7 137 7 5 1 12
21.1 15.4 2.6 51.5 2.6 1.9 0.4 4.5
188 67 8 1 2
70.6 25.2 3.0 0.4 0.8
9 257
3.4 96.6
23 243
8.6 91.4
41
15.4
Table II. Prevalence of asymptomatic bacteriuria and associated organisms. Variable Asymptomatic bacteriuria Yes No Isolated organisms (n ⫽ 23) E. coli Enterococcus faecalis Klebsiella Proteus Pseudomonas aeruginosa Staph. albus Staph. aureus
n
(%)
23 243
8.6 91.4
6 4 3 1 1 3 5
26.1 17.4 13.1 4.3 4.3 13.1 21.7
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting 27 Table III. Antibiotics sensitive patterns of isolated organisms. Variables
E. coli
E. faecalis
Klebsiella
Proteus
Pseudomonas
S. albus
S. aureus
S R R R S S S – – – R R S
S S – – – S S R S S – R S
S PS R R – S S – – – R R S
S R S R – S S – – – – R S
S S S S S S S – – – – R S
S – – S – S S R – – – R S
PS PS S R – PS S R S R – R S
Cotrimoxazole Gentamycin Nalidixic acid Nitrofurantoin Streptomycin Amoxicillin Augmentin Erythromycin Cloxacillin Chloramphenicol Ciprofloxacin Ofloxacin Cefuroxime
S, sensitive; PS, partial sensitivity; R, resistant.
Table IV. Association between respondents’ sociodemographic features and asymptomatic bacteriuria. Asymptomatic bacteriuria
Downloaded by [New York University] at 04:15 02 September 2015
Yes Variable Age (years) ⱕ 24 25–34 35–44 ⱖ 45 Parity ⱕ1 2–3 ⱖ4 GA (weeks) ⱕ 20 20–27 28–34 ⬎ 34 BMI (kg/m2) ⬍20 20–30 ⬎ 30 Educational level No formal Primary Secondary Tertiary Occupation Skilled Semi-skilled Unskilled Blood group A⫹ B⫹ AB⫹ O⫹ A– B– AB– O– Genotype AA AS AC SC SS HIV status Positive Negative HBsAg status Positive Negative GDM Screening Positive Negative
No
Total
n
(%)
n
(%)
n
(%)
Adjusted odds ratio
95% CI
2 18 3 0
8.0 9.8 5.6 0
23 166 51 3
92.0 90.2 94.4 100
25 184 54 3
100 100 100 100
1.04 1.00 1.63 0.78
0.28–5.57
17 6 0
9.3 8.1 0
166 68 9
90.7 91.9 100
183 74 9
100 100 100
1.00 1.11 2.00
4 11 4 4
4.7 11.5 6.8 16.0
82 85 55 21
95.3 88.5 93.2 84
86 96 59 25
100 100 100 100
2.47 1.00 1.66 0.64
0 15 8
0 8.2 10.7
8 168 67
100 91.8 89.3
8 183 75
100 100 100
1.56 1.00 0.73
1 3 3 16
11.1 20.0 6.4 8.2
8 12 44 179
88.9 80.0 93.6 91.8
9 15 47 195
100 100 100 100
0.52 0.33 1.17 1.00
0.09–5.42 0.10–1.34 0.37–4.64
5 9 9
9.1 9.1 8.0
50 90 103
90.9 90.9 92.0
55 99 112
100 100 100
0.84 0.87 1.00
0.28–2.72 0.33–2.29
3 8 0 11 0 0 0 1
5.4 19.5 0 8.0 0 0 0 8.3
53 33 7 126 7 5 1 11
94.6 80.5 100 92.0 100 100 100 91.7
56 41 7 137 7 5 1 12
100 100 100 100 100 100 100 100
1.39 0.36 1.36 1.00 1.36 1.00 0.27 0.70
0.42–5.69 0.14–0.96∗ 0.09–21.21 0.09–21.21 0.07–15.04 0.0022–∞ 0.12–7.49
15 8 0 0 0
8.0 11.9 0 0 0
173 59 8 1 2
92.0 88.1 100 100 100
188 67 8 1 2
100 100 100 100 100
1.00 0.63 1.52 0.27 0.45
0.26–1.58 0.10–23.49 0.0022–∞ 0.0157–∞
2 21
22.2 8.2
7 236
77.8 91.8
9 257
100 100
0.27 1.00
0.07–1.46
1 22
4.3 9.1
22 221
95.7 90.9
23 243
100 100
1.52 1.00
0.29–16.31
4 19
9.8 8.4
37 206
90.2 91.6
41 225
100 100
1.27 1.00
0.38–3.60
GA, gestational age; BMI, body mass index; ∞, infinity. ∗Significant association.
0.53–6.44 0.06–10.58
0.44–3.05 0.13–31.00 0.82–8.61 0.54–5.82 0.20–2.30 0.10–24.19 0.30–1.84
Downloaded by [New York University] at 04:15 02 September 2015
28
J. O. Awoleke et al.
B-rhesus-positive significantly predicts the likelihood of having AB during pregnancy. The prevalence of AB obtained in our study correlates well with most observational studies around the world (Abdullah and Al-Moslih 2005; Fatima and Ishrat 2006; Sharma and Thapa 2007), with few studies reporting much higher rates (Akerele et al. 2001; Kehinde et al. 2011). Discrepancy in prevalence can be attributed to differences in study methodology and location. The role of host factor in predicting acquisition of AB in pregnancy has been a subject of controversy in the literature (Thurman et al. 2006; Sharma and Thapa 2007). Effects of sociodemographic and obstetrics characteristics, such as age, race, social status, parity, etc. on AB during pregnancy are less clear, owing to a lack of consistency in study findings (Schnarr and Smaill 2008). However, it is recognised that environment and clinical setting may influence identified predictors and therefore must be borne in mind when interpreting results. The identification of blood group B-rhesus-positive as a predictor of AB in pregnancy in our environment is a novel finding. It may be because most previous local studies have not considered this factor in their analysis. Therefore, they have missed this predictor over time. Age did not influence the occurrence of AB, even though high preponderance of the condition was found among the age group 25–34, which is consistent with the observation by Awonuga et al. (2010). We observed that occupation had no impact in predicting AB in pregnancy, and, contrary to reports that lower education is associated with increased incidence of AB (Faro and Fenner 1998), diagnosis of the condition was higher in those with tertiary education. Our finding suggests that higher education may not necessarily translate to better hygienic behaviour. Similar to earlier findings by Awonuga et al. (2010), AB was commoner among low parity women, though it was not statistically significant. It negates an earlier assertion by Patterson and Andriole (2003) that AB in pregnancy increases with parity. Although some have reported a high incidence of AB among patients with sickle cell traits (Baill and Witter 1990), our observation was contrary to this. Instead, it is in tandem with a retrospective study by Thurman et al. (2006), which found that sickle cell trait does not increase the prevalence of AB when compared with control patients. Those who were positive for human immunodeficiency virus (HIV) infection, hepatitis B and/or glucose tolerance screening were also not more predisposed to AB in this study. Routine screening for AB in pregnancy is a recognised standard of obstetrics practice and most regulating bodies recommend it (Nicolle et al. 2005). But, the overall cost implication has made adherence difficult in developing world; our environment not being an exception. In view of this, some authors have suggested that a designed screening algorithm, which incorporates identified risk factors may be cost-effective, while still maintaining optimal maternal and neonatal outcome (Smaill 2007). Based on our research findings, a subset of pregnant women who are of blood group B-rhesus-positive, within the ages of 25–34 years, of low parity and higher education, will best fit into the criteria of the screening algorithm. Escherichia coli, the commonest isolate in our urine cultures, is known to be the most common aetiological agent in AB (Abdullah and Al-Moslih 2005; Smaill 2007). As equally found by our study, Staphylococcus aureus is becoming a prominent urine culture isolate in Nigeria (Amadi et al. 2007; Awonuga et al. 2010; Imade et al. 2010). Antibiotics sensitivity to the
cultured microorganisms shows local peculiarity when compared with studies from other parts of Nigeria (Oyetunji et al. 2006; Imade et al. 2010). This invariably supports the need for regional guidelines. Our research is not without limitation. Pre-pregnancy urinary tract infection (UTI) and antepartum UTI prior to commencement of prenatal care were not considered as likely predictors during the conduct of the study. Future research on this subject in our locality should put these into consideration. In conclusion, blood group B-rhesus-positive predicts development of AB in pregnancy in our environment. AB was also found to be commoner among patients who are in the age range of 25–34 years, with low parity and higher education. These features could form guidelines for a screening algorithm. A larger multi-centre study to further validate this observation is suggested. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References Abdullah AA, Al-Moslih MI. 2005. Prevalence of asymptomatic bacteriuria in pregnant women in Sharjah, United Arab Emirates. Eastern Mediterranean Health Journal 11:1045–1052. Akerele J, Abhulimen P, Okonofua F. 2001. Prevalence of asymptomatic bacteriuria among pregnant women in Benin City, Nigeria. Journal of Obstetrics and Gynaecology 21:141–144. Amadi ES, Enemuo OB, Uneke CJ, Nwosu OK, Onyeagba RA, Ugbogu OC. 2007. Asymptomatic bacteriuria among pregnant women in Abakaliki, Ebonyi State, Nigeria. Journal of Medical Sciences 7:698–700. American Diabetes Association. 2009. Diagnosis and classification of diabetes mellitus. Diabetes Care 32:S62–S67. Awolude OA, Adesina OA, Oladokun A, Mutiu WB, Adewole IF. 2010. Asymptomatic bacteriuria among HIV positive pregnant women. Virulence 1:130–133. Awonuga DA, Fawole AO, Dada-Adegbola HA, Olola FA, Awonuga OM. 2010. Predictors of asymptomatic bacteriuria among obstetric population in Ibadan. Nigerian Medical Journal 19:188–193. Baill IC, Witter FR. 1990. Sickle trait and its association with birthweight and urinary tract infections in pregnancy. International Journal of Gynecology and Obstetrics 33:19–21. Enayat K, Fariba F, Bahram N. 2008. Asymptomatic bacteriuria among pregnant women referred to outpatient clinics in Sanandaj, Iran. International Brazilian Journal of Urology 34:699–707. Faro S, Fenner DE. 1998. Urinary tract infections. Clinical Obstetrics and Gynecology 41:744–754. Fatima N, Ishrat S. 2006. Frequency and risk factors of asymptomatic bacteriuria during pregnancy. Journal of the College of Physicians and Surgeons, Pakistan 16:273–275. Imade PE, Izekor PE, Eghafona NO, Enabulele OI, Ophori E. 2010. Asymptomatic bacteriuria among pregnant women. North American Journal of Medical Sciences 2:263–266. Kehinde OK, Adedapo KS, Aimaikhu CO, Odukogbe AA, Olayemi O, Salako B. 2011. Significant bacteriuria among asymptomatic antenatal clinic attendees in Ibadan, Nigeria. Tropical Medicine and Health 39: 73–76. Naber KG, Bergman B, Bishop MC, Bjerklund-Johansen TE, Botto H, Lobel B et al. 2001. EAU guidelines for the management of urinary and male genital tract infections. Urinary Tract Infection (UTI) Working Group of the Health Care Office (HCO) of the European Association of Urology (EAU). European Urology 40:576–588. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM. 2005. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clinical Infectious Diseases 440:643–654. Oyetunji JA, Ahmed Y, Nwobodo EI, Airede LR, Ekele BA. 2006. Asymptomatic bacteriuria in pregnancy in Sokoto, Nigeria. Sahel Medical Journal 9:1–6. Patterson TF, Andriole VT. 2003. Bacteriuria in pregnancy. Current Treatment Options in Infectious Diseases 5:81–87.
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting 29
Downloaded by [New York University] at 04:15 02 September 2015
Romero R, Oyarzun E, Mazor M. 1989. Meta-analysis of the relationship between asymptomatic bacteriuria and preterm delivery/low birth weight. Obstetrics and Gynecology 73:576–582. Schnarr J, Smaill F. 2008. Asymptomatic bacteriuria and symptomatic urinary tract infection in pregnancy. European Journal of Clinical Investigation 38(Suppl 2):50–57. Sharma P, Thapa L. 2007. Acute pyelonephritis in pregnancy: a retrospective study. Australian and New Zealand Journal of Obstetrics and Gynaecology 47:313–315.
Smaill F. 2007. Asymptomatic bacteriuria in pregnancy. Best Practice and Research. Clinical Obstetrics and Gynaecology 21:439–450. Thurman AR, Steed LL, Hulsey T, Soper DE. 2006. Bacteriuria in pregnant women with sickle cell trait. American Journal of Obstetrics and Gynecology 194:1366–1370. US Preventative Services Task Force. 2008. Screening for asymptomatic bacteriuria: U.S. Preventative Services Task Force reaffirmation recommendation statement. Annals of Internal Medicine 149:43–47. Whalley P. 1967. Bacteriuria of pregnancy. American Journal of Obstetrics and Gynecology 97:723–738.
Journal of Obstetrics and Gynaecology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ijog20
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting a
a
b
c
J. O. Awoleke , A. I. Adanikin , D. D. Ajayi & O. S. Ayosanmi a
Department of Obstetrics and Gynaecology, Ekiti State University Teaching Hospital, AdoEkiti, Ekiti State, Nigeria b
Department of Microbiology and Parasitology, Ekiti State University Teaching Hospital, AdoEkiti, Ekiti State, Nigeria c
Department of Family Medicine, Ekiti State University Teaching Hospital, Ado-Ekiti, Ekiti State, Nigeria Published online: 16 Jul 2014.
Click for updates To cite this article: J. O. Awoleke, A. I. Adanikin, D. D. Ajayi & O. S. Ayosanmi (2015) Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting, Journal of Obstetrics and Gynaecology, 35:1, 25-29, DOI: 10.3109/01443615.2014.935724 To link to this article: http://dx.doi.org/10.3109/01443615.2014.935724
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Obstetrics and Gynaecology, January 2015; 35: 25–29 © 2014 Informa UK, Ltd. ISSN 0144-3615 print/ISSN 1364-6893 online DOI: 10.3109/01443615.2014.935724
OBSTETRICS
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting J. O. Awoleke1, A. I. Adanikin1, D. D. Ajayi2 & O. S. Ayosanmi3
Downloaded by [New York University] at 04:15 02 September 2015
Departments of 1Obstetrics and Gynaecology, 2Microbiology and Parasitology and 3Family Medicine, Ekiti State University Teaching Hospital, Ado-Ekiti, Ekiti State, Nigeria
This study aims at identifying predictors of asymptomatic bacteriuria (AB) among pregnant women in a low-resource setting, with the intent of recommending a guideline for screening during antenatal care. A total of 266 healthy pregnant women were antenatally recruited after informed consent. They had routine antenatal investigations, a 1 h 50-g oral glucose tolerance test and quantitative urine culture and sensitivity. The data collected were analysed using statistical software package SPSS v. 17. Prevalence of AB was 23 (8.6%). Escherichia coli was the commonest isolate (6, 26.1%), closely followed by Staphylococcus aureus (5, 21.7%). AB was commoner among patients aged 25–34 years, of low parity and higher education. Blood group B- rhesus-positive significantly predicts the likelihood of developing AB in pregnancy (adjusted OR: 0.36; 95% CI: 0.14–0.96). We conclude that blood group B-rhesuspositive in association with other patients’ characteristics, such as age 25–34 years, low parity and higher education could form guidelines for a screening algorithm in our environment.
likely to be at increased risk of the condition; this group may then benefit from routine prenatal screening and treatment. To this effect, some studies have reported higher prevalence of AB in pregnant women with sickle cell traits, diabetes mellitus, anaemia, HIV infection and low socioeconomic status (Smaill 2007; Enayat et al. 2008; Awolude et al. 2010). The body of research however still continues to grow, with varying screening guidelines promulgated by different nations and professional bodies, based on the peculiarity of identifiable risk factors and settings of clinical practice. To date, in our environment, AB is not routinely screened during pregnancy and no guideline exists. This study aims to identify predictors of the condition among our pregnant women with the intent of recommending an acceptable guideline for screening during antenatal care.
Keywords: Asymptomatic bacteriuria, pregnancy, screening
This cross-sectional study was conducted at the Ekiti State University Teaching Hospital, Ado-Ekiti between February and April, 2011. The health institution is located in a State capital within the South-west zone of Nigeria. The hospital has an average delivery rate of 2,500 births per year. All healthy pregnant women who came for the antenatal booking visit at the health facility during the study period were eligible. Using AB prevalence of 10.7% among pregnant women (Awonuga et al. 2010), we calculated that a minimum sample size of 147 participants was required for a precision of 0.05 at a 95% confidence interval. However, 266 pregnant women were recruited to increase the power of the study. The women were adequately counselled about AB and those who gave informed consent to participate were recruited. Women with symptoms of urinary tract infection (frequency, dysuria, urgency, etc.), antibiotic use in the index pregnancy or known underlying renal disease were excluded. Sociodemographic and obstetrics characteristics of respondents were entered into the study proforma. A 1-h, 50-g oral glucose challenge test was given to participants with a cut-off value set at ⬎ 130 mg/dl (7.2 mmol/l), which identifies 90% of women with GDM (American Diabetes Association 2009). Samples of routine antenatal investigations (blood group, genotype, HIV test, hepatitis B surface antigen status, etc.) were also collected.
Introduction Asymptomatic bacteriuria (AB) is defined as the quantitative growth of the same bacteria organism, ⱖ 105 colony forming units/ml of an aseptically collected midstream urine specimen, in the absence of symptoms of urinary tract infection (Awolude et al. 2010). Its prevalence in pregnancy varies from 2% to 10% (Schnarr and Smaill 2008). Interest in AB has grown over the years owing to the propensity for adverse medical and obstetrics outcomes if left unchecked in some patients. Documented evidence has shown that if AB is not treated, as many as 30% of pregnant women develop overt acute pyelonephritis (Whalley 1967; Abdullah and Al-Moslih 2005). AB has also been associated with preterm delivery, fetal loss and pre-eclampsia (Romero et al. 1989). Based on the impact that the condition could have on pregnancy outcome, a recommendation for universal screening of all parturients was made (Naber et al. 2001; US Preventative Services Task Force 2008); however the logistic feasibility and financial implications made the recommendation unpopular, especially in low-resource settings (Awonuga et al. 2010). Thus, attention is shifting to identifying the subset of pregnant women that are
Methodology
Correspondence: A. I. Adanikin, Department of Obstetrics and Gynaecology, Ekiti State University Teaching Hospital, Ado-Ekiti, Nigeria. E-mail: [email protected]
Downloaded by [New York University] at 04:15 02 September 2015
26
J. O. Awoleke et al.
In addition, while at the booking clinic, these patients were instructed to obtain a midstream urine specimen as follows: after an initial cleaning of the perineum with water, a portion of the urine is voided before about 10 ml of urine is collected into sterile universal bottles which had earlier been correctly labelled and distributed to them. Any other urine in the bladder is then voided into the toilet. The urine samples in the sterile universal bottles were transported to the laboratory for processing within 1 h of voiding. Where immediate processing was not possible, the samples were promptly refrigerated at 4°C to avoid multiplication of bacteria at room temperature. Samples were subjected to routine microscopy, culture and sensitivity according to standard practice. Suspected pathogens were identified using standard biochemical and sugar utilisation tests. Bacteriuria was diagnosed as the quantitative growth of the same bacteria organism, ⱖ 105 colony forming units/ml of aseptically collected midstream urine specimen. Based on antibiotic sensitivity of the isolated organisms, those with AB were treated. Data entry and analysis were done with SPSS v. 17. Statistical analysis was performed with the χ2-test, Fisher’s exact test and Student’s t-test as appropriate and, level of confidence was set at 95%. Ethical clearance for the study was obtained from the ethics committee of Ekiti State University Teaching Hospital.
Results The mean age of respondents was 30.66 ⫾ 4.96 years; most of them, 189 (69.2%), were between the age of 25–34 years. A total of 86 (32.3%) women were ⬍ 20 weeks pregnant, while 25 (9.4%) were ⬎ 34 weeks pregnant. The majority had blood group O-rhesus-positive followed by A-rhesus-positive and then B-rhesus-positive. Only three (1.2%) participants had sickle cell disease; nine (3.4%) had HIV infection and 41 (15.4%) were positive on the 1-h oral glucose challenge test (Table I). Table II shows the prevalence of asymptomatic bacteriuria and isolated organisms on culture. In total, 23 (8.6%) respondents had asymptomatic bacteriuria. Among these, Escherichia coli, Staphylococcus aureus, Enterococcus faecalis and Klebsiella were isolated in six (26.1%), five (21.7%), four (17.4%) and three (13.1%) urine specimens, respectively. Table III highlights the antibiotics sensitivity patterns of the isolated organisms. Escherichia coli, the most common isolate, showed sensitivity to cotrimoxazole, streptomycin, amoxicillin, augmentin and cefuroxime. The next prominent isolate, Staphylococcus aureus, was sensitive to nalidixic acid, augmentin, cloxacillin and cefuroxime. In general, all the organisms were sensitive to augmentin and cefuroxime. Amoxicillin and cotrimoxazole equally showed a promising therapeutic efficacy, except partial sensitivity of Staphylococcus aureus to them. Table IV is a display of the multiple logistic regression analysis of association between the respondents’ sociodemographic features and presence of asymptomatic bacteriuria. Blood group B-rhesus-positive predicts the likelihood of having asymptomatic bacteriuria (adjusted OR: 0.36; 95% CI: 0.14–0.96).
Discussion This study found the prevalence of AB to be 8.6% among pregnant women presenting for antenatal booking at the Ekiti State University Teaching Hospital. Escherichia coli was the commonest isolate. Analysis of the sociodemographic and obstetrics characteristics of the respondents showed that blood group
Table I. Sociodemographic features of respondents. Variable Age (years) ⱕ 24 25–34 35–44 ⱖ 45 Parity ⱕ1 2–3 ⱖ4 Gestational age (weeks) ⱕ 20 20–27 28–34 ⬎ 34 Body mass index (kg/m2) ⬍20 20–30 ⬎ 30 Educational level No formal Primary Secondary Tertiary Occupation Skilled Semi-skilled Unskilled Blood group A⫹ B⫹ AB⫹ O⫹ A– B– AB– O– Genotype AA AS AC SC SS HIV status Positive Negative HBsAg status Positive Negative GDM screening Positive
n
(%)
25 184 54 3
9.4 69.2 20.3 1.1
183 74 9
68.8 27.8 3.4
86 96 59 25
32.3 36.1 22.2 9.4
8 183 75
3.0 68.8 28.2
9 15 47 195
3.4 5.6 17.7 73.3
55 99 112
20.7 37.2 42.1
56 41 7 137 7 5 1 12
21.1 15.4 2.6 51.5 2.6 1.9 0.4 4.5
188 67 8 1 2
70.6 25.2 3.0 0.4 0.8
9 257
3.4 96.6
23 243
8.6 91.4
41
15.4
Table II. Prevalence of asymptomatic bacteriuria and associated organisms. Variable Asymptomatic bacteriuria Yes No Isolated organisms (n ⫽ 23) E. coli Enterococcus faecalis Klebsiella Proteus Pseudomonas aeruginosa Staph. albus Staph. aureus
n
(%)
23 243
8.6 91.4
6 4 3 1 1 3 5
26.1 17.4 13.1 4.3 4.3 13.1 21.7
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting 27 Table III. Antibiotics sensitive patterns of isolated organisms. Variables
E. coli
E. faecalis
Klebsiella
Proteus
Pseudomonas
S. albus
S. aureus
S R R R S S S – – – R R S
S S – – – S S R S S – R S
S PS R R – S S – – – R R S
S R S R – S S – – – – R S
S S S S S S S – – – – R S
S – – S – S S R – – – R S
PS PS S R – PS S R S R – R S
Cotrimoxazole Gentamycin Nalidixic acid Nitrofurantoin Streptomycin Amoxicillin Augmentin Erythromycin Cloxacillin Chloramphenicol Ciprofloxacin Ofloxacin Cefuroxime
S, sensitive; PS, partial sensitivity; R, resistant.
Table IV. Association between respondents’ sociodemographic features and asymptomatic bacteriuria. Asymptomatic bacteriuria
Downloaded by [New York University] at 04:15 02 September 2015
Yes Variable Age (years) ⱕ 24 25–34 35–44 ⱖ 45 Parity ⱕ1 2–3 ⱖ4 GA (weeks) ⱕ 20 20–27 28–34 ⬎ 34 BMI (kg/m2) ⬍20 20–30 ⬎ 30 Educational level No formal Primary Secondary Tertiary Occupation Skilled Semi-skilled Unskilled Blood group A⫹ B⫹ AB⫹ O⫹ A– B– AB– O– Genotype AA AS AC SC SS HIV status Positive Negative HBsAg status Positive Negative GDM Screening Positive Negative
No
Total
n
(%)
n
(%)
n
(%)
Adjusted odds ratio
95% CI
2 18 3 0
8.0 9.8 5.6 0
23 166 51 3
92.0 90.2 94.4 100
25 184 54 3
100 100 100 100
1.04 1.00 1.63 0.78
0.28–5.57
17 6 0
9.3 8.1 0
166 68 9
90.7 91.9 100
183 74 9
100 100 100
1.00 1.11 2.00
4 11 4 4
4.7 11.5 6.8 16.0
82 85 55 21
95.3 88.5 93.2 84
86 96 59 25
100 100 100 100
2.47 1.00 1.66 0.64
0 15 8
0 8.2 10.7
8 168 67
100 91.8 89.3
8 183 75
100 100 100
1.56 1.00 0.73
1 3 3 16
11.1 20.0 6.4 8.2
8 12 44 179
88.9 80.0 93.6 91.8
9 15 47 195
100 100 100 100
0.52 0.33 1.17 1.00
0.09–5.42 0.10–1.34 0.37–4.64
5 9 9
9.1 9.1 8.0
50 90 103
90.9 90.9 92.0
55 99 112
100 100 100
0.84 0.87 1.00
0.28–2.72 0.33–2.29
3 8 0 11 0 0 0 1
5.4 19.5 0 8.0 0 0 0 8.3
53 33 7 126 7 5 1 11
94.6 80.5 100 92.0 100 100 100 91.7
56 41 7 137 7 5 1 12
100 100 100 100 100 100 100 100
1.39 0.36 1.36 1.00 1.36 1.00 0.27 0.70
0.42–5.69 0.14–0.96∗ 0.09–21.21 0.09–21.21 0.07–15.04 0.0022–∞ 0.12–7.49
15 8 0 0 0
8.0 11.9 0 0 0
173 59 8 1 2
92.0 88.1 100 100 100
188 67 8 1 2
100 100 100 100 100
1.00 0.63 1.52 0.27 0.45
0.26–1.58 0.10–23.49 0.0022–∞ 0.0157–∞
2 21
22.2 8.2
7 236
77.8 91.8
9 257
100 100
0.27 1.00
0.07–1.46
1 22
4.3 9.1
22 221
95.7 90.9
23 243
100 100
1.52 1.00
0.29–16.31
4 19
9.8 8.4
37 206
90.2 91.6
41 225
100 100
1.27 1.00
0.38–3.60
GA, gestational age; BMI, body mass index; ∞, infinity. ∗Significant association.
0.53–6.44 0.06–10.58
0.44–3.05 0.13–31.00 0.82–8.61 0.54–5.82 0.20–2.30 0.10–24.19 0.30–1.84
Downloaded by [New York University] at 04:15 02 September 2015
28
J. O. Awoleke et al.
B-rhesus-positive significantly predicts the likelihood of having AB during pregnancy. The prevalence of AB obtained in our study correlates well with most observational studies around the world (Abdullah and Al-Moslih 2005; Fatima and Ishrat 2006; Sharma and Thapa 2007), with few studies reporting much higher rates (Akerele et al. 2001; Kehinde et al. 2011). Discrepancy in prevalence can be attributed to differences in study methodology and location. The role of host factor in predicting acquisition of AB in pregnancy has been a subject of controversy in the literature (Thurman et al. 2006; Sharma and Thapa 2007). Effects of sociodemographic and obstetrics characteristics, such as age, race, social status, parity, etc. on AB during pregnancy are less clear, owing to a lack of consistency in study findings (Schnarr and Smaill 2008). However, it is recognised that environment and clinical setting may influence identified predictors and therefore must be borne in mind when interpreting results. The identification of blood group B-rhesus-positive as a predictor of AB in pregnancy in our environment is a novel finding. It may be because most previous local studies have not considered this factor in their analysis. Therefore, they have missed this predictor over time. Age did not influence the occurrence of AB, even though high preponderance of the condition was found among the age group 25–34, which is consistent with the observation by Awonuga et al. (2010). We observed that occupation had no impact in predicting AB in pregnancy, and, contrary to reports that lower education is associated with increased incidence of AB (Faro and Fenner 1998), diagnosis of the condition was higher in those with tertiary education. Our finding suggests that higher education may not necessarily translate to better hygienic behaviour. Similar to earlier findings by Awonuga et al. (2010), AB was commoner among low parity women, though it was not statistically significant. It negates an earlier assertion by Patterson and Andriole (2003) that AB in pregnancy increases with parity. Although some have reported a high incidence of AB among patients with sickle cell traits (Baill and Witter 1990), our observation was contrary to this. Instead, it is in tandem with a retrospective study by Thurman et al. (2006), which found that sickle cell trait does not increase the prevalence of AB when compared with control patients. Those who were positive for human immunodeficiency virus (HIV) infection, hepatitis B and/or glucose tolerance screening were also not more predisposed to AB in this study. Routine screening for AB in pregnancy is a recognised standard of obstetrics practice and most regulating bodies recommend it (Nicolle et al. 2005). But, the overall cost implication has made adherence difficult in developing world; our environment not being an exception. In view of this, some authors have suggested that a designed screening algorithm, which incorporates identified risk factors may be cost-effective, while still maintaining optimal maternal and neonatal outcome (Smaill 2007). Based on our research findings, a subset of pregnant women who are of blood group B-rhesus-positive, within the ages of 25–34 years, of low parity and higher education, will best fit into the criteria of the screening algorithm. Escherichia coli, the commonest isolate in our urine cultures, is known to be the most common aetiological agent in AB (Abdullah and Al-Moslih 2005; Smaill 2007). As equally found by our study, Staphylococcus aureus is becoming a prominent urine culture isolate in Nigeria (Amadi et al. 2007; Awonuga et al. 2010; Imade et al. 2010). Antibiotics sensitivity to the
cultured microorganisms shows local peculiarity when compared with studies from other parts of Nigeria (Oyetunji et al. 2006; Imade et al. 2010). This invariably supports the need for regional guidelines. Our research is not without limitation. Pre-pregnancy urinary tract infection (UTI) and antepartum UTI prior to commencement of prenatal care were not considered as likely predictors during the conduct of the study. Future research on this subject in our locality should put these into consideration. In conclusion, blood group B-rhesus-positive predicts development of AB in pregnancy in our environment. AB was also found to be commoner among patients who are in the age range of 25–34 years, with low parity and higher education. These features could form guidelines for a screening algorithm. A larger multi-centre study to further validate this observation is suggested. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References Abdullah AA, Al-Moslih MI. 2005. Prevalence of asymptomatic bacteriuria in pregnant women in Sharjah, United Arab Emirates. Eastern Mediterranean Health Journal 11:1045–1052. Akerele J, Abhulimen P, Okonofua F. 2001. Prevalence of asymptomatic bacteriuria among pregnant women in Benin City, Nigeria. Journal of Obstetrics and Gynaecology 21:141–144. Amadi ES, Enemuo OB, Uneke CJ, Nwosu OK, Onyeagba RA, Ugbogu OC. 2007. Asymptomatic bacteriuria among pregnant women in Abakaliki, Ebonyi State, Nigeria. Journal of Medical Sciences 7:698–700. American Diabetes Association. 2009. Diagnosis and classification of diabetes mellitus. Diabetes Care 32:S62–S67. Awolude OA, Adesina OA, Oladokun A, Mutiu WB, Adewole IF. 2010. Asymptomatic bacteriuria among HIV positive pregnant women. Virulence 1:130–133. Awonuga DA, Fawole AO, Dada-Adegbola HA, Olola FA, Awonuga OM. 2010. Predictors of asymptomatic bacteriuria among obstetric population in Ibadan. Nigerian Medical Journal 19:188–193. Baill IC, Witter FR. 1990. Sickle trait and its association with birthweight and urinary tract infections in pregnancy. International Journal of Gynecology and Obstetrics 33:19–21. Enayat K, Fariba F, Bahram N. 2008. Asymptomatic bacteriuria among pregnant women referred to outpatient clinics in Sanandaj, Iran. International Brazilian Journal of Urology 34:699–707. Faro S, Fenner DE. 1998. Urinary tract infections. Clinical Obstetrics and Gynecology 41:744–754. Fatima N, Ishrat S. 2006. Frequency and risk factors of asymptomatic bacteriuria during pregnancy. Journal of the College of Physicians and Surgeons, Pakistan 16:273–275. Imade PE, Izekor PE, Eghafona NO, Enabulele OI, Ophori E. 2010. Asymptomatic bacteriuria among pregnant women. North American Journal of Medical Sciences 2:263–266. Kehinde OK, Adedapo KS, Aimaikhu CO, Odukogbe AA, Olayemi O, Salako B. 2011. Significant bacteriuria among asymptomatic antenatal clinic attendees in Ibadan, Nigeria. Tropical Medicine and Health 39: 73–76. Naber KG, Bergman B, Bishop MC, Bjerklund-Johansen TE, Botto H, Lobel B et al. 2001. EAU guidelines for the management of urinary and male genital tract infections. Urinary Tract Infection (UTI) Working Group of the Health Care Office (HCO) of the European Association of Urology (EAU). European Urology 40:576–588. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM. 2005. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clinical Infectious Diseases 440:643–654. Oyetunji JA, Ahmed Y, Nwobodo EI, Airede LR, Ekele BA. 2006. Asymptomatic bacteriuria in pregnancy in Sokoto, Nigeria. Sahel Medical Journal 9:1–6. Patterson TF, Andriole VT. 2003. Bacteriuria in pregnancy. Current Treatment Options in Infectious Diseases 5:81–87.
Predictors of asymptomatic bacteriuria among pregnant women in a low-resource setting 29
Downloaded by [New York University] at 04:15 02 September 2015
Romero R, Oyarzun E, Mazor M. 1989. Meta-analysis of the relationship between asymptomatic bacteriuria and preterm delivery/low birth weight. Obstetrics and Gynecology 73:576–582. Schnarr J, Smaill F. 2008. Asymptomatic bacteriuria and symptomatic urinary tract infection in pregnancy. European Journal of Clinical Investigation 38(Suppl 2):50–57. Sharma P, Thapa L. 2007. Acute pyelonephritis in pregnancy: a retrospective study. Australian and New Zealand Journal of Obstetrics and Gynaecology 47:313–315.
Smaill F. 2007. Asymptomatic bacteriuria in pregnancy. Best Practice and Research. Clinical Obstetrics and Gynaecology 21:439–450. Thurman AR, Steed LL, Hulsey T, Soper DE. 2006. Bacteriuria in pregnant women with sickle cell trait. American Journal of Obstetrics and Gynecology 194:1366–1370. US Preventative Services Task Force. 2008. Screening for asymptomatic bacteriuria: U.S. Preventative Services Task Force reaffirmation recommendation statement. Annals of Internal Medicine 149:43–47. Whalley P. 1967. Bacteriuria of pregnancy. American Journal of Obstetrics and Gynecology 97:723–738.
