Curable sexually transmitted infections (STIs) in pregnant women, specifically Treponema pallidum (syphilis), Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT), and Trichomonas vaginalis (TV), may lead to various adverse outcomes including premature rupture of membranes, preterm labor, preterm delivery, chorioamnionitis, low birth weight, congenital infection, and even stillbirth or neonatal mortality.1–9 3,10,11
Antenatal screening practices for curable STIs vary around the world, differing by country and particular STI. The World Health Organization (WHO) has implemented guidelines for testing and treatment of syphilis in pregnancy. Early successes of the congenital syphilis elimination program have been demonstrated by the elimination of mother-to-child transmission of syphilis in Cuba.12–14 15 10
Current literature comparing the prevalence rates of curable STIs in various global regions is limited. A recent review article by Chico et al.16
METHODS
We used the PRISMA guidelines to conduct a systematic review to assess the prevalence of CT, NG, TV and syphilis in pregnancy from studies published between January 1, 2010, and March 1, 2015. The cited data were collected earlier in many studies, ranging from 1999 to 2014.17 Fig. 1 ). H.S. reviewed the PubMed search results, and D.J.D. cross-checked results, validated the data, and resolved discrepancies. We excluded studies on sex workers, women with ectopic pregnancy and symptomatic women; however, we did include HIV-infected pregnant women in the analysis. We did not have exclusion criteria based on testing or screening protocols, other than excluding studies if the testing was syndromic or if the results were self-reported. There were no requirements for sample size for the selected articles, though the sample size was adjusted for in the analysis.
Figure 1: PRISMA flow diagram of publications searched.
Definitions of low- and middle-income countries were obtained from the World Bank (http://data.worldbank.org/income-level/LMY
We stratified our prevalence estimates by region and adjusted for health care setting (eg, hospital-, clinic-, or community-based study), age of pregnant women in the study, and diagnostic tests used. Prevalence values in the included articles were calculated as the number of pregnant women who were diagnosed with an STI over the total number of pregnant women tested.
For syphilis, tests included venereal disease research laboratory, rapid plasma reagin, Treponema pallidum hemagglutination, Toluidine Red Unheated Serum Test, Treponema pallidum particle agglutination assay, enzyme immunoassay, fluorescent treponemal antibody absorption, and rapid diagnostic test. However, 23 of 54 (43%) studies on syphilis only reported venereal disease research laboratory, rapid plasma reagin, or Treponema pallidum hemagglutination but no second test. For CT and NG, tests included nucleic acid amplification testing (NAAT), enzyme immunoassay, IgG antibody screen, culture, Aptima combo 2 and microscopy. For TV, tests included polymerase chain reaction, culture, and microscopy. Data for diagnostic test used was extracted from the studied articles. Due to the variance in performance of different diagnostic tests, estimated sensitivities and specificities were collected from the current literature for each reported diagnostic test used.18–22
All studies that satisfied the previously mentioned inclusion criteria were analyzed and those with missing data points for any factors are denoted in the final analysis. Site of data collection was stratified in a stepdown method to 3 subgroups: at a hospital, at an antenatal or community clinic, or as part of a study or community screening program. Studies reporting more than 1 type of location for data collection or crossover within a location, that is, an antenatal clinic within a hospital, were considered to have occurred at the higher-level care center. Studies directly reporting mean or median ages for the women were used for portion of the analysis whereas studies that either stratified age as a categorical variable without reporting mean age or did not report age as a factor were noted as missing in the final analysis.
Statistical Analyses
We stratified results by subregion (East Africa, West Africa, Southern Africa, Latin America, and Asia). Asia included South Asia, and the Middle East and Pacific Regions, and Latin American included both Central and South America, due to the small number of studies from these regions. We calculated the total number of positive pregnant women per STI per region, the median number with positive diagnoses, the study sample size, the mean age, and the mean sensitivity and specificity for each diagnostic test used (if not counted, then was reported as missing). We developed multivariable linear regression models to estimate adjusted mean prevalence by STI and region, and 95% confidence intervals (CI) for all strata. We adjusted for health care setting (eg, hospital-, clinic-, or community-based study), women's mean age, study sample size, and STI test sensitivity. The specificity was not included in the final model due to collinearity with sensitivity. We used STATA 13.1 (College Station, TX) for all analyses.23
RESULTS
We identified a total of 376 potentially relevant reports from January 2010 to March 2015. Only 75 studies from 30 low- and middle-income countries met inclusion criteria, providing 116 point prevalence estimates for curable STIs in pregnant women, including a total of 3,489,621 women (Fig. 1 ). The diagnostic test used was reported in 94.7% of included articles. The greatest number of published studies were from Latin America (n = 23 studies, n = 206,848 pregnant women), followed by East Africa (n = 20 studies, n = 23,413 pregnant women), Asia (n = 18 studies, n = 3,109,314 pregnant women), Southern Africa (n = 15 studies, n = 128,467 pregnant women), and West Africa (n = 6 studies, n = 10,790 pregnant women). The total number of studies is greater than the 75 studies included because some studies had more than 1 country in the analysis. The number of women and numbers of tests per woman varied considerably from a sample size of 12 (in Brazil) to a sample size of over 2 million (in China).
Overall, the region with the highest adjusted mean prevalence of curable STIs among pregnant women was Southern Africa. Our analyses included studies in the following countries: South Africa, Malawi, Madagascar, Zambia, Mozambique, and Zimbabwe. In Southern Africa, TV was the most prevalent STI overall, with a adjusted mean prevalence of 24.6% (95% CI, 17.9–31.4) in 3 studies. Next was syphilis with a prevalence of 6.5% (95% CI, 4.70–8.3) in 8 studies. Neisseria gonorrhoeae and CT were similarly high at 4.6% (95% CI, 4.0–5.2) in 3 studies, and 4.4% (95% CI, 2.3–6.6) in 3 studies, respectively (Fig. 2 ).
Figure 2: Adjusted mean STI prevalence by region (N=75 studies of STI prevalence among 3,489,621 pregnant women 2010–2015).
In East Africa, we included studies from the following countries: Kenya, Tanzania, Somalia, Ethiopia, Uganda, and Sudan. Eight studies demonstrated a adjusted mean prevalence of syphilis of 4.6% (95% CI, 3.7–5.4), the second highest prevalence after Southern Africa. The adjusted mean prevalence was similarly high for TV in 3 studies at 6.8% (95% CI, 4.6–9.0). The adjusted mean prevalence of CT in 3 studies was 4.2% (95% CI, 2.8–5.6), followed by NG with a prevalence of 2.3% (95% CI, 2.0–2.5) in 3 studies (Fig. 2 ).
In West Africa, we included studies from Benin, Democratic Republic of Congo, Nigeria, and Burkina Faso. In these countries, the adjusted mean prevalence of CT was 7.2% (95% CI, 0.0–14.6) in 1 study. The adjusted mean prevalence of syphilis was 4.0% (95% CI, 1.7–6.3) in 4 studies (Fig. 2 ).
For Latin America, we included studies from Peru, Brazil, Ecuador, Argentina, and Guatemala. The adjusted mean prevalence of TV among pregnant women was 3.9% (95% CI, 1.1–5.6) in the 3 studies included. The adjusted mean prevalence of CT in Latin America was 11.2% (95% CI, 7.3–17.1) in 7 studies, which is higher than the mean prevalence in Southern and East Africa. Syphilis had a mean prevalence of 2.6% (95% CI, 1.2–3.9) in 15 studies. The mean prevalence of NG was very low at 0.3% (95% CI, 0.1–2.1) in 3 studies (Fig. 2 ).
In Asia, we included studies from China, India, Bangladesh, Papua New Guinea, Turkey, Pakistan, Iran, Myanmar, and Cambodia. The mean prevalence of STIs among pregnant women was lower here than the other regions. Trichomonas vaginalis was most prevalent with a mean prevalence of 13.6% (95% CI, 6.8–20.4) in 1 study, followed by NG at 2.8% (95% CI, 2.4–3.3) in 1 study, and CT at 0.8% (95% CI, 0.4–1.1) in 6 studies. The mean prevalence of syphilis was also lowest in Asia at 1.1% (95% CI, 0.5–1.6) in 13 studies controlling for potential confounders (see Table 1 ).
TABLE 1: Adjusted Mean STI Prevalence Among Pregnant Women Adjusting for Potential Confounders, 2010–2015 (Stratified by Region)
DISCUSSION
Our study found that the prevalence of curable STIs among pregnant women was substantial throughout low- and middle-income countries. Importantly, our review found a lack of recent data on STI prevalence among pregnant women in many parts of the world. We also note that the variation in diagnostic tests used and populations tested makes it difficult to compare the prevalence between the different regions. Inconsistencies between research and practice may play a role in why the WHO has not implemented clear screening guidelines and policies for STI screening, other than for syphilis and HIV, in pregnancy.13,14 15,16,18–23 18,19
Other systematic reviews of STI prevalence in pregnant women have found similarly high rates of STIs. A review article by Chico et al.16
Despite persistent high level of STIs among pregnant women, there is still a limited focus on CT, NG, and TV. All of those are curable STIs that are risk factors for adverse birth and neonatal outcomes. Despite the well-known negative outcomes of these curable STIs, our systematic review revealed a serious lack of necessary prevalence data, which impedes an accurate assessment of the STIs among pregnant women in multiple regions worldwide, thereby preventing the timely diagnosis and treatment of pregnant women (and their partners and infants) to prevent known complications.
Our findings are particularly relevant for CT and NG, which are largely asymptomatic infections. However, TV and syphilis, which may present with the symptoms of genital discharge and ulceration, also go underdiagnosed.8 24 25
LIMITATIONS
Our study was subject to some limitations. We only used PubMed for the search and may have missed other publications as a result. Although PubMed (Medline) and EMBASE are similar, their coverage of the published literature differs. For example, EMBASE is used more frequently in Europe, and PubMed in the United States. As a result of limiting our search to PubMed, we may have excluded European or abstract citations. Further, the quality of the studies included in this analysis varied considerably, including different sampling strategies, diagnostic tests used, testing strategies, and HIV coinfection rates. We attempted to control for that heterogeneity by adjusting for women's mean age, sensitivity of diagnostic test used (when reported), and number of women included in the sample size. Our estimates though may be underestimations because we excluded studies on sex workers (n = 2) and symptomatic women. Additionally, in countries with limited access to STI care, the prevalence studies often used convenience sampling, which may underestimate the true burden in pregnancy. Also, diagnostic tests with poor sensitivity will tend to underdiagnose true-positive cases and underreport STI prevalence as a result. Conversely, studies not performing treponemal specific testing may overreport syphilis prevalence. The limited number of studies on NG and TV might limit generalizability or precision of the estimates. Where possible, we included more than 2 studies; however, there were instances where more than 1 recent study was not available (eg, CT in West Africa, NG and TV in Asia). We excluded studies that only reported estimates of STI prevalence, but did not present data as to where those estimates came from (eg, surveys, subjective or self-reported estimates), which could have caused underrepresentation of studies from West and Central Africa or Asia. Finally, due to the significant heterogeneity in socioeconomic status within each region, regional prevalence studies may not be representative of population-level burden of STIs among pregnant women.
CONCLUSIONS
Our study highlights the urgent need to collect reliable measures of STI prevalence in low- and middle-income countries, where the burden among pregnant women is greatest. We advocate for strengthening prevalence monitoring as a method of STI surveillance in pregnant women worldwide.26 1–9 12,15
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Appendix 1
Search terms used
(“sexually transmitted infections”[text word] OR “sexually transmitted diseases”[text word] OR “genital tract infections” [text word] OR “reproductive tract infections”[text word] OR “syphilis”[text word] OR “treponema pallidum”[text word] OR “gonorrhea”[text word] OR “Neisseria gonorrhea ”[text word] OR “chlamydia”[text word] OR “chlamydia trachomatis”[text word] OR “trichomonas”[text word] OR “trichomonas vaginalis” [text word] OR “sexually transmitted diseases, bacterial”[Mesh] OR “reproductive tract infections”[Mesh] OR “trichomonas”[Mesh] OR “treponema pallidum”[Mesh] OR “chlamydia” [Mesh] OR “Neisseria gonorrhoeae”[Mesh])
AND
(“pregnancy” [text word] OR “pregnant women” [text word] OR “antenatal” [text word] OR “pregnant women” [Mesh] OR “pregnancy” [Mesh] OR “prenatal care” [Mesh] OR “perinatal care” [Mesh])
AND
(“developing country”[text word] OR “developing countries” [text word] OR “Africa”[text word] OR “Mexico”[text word] OR “Caribbean”[text word] OR “central America”[text word] OR “Latin America”[text word] OR “south America”[text word] OR “Americas”[text word] OR “Asia”[text word] OR “China” [text word] OR “Oceania”[text word] OR “Eastern Europe”[text word] OR “developing countries”[Mesh] OR “Africa”[Mesh] OR “Mexico”[Mesh] OR “Caribbean region”[Mesh] OR “central America”[Mesh] OR “Latin America”[Mesh] OR “south America” [Mesh] OR “Asia”[Mesh] OR “Transcaucasia”[Mesh] OR “Indian ocean islands”[Mesh] OR “Pacific Islands”[Mesh] OR “Europe, eastern”[Mesh])
AND
(“prevalence” [Mesh] OR “morbidity” [Mesh] OR “epidemiology” [Subheading] OR “statistics and numerical data” [Subheading] OR prevalence [text word] OR morbidity [text word] OR epidemiology [text word] OR statistic*[text word])
NOT (“animals” [Mesh] NOT “humans” [Mesh])
Appendix 2
Publications included in analysis
1. Wangnapi RA, Soso S, Unger HW, Sawera C, Ome M, Umbers AJ, et al. Prevalence and risk factors for Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis infection in pregnant women in Papua New Guinea. Sex Transm Infect. 2015 May;91(3):194-200. doi: 10.1136/sextrans-2014-051670. Epub 2014 Oct 13. PubMed PMID: 25313204.
2. Cabeza J, García PJ, Segura E, García P, Escudero F, La Rosa S, León S, et al. Feasibility of Chlamydia trachomatis screening and treatment in pregnant women in Lima, Peru: a prospective study in two large urban hospitals. Sex Transm Infect. 2015 Feb;91(1):7-10. doi: 10.1136/sextrans-2014-051531. Epub 2014 Aug 8. PubMed PMID: 25107711; PubMed Central PMCID: PMC4417475.
3. Chopra S, Garg A, Chopra M, Ghosh A, Sreenivas V, Sood S, et al. Declining trends of Syphilis seroprevalance among antenatal clinic cases and STD clinic cases in a tertiary care centre: from January 2002 to December 2012. Indian J Med Microbiol. 2015 Feb;33 Suppl:126-8. doi: 10.4103/0255-0857.150917. PubMed PMID: 25657130.
4. Lawi JD, Mirambo MM, Magoma M, Mushi MF, Jaka HM, Gumodoka B, et al. Sero-conversion rate of Syphilis and HIV among pregnant women attending antenatal clinic in Tanzania: a need for re-screening at delivery. BMC Pregnancy Childbirth. 2015 Jan 22;15:3. doi: 10.1186/s12884-015-0434-2. PubMed PMID: 25613487; PubMed Central PMCID: PMC4307991.
5. Unger HW, Ome-Kaius M, Wangnapi RA, Umbers AJ, Hanieh S, Suen CS, et al. Sulphadoxine-pyrimethamine plus azithromycin for the prevention of low birthweight in Papua New Guinea: a randomised controlled trial. BMC Med. 2015 Jan 16;13:9. doi:
6. Manabe YC, Namale G, Nalintya E, Sempa J, Ratanshi RP, Pakker N, Katabira E. Integration of antenatal syphilis screening in an urban HIV clinic: a feasibility study. BMC Infect Dis. 2015 Jan 13;15:15. doi: 10.1186/s12879-014-0739-1. PubMed PMID: 25583097; PubMed Central PMCID: PMC4302122.
7. Moodley D, Moodley P, Sebitloane M, Soowamber D, McNaughton-Reyes HL, Groves AK, Maman S. High prevalence and incidence of asymptomatic sexually transmitted infections during pregnancy and postdelivery in KwaZulu Natal, South Africa. Sex Transm Dis. 2015 Jan;42(1):43-7. doi: 10.1097/OLQ.0000000000000219. PubMed PMID: 25504300.
8. Taylor MM, Ebrahim S, Abiola N, Kinkodi DK, Mpingulu M, Kabuayi JP, et al. Correlates of syphilis seropositivity and risk for syphilis-associated adverse pregnancy outcomes among women attending antenatal care clinics in the Democratic Republic of Congo. Int J STD AIDS. 2014 Sep;25(10):716-25. doi: 10.1177/0956462413518194. Epub 2014 Jan 22. PubMed PMID: 24452733.
9. De Paschale M, Ceriani C, Cerulli T, Cagnin D, Cavallari S, Cianflone A, et al. Antenatal screening for Toxoplasma gondii, Cytomegalovirus, rubella and Treponema pallidum infections in northern Benin. Trop Med Int Health. 2014 Jun;19(6):743-746. doi: 10.1111/tmi.12296. Epub 2014 Mar 10. PubMed PMID: 24612218.
10. Abdelaziz ZA, Ibrahim ME, Bilal NE, Hamid ME. Vaginal infections among pregnant women at Omdurman Maternity Hospital in Khartoum, Sudan. J Infect Dev Ctries. 2014 Apr 15;8(4):490-7. doi: 10.3855/jidc.3197. PubMed PMID: 24727516.
11. Soeiro CM, Miranda AE, Saraceni V, Santos MC, Talhari S, Ferreira LC. Syphilis in pregnancy and congenital syphilis in Amazonas State, Brazil: an evaluation using database linkage. Cad Saude Publica. 2014 Apr;30(4):715-23. PubMed PMID: 24896047.
12. Hong FC, Yang YZ, Liu XL, Feng TJ, Liu JB, Zhang CL, Lan LN, Yao MZ, Zhou H. Reduction in mother-to-child transmission of syphilis for 10 years in Shenzhen, China. Sex Transm Dis. 2014 Mar;41(3):188-93. doi: 10.1097/OLQ.0000000000000097. PubMed PMID: 24521725.
13. Archana BR, Prasad SR, Beena PM, Okade R, Sheela SR, Beeregowda YC. Maternal and congenital syphilis in Karnataka, India. Southeast Asian J Trop Med Public Health. 2014 Mar;45(2):430-4. PubMed PMID: 24968685.
14. Sánchez-Gómez A, Grijalva MJ, Silva-Aycaguer LC, Tamayo S, Yumiseva CA, Costales JA, et al. HIV and syphilis infection in pregnant women in Ecuador: prevalence and characteristics of antenatal care. Sex Transm Infect. 2014 Feb;90(1):70-5. doi: 10.1136/sextrans-2013-051191. Epub 2013 Nov 26. PubMed PMID: 24282329.
15. Qin JB, Feng TJ, Yang TB, Hong FC, Lan LN, Zhang CL, et al. Risk factors for congenital syphilis and adverse pregnancy outcomes in offspring of women with syphilis in Shenzhen, China: a prospective nested case-control study. Sex Transm Dis. 2014 Jan;41(1):13-23. doi: 10.1097/OLQ.0000000000000062. PubMed PMID: 24326577.
16. Rahman M, Chowdhury SB, Akhtar N, Jahan M, Jahan MK, Jebunnahar S. Chlamydia trachomatis IgM seropositivity during pregnancy and assessment of its risk factors. Mymensingh Med J. 2014 Jan;23(1):62-8. PubMed PMID: 24584375.
17. van den Broek NR, Jean-Baptiste R, Neilson JP. Factors associated with preterm, early preterm and late preterm birth in Malawi. PLoS One. 2014 Mar 3;9(3):e90128. doi: 10.1371/journal.pone.0090128. eCollection 2014. PubMed PMID: 24595186; PubMed Central PMCID: PMC3940843.
18. Jespers V, Crucitti T, Menten J, Verhelst R, Mwaura M, Mandaliya K, et al. Prevalence and correlates of bacterial vaginosis in different sub-populations of women in sub-Saharan Africa: a cross-sectional study. PLoS One. 2014 Oct 7;9(10):e109670. doi: 10.1371/journal.pone.0109670. eCollection 2014. PubMed PMID: 25289640; PubMed Central PMCID: PMC4188821.
19. Mobasheri M, Saeedi Varnamkhast N, Karimi A, Banaeiyan S. Prevalence study of genital tract infections in pregnant women referred to health centers in Iran. Turk J Med Sci. 2014;44(2):232-6. PubMed PMID: 25536729.
20. Dinh TH, Kamb ML, Msimang V, Likibi M, Molebatsi T, Goldman T, Lewis DA. Integration of preventing mother-to-child transmission of HIV and syphilis testing and treatment in antenatal care services in the Northern Cape and Gauteng provinces, South Africa. Sex Transm Dis. 2013 Nov;40(11):846-51. doi: 10.1097/OLQ.0000000000000042. PubMed PMID: 24113405.
21. Borborema-Alfaia AP, Freitas NS, Astolfi Filho S, Borborema-Santos CM. Chlamydia trachomatis infection in a sample of northern Brazilian pregnant women: prevalence and prenatal importance. Braz J Infect Dis. 2013 Sep-Oct;17(5):545-50. doi: 10.1016/j.bjid.2013.01.014. Epub 2013 Jul 4. PubMed PMID: 23831212.
22. Berini CA, Delfino C, Torres O, García G, Espejo R, Pianciola L, et al. HTLV-1 cosmopolitan and HTLV-2 subtype b among pregnant women of non-endemic areas of Argentina. Sex Transm Infect. 2013 Jun;89(4):333-5. doi: 10.1136/sextrans-2012-050594. Epub 2012 Dec 8. PubMed PMID: 23220782.
23. Agholor K, Omo-Aghoja L, Okonofua F. Association of anti-Chlamydia antibodies with ectopic pregnancy in Benin city, Nigeria: a case-control study. Afr Health Sci. 2013 Jun;13(2):430-40. doi: 10.4314/ahs.v13i2.33. PubMed PMID: 24235946; PubMed Central PMCID: PMC3824483.
24. Araújo MA, de Freitas SC, de Moura HJ, Gondim AP, da Silva RM. Prevalence and factors associated with syphilis in parturient women in Northeast, Brazil. BMC Public Health. 2013 Mar 7;13:206. doi: 10.1186/1471-2458-13-206. PubMed PMID: 23497370; PubMed Central PMCID: PMC3641976.
25. Nóbrega I, Dantas P, Rocha P, Rios I, Abraão M, Netto EM, Brites C. Syphilis and HIV-1 among parturient women in Salvador, Brazil: low prevalence of syphilis and high rate of loss to follow-up in HIV-infected women. Braz J Infect Dis. 2013 Mar-Apr;17(2):184-93. doi: 10.1016/j.bjid.2012.10.018. Epub 2013 Feb 28. PubMed PMID: 23453946.
26. Karaer A, Mert I, Cavkaytar S, Batioglu S. Serological investigation of the role of selected sexually transmitted infections in the aetiology of ectopic pregnancy. Eur J Contracept Reprod Health Care. 2013 Feb;18(1):68-74. doi: 10.3109/13625187.2012.744818. Epub 2012 Dec 21. PubMed PMID: 23256948.
27. Abdelaziz ZA, Ibrahim ME, Bilal NE, Hamid ME. Vaginal infections among pregnant women at Omdurman Maternity Hospital in Khartoum, Sudan. J Infect Dev Ctries. 201
28. Borborema-Alfaia AP, Freitas NS, Astolfi Filho S, Borborema-Santos CM. Chlamydia trachomatis infection in a sample of northern Brazilian pregnant women: prevalence and prenatal importance. Braz J Infect Dis. 2013 Sep-Oct;17(5):545-50. doi: 10.1016/j.bjid.2013.01.014. Epub 2013 Jul 4. PubMed PMID: 23831212. 4 Apr 15;8(4):490-7. doi: 10.3855/jidc.3197. PubMed PMID: 24727516.
29. De Jongh M, Lekalakala MR, Le Roux M, Hoosen AA. Risk of having a sexually transmitted infection in women presenting at a termination of pregnancy clinic in Pretoria, South Africa. J Obstet Gynaecol. 2010;30(5):480-3. doi: 10.3109/01443611003797687. PubMed PMID: 20604651.
30. Temmerman M, Gichangi P, Fonck K, Apers L, Claeys P, Van Renterghem L, et al. Effect of a syphilis control programme on pregnancy outcome in Nairobi, Kenya. Sex Transm Infect. 2000 Apr;76(2):117-21. PubMed PMID: 10858713; PubMed Central PMCID: PMC1758283.
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