|Year : 2017 | Volume
| Issue : 3 | Page : 79-86
Risk factors for Group B streptococcal infection among women attending antenatal clinic in a tertiary health institution in Edo State, Nigeria
Sunday Yerumoh1, Innocent O Alenoghena2, Peter Isabu3, Gbolagade Adewusi4
1 Department of Primary Health Care, Akoko-Edo Local Government Council, Irrua, Edo State, Nigeria
2 Department of Primary Health Care, Owan East Local Government Council, Irrua, Edo State, Nigeria
3 Department of Obstetrics and Gynaecology, Irrua Specialist Teaching Hospital, Irrua, Edo State, Nigeria
4 Department of Micobiology, Irrua Specialist Teaching Hospital, Irrua, Edo State, Nigeria
|Date of Web Publication||2-Apr-2018|
Innocent O Alenoghena
Department of Primary Health Care, Owan East Local Government Council, Edo State
Source of Support: None, Conflict of Interest: None
Introduction: Group B Streptococcus (GBS) colonisation of the anus, rectum and/or vagina in pregnant women is a known risk factor for GBS neonatal infection with high morbidity and mortality as a result of pneumonia and septicaemia mainly and less commonly from meningitis, bone and joint infections, cellulitis, otitis media, conjunctivitis, pleural empyema, peritonitis, endocarditis and deep abscess.
Objectives: The aim of this study was to assess the proportion women with risk factors for Group B streptococcal infection and the association between the risk factors and recto-vaginal colonisation with GBS among women attending antenatal clinic.
Materials and Methods: A cross-sectional study was conducted in Irrua specialist Teaching Hospital, South-South geo-political zone of Nigeria. A total population study was conducted among 234 pregnant women who attained 35–37 weeks gestation, and those who were admitted for preterm labour at earlier gestations were involved in the study. An interviewer-administered questionnaire was used for data collection. Data were analysed using the Statistical Package for the Social Sciences version 17.0 software (SPSS Inc., Chicago, IL, United States).
Results: A total of 234 respondents were assessed in this study. Most respondents had tertiary education (53.4%). The risk factors for GBS were present in the following proportions: not living with their partners, 21.8%, previous miscarriage(s) 10.7% and multiple pregnancies, 5.6%. Other risk factors included previous preterm births, 7.7%, and preterm rupture of membranes. There was a statistically significant (P = 0.001) association between respondents’ history of previous miscarriages and GBS colonisation. There was no statistically significant association between GBS colonisation and diabetes mellitus (P = 1.000), multiple sexual partners (P = 0.425), rupture of membranes >18 (P = 0.623) and preterm labour (P = 1.000).
Conclusion: The proportion of clients with risk factors for GBS colonisation was moderate (compared with other sub-Saharan countries). Identified risk factors in favour of the higher rates of GBS colonisation included frequent sexual intercourse while previous miscarriage, previous preterm birth, diabetes in pregnancy, where associated with lower rates of colonisation. There was a statistically significant relationship between the GBS status and a history of previous miscarriage (P = 0.001) and a history of previous preterm birth (P = 0.229). Guidelines on the prevention and management of GBS infection for clients attending antenatal clinics and delivery should be made available at all levels of care by regulatory agencies in Nigeria. There should be health education at all levels of care by the Federal, State and Local Government on preventing of and control GBS infection, especially at the community level.
Keywords: Group B streptococcal colonisation, pregnant women, risk factors, South geo-political zone
|How to cite this article:|
Yerumoh S, Alenoghena IO, Isabu P, Adewusi G. Risk factors for Group B streptococcal infection among women attending antenatal clinic in a tertiary health institution in Edo State, Nigeria. Sub-Saharan Afr J Med 2017;4:79-86
|How to cite this URL:|
Yerumoh S, Alenoghena IO, Isabu P, Adewusi G. Risk factors for Group B streptococcal infection among women attending antenatal clinic in a tertiary health institution in Edo State, Nigeria. Sub-Saharan Afr J Med [serial online] 2017 [cited 2023 Jan 28];4:79-86. Available from: https://www.ssajm.org/text.asp?2017/4/3/79/228976
| Introduction|| |
Streptococcus is a genus of spherical, gram-positive bacteria of the phylum Firmicutes. Streptococcus agalactiae is characterised by the presence of Group B Lancefield antigen, and so takes the name Group B Streptococcus (GBS). GBS colonisation of the anus, rectum and/or vagina in pregnant women is a known risk factor for GBS neonatal infection with high morbidity and mortality as a result of pneumonia and septicaemia mainly,,, and less commonly from meningitis, bone and joint infections, cellulitis, otitis media, conjunctivitis, pleural empyema, peritonitis, endocarditis and deep abscess.,,,,
In the pregnant woman, it can cause preterm labour, premature rupture of membranes, chorioamnionitis, urinary tract infection, postpartum wound infection, postpartum endometritis and meningitis. GBS can cause serious illness and even death in new born, the elderly, in the immunocompromised and also in pregnant women.,,,,,,,,,,, It is a leading cause of septicaemia, meningitis and pneumonia in neonates in the developed countries. However, information on the prevalence in the developing countries is lacking,, including Nigeria.
Risk factors for maternal colonisation by the organism include the use of an intrauterine contraceptive device and age younger than 20 years. Heavy colonisation occurs in women with asymptomatic GBS bacteriuria, African-American women and diabetes mellitus.,,, Significantly lower rates have been reported in women who are sexually inexperienced, older than 20 years or multiparous. In a study, Vaginal Infection and Preterm Study, GBS was shown to be more common among older women, women of low parity and those with extreme sexual activities (frequent intercourse and multiple sexual partners in the previous year) but less common in women living with their partners, currently smoking and in women with more education. However, pregnancy itself does not influence the prevalence of colonisation. Risk factors for GBS bacteraemia unrelated to pregnancy include the elderly age group, black race and underlying invasive diseases namely diabetes mellitus, liver disease and or history of alcohol abuse, neurological impairment (including seizure disorder), malignancy, cardiovascular diseases, pulmonary diseases, urological diseases, peripheral vascular diseases, human immunodeficiency virus infection, functional or surgical splenectomy, etc.,,,,,,, Reported case-fatality in non-pregnant adult was previously 8–70%,, but now 21–34%,,,,, which may be related to an increase in chronic diseases namely diabetes, breast cancer, liver cirrhosis, neurogenic bladder disease, etc., which invariably complicates the condition.,
The aim of this study was to assess the proportion of women with risk factors for Group B streptococcal infection and determine the association between the risk factors and recto-vaginal colonisation with GBS among women attending antenatal clinic in Irrua Specialist Teaching Hospital, Irrua, Edo State, Nigeria.
| Materials and methods|| |
This descriptive, cross-sectional study was conducted in Irrua specialist Teaching Hospital, South-South geo-political zone of Nigeria. The hospital mainly serves the Central and Northern Senatorial Districts of Edo State. It also receives patients from the neighbouring states of Delta, Kogi and Ondo. The Department of Obstetrics and Gynecology is particularly busy with clients for antenatal care because of its full complements of specialist and its capacity to handle numerous conditions in pregnancy.
The estimated sample size for the survey was 234, using the formula: nf = n/[1 + (n/N)], where nf = desired sample size when population is <10,000; n = the desired sample size when population is more than 10,000; N = the estimated population size. And reported colonisation rates ranging from 5 to 40% (with an average of 20%).
The study population included all pregnant women attending antenatal clinic in Irrua Specialist Teaching Hospital, Irrua, between January and June 2015, who attained 35–37 weeks gestation, and those who were admitted for preterm labour at earlier gestations. They were enlisted in the order of arrival, until the desired sample size was achieved. Pregnant women who were on antibiotic intervention within this period were, however, excluded from the study population.
Data were collected using an interviewer-administered questionnaire.
Swabs were taken from both the lower one-third of the vagina and the anal region using sterile cotton swabs. No antiseptic preparation on the perineum or vulva was used before swabbing. These were inoculated directly into Todd Hewitt Broth (Oxoid Ltd.) and transported to the microbiology laboratory of the hospital for processing.
Specimen culture isolation and identification and microscopy
The collected swabs were cultured individually using selective Todd–Hewitt broth supplemented with gentamicin (10 μg/ml) and nalidixic acid (15 μg/ml). The inoculated selective medium was incubated for 18–24 h and then subcultured onto sheep blood agar. If GBS was not identified after the incubation of 18–24 h, the blood agar plate was re-incubated and examined at 48 h to identify suspected organisms. Presumptive identification of GBS was made by traditional physiological and biochemical methods. These included Gram stain, catalase reaction, hemolytic activity on sheep blood agar plates, hippurate and “Christie-Atkins-Munch-Petersen” test. Antimicrobial susceptibility of all GBS isolates was determined by Kirby–Bauer disc diffusion method.
Test for bacteriuria and glucose screening
This was followed for all clients registering for antenatal care at the institution. It is routinely conducted during the first visit. It involves collection of clean catch midstream urine into a sterile universal container. Microscopy, culture and sensitivity tests are then conducted on the urine sample and its isolates for presence of bacteria.
Routine glucose screening is also conducted among clients attending antenatal clinic between 24 and 48 weeks to check for gestational diabetes.
Pre-testing was conducted before the main study to ensure adherence to the protocol for the isolation of GBS and for improved validity of the questionnaire. The samples were then collected in triplicates, and the results cross-checked daily by the principal investigator.
Data analysis was conducted with the use of the Statistical Package for the Social Sciences (SPSS) version 17.0 software (SPSS Inc., Chicago, IL, United States). Chi square statistical test of significance was used to test for associations between socio-demographic variables and GBS colonisation. Microsoft Office Excel 2007 was used to construct bar chart. Statistical significance was set at P < 0.05.
Approval for the study was obtained from the Ethical Committee of the Irrua Specialist Teaching Hospital, and written informed consent was obtained from the respondents before participating in the study.
| Results|| |
[Table 1] shows the socio-demographic variables among the respondents. The respondents were mainly in the 26–30 and 31–35 years age groups (47.4 and 34.6%), respectively. Mean age of respondents was 30.11 ± 3.9 years. Most respondents had tertiary education (53.4%). The majority of the respondents were of Esan ethnic group (72.6%). Most presented were in labour at term (86.7%); mean gestational age at delivery was 37.6 ± 1.6 weeks.
[Table 2] shows the distribution of risk factors for GBS among respondents. Among the respondents, 21.8% were not living with their partners, 10.7% had previous miscarriage(s), and 5.6% had multiple pregnancies. None of the respondents were a smoker, had GBS bacteriuria or had a previous baby affected by GBS. On presentation in labour, 7.7% had previous preterm birth, 5.6% had duration of rupture of membranes longer than 18 h, and 5.1% had intrapartum fever >38°C.
[Figure 1] shows the distribution of respondents based on parity. Among the respondents, 37% were nulliparae, 31% were primiparae, 11% were para 2, 5% were para 3, 10% were para 4 whereas 3% were para 5 and 6 each.
[Table 3] shows the GBS test results among respondents. The majority of the respondents tested negative to GBS (90.2%) whereas the others (9.8%) were positive. Among the respondents with positive results, 65.2% had positive test results from both the rectum and vagina, whereas 21.7% had positive vaginal test result only, and 13.1% had positive rectal test result only for GBS. Vaginal colonisation rate was, therefore, 8.5%, and rectal colonisation rate was 7.7% among the respondents.
[Table 4] shows the socio-demographic characteristics of respondents and their GBS colonisation status. The largest proportion of respondents with GBS colonisation was in the 26–30 years age group (11.7%) whereas there were none in ages ≤20 years. From Fisher’s exact test (P = 0.917), there was no statistically significant association between the age of respondents and their GBS status. Para 0 women had the highest proportion of GBS colonisation (14%) followed by para 1 (13.7%) and para 4 (4.2%). There were none among women with 2, 3, 5 and 6 parity. From Fisher’s exact test (P = 0.229), there was no statistically significant association between the parity of respondents and their GBS status. Patients with tertiary education had the highest rate of colonisation (10.4%) followed by secondary (9.3%) and lastly primary education (8.3%). From Fisher’s exact test (P = 0.932), there was no statistically significant association between the level of education of respondents and their GBS status.
|Table 4: Socio-demographic characteristics of respondents and their GBS colonisation status|
Click here to view
[Table 5] shows the presence of clinical risk factors for GBS colonisation among respondents and their GBS colonisation status. Among respondents with previous miscarriage, 4% had GBS colonisation whereas 20% of those with no previous miscarriage had GBS colonisation. There was a statistically significant (P = 0.001) association between respondents’ history of previous miscarriages and GBS colonisation. Among respondents with a positive history of preterm birth, there was no positive test result, 0 (0%). Twenty-three (10.6%) of those without any history of preterm birth had positive GBS test. Record based on blood sugar revealed that 23 (9.9%) of those without diabetes had positive GBS colonisation. In addition, respondents with positive GBS test results all had no multiple pregnancy, and this made up 10.4% of respondents with no multiple pregnancy. Among respondents who do not reside with their partners, 5.9% had GBS colonisation whereas 10.9% of those who do reside with their partners had GBS colonisation. No respondent with multiple sexual partners in the last 1 year had GBS colonisation whereas 9.9% of those who have not had multiple sexual partners had GBS colonisation. Among respondents with preterm labour, 9.7% had GBS colonisation whereas 9.9% of those not in preterm labours had GBS colonisation. None of those with rupture of membranes for >18 h had colonisation while 10.4% of those without 18 h rupture of membranes had colonisation. Among respondents with fever >38°C, 8.3% had colonisation whereas 9.9% of those without fever >38°C had colonisation. However, there was no statistically significant association between the presence of these risk factors for GBS colonisation in the respondents and their GBS status.
|Table 5: Presence of risk factors for GBS colonisation among respondents and their GBS colonisation status|
Click here to view
| Discussion|| |
GBS colonisation in pregnancy is important because of the maternal morbidities, perinatal morbidities and mortality associated with invasive disease from the organism.
The respondents were mainly aged 26–35 years (82%). This may be because this is the age range most women of reproductive age get married and produce a family. Over half of the respondents had at tertiary education. This was not surprising, as most women with better education were more likely to have better jobs and attend antenatal care at the tertiary institutions. Conversely, the less educated women were more likely to seek care at State and Local Government facilities, which often provided antenatal care services at a relatively cheaper cost. The respondents were mainly Esan (72.6%) with Bini, Etsako, Owan, Igbo and Yoruba forming a smaller proportion. This may be because of the location of the facility which is in Esanland and is convenient for those around to attend. In addition, the University of Benin Teaching Hospital, a major federal tertiary institution is in Benin City and so the Binis, who form the major ethnic group in Edo State, are more likely to patronise this due to proximity. The respondents fell mainly into 37, 38 and 39 gestational weeks. This was not surprising as most deliveries take place at term, and this study was completed about the period when each woman presented in labour, at which time the intrapartum risk factors were assessed, and the parturients who had tested positive on GBS culture (followed by antimicrobial susceptibility test) were given antibiotics in labour. This is the practice at the centre and is based on CDC 2002 guideline.
The prevalence rate from this study was 9.8%. This is similar to the findings in a recent study conducted in North-eastern Nigeria (9.8%), in which only vaginal specimens were taken. This is, however, lower than recent reports from Ife (11.3%, using only vaginal samples), Nsukka (18%, using both vaginal and rectal specimens), Zimbabwe (31.6%), Tanzania (23%), the sub-Saharan average of 19%, Iran (12.44%), Middle East and North Africa (22%), Central and South America (14%), UK (15–28%) and the US (26%). However, it is higher than the prevalence reported from Ibadan (1.8%) and India (2.33%). These reported differences in prevalence have been attributed to socio-economic factors, age, parity, gestational age, obstetrics history, culture techniques, sampling procedures, geographical location, studied population, isolation techniques, racial and genetic factors environmental factors such as hygiene and nutrition.,,
In this study, review of previously reported factors that determined the prevalence of colonisation showed the highest colonisation rate was among women aged 26–30 years (11.7%) with younger women showing lower colonisation rates with no colonisation found in women under 20 years. This is, however, not statistically significant. This finding is similar to the finding in North-eastern Nigeria where the highest prevalence was in the 20–29 years age group (3.8%) and least in the 10–19 years (0.8%). It is also similar to finding in Ife (12.79% for age ≥30 years and 9.38% in women 18–29 years) but differ from findings in Nsukka where higher rates were reported for respondents at both extremes of age (19.05% for 15–20 years and 21.05% for the 32–45 years groups)., The Tanzanian study reported similar pattern as the findings in this study: 32% in the 30–34 years and 15.4% in women <20 years of age). Though these studies all showed that age did not necessarily be significant, younger age has, however, been reported as a risk factor for GBS colonisation. In contrast to the findings on culture in this study, the presence of one or more obstetric risk factors was highest among respondents aged <20 years (100%). This was also not statistically significant.
GBS colonisation was found in this study to be higher among women of low parity: 14 and 13.7% for nulliparous and primiparous women, respectively, but this did not reach statistical significance. This is similar to the findings from the Vaginal Infection and Preterm Study wherein GBS was shown to be more common in women of low parity. It is, however, different from the findings in North-eastern Nigeria (where 12 of 13 GBS isolates were from multiparous women), from the Tanzanian study (where colonisation occurred in 50% of multiparous women and 19.8% of primiparous women) and from the Indian study where it was more frequent in multigravid women.,, Among women in Nsukka, intermediate parities were found with more colonisation (25.53 and 21.74% for para 2 and para 3 women, respectively). The variation within various parity groups has been explained on the basis of the differences in hygiene status of different populations. However, more frequent sexual intercourse among women of lower parity may be an explanation for the variation. In contrast to the findings on culture in this study, the presence of one or more obstetric risk factors was higher in women of intermediate parity, 38.5 and 34.6% for para 2 and para 3 respondents, respectively. This was also not statistically significant.
A progressive increase in GBS colonisation rate with increasing level of education was found among the respondents, though not statistically significant: 8.3, 9.3 and 10.4% for the respondents with primary, secondary and tertiary levels of education, respectively. This trend is similar to the findings from North-eastern Nigeria but different from previous reports from the Vaginal Infection and Preterm Study group (colonisation less common among women with more education) and the Tanzanian study (where the incidence was highest among those with no formal education − 34.8%). Having multiple sexual partners may be a reason for the higher rates among women with higher educational levels since they will more likely defer marriage till later because of their educational pursuits. In contrast to the findings on culture in this study, the presence of one or more obstetric risk factors was similar and higher in respondents with primary and tertiary (83.3 and 83.2%, respectively). This was also not statistically significant.
Assessment of antenatal risk factors among respondents showed a higher rate of colonisation in women having frequent sexual intercourse while those with the following risk factors have lower rates of colonisation than those without the risk factors: previous miscarriage, previous preterm birth and diabetes in pregnancy, multiple pregnancy, not cohabiting with partners and having multiple sexual partners. However, these did not reach statistical significance, except for the history of previous miscarriages. Previous reports have shown all these to be risk factors for GBS colonisation.,,,, The finding in this study of lower GBS colonisation rate among respondents with previous preterm delivery was similarly reported in Tanzania, but the study in North-eastern Nigeria found otherwise., A possible explanation for this difference is that the North-eastern Nigerian study only sampled the vagina for GBS colonisation, excluding the rectum and anus. The finding that not living with partner was associated with lower GBS colonisation among respondents is different from previous report in the Vaginal Infection and Preterm Study. Diabetes in the respondents was associated with lower rate of colonisation unlike the report from Iran. Also the finding of a higher colonisation rate in respondents reporting frequent sexual intercourse is similar to the findings in the Vaginal Infection and Preterm Study but different from a study among college women., This study also showed that women with multiple partners in the last 1 year had lower rates of colonisation than those with single partners. This finding is different from the Vaginal Infection and Preterm Study and the study among college women., Though having a previous GBS affected baby and GBS bacteriuria are known risk factors for colonisation, these were not found among the respondents. This is not surprising as GBS is not routinely tested in laboratories in this area, and so will not be specifically reported from cultures. Tobacco smoking has been reported to be protective against GBS colonisation, but none of the respondents in this study engaged in tobacco smoking.
| Conclusion|| |
The proportion of respondents with risk factors for GBS infection was moderate compared to most countries in sub-Saharan Africa. Identified risk factors in favour of higher rates of GBS colonisation included frequent sexual intercourse while previous miscarriage, previous preterm birth, diabetes in pregnancy, multiple pregnancy, not cohabiting with partners and having multiple sexual partners where associated with lower rates of colonisation.
The association between the risk factors for GBS colonisation and the respondents’ actual GBS status was relatively strong for those with a history of previous preterm birth (P = 0.229) and non-existent for history of multiple sexual partners (P = 1.000). In all, no statistically significant association was established.
Guidelines on prevention and management of GBS infection for clients attending antenatal clinics and delivery should be made available at all levels of care by regulatory agencies in Nigeria.
There should be health education at all levels of care by the Federal, State and Local Government on the prevention and control GBS infection, especially at the community level. These preventive measures should be made a part of the curriculums of various training institutions for health workers in Nigeria.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Maisey HC, Hensler M, Nizet V, Doran KS. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 2007;189:1464. PMID: 17041051.
Gillespie SH, Bamford KB. Streptococcal infection. Medical Microbiology and Infections at a Glance. Oxford: Blackwell Science Ltd.; 2000.
Kimberlin DW. Meningitis in the neonate. Curr Treat Options Neurol 2002;4:239-48.
Hwang YS, Sande MA. Obstetrics and gynecologic infections. In: Wilson WR, Sande MA, editors. Current Diagnosis and Treatment in Infectious Diseases. 1st
ed. McGraw-Hill/Appleton and Lange; 2001. p. 228-46.
Edwards MS, Baker CJ, Wagner ML, Taber LH, Barrett FF. An etiologic shift in infantile osteomyelitis: The emergence of the Group B Streptococcus. J Pediatr 1978;93:578-83.
Baker CJ, Edwards MS. Group B streptococcal infections. In: Remington JS, Klein JO, editors. Infectious Diseases of the Fetus and Newborn Infant. 4th
ed. Philadelphia: WB Saunders; 1995: p. 980-1054.
Infectious diseases. In: Cunningham FG, Leveno KJ, Bloom SL, Hauth JC, Rouse DJ, Spong CY, editors. Williams Obstetrics. 23rd
ed. McGraw-Hill Companies; 2010. p. 58.
Persson K, Christensen KK, Christensen P, Forsgren A, Jorgensen C, Persson PH. Asymptomatic bacteriuria during pregnancy with special reference to Group B streptococci. Scand J Infect Dis 1985;17:195-9.
Wood EG, Dillon HC. A prospective study of Group B streptococcal bacteriuria in pregnancy. Am J Obstet Gynecol 1981;140:515-20.
Pass MA, Gray BM, Dillon HC. Puerperal and perinatal infections with Group B streptococci. Am J Obstet Gynecol 1982;143:147-52.
Bobitt JR, Ledger WJ. Amniotic fluid analysis: its role in maternal and neonatal infection. Obstet Gynecol 1978;51:56-62.
Braun TI, Pinover W, Sih P. Group B Streptococcal meningitis in a pregnant woman before the onset of labor. Clin Infect Dis 1995;21:1042-3.
Yancey MK, Duff P, Clark P, Kurtzer T, Frentzen BH, Kubilis P. Peripartum infection associated with vaginal Group B Streptococcal colonization. Obstet Gynecol 1994;84:816-9.
Fox BC. Delayed-onset postpartum meningitis due to Group B streptococcus. Clin Infect Dis 1994;19:350. [Letter].
Aharoni A, Potasman I, Levitan Z, Golan D, Sharf M. Postpartum maternal Group B Streptococcal meningitis. Rev Infect Dis 1990;12:273-6.
Barbosa-Cesnik C, Schwartz K, Foxman B. Lactation mastitis. JAMA 2003;289:1609. PMID:12672715.
Berkowitz K, McCaffrey R. Postpartum osteomyelitis caused by Group B streptococcus. Am J Obstet Gynecol 1990;163:1200. PMID: 2220928.
Schrag S, Gorwitz R, Fultz-Butts K, Schuchat A. Prevention of perinatal Group B streptococcal disease. Revised guidelines from CDC. MMWR 2002;51:1-22.
Farley MM, Harvey C, Stull T, Smith JD, Schuchat A, Wenger JD et al.
A population-based assessment of invasive disease due to Group B Streptococcus in nonpregnant adults. NEJM 328; 1993:1807-11.
Joachim A, Matee MI, Massawe FA, Lyamuya EF. Maternal and neonatal colonisation of Group B Streptococcus at Muhimbili National Hospital in Dar es Salaam, Tanzania: prevalence, risk factors and antimicrobial resistance. BMC Public Health 2009;9:437.
Vaciloto E, Richtmann R, de Paula Fiod Costa H, Kusano EJ, de Almeida MF, Amaro ER. A survey of the incidence of neonatal sepsis by Group B Streptococcus during a decade in a Brazilian maternity hospital. Braz J Infect Dis 2002;6. ISSN 1413-8670.
Person K, Bjerre B, Elfstrom L, Forsgren A. A longitudinal study of Group B streptococcal carriage during late pregnancy. Scand J Infect Dis 1987;19:325-9.
Newton ER, Butler MC, Shain RN. Sexual behaviour and vaginal colonisation by Group B Streptococcus among minority women. Obstet Gynecol 1996;88:577-82.
Ramos E, Gaudier FL, Hearing LR, Del Valle GO, Jenkins S, Briones D. Group B Streptococcus colonization in pregnant diabetic women. Obstet Gynecol 1997;89:257-60.
Baker CJ, Goroff DK, Alpert S, Crockett VA, Zinner SH, Evrard JR et al.
Vaginal colonisation with Group B Streptococcus: A study in college women. J Infect Dis 1977;135:392-7.
Regan JA, Klebanoff MA, Nugent RP, Vaginal Infections and Prematurity Study Group. The epidemiology of Group B streptococcal colonization in pregnancy. Obstet Gynecol 1991;77:604-10.
Edwards MS, Baker CJ. Streptococcus agalactiae (Group B Streptococcus). Mandell, Douglas and Bennett’s Principle and Practice of Infectious Diseases. 5th
ed. Churchill Livingstone; 2000. p. 2156-67.
Farley MM. Group B streptococcal infection in older patients. Drugs Aging 1995;6:293-300.
Opal SM, Cross A, Palmer M, Almazan R. Group B streptococcal sepsis in adults and infants. Contrast and comparisons. Arch Intern Med 1988;148:641-5.
Gallagher PG, Watanakunakorn C. Group B streptococcal bacteremia in a community teaching hospital. Am J Med 1985;78:795-800.
Verghese A, Mireault K, Arbeit RD. Group B streptococcal bacteremia in men. Rev Infect Dis 1986;8:912-7.
Lerner PI, Gopalakrishna KV, Wolinsky E, McHenry MC, Tan JS, Rosenthal M. Group B Streptococcus (S. agalactiae
) bacteremia in adults: Analysis of 32 cases and review of literature. Medicine (Baltimore) 1977;56:457-73.
Schwartz B, Schuchat A, Oxtoby MJ, Cochi SL, Hightower A, Broome CV. Invasive Group B streptococcal disease in adults. A population-based study in metropolitan Atlanta. JAMA 1991;266:1112-4.
Muñoz P, Llancaqueo A, Rodríguez-Créixems M, Peláez T, Martin L, Bouza E. Group B Streptococcus bacteremia in nonpregnant adults. Arch Intern Med 1997;157:213-6.
Bayer AS, Chow AW, Anthony BF, Guze LB. Serious infections in adults due to Group B streptococci. Clinical and serotypic characterization. Am J Med 1976;61:498-503.
Colford JM, Mohle-Boetani J, Vosti KL. Group B streptococcal bacteremia in adults: Five years’ experience and a review of the literature. Medicine 1995;74:176-90.
Roberts FJ. Group A and Group B beta-hemolytic streptococcal bacteremia. Rev Infect Dis 1988;10:228-9.
Araoye MO. Research Methodology With Statistics for Health and Social Sciences. Ilorin: Nathadex Publishers; 2003. p. 115-21, 201-8.
Okon KO, Usman H, Umar Z, Balogun ST. Prevalence of Group B Streptococcus (GBS) colonization among pregnant women attending antenatal clinic of a tertiary hospital in northeastern Nigeria. Am J Res Commun 2013;1:54-66.
Onipede A, Adefusi O, Adeyemi A, Adejuyigbe E, Oyelese A, Ogunniyi T. Group B Streptococcus carriage during late pregnancy in Ile-Ife, Nigeria. Afr J Clin Exp Microbiol 2012;13:135-43.
Ezeonu IM, Agbo MC. Incidence and anti-microbial resistance profile of Group B Streptococcus (GBS) infection in pregnant women in Nsukka, Enugu State, Nigeria. Afr J Microbiol Res 2014;8:91-5.
Gilbert R. Prenatal screening for Group B streptococcal infection: Gaps in the evidence. Int J Epidemiol 2003;33:2-8.
Moghaddam MN. Recto-vaginal colonization of Group B Streptococcus in pregnant women referred to a hospital in Iran and its effect on Lactobaccillus normal flora. J Biol Sci 2010;10:166-9.
Olanisebe SB, Adetosoye AL. Determination of asymptomatic carrier rate of beta-heamolytic Group B Streptococcus in vagina of pregnant women in Ibadan, Nigeria. Zent Blast Bakteriol Mikrobiol Hyg 1986;261;248-53.
Sharmila V, Joseph NM, Babu TA, Chaturvedula L, Sistla S. Genital tract Group B streptococcal colonization in pregnant women: A South Indian perspective. J Infect Dev Ctries 2011;5:592-5.
Baker CJ, Barrett FF, Gordon RC, Yow MD. Suppurative meningitis due to streptococci of Lancefield Group B: A study of 33 infants. J Pediatr 1973;82:724-9.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]