Jundishapur Journal of Microbiology
Jundishapur Journal of Microbiology

article information

Jundishapur Journal of Microbiology: Vol.13, issue 7; e102314
published online: September 27, 2020
article type: Systematic Review
received: March 9, 2020
revised: July 22, 2020
accepted: July 25, 2020
DOI: https://doi.org/10.5812/jjm.102314
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Distribution of Streptococcus agalactiae Among Iranian Women from 1992 to 2018: A Systematic Review and Meta-Analysis

authors:

avatar Maryam Sadeh ORCID 1 , avatar Amin Salehi-Abargouei ORCID 2 , avatar Nastaran Azartoos ORCID 3 , avatar Farzaneh Mirzaei ORCID 4 , avatar Mohammad Bagher Khalili ORCID 3 , *

Department of Laboratory Sciences, Faculty of Paramedical Sciences, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Nutrition and Food Security Research Center, Department of Nutrition, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Department of Microbiology, Faculty of Medicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Department of Parasitology, Faculty of Medicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

how to cite: Sadeh M, Salehi-Abargouei A, Azartoos N, Mirzaei F , Khalili M B. Distribution of Streptococcus agalactiae Among Iranian Women from 1992 to 2018: A Systematic Review and Meta-Analysis. Jundishapur J Microbiol. 2020;13(7):e102314. https://doi.org/10.5812/jjm.102314.

Abstract

Context:

Group B Streptococcus has the capacity of being colonized in the rectovaginal organ of women and causes infections in a mother and her fetus, thereby leading to neonatal diseases.

Evidence Acquisition:

The aim of this review was to summarize all of the relevant articles published to highlight the prevalence of group B Streptococcus colonization or infection in different regions of Iran. A systematic literature review was conducted by searching PubMed, Scopus, Web of Science (ISI), ScienceDirect, Google Scholar, and domestic databases for papers published in English or Persian from 1992 up to July 2019, concerning the prevalence of group B Streptococcus among Iranian women. All information regarding year, location of cases, frequency, author’s name, date of publication, participants, pregnancy period, sampling, and quality assessment were recorded. Summary effects were derived using the random effects model.

Results:

Among 61 suitable papers, data revealed that 36,807 cases of pregnant and non-pregnant women had been tested for group B Streptococcus during 1992-2018. Overall, 11.9% of pregnant and 5.3% of non-pregnant women were positive. Further results were as follows: vaginal, recto-vaginal, rectal, and endocervical colonization rates were 12.9%, 9.7%, 18.5%, and 3.7%, respectively. Group B Streptococcus incidence was the highest in Sanandaj (61.5%), and the lowest in Tabriz (1.8%).

Conclusions:

Although the prevalence distribution in Iran seems to be acceptable, more investigations are needed to represent the real incidence of group B Streptococcus around the country. In addition, a program with a standard lab technique is needed to screen pregnant women for further treatment before birth.

1. Context

As group B Streptococcus is a pathogen commonly found in rectovaginal mucosa of pregnant women, it appears reasonable to label this bacterium as a cause of neonatal diseases at birth (1). Several investigations have revealed that about 10 - 40% of healthy women carry group B Streptococcus in their vagina and/or rectum. Much as the bacterium threatens the fetus in pregnant women, it can also induce infection of the endometrium or amniotic membrane, bacteremia, as well as sepsis and meningitis in susceptible women (2, 3). Since 1970, the etiological role of group B Streptococcus in diseases was highlighted, especially with regard to its ability to cause newborn infections. Recently, two kinds of infantile diseases have been attributed to group B Streptococcus; early-onset diseases and late-onset diseases. The early-onset diseases are usually manifested during the first week after birth, while late-onset diseases may appear 2 - 3 months after birth. Pneumonia and sepsis are both attributed to early-onset diseases; however, late-onset diseases likely engender meningitis in newborn infants.

Albeit different structures have been identified as group B Streptococcus virulence factors, a polysaccharide capsule is known to carry the most important role in this regard (4). It has antiphagocytic function. Other virulence factors include secreted hemolysin, superoxide dismutase, D-alanylated lipoteichoic acid, and some of the surface proteins such as the surface-localized protease CspA. Although surface proteins of Streptococcus agalactiae may have considerable roles during various stages of infection, they attract more and more importance regarding the development of a vaccine. Adhesion to epithelial cells, interactions with human extracellular matrix or plasma proteins, and escape from host immunity are other possible roles of surface proteins of group B Streptococcus (5).

Based on the proportion of cps, group B Streptococcus has been classified into 10 serotypes; Ia, Ib, and II-IX (1, 6). The prevalence rate of group B Streptococcus infections in both pregnant and non-pregnant women varies widely depending on the population studied; however, group B Streptococcus is usually isolated from 10% - 30% of women. In Iran, an estimated average of 9.8% of women is rectovaginally infected; however, the colonization rate of their neonates at birth is not clearly known (7). Some authors believe that about 50 - 75% of infants are exposed to the organism during the birth process (8-10). The major infant’s diseases are attributed to meningitis and septicemia (11, 12). Furthermore, transmission of group B Streptococcus infection to infants at the time of birth, other group B Streptococcus-related infection complications, including premature rupture of membrane, low birth weight, and preterm labor may develop during pregnancy (13).

2. Evidence Acquisition

In the present study, almost all of the literature published from 1992 to July 2019 were reviewed to determine the prevalence of group B Streptococcus carrier state in different regions of Iran. In addition, this study shows the relative frequency of group B Streptococcus positivity with respect to geographical area, date of sampling, and type of the swab specimen.

2.1. Search Strategy

The strategy employed for identifying group B Streptococcus prevalence was searching in PubMed, Scopus, Web of Science (ISI), ScienceDirect, Google Scholar, and domestic databases for papers published in English or Persian. Terms such as S. agalactiae, group B Streptococcus, S. agalactiae, Streptococcus group B, and Iran were used as keywords to find the relevant published works. In order to find the maximum number of related papers and also gray literature, three local search engines, including the Iranian Scientific Information Database (www.sid.ir), Medlib (www.medlib.ir), and Magiran (www.magiran.com) were used. No limitations were applied when searching the mentioned databases. Extracted references were all reviewed, and the irrelevant titles/abstracts were excluded from the collection. The study selection process was handled by three researchers (MS, AS, NA). To reach a consensus on the selection of the relevant articles, any disagreement was discussed by the team members.

2.2. Inclusion Criteria

The following publications were identified as eligible to be included in the present systematic review and meta-analysis:

A) Investigations assessing the prevalence of S. agalactiae in the Iranian women,

B) Group B Streptococcus sampling from the vaginal, rectovaginal, endocervical, and rectal regions as well as the urine, and

C) Using culturing and/or PCR method as techniques applied for the detection of group B Streptococcus.

2.3. Exclusion Criteria

Studies were excluded if:

A) They had failed to use a standard method for group B Streptococcus isolation,

B) They had an irrelevant source of sampling (from men, animal, etc.),

C) They were review, meta-analysis or systematic review, or a duplicate publication of the same study.

2.4. Data Collection

Two authors conducted the data extraction, and the following information was collected: The first author’s name and the date of publication, the participants’ status, including the pregnancy period, geographic location, group B Streptococcus isolation, and finally, the number of group B Streptococcus carriers were all noted for further investigation. Any disagreement as for data collection was discussed by the colleagues to reach the final decision (Figure 1).

Flow diagram of the study process
Flow diagram of the study process
Figure 1.

Flow diagram of the study process

2.5. Quality Assessment

In this study, a checklist recommended by Hoy et al. (14) was used for the evaluation of the methodological quality. The checklist consisted of nine questions, representing the sampling-related information, technique of sampling, the response rate, the technique applied for data collection, tools for measurement, definition of cases, and the statistical method. Each question was scored 1 or 0, defined as low- or high-risk bias, respectively. Scores 0 to 9 were selected and defined as follows: 0 to 3 as “high-risk”, 4 to 6 “moderate-risk”, and 7 to 9 as “low-risk” bias.

2.6. Limitations

The overall prevalence of group B Streptococcus carriers in our query could not be determined comprehensively. Different factors such as geographical region, collection of samples, site of sampling, socioeconomic status, and microbiological methods all contributed to the results obtained. Also, due to lack of group B Streptococcus prevalence works in some provinces such as Golestan, Semnan, Mazandaran, Zanjan, Qom, South Khorasan, North Khorasan, Sistan and Baluchestan, Hormozgan, Kohgiluyeh and Boyer-Ahmad, Alborz, Qazvin, and West Azarbaijan, this review paper failed to present a full account of group B Streptococcus prevalence in Iran (Figure 2).

Incidence of Group B streptococcus-positive in different cities in Iran. Source: Map of Iran powered by http://www.wikipedia.com/ (Note: Rect, rectovaginal; Vag, vaginal)
Incidence of Group B streptococcus-positive in different cities in Iran. Source: Map of Iran powered by http://www.wikipedia.com/ (Note: Rect, rectovaginal; Vag, vaginal)
Figure 2.

Incidence of Group B streptococcus-positive in different cities in Iran. Source: Map of Iran powered by http://www.wikipedia.com/ (Note: Rect, rectovaginal; Vag, vaginal)

2.7. Statistical Analysis

The total number of the participants and the number of samples with S. agalactiae were used to calculate the event rate and confidence interval. The summary estimates were derived using the DerSimonial and Laird random effects model by taking inter-study heterogeneity into account. The I-squared and Cochran’s Q tests were used to assess heterogeneity between the studies. Subgroup analysis was used to explore the prevalence rates according to the sampling year, the province in which the study was conducted, and the quality of studies. Sensitivity analysis was carried out to explore the extent to which the overall calculations might depend on a specific study. All analyses were performed using the STATA software version 11.2 (STATA Corp, College Station, TX, USA).

3. Results

According to Databases, 927 articles were selected, among which 563 duplicated articles were excluded. Following reviewing all abstracts of the published works, 292 articles were deleted because of being irrelevant. Full texts of 82 articles were carefully considered, and again, 21 articles that were directly related to infertile women, neonates, adults, and those with ambiguous methods were all excluded from the study. Overall, the remaining 61 articles were approved for further investigation (Figure 1).

3.1. Prevalence of Group B Streptococcus in Iranian Women

Extraction of the information of these articles revealed 36,807 pregnant and non-pregnant women had been examined for group B Streptococcus detection during 1992 - 2018, out of which 2,930 cases (9.7%) were found positive for group B Streptococcus (Table 1). Observed data demonstrated the prevalence of group B Streptococcus among pregnant women to be 11.9% (95% CI: 0.103 - 0.135). Based on swab sampling technique, positive cases were found as the following: (1) vaginal samples with 34 studies (12.9%) (95% CI: 0.103 - 0.155), (2) recto-vaginal samples with 25 studies (9.7%) (95% CI: 0.075 - 0.120), rectum samples with 10 studies (18.5%) (95% CI: 0.096 - 0.275), endocervical samples with one study (3.7%) (95% CI: -0.003 - 0.077), vaginal and urine with one study (6.1%) (95% CI: 0.030 - 0.092), and urine with three studies (2.3%) (95% CI: 0.001 - 0.044). When the recorded data regarding distribution of group B Streptococcus among non-pregnant women were extracted, 5.3% (95% CI: 0.034 - 0.072) of the cases were identified as group B Streptococcus colonized.

Table 1.

Characteristics of the Studies Included in the Systematic Review and Meta-Analysis

First Author (Ref. No.)Place (City)Year (yr)AgePregnancyPregnancy Age (wk)Swab SamplesIdentification MethodSample SizeNo. Positive GBSCarriers (%)Quality Assessment
Aali (15)Kerman200525.6Preg38-40VagCult10576.7Low-risk
Absalan (16)Yazd200215-40PregRecto-VagCult. PCR2504919.6Low-risk
Ahmadi (17)Sanandaj201719-43Preg35-37EndocervicalPCR10943.7Moderate-risk
Akhlaghi (18)Mashhad2007NAPreg33-37VagCult4337Moderate-risk
Arzanlou (2)Ardabil2008NAPreg35-37Recto- VagCult4205613.3Low-risk
Bakhtiari (19)Tehran2011NAPreg28-38Recto- VagCult. PCR375359.3Moderate-risk
Bidgani (20)Ahvaz2013-201416-45Preg28-38VagCult. PCR1373827.7Moderate-risk
PregRectCult. PCR1374230.7Moderate-risk
Bornasi (21)Arak2012NAPreg35-37VagCult. PCR5006012Moderate-risk
Soltan Dalal (22)Tehran2008NAPreg35-37Recto- VagCult. PCR125108Low-Risk
Darabi (23)Tehran2014-201518-35Preg35-37Recto- VagCult1862211.8Moderate-risk
Daramroodi (24)Kermanshah2017NAPreg35-37VagCult. PCR10055Moderate-risk
Fatemi (25)Tehran200816-40Preg35-37VagCult, PCR3306820.6Moderate-risk
Fazeli (26)Amol2013NAPreg35-37VagCult, PCR10044Moderate-risk
RectCult, PCR10033Moderate-risk
Recto- VagCult, PCR10033Moderate-risk
Frouhesh (27)Tehran2011-2012NANon-preg-UrineCult50001042.1High-risk
Ghanbarzadeh (28)Birjand2013-201416-37Preg30Recto- VagCult500265.2Moderate-risk
Goudarzi (29)Khorramabad2012NAPreg35-37Recto- VagCult, Real-time PCR1001717Moderate-risk
Habibzadeh (30)Ardabil2010NAPreg35-37VagCult420194.5Moderate-risk
RectCult420194.5Moderate-risk
Recto- VagCult420245.7Moderate-risk
Hadavand (31)Tehran2010-1115-44Preg35-37Recto- VagCult21073.3Moderate-risk
Hamedi (32)Mashhad2008-200915-39Preg34-40Recto- VagCult200126Moderate-risk
Hassanzadeh (33)Shiraz2006-200719-35Preg< 20Recto- VagCult3104313.9Low-risk
Jannati (2)Ardabil2012NAPreg35-37Recto- VagCult4205613.3Moderate-risk
Javadi (34) Isfahan2004NAPreg35-37Recto- VagCult1703118.2
Javanmanesh (35)Tehran201216-42Preg35-37Recto- VagCult102823422.8Low-risk
Kabiri (36)Jahrom201416-40Preg35-37VagCult4036616.4Low-risk
Rect215.2Low-risk
Recto- Vag71.7Low-risk
Kalantar (37)Sanandaj2011-201218-37Preg28-38VagPCR20012361.5Moderate-risk
RectPCR20016080Moderate-risk
Kasraeian (38)Shiraz200718-36Preg18UrineCult38910.3Low-risk
Khoshkhoutabar (39)Arak2013Preg35-37Recto- VagCult268145.2Moderate-risk
Malek-Jafarian (40)Mashhad201515-40Non-pregUrine VagCult1200463.8Moderate-risk
Mansouri (41)Kerman2006-200720-35Preg35-37VagCult602559.1Moderate-risk
Mashouf (42)Hamadan2013-2014NAPreg35-37VagCult. PCR203157.4Moderate-risk
Mobasheri (43)Ardal201017-38Preg0-40VagCult8522.3Moderate-risk
Nakhaei Moghaddam (44)Mashhad2005-200716-40Preg35-37VagCult2012210.9Moderate-risk
RectCult2012411.9Moderate-risk
Mohamadi (45)Ilam,2014-201516-42Preg< 35VagCult9044.4Moderate-risk
Mousavi (46)Hamadan2013-2014NAPreg35-37VagCult. PCR203157.4Moderate-risk
Saghafi (47)Mashhad2015-201615-42Preg27-37VagCult20032Moderate-risk
Nahaei (13)Tabriz2001-2002NAPregNA*VagCult965171.8Moderate-risk
Namavar Jahromi (48)Shiraz200314-45Preg> 24Recto- VagCult11971109.2Moderate-risk
Nasri (49)Arak201016-39Preg35-37VagCult1863016.1Moderate-risk
Nazari (50)Yazd2015-201615-40PregNAVagCult3465716.5Moderate-risk
UrineCult346339.5Moderate-risk
Nazer (51)Khorram Abad200918-39Preg28-37VagCult1001414Low-risk
Pirouz (52)Tehran199215-43Preg> 37VagCult2003417Moderate-risk
Rabiee (53)Hamadan200618-35Preg> 20VagCult54414526.7Moderate-risk
Rahbar (54)Tehran201026.6 ± 19.37 (mean)PregNAUrineCult11800190.2Moderate-risk
Non-Preg-UrineCult118004794.1Moderate-risk
Sadeh (9)Yazd2013-201415-40PregNARecto- VagCult. PCR2373012.7Moderate-risk
Non-Preg-Recto- VagCult. PCR4137016.9Moderate-risk
Zarean Seyyed (55)Isfahan2010-201117-42Preg37RectCult1783016.9Low-risk
17-3620-37 (Preterm labor)RectCult1515536.4Low-risk
17-4237VagCult1783620.2Low-risk
17-3620-37 (Preterm labor)VagCult1515939.1Low-risk
Sharifi (56)Tehran2011NAPreg35-37Recto- VagCult250218.4Moderate-risk
Shirazi (57)Tehran2009-201119-50Preg35-37VagCult980484.9Low-risk
Tajbakhsh (58)Bushehr2010-201126.39 ± 5.33 meanPreg35-42VagCult285279.5Low-risk
Yasini (59)Kashan2011-201216-45Preg28-37VagCult382369.4Moderate-risk
Zamanzad (60) (unpublished Persian article)Shahrekord2000NAPregVagCult62411017.6Moderate-risk
Amirmozafari (61)Rasht2005Preg28-37VagCult1001515High-risk
Haghshenas Mojaveri (62)Babol201425.9 ± 4.2 (mean)Preg35-37VagCult400317.8Low-risk
RectCult400205Low-risk
Recto- VagCult400102.5Low-risk
Jahed (63)Tehran2008NAPreg35-37Recto- VagCult246135.3Moderate-risk
Khataie (64)Tehran1998NAPreg37VagCult1912814.7Moderate-risk
Nasrollahi1 (65)Sari2018< 25-30 >Preg35-37Vag, UrineCult, PCR246156.1Moderate-risk
Rostami (66)Isfahan201529.35 ± 5.509 (mean)Preg35-37VagCult, PCR2002211Low-risk
RectCult, PCR20073.5Low-risk
Sahraee (67)Rasht2017-2018NAPreg35-37VagCult, PCR245197.8Moderate-risk
Rect245249.8Moderate-risk
Abdollahi Fard (68)Tabriz200622.96 ± 3.89 (mean)Preg35-37Vag, RectCult250249.6Moderate-risk
Akbarian Rad (69)Babol2012-201425.7 ± 5.55 (mean)Preg> 26Vag, RectCult4104611.2Moderate-risk
Shahbazian (70)Ahvaz2007NAPreg35-37Vag, RectCult2503313.2High-risk
Sarafrazi (71)Kashan2000NAPreg35-37VagCult400325.8High-risk

Abbreviations: Cult, culture; GBS, Group B Streptococcus; NA, not available; Preg, pregnant; Rect, rectal; Rect-Vag, rectovaginal; Vag, vaginal.

3.2. Prevalence of Group B Streptococcus in Vaginal and Rectovaginal Swabs of Pregnant Women

The majority of group B Streptococcus research works were based on vaginal or rectovaginal samples. Therefore, an effort was made to analyze and record the data in terms of city, quality assessment index, and year of publication (Tables 1 and 2). The papers were then classified into high-, moderate-, and low-quality index, and consequently, we found vaginal swab samples were in the low-risk (13.7%) group, while rectovaginal cases were in the high-risk (13%) group. Further observation indicated the prevalence of group B Streptococcus from vaginal samples was 15.8% before the year 2000; the city of Sanandaj carried the highest rate with 61.5%, and Tabriz recorded the lowest incidence with 1.8% (Table 2). Data observed from rectovaginal samples (Table 3) revealed that the highest incidence of group B Streptococcus had been observed in 2000 - 2009, during which Isfahan had suffered from the highest rate (18.2%), but Jahrom had the lowest rate (1.7%).

Table 2.

Status of Group B Streptococcus Prevalence in Vaginal Samples

SampleNumber of StudiesPrevalence95% CIHeterogeneityP Value
Q- StatisticI-Squared (%)P Value
Experiment date
< 2000215.80.122-0.1940.400.00.528< 0.001
2000 - 20091211.80.076-0.160339.1296.80.000
≥ 20102013.40.096-0.172454.2495.60.000
City< 0.001
Kerman28.70.066-0.1080.760.00.384
Yazd116.50.126-0.2040.00
Sanandaj161.50.548-0.6820.00
Mashhad36.4-0.003-0.13113.2584.90.001
Ardabil24.10.023-0.0590.840.00.359
Tehran414.10.053-0.23068.9795.70.000
Ahvaz127.70.203-0.3520.00
Arak213.40.096-0.1731.8044.40.180
Kermanshah150.003-0.0970.00
Amol14-0.003-0.0830.00
Khorramabad1140.071-0.2090.00
Isfahan223.10.082-0.38138.7794.80.000
Jahrom116.40.128-0.2000.00
Hamadan313.80.012-0.26469.1797.10.000
Ilam14.4-0.003-0.0920.00
Tabriz11.80.009-0.0260.00
Bushehr19.50.060-0.1290.00
Kashan28.60.067-0.1060.480.00.487
Shahrekord117.60.146-0.2060.00
Rasht210.70.037-0.1773.2669.30.071
Babol17.80.051-0.1040.00
Quality assessment< 0.001
Low-risk813.70.090-0.184124.6293.60.000
Moderate-risk2412.80.093-0.163729.0196.80.000
High-risk210.70.040-0.1743.2869.50.000
Overall3412.90.103-0.155865.9196.10.000< 0.001
Table 3.

Status of Group B Streptococcus Prevalence in Rectovaginal Samples

SampleNumber of StudiesPrevalence95% CIHeterogeneityP Value
Q- StatisticI-Squared (%)P Value
Experiment date< 0.001
< 20000---
2000 - 20091011.30.087-0.13949.3981.80.000
≥ 2010158.70.056-0.117286.0095.10.000
City< 0.001
Yazd2160.092-0.2284.3677.10.037
Mashhad160.026-0.0940.00..
Ardabil310.70.052-0.16221.4090.70.000
Tehran79.90.041-0.156132.4195.50.793
Ahvaz113.20.090-0.1740.00.0.000
Arak15.20.025-0.0800.00..
Amol13-0.010-0.0700.00..
Birjand15.20.032-0.0720.00..
Khorramabad1170.096-0.2440.00..
Shiraz211.20.067-0.1574.7779.00.029
Isfahan118.20.124-0.2410.00..
Jahrom11.70.004-0.0310.00..
Tabriz19.60.059-0.1330.00..
Babol26.8-0.018-0.15324.2395.90.000
Quality assessment< 0.001
Low-risk612.20.049-0.195281.5798.20.000
Moderate-risk168.10.065-0.09767.9877.90.000
High-risk3130.076-0.1837.0171.50.000
Overall259.70.075-0.120373.4193.60.000< 0.001

4. Discussion and Conclusions

The present systematic review and meta-analysis has summarized 61 published works on group B Streptococcus distribution in Iran. Among 36,807 samples examined, 2,930 samples (9.7%) were reported positive for group B Streptococcus. The prevalence was estimated to be 11.9% in pregnant and 5.3% in non-pregnant women (Table 1). The worldwide investigations show that a total of 11% - 30% of women are carriers of group B Streptococcus in their genital system. The important point is that contaminated women may transfer the bacterium to their fetus or neonates (9, 45, 72).

The knowledge resulting from the present review of group B Streptococcus colonization allows us to conclude that since up to 9.7% of females have been found to be group B Streptococcus-positive, it seems reasonable to suggest a strengthened program for screening the pregnant women to illuminate the more accurate prevalence of group B Streptococcus among the Iranian population. Moreover, a variation was discovered in the reported data, which could be mainly due to different methods for group B Streptococcus detection. Therefore, it is essential to document a more sensitive method for the studies to come. Furthermore, more serious measures are needed to represent an account of group B Streptococcus in infected pregnant women for preventing the transmission of bacterium to their neonates. Additionally, a treatment program must be optimized to eradicate the infection in pregnant women and carriers. Finally, despite controversy in reported data from different populations, group B Streptococcus is surely present in different races around our country. As a result, documenting a legal program is highly recommended for screening pregnant women in rural and low-income populations in this country.

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