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Published in: BMC Infectious Diseases 1/2015

Open Access 01-12-2015 | Research article

Prevalence of 7 sexually transmitted organisms by multiplex real-time PCR in Fallopian tube specimens collected from Saudi women with and without ectopic pregnancy

Authors: Ahmed Mohamed Ashshi, Sarah Abdullah Batwa, Seham Yahia Kutbi, Faizah Ahmed Malibary, Mohamed Batwa, Bassem Refaat

Published in: BMC Infectious Diseases | Issue 1/2015

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Abstract

Background

Ectopic pregnancy (EP) is associated with maternal morbidity and occasionally mortality during the first trimester. A history of sexually transmitted infection (STI) and pelvic inflammatory disease have been implicated as major risk factors for EP. Our aim was to measure the prevalence of Chlamydia trachomatis (CT), Neisseria gonorrhoeae, Mycoplasma genitalium (MG), Ureaplasma parvum/urealyticum, Gardnerella vaginalis, Trichomonas vaginalis and herpes simplex virus (HSV)-1&2 in Fallopian tubes collected from EP and the results were compared with those obtained from total abdominal hysterectomy (TAH) and tubal ligation.

Methods

This was a prospective case–control study and tubal samples were collected from 135 Saudi women recruited from 3 centres in the Western region as follow: 84 EPs, 20 TAH and 31 tubal ligations. Multiplex TaqMan PCR was performed using an IVD CE kit for the simultaneous detection of candidate pathogens following DNA extraction.

Results

Infections were detected in 31.8 % of the 135 participants either as single (11.1 %) or co-infections (20.7 %) and the frequencies were significantly higher in EP (42.85 %) compared with control (13.72 %). The rates of CT (27.4 %; P = 0.001); MG (20.2 %; P = 0.009) and HSV-1/2 (21.4 %; P = 0.01) were significantly higher in EP. No significant difference between the study groups was observed for the other pathogens (P > 0.05). Binary logistic regression also showed that infection with ≥ 2 pathogens (OR 4.9; 95 % CI: 2.2 – 11.6; P = 0.006), CT (OR 3.07; 95 % CI: 1.3 – 12.3; P = 0.002), MG (OR 2.3; 95 % CI: 1.1 – 8.6; P = 0.03) and HSV-1/2 (OR 1.7; 95 % CI: 0.75 – 5.7; P = 0.004) were associated with a significantly higher risk of developing EP.

Conclusions

STIs are frequent in the upper genital tract of Saudi women during the reproductive age and, CT, MG and HSV-1/2 were more prevalent in EP. The observed high rates of co-infection advocate the necessity of establishing national guidelines and/or screening program utilising multiplex PCR approach for the detection of common STIs among high risk groups in the kingdom. Further studies are needed to measure the adverse reproductive outcomes associated with STIs in Saudi Arabia.
Literature
1.
go back to reference Refaat B, Dalton E, Ledger WL. Ectopic pregnancy secondary to in vitro fertilisation-embryo transfer: pathogenic mechanisms and management strategies. Reproductive Biology and Endocrinology. 2015;13(1):30.PubMedCentralPubMedCrossRef Refaat B, Dalton E, Ledger WL. Ectopic pregnancy secondary to in vitro fertilisation-embryo transfer: pathogenic mechanisms and management strategies. Reproductive Biology and Endocrinology. 2015;13(1):30.PubMedCentralPubMedCrossRef
2.
3.
go back to reference Horne AW, Critchley HO. Mechanisms of disease: the endocrinology of ectopic pregnancy. Expert Rev Mol Med. 2012;14, e7.PubMedCrossRef Horne AW, Critchley HO. Mechanisms of disease: the endocrinology of ectopic pregnancy. Expert Rev Mol Med. 2012;14, e7.PubMedCrossRef
5.
go back to reference Al-Turki HA. A review of 33 years (1980–2013) of data indicating a rise in ectopic pregnancy in Saudi Arabia. Int J Gynaecol Obstet. 2015;128(1):33–5.PubMedCrossRef Al-Turki HA. A review of 33 years (1980–2013) of data indicating a rise in ectopic pregnancy in Saudi Arabia. Int J Gynaecol Obstet. 2015;128(1):33–5.PubMedCrossRef
6.
go back to reference Khan KS, Wojdyla D, Say L, Gulmezoglu AM, Van Look PF. WHO analysis of causes of maternal death: a systematic review. Lancet. 2006;367(9516):1066–74.PubMedCrossRef Khan KS, Wojdyla D, Say L, Gulmezoglu AM, Van Look PF. WHO analysis of causes of maternal death: a systematic review. Lancet. 2006;367(9516):1066–74.PubMedCrossRef
7.
go back to reference Barnhart KT, Sammel MD, Gracia CR, Chittams J, Hummel AC, Shaunik A. Risk factors for ectopic pregnancy in women with symptomatic first-trimester pregnancies. Fertil Steril. 2006;86(1):36–43.PubMedCrossRef Barnhart KT, Sammel MD, Gracia CR, Chittams J, Hummel AC, Shaunik A. Risk factors for ectopic pregnancy in women with symptomatic first-trimester pregnancies. Fertil Steril. 2006;86(1):36–43.PubMedCrossRef
8.
go back to reference Karaer A, Avsar FA, Batioglu S. Risk factors for ectopic pregnancy: a case–control study. Aust N Z J Obstet Gynaecol. 2006;46(6):521–7.PubMedCrossRef Karaer A, Avsar FA, Batioglu S. Risk factors for ectopic pregnancy: a case–control study. Aust N Z J Obstet Gynaecol. 2006;46(6):521–7.PubMedCrossRef
9.
go back to reference Rana P, Kazmi I, Singh R, Afzal M, Al-Abbasi FA, Aseeri A, et al. Ectopic pregnancy: a review. Arch Gynecol Obstet. 2013;288(4):747–57.PubMedCrossRef Rana P, Kazmi I, Singh R, Afzal M, Al-Abbasi FA, Aseeri A, et al. Ectopic pregnancy: a review. Arch Gynecol Obstet. 2013;288(4):747–57.PubMedCrossRef
10.
go back to reference Baecher-Lind LE, Miller WC, Wilcox AJ. Infectious disease and reproductive health: a review. Obstet Gynecol Surv. 2010;65(1):53–65.PubMedCrossRef Baecher-Lind LE, Miller WC, Wilcox AJ. Infectious disease and reproductive health: a review. Obstet Gynecol Surv. 2010;65(1):53–65.PubMedCrossRef
11.
go back to reference Gimenes F, Medina FS, Abreu AL, Irie MM, Esquicati IB, Malagutti N, et al. Sensitive simultaneous detection of seven sexually transmitted agents in semen by multiplex-PCR and of HPV by single PCR. PLoS One. 2014;9(6), e98862.PubMedCentralPubMedCrossRef Gimenes F, Medina FS, Abreu AL, Irie MM, Esquicati IB, Malagutti N, et al. Sensitive simultaneous detection of seven sexually transmitted agents in semen by multiplex-PCR and of HPV by single PCR. PLoS One. 2014;9(6), e98862.PubMedCentralPubMedCrossRef
12.
go back to reference Ross J, Judlin P, Jensen J. 2012 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS. 2014;25(1):1–7.PubMedCrossRef Ross J, Judlin P, Jensen J. 2012 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS. 2014;25(1):1–7.PubMedCrossRef
13.
go back to reference Taylor BD, Darville T, Haggerty CL. Does bacterial vaginosis cause pelvic inflammatory disease? Sex Transm Dis. 2013;40(2):117–22.PubMed Taylor BD, Darville T, Haggerty CL. Does bacterial vaginosis cause pelvic inflammatory disease? Sex Transm Dis. 2013;40(2):117–22.PubMed
14.
go back to reference Yadav M, Verma N, Dhanda RS. Impact of sexually transmitted infections on women health. Health. 2013;2013. Yadav M, Verma N, Dhanda RS. Impact of sexually transmitted infections on women health. Health. 2013;2013.
16.
go back to reference Alzahrani AJ, Obeid OE, Hassan MI, Almulhim AA. Screening of pregnant women attending the antenatal care clinic of a tertiary hospital in eastern Saudi Arabia for Chlamydia trachomatis and Neisseria gonorrhoeae infections. Indian J Sex Transm Dis. 2010;31(2):81–6.PubMedCentralPubMedCrossRef Alzahrani AJ, Obeid OE, Hassan MI, Almulhim AA. Screening of pregnant women attending the antenatal care clinic of a tertiary hospital in eastern Saudi Arabia for Chlamydia trachomatis and Neisseria gonorrhoeae infections. Indian J Sex Transm Dis. 2010;31(2):81–6.PubMedCentralPubMedCrossRef
17.
go back to reference Al-Jiffri O. Detection of Chlamydia trachomatis among infected women. Middle East Journal of Scientific Research. 2011;8:450–6. Al-Jiffri O. Detection of Chlamydia trachomatis among infected women. Middle East Journal of Scientific Research. 2011;8:450–6.
18.
go back to reference Kabbash IA, Al-Mazroa MA, Memish ZA. Evaluation of syndromic management of sexually transmitted infections in Saudi Arabia. Journal of infection and public health. 2011;4(2):73–9.PubMedCrossRef Kabbash IA, Al-Mazroa MA, Memish ZA. Evaluation of syndromic management of sexually transmitted infections in Saudi Arabia. Journal of infection and public health. 2011;4(2):73–9.PubMedCrossRef
19.
go back to reference Fageeh WM. Sexually transmitted infections among patients with herpes simplex virus at King Abdulaziz University Hospital. BMC research notes. 2013;6(1):301.PubMedCentralPubMedCrossRef Fageeh WM. Sexually transmitted infections among patients with herpes simplex virus at King Abdulaziz University Hospital. BMC research notes. 2013;6(1):301.PubMedCentralPubMedCrossRef
20.
go back to reference Fageeh W, Badawood S, Al Thagafi H, Yasir M, Azhar E, Farraj S, et al. Chlamydia trachomatis infection among female inmates at Briman prison in Saudi Arabia. BMC Public Health. 2014;14(1):267.PubMedCentralPubMedCrossRef Fageeh W, Badawood S, Al Thagafi H, Yasir M, Azhar E, Farraj S, et al. Chlamydia trachomatis infection among female inmates at Briman prison in Saudi Arabia. BMC Public Health. 2014;14(1):267.PubMedCentralPubMedCrossRef
21.
go back to reference Alfarraj DA, Somily AM, Alssum RM, Abotalib ZM, El-Sayed AA, Al-Mandeel HH. The prevalence of Chlamydia trachomatis infection among Saudi women attending the infertility clinic in Central Saudi Arabia. Saudi medical journal. 2015;36(1):61.PubMedCentralPubMedCrossRef Alfarraj DA, Somily AM, Alssum RM, Abotalib ZM, El-Sayed AA, Al-Mandeel HH. The prevalence of Chlamydia trachomatis infection among Saudi women attending the infertility clinic in Central Saudi Arabia. Saudi medical journal. 2015;36(1):61.PubMedCentralPubMedCrossRef
23.
24.
go back to reference Trembizki E, Costa AM, Tabrizi SN, Whiley DM, Twin J. Opportunities and pitfalls of molecular testing for detecting sexually transmitted pathogens. Pathology. 2015;47(3):219–26.PubMedCrossRef Trembizki E, Costa AM, Tabrizi SN, Whiley DM, Twin J. Opportunities and pitfalls of molecular testing for detecting sexually transmitted pathogens. Pathology. 2015;47(3):219–26.PubMedCrossRef
25.
go back to reference Samra Z, Rosenberg S, Madar-Shapiro L. Direct simultaneous detection of 6 sexually transmitted pathogens from clinical specimens by multiplex polymerase chain reaction and auto-capillary electrophoresis. Diagn Microbiol Infect Dis. 2011;70(1):17–21.PubMedCrossRef Samra Z, Rosenberg S, Madar-Shapiro L. Direct simultaneous detection of 6 sexually transmitted pathogens from clinical specimens by multiplex polymerase chain reaction and auto-capillary electrophoresis. Diagn Microbiol Infect Dis. 2011;70(1):17–21.PubMedCrossRef
26.
go back to reference Refaat B, Al-Azemi M, Geary I, Eley A, Ledger W. Role of activins and inducible nitric oxide in the pathogenesis of ectopic pregnancy in patients with or without Chlamydia trachomatis infection. Clin Vaccine Immunol. 2009;16(10):1493–503.PubMedCentralPubMedCrossRef Refaat B, Al-Azemi M, Geary I, Eley A, Ledger W. Role of activins and inducible nitric oxide in the pathogenesis of ectopic pregnancy in patients with or without Chlamydia trachomatis infection. Clin Vaccine Immunol. 2009;16(10):1493–503.PubMedCentralPubMedCrossRef
27.
go back to reference Luijt D, Di Lorenzo C, van Loon AM, Unemo M. Most but not all laboratories can detect the recently emerged Neisseria gonorrhoeae porA mutants - results from the QCMD 2013 N. gonorrhoeae external quality assessment programme. Euro Surveill. 2014;19(8):20711.PubMedCrossRef Luijt D, Di Lorenzo C, van Loon AM, Unemo M. Most but not all laboratories can detect the recently emerged Neisseria gonorrhoeae porA mutants - results from the QCMD 2013 N. gonorrhoeae external quality assessment programme. Euro Surveill. 2014;19(8):20711.PubMedCrossRef
28.
go back to reference Haggerty CL, Gottlieb SL, Taylor BD, Low N, Xu F, Ness RB. Risk of sequelae after Chlamydia trachomatis genital infection in women. J Infect Dis. 2010;201 Suppl 2:S134–55.PubMedCrossRef Haggerty CL, Gottlieb SL, Taylor BD, Low N, Xu F, Ness RB. Risk of sequelae after Chlamydia trachomatis genital infection in women. J Infect Dis. 2010;201 Suppl 2:S134–55.PubMedCrossRef
29.
go back to reference Akande V, Turner C, Horner P, Horne A, Pacey A. Impact of Chlamydia trachomatis in the reproductive setting: British Fertility Society Guidelines for practice. Hum Fertil (Camb). 2010;13(3):115–25.CrossRef Akande V, Turner C, Horner P, Horne A, Pacey A. Impact of Chlamydia trachomatis in the reproductive setting: British Fertility Society Guidelines for practice. Hum Fertil (Camb). 2010;13(3):115–25.CrossRef
30.
go back to reference Kazandi M, Turan V. Ectopic pregnancy; risk factors and comparison of intervention success rates in tubal ectopic pregnancy. Clin Exp Obstet Gynecol. 2011;38(1):67–70.PubMed Kazandi M, Turan V. Ectopic pregnancy; risk factors and comparison of intervention success rates in tubal ectopic pregnancy. Clin Exp Obstet Gynecol. 2011;38(1):67–70.PubMed
31.
go back to reference Mitchell C, Prabhu M. Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment. Infect Dis Clin North Am. 2013;27(4):793–809.PubMedCrossRef Mitchell C, Prabhu M. Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment. Infect Dis Clin North Am. 2013;27(4):793–809.PubMedCrossRef
32.
go back to reference Al-Meshari AA, Chowdhury N, Adelusi B. Ectopic pregnancy in a defined Saudi population. Ann Saudi Med. 1993;13(6):530–4.PubMed Al-Meshari AA, Chowdhury N, Adelusi B. Ectopic pregnancy in a defined Saudi population. Ann Saudi Med. 1993;13(6):530–4.PubMed
33.
go back to reference Ogbonna BN, Al-Nemr A, Moghanam M. Ectopic pregnancy in King Fahad Hofuf Hospital: A five year experience. Ann Saudi Med. 1992;12(6):544–7.PubMed Ogbonna BN, Al-Nemr A, Moghanam M. Ectopic pregnancy in King Fahad Hofuf Hospital: A five year experience. Ann Saudi Med. 1992;12(6):544–7.PubMed
34.
go back to reference Al-Turki HA. Ectopic pregnancy. Prevalence and risk factors in women attending a tertiary care hospital in Saudi Arabia. Saudi Med J. 2012;33(8):875–8.PubMed Al-Turki HA. Ectopic pregnancy. Prevalence and risk factors in women attending a tertiary care hospital in Saudi Arabia. Saudi Med J. 2012;33(8):875–8.PubMed
35.
go back to reference Paukku M, Puolakkainen M, Paavonen T, Paavonen J. Plasma cell endometritis is associated with Chlamydia trachomatis infection. Am J Clin Pathol. 1999;112(2):211–5.PubMed Paukku M, Puolakkainen M, Paavonen T, Paavonen J. Plasma cell endometritis is associated with Chlamydia trachomatis infection. Am J Clin Pathol. 1999;112(2):211–5.PubMed
36.
go back to reference Pavletic AJ, Wolner-Hanssen P, Paavonen J, Hawes SE, Eschenbach DA. Infertility following pelvic inflammatory disease. Infect Dis Obstet Gynecol. 1999;7(3):145–52.PubMedCentralPubMedCrossRef Pavletic AJ, Wolner-Hanssen P, Paavonen J, Hawes SE, Eschenbach DA. Infertility following pelvic inflammatory disease. Infect Dis Obstet Gynecol. 1999;7(3):145–52.PubMedCentralPubMedCrossRef
37.
go back to reference Paavonen J. Chlamydia trachomatis infections of the female genital tract: state of the art. Ann Med. 2012;44(1):18–28.PubMedCrossRef Paavonen J. Chlamydia trachomatis infections of the female genital tract: state of the art. Ann Med. 2012;44(1):18–28.PubMedCrossRef
38.
go back to reference Hornung S, Thuong BC, Gyger J, Kebbi-Beghdadi C, Vasilevsky S, Greub G, et al. Role of Chlamydia trachomatis and emerging Chlamydia-related bacteria in ectopic pregnancy in Vietnam. Epidemiol Infect. 2015;143(12):2635–8.PubMedCrossRef Hornung S, Thuong BC, Gyger J, Kebbi-Beghdadi C, Vasilevsky S, Greub G, et al. Role of Chlamydia trachomatis and emerging Chlamydia-related bacteria in ectopic pregnancy in Vietnam. Epidemiol Infect. 2015;143(12):2635–8.PubMedCrossRef
39.
go back to reference Short VL, Totten PA, Ness RB, Astete SG, Kelsey SF, Haggerty CL. Clinical presentation of Mycoplasma genitalium Infection versus Neisseria gonorrhoeae infection among women with pelvic inflammatory disease. Clin Infect Dis. 2009;48(1):41–7.PubMedCentralPubMedCrossRef Short VL, Totten PA, Ness RB, Astete SG, Kelsey SF, Haggerty CL. Clinical presentation of Mycoplasma genitalium Infection versus Neisseria gonorrhoeae infection among women with pelvic inflammatory disease. Clin Infect Dis. 2009;48(1):41–7.PubMedCentralPubMedCrossRef
40.
go back to reference Cohen CR, Mugo NR, Astete SG, Odondo R, Manhart LE, Kiehlbauch JA, et al. Detection of Mycoplasma genitalium in women with laparoscopically diagnosed acute salpingitis. Sex Transm Infect. 2005;81(6):463–6.PubMedCentralPubMedCrossRef Cohen CR, Mugo NR, Astete SG, Odondo R, Manhart LE, Kiehlbauch JA, et al. Detection of Mycoplasma genitalium in women with laparoscopically diagnosed acute salpingitis. Sex Transm Infect. 2005;81(6):463–6.PubMedCentralPubMedCrossRef
41.
go back to reference Haggerty CL. Evidence for a role of Mycoplasma genitalium in pelvic inflammatory disease. Curr Opin Infect Dis. 2008;21(1):65–9.PubMedCrossRef Haggerty CL. Evidence for a role of Mycoplasma genitalium in pelvic inflammatory disease. Curr Opin Infect Dis. 2008;21(1):65–9.PubMedCrossRef
42.
go back to reference Svenstrup HF, Fedder J, Kristoffersen SE, Trolle B, Birkelund S, Christiansen G. Mycoplasma genitalium, Chlamydia trachomatis, and tubal factor infertility--a prospective study. Fertil Steril. 2008;90(3):513–20.PubMedCrossRef Svenstrup HF, Fedder J, Kristoffersen SE, Trolle B, Birkelund S, Christiansen G. Mycoplasma genitalium, Chlamydia trachomatis, and tubal factor infertility--a prospective study. Fertil Steril. 2008;90(3):513–20.PubMedCrossRef
43.
go back to reference el Borai N, Inoue M, Lefevre C, Naumova EN, Sato B, Yamamura M. Detection of herpes simplex DNA in semen and menstrual blood of individuals attending an infertility clinic. J Obstet Gynaecol Res. 1997;23(1):17–24.PubMedCrossRef el Borai N, Inoue M, Lefevre C, Naumova EN, Sato B, Yamamura M. Detection of herpes simplex DNA in semen and menstrual blood of individuals attending an infertility clinic. J Obstet Gynaecol Res. 1997;23(1):17–24.PubMedCrossRef
44.
go back to reference Adelson ME, Feola M, Trama J, Tilton RC, Mordechai E. Simultaneous detection of herpes simplex virus types 1 and 2 by real-time PCR and Pyrosequencing. J Clin Virol. 2005;33(1):25–34.PubMedCrossRef Adelson ME, Feola M, Trama J, Tilton RC, Mordechai E. Simultaneous detection of herpes simplex virus types 1 and 2 by real-time PCR and Pyrosequencing. J Clin Virol. 2005;33(1):25–34.PubMedCrossRef
45.
go back to reference Clarke LM, Duerr A, Yeung KH, Brockman S, Barbosa C, Macasaet M. Recovery of cytomegalovirus and herpes simplex virus from upper and lower genital tract specimens obtained from women with pelvic inflammatory disease. J Infect Dis. 1997;176(1):286–8.PubMedCrossRef Clarke LM, Duerr A, Yeung KH, Brockman S, Barbosa C, Macasaet M. Recovery of cytomegalovirus and herpes simplex virus from upper and lower genital tract specimens obtained from women with pelvic inflammatory disease. J Infect Dis. 1997;176(1):286–8.PubMedCrossRef
46.
go back to reference Lehtinen M, Rantala I, Teisala K, Heinonen PK, Lehtinen T, Aine R, et al. Detection of herpes simplex virus in women with acute pelvic inflammatory disease. J Infect Dis. 1985;152(1):78–82.PubMedCrossRef Lehtinen M, Rantala I, Teisala K, Heinonen PK, Lehtinen T, Aine R, et al. Detection of herpes simplex virus in women with acute pelvic inflammatory disease. J Infect Dis. 1985;152(1):78–82.PubMedCrossRef
47.
go back to reference Paavonen J, Teisala K, Heinonen PK, Aine R, Miettinen A, Lehtinen M, et al. Endometritis and acute salpingitis associated with Chlamydia trachomatis and herpes simplex virus type two. Obstet Gynecol. 1985;65(2):288–91.PubMed Paavonen J, Teisala K, Heinonen PK, Aine R, Miettinen A, Lehtinen M, et al. Endometritis and acute salpingitis associated with Chlamydia trachomatis and herpes simplex virus type two. Obstet Gynecol. 1985;65(2):288–91.PubMed
48.
go back to reference Medvedev BI, Teplova SN, Zainetdinova LF. [Diagnostics of genital herpesvirus infection in women with tubal-peritoneal infertility]. Zh Mikrobiol Epidemiol Immunobiol. 2009;2:80–5.PubMed Medvedev BI, Teplova SN, Zainetdinova LF. [Diagnostics of genital herpesvirus infection in women with tubal-peritoneal infertility]. Zh Mikrobiol Epidemiol Immunobiol. 2009;2:80–5.PubMed
49.
go back to reference Tuomivaara LM. Ectopic pregnancy and genital infections: a case–control study. Ann Med. 1990;22(1):21–4.PubMedCrossRef Tuomivaara LM. Ectopic pregnancy and genital infections: a case–control study. Ann Med. 1990;22(1):21–4.PubMedCrossRef
50.
go back to reference Lefrancq T, Orain I, Michalak S, Hourseau M, Fetissof F. Herpetic salpingitis and fallopian tube prolapse. Histopathology. 1999;34(6):548–50.PubMedCrossRef Lefrancq T, Orain I, Michalak S, Hourseau M, Fetissof F. Herpetic salpingitis and fallopian tube prolapse. Histopathology. 1999;34(6):548–50.PubMedCrossRef
51.
go back to reference Kaul R, Nagelkerke NJ, Kimani J, Ngugi E, Bwayo JJ, Macdonald KS, et al. Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis. 2007;196(11):1692–7.PubMedCrossRef Kaul R, Nagelkerke NJ, Kimani J, Ngugi E, Bwayo JJ, Macdonald KS, et al. Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis. 2007;196(11):1692–7.PubMedCrossRef
52.
go back to reference Alberts CJ, van der Loeff MF S, Papenfuss MR, da Silva RJ, Villa LL, Lazcano-Ponce E, et al. Association of Chlamydia trachomatis infection and herpes simplex virus type 2 serostatus with genital human papillomavirus infection in men: the HPV in men study. Sex Transm Dis. 2013;40(6):508–15.PubMedCentralPubMedCrossRef Alberts CJ, van der Loeff MF S, Papenfuss MR, da Silva RJ, Villa LL, Lazcano-Ponce E, et al. Association of Chlamydia trachomatis infection and herpes simplex virus type 2 serostatus with genital human papillomavirus infection in men: the HPV in men study. Sex Transm Dis. 2013;40(6):508–15.PubMedCentralPubMedCrossRef
53.
go back to reference De Seta F, Banco R, Turrisi A, Airoud M, De Leo R, Stabile G, et al. Pelvic inflammatory disease (PID) from Chlamydia trachomatis versus PID from Neisseria gonorrhea: from clinical suspicion to therapy. G Ital Dermatol Venereol. 2012;147(5):423–30.PubMed De Seta F, Banco R, Turrisi A, Airoud M, De Leo R, Stabile G, et al. Pelvic inflammatory disease (PID) from Chlamydia trachomatis versus PID from Neisseria gonorrhea: from clinical suspicion to therapy. G Ital Dermatol Venereol. 2012;147(5):423–30.PubMed
54.
go back to reference Anschuetz GL, Asbel L, Spain CV, Salmon M, Lewis F, Newbern EC, et al. Association between enhanced screening for Chlamydia trachomatis and Neisseria gonorrhoeae and reductions in sequelae among women. J Adolesc Health. 2012;51(1):80–5.PubMedCrossRef Anschuetz GL, Asbel L, Spain CV, Salmon M, Lewis F, Newbern EC, et al. Association between enhanced screening for Chlamydia trachomatis and Neisseria gonorrhoeae and reductions in sequelae among women. J Adolesc Health. 2012;51(1):80–5.PubMedCrossRef
55.
go back to reference Qi H, Liu X, Gu M. Chlamydia trachomatis and Ureaplasma urealyticum infection in patients with tubal pregnancy. Zhonghua Fu Chan Ke Za Zhi. 1997;32(2):93–6.PubMed Qi H, Liu X, Gu M. Chlamydia trachomatis and Ureaplasma urealyticum infection in patients with tubal pregnancy. Zhonghua Fu Chan Ke Za Zhi. 1997;32(2):93–6.PubMed
56.
go back to reference Deng YQ, Wu RF, Guo YY, Wang YJ, Liu ZH. Comparative study of genital tract infection in patients with tubal pregnancy. Zhonghua Fu Chan Ke Za Zhi. 2004;39(2):94–6.PubMed Deng YQ, Wu RF, Guo YY, Wang YJ, Liu ZH. Comparative study of genital tract infection in patients with tubal pregnancy. Zhonghua Fu Chan Ke Za Zhi. 2004;39(2):94–6.PubMed
57.
go back to reference Zhou Y, Xu XL, Wang CP, Zhou M, Zeng XH. Detection and the antibiotic susceptibility analysis of mycoplasma and chlamydia in urogenital tract infections of 327 cases patients with tubal infertility. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 2011;25(3):201–4.PubMed Zhou Y, Xu XL, Wang CP, Zhou M, Zeng XH. Detection and the antibiotic susceptibility analysis of mycoplasma and chlamydia in urogenital tract infections of 327 cases patients with tubal infertility. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 2011;25(3):201–4.PubMed
58.
go back to reference Grzesko J, Elias M, Maczynska B, Kasprzykowska U, Tlaczala M, Goluda M. Frequency of detection of Ureaplasma urealyticum and Mycoplasma hominis in cervical canal and the Douglas pouch of infertile and fertile women. Med Dosw Mikrobiol. 2007;59(2):169–75.PubMed Grzesko J, Elias M, Maczynska B, Kasprzykowska U, Tlaczala M, Goluda M. Frequency of detection of Ureaplasma urealyticum and Mycoplasma hominis in cervical canal and the Douglas pouch of infertile and fertile women. Med Dosw Mikrobiol. 2007;59(2):169–75.PubMed
59.
go back to reference Guven MA, Dilek U, Pata O, Dilek S, Ciragil P. Prevalance of Chlamydia trochomatis, Ureaplasma urealyticum and Mycoplasma hominis infections in the unexplained infertile women. Arch Gynecol Obstet. 2007;276(3):219–23.PubMedCrossRef Guven MA, Dilek U, Pata O, Dilek S, Ciragil P. Prevalance of Chlamydia trochomatis, Ureaplasma urealyticum and Mycoplasma hominis infections in the unexplained infertile women. Arch Gynecol Obstet. 2007;276(3):219–23.PubMedCrossRef
60.
go back to reference Liang X, Gu T, Wang J, Cui H, Wei L. Relationship between ureaplasma urealyticum infection and ectopic pregnancy. Zhonghua Fu Chan Ke Za Zhi. 2007;42(6):370–3.PubMed Liang X, Gu T, Wang J, Cui H, Wei L. Relationship between ureaplasma urealyticum infection and ectopic pregnancy. Zhonghua Fu Chan Ke Za Zhi. 2007;42(6):370–3.PubMed
61.
go back to reference Kasprzykowska U, Elias J, Elias M, Maczynska B, Sobieszczanska BM. Colonization of the lower urogenital tract with Ureaplasma parvum can cause asymptomatic infection of the upper reproductive system in women: a preliminary study. Arch Gynecol Obstet. 2014;289(5):1129–34.PubMedCrossRef Kasprzykowska U, Elias J, Elias M, Maczynska B, Sobieszczanska BM. Colonization of the lower urogenital tract with Ureaplasma parvum can cause asymptomatic infection of the upper reproductive system in women: a preliminary study. Arch Gynecol Obstet. 2014;289(5):1129–34.PubMedCrossRef
62.
go back to reference Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, et al. A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol. 2005;162(6):585–90.PubMedCrossRef Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, et al. A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol. 2005;162(6):585–90.PubMedCrossRef
64.
go back to reference Gasanova TA. Parasitic diseases are a risk factor of inflammations of the small pelvis organs. Trichomoniasis. Med Parazitol (Mosk). 2002;1:3–8. Gasanova TA. Parasitic diseases are a risk factor of inflammations of the small pelvis organs. Trichomoniasis. Med Parazitol (Mosk). 2002;1:3–8.
65.
go back to reference Cherpes TL, Wiesenfeld HC, Melan MA, Kant JA, Cosentino LA, Meyn LA, et al. The associations between pelvic inflammatory disease, Trichomonas vaginalis infection, and positive herpes simplex virus type 2 serology. Sex Transm Dis. 2006;33(12):747–52.PubMedCrossRef Cherpes TL, Wiesenfeld HC, Melan MA, Kant JA, Cosentino LA, Meyn LA, et al. The associations between pelvic inflammatory disease, Trichomonas vaginalis infection, and positive herpes simplex virus type 2 serology. Sex Transm Dis. 2006;33(12):747–52.PubMedCrossRef
66.
go back to reference Hammond TL, Hankins GD, Snyder RR. Transvaginal-peritoneal migration of Trichomonas vaginalis as a cause of ascites. A report of two cases. J Reprod Med. 1990;35(2):179–81.PubMed Hammond TL, Hankins GD, Snyder RR. Transvaginal-peritoneal migration of Trichomonas vaginalis as a cause of ascites. A report of two cases. J Reprod Med. 1990;35(2):179–81.PubMed
67.
go back to reference Suriyanon V, Nelson KE, Choomsai na Ayudhya V. Trichomonas vaginalis in a perinephric abscess. A case report. Am J Trop Med Hyg. 1975;24(5):776–80.PubMed Suriyanon V, Nelson KE, Choomsai na Ayudhya V. Trichomonas vaginalis in a perinephric abscess. A case report. Am J Trop Med Hyg. 1975;24(5):776–80.PubMed
68.
go back to reference Paisarntantiwong R, Brockmann S, Clarke L, Landesman S, Feldman J, Minkoff H. The relationship of vaginal trichomoniasis and pelvic inflammatory disease among women colonized with Chlamydia trachomatis. Sex Transm Dis. 1995;22(6):344–7.PubMedCrossRef Paisarntantiwong R, Brockmann S, Clarke L, Landesman S, Feldman J, Minkoff H. The relationship of vaginal trichomoniasis and pelvic inflammatory disease among women colonized with Chlamydia trachomatis. Sex Transm Dis. 1995;22(6):344–7.PubMedCrossRef
69.
go back to reference Coleman JS, Gaydos CA, Witter F. Trichomonas vaginalis vaginitis in obstetrics and gynecology practice: new concepts and controversies. Obstet Gynecol Surv. 2013;68(1):43–50.PubMedCentralPubMedCrossRef Coleman JS, Gaydos CA, Witter F. Trichomonas vaginalis vaginitis in obstetrics and gynecology practice: new concepts and controversies. Obstet Gynecol Surv. 2013;68(1):43–50.PubMedCentralPubMedCrossRef
70.
go back to reference Fettweis JM, Serrano MG, Huang B, Brooks JP, Glascock AL, Sheth NU, et al. An emerging mycoplasma associated with trichomoniasis, vaginal infection and disease. PLoS One. 2014;9(10), e110943.PubMedCentralPubMedCrossRef Fettweis JM, Serrano MG, Huang B, Brooks JP, Glascock AL, Sheth NU, et al. An emerging mycoplasma associated with trichomoniasis, vaginal infection and disease. PLoS One. 2014;9(10), e110943.PubMedCentralPubMedCrossRef
72.
go back to reference Bashi S. Chlamydial genital infection. Saudi Med J. 1986;7:484–9. Bashi S. Chlamydial genital infection. Saudi Med J. 1986;7:484–9.
73.
go back to reference Bashi S, Siddique M, Al-Shawaf T. Chlamydial infection in Riyadh, Saudi Arabia: A sero-epidemiological survey. Saudi Med J. 1987;8:387–90. Bashi S, Siddique M, Al-Shawaf T. Chlamydial infection in Riyadh, Saudi Arabia: A sero-epidemiological survey. Saudi Med J. 1987;8:387–90.
74.
go back to reference Ghazi HO, Daghestani MH, Mohamed MF. Seropositivity of Chlamydia trachomatis among saudi pregnant women in makkah. J Family Community Med. 2006;13(2):61–4.PubMedCentralPubMed Ghazi HO, Daghestani MH, Mohamed MF. Seropositivity of Chlamydia trachomatis among saudi pregnant women in makkah. J Family Community Med. 2006;13(2):61–4.PubMedCentralPubMed
75.
go back to reference Jamjoom GA, Gozar JC, Quli SK. Low rate of isolation of Chlamydia trachomatis from Saudi Obstretrics/Gynaecology Patients. Saudi Med J. 1994;15:143–6. Jamjoom GA, Gozar JC, Quli SK. Low rate of isolation of Chlamydia trachomatis from Saudi Obstretrics/Gynaecology Patients. Saudi Med J. 1994;15:143–6.
76.
go back to reference Al-Gelban KS, Al-Shahrani MS, Al Sunaidi MI, Mostafa OA. Screening for Chlamydia genital infection among females undergoing in vitro fertilization in Saudi Arabia. The Medical Journal of Cairo University. 2010;78:251-256. Al-Gelban KS, Al-Shahrani MS, Al Sunaidi MI, Mostafa OA. Screening for Chlamydia genital infection among females undergoing in vitro fertilization in Saudi Arabia. The Medical Journal of Cairo University. 2010;78:251-256.
77.
go back to reference Hossain A. Herpes simplex virus type 1 (HSV-1) and varicella-zoster virus (VZV) infections in Saudi Arabia. J Trop Pediatr. 1989;35(4):171–4.PubMedCrossRef Hossain A. Herpes simplex virus type 1 (HSV-1) and varicella-zoster virus (VZV) infections in Saudi Arabia. J Trop Pediatr. 1989;35(4):171–4.PubMedCrossRef
78.
go back to reference Hossain A, Bakir TM. Rubella and cytomegalovirus (CMV) infections: laboratory aspects of investigation of antenatal, congenital, persistent, and subclinical infections. J Trop Pediatr. 1989;35(5):225–9.PubMedCrossRef Hossain A, Bakir TM. Rubella and cytomegalovirus (CMV) infections: laboratory aspects of investigation of antenatal, congenital, persistent, and subclinical infections. J Trop Pediatr. 1989;35(5):225–9.PubMedCrossRef
79.
go back to reference Ghazi HO, Telmesani AM, Mahomed MF. TORCH agents in pregnant Saudi women. Med Princ Pract. 2002;11(4):180–2.PubMedCrossRef Ghazi HO, Telmesani AM, Mahomed MF. TORCH agents in pregnant Saudi women. Med Princ Pract. 2002;11(4):180–2.PubMedCrossRef
80.
go back to reference Obeid OE. Prevalence of herpes simplex virus types 1 and 2 and associated sociodemographic variables in pregnant women attending king fahd hospital of the university. J Family Community Med. 2007;14(1):3–7.PubMedCentralPubMed Obeid OE. Prevalence of herpes simplex virus types 1 and 2 and associated sociodemographic variables in pregnant women attending king fahd hospital of the university. J Family Community Med. 2007;14(1):3–7.PubMedCentralPubMed
81.
go back to reference Refaat B, Ashshi AM, Batwa SA, El-Shemi AG. Seroprevalence of Chlamydia trachomatis, cytomegalovirus, herpes simplex virus 1 and 2 in Saudi women with normal and abnormal early pregnancy: A case control study. African Journal of Microbiology Research. 2014;8(40):3565–9.CrossRef Refaat B, Ashshi AM, Batwa SA, El-Shemi AG. Seroprevalence of Chlamydia trachomatis, cytomegalovirus, herpes simplex virus 1 and 2 in Saudi women with normal and abnormal early pregnancy: A case control study. African Journal of Microbiology Research. 2014;8(40):3565–9.CrossRef
Metadata
Title
Prevalence of 7 sexually transmitted organisms by multiplex real-time PCR in Fallopian tube specimens collected from Saudi women with and without ectopic pregnancy
Authors
Ahmed Mohamed Ashshi
Sarah Abdullah Batwa
Seham Yahia Kutbi
Faizah Ahmed Malibary
Mohamed Batwa
Bassem Refaat
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2015
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-015-1313-1

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