Experimental intravaginal and intrauterine endometritis model: which model is more useful?
Year 2022,
Volume: 7 Issue: 3, 366 - 375, 31.12.2022
Mustafa Makav
,
Mushap Kuru
,
Hatice Beşeren
,
Yasemen Adalı
,
Mustafa Reha Coşkun
,
Hüseyin Avni Eroğlu
Abstract
Objectives: This study aims to compare the newly created intravaginal endometritis model (IVM) with the intrauterine endometritis model (IUM).
Methods: E. coli infusion was performed as intravaginally to the IVM and as intrauterinally to the IUM. The lives of all animals were terminated on the 7th day. Histopathological and biochemical analyses (GSH, MDA, Endocan, Endoglin) were performed.
Results: A significant inflammation was determined in IVM and IUM compared to the control. A significant decrease in GSH and a significant increase in MDA and Endoglin were determined in IVM and IUM compared to the control. There was a statistical increase in the IUM and a numerical increase in the IVM compared to the control. Endometritis was determined by histopathological and biochemical analyses in both IUM and IVM as a result.
Conclusion: It is predicted in this context that intravaginal administration, which is easier to perform, can be used in experimental studies.
Supporting Institution
Scientific Research Projects Coordinatorship of Kafkas University
Project Number
2022-TS-13
References
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Cicinelli, E., De Ziegler, D., Nicoletti, R., Colafiglio, G., Saliani, N., Resta, L., Rizzi, D., & De Vito, D. (2008). Chronic endometritis: Correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertility and Sterility, 89(3), 677–684. https://doi.org/10.1016/j.fertnstert.2007.03.074
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- Cohen, C. R., Manhart, L. E., Bukusi, E. A., Astete, S., Brunham, R. C., Holmes, K. K., Sinei, S. K., Bwayo, J. J., & Totten, P. A. (2002). Association between mycoplasma genitalium and acute endometritis. The Lancet, 359(9308), 765–766. https://doi.org/10.1016/S0140-6736(02)07848-0
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- Demirel, M. A., Han, S., Tokmak, A., Gokay, N. E., Uludag, M. O., Ustun, T. Y., & Cicek, A. F. (2019). Therapeutic effects of resveratrol in Escherichia coli-induced rat endometritis model. Naunyn-Schmiedeberg’s Archives of Pharmacology, 392(12), 1577–1589.
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- Herath, S., Lilly, S. T., Fischer, D. P., Williams, E. J., Dobson, H., Bryant, C. E., & Sheldon, I. M. (2009). Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin F2α to prostaglandin E2 in bovine endometrium. Endocrinology, 150(4), 1912–1920.
- Kaygusuzoglu, E., Caglayan, C., Kandemir, F. M., Yıldırım, S., Kucukler, S., Kılınc, M. A., & Saglam, Y. S. (2018). Zingerone ameliorates cisplatin‐induced ovarian and uterine toxicity via suppression of sex hormone imbalances, oxidative stress, inflammation and apoptosis in female wistar rats. Biomedicine & Pharmacotherapy, 102, 517–530. https://doi.org/10.1016/j.biopha.2018.03.119
- Kitaya, K., Matsubayashi, H., Takaya, Y., Nishiyama, R., Yamaguchi, K., Takeuchi, T., & Ishikawa, T. (2017). Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure. American Journal of Reproductive Immunology, 78(5), e12719. https://doi.org/10.1111/aji.12719
- Kitaya, K., Takeuchi, T., Mizuta, S., Matsubayashi, H., & Ishikawa, T. (2018). Endometritis: New time, new concepts. Fertility and Sterility, 110(3), 344–350. https://doi.org/10.1016/j.fertnstert.2018.04.012
- Kiviat, N. B., Wølner-Hanssen, P., Eschenbach, D. A., Wasserheit, J. N., Paavonen, J. A., Bell, T. A., Critchlow, C. W., Stamm, W. E., Moore, D. E., & Holmes, K. K. (1990). Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis. The American Journal of Surgical Pathology, 14(2), 167–175.
- Kuru, M., Öğün, M., Kulaksız, R., Kükürt, A., & Oral, H. (2018). Comparison of oxidative/nitrosative stress, leptin and progesterone concentrations in pregnant and non-pregnant abaza goats synchronized with controlled internal drug release application. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(6), 887–892.
- Laloglu, E., Kumtepe, Y., Aksoy, H., & Yilmaz, E. P. T. (2017). Serum endocan levels in endometrial and ovarian cancers. Journal of Clinical Laboratory Analysis, 31(5), e22079. https://doi.org/10.1002/jcla.22079
- Mazaheri-Tirani, M., & Madadkar Haghjou, M. (2019). Reactive oxygen species (ROS), Total antioxidant capacity (AOC) and Malondialdehyde (MDA) make a triangle in evaluation of Zinc stress extension. Journal of Animal and Plant Sciences, 29.
- McQueen, D. B., Perfetto, C. O., Hazard, F. K., & Lathi, R. B. (2015). Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss. Fertility and Sterility, 104(4), 927–931. https://doi.org/10.1016/j.fertnstert.2015.06.044
- Mitsui, H., Shibata, K., Mano, Y., Suzuki, S., Umezu, T., Mizuno, M., Yamamoto, E., Kajiyama, H., Kotani, T., Senga, T., & Kikkawa, F. (2013). The expression and characterization of endoglin in uterine leiomyosarcoma. Clinical & Experimental Metastasis, 30(6), 731–740. https://doi.org/10.1007/s10585-013-9574-9
- Mohammed, Z. A., Mann, G. E., & Robinson, R. S. (2019). Impact of endometritis on post-partum ovarian cyclicity in dairy cows. The Veterinary Journal, 248, 8–13. https://doi.org/10.1016/j.tvjl.2019.03.008
- Ness, R., & Brooks-nelson, D. (2000). 29—Pelvic Inflammatory Disease. In M. B. Goldman & M. C. Hatch (Eds.), Women and Health (pp. 369–380). Academic Press. https://doi.org/10.1016/B978-012288145-9/50033-4
- Ngô, C., Chéreau, C., Nicco, C., Weill, B., Chapron, C., & Batteux, F. (2009). Reactive oxygen species controls endometriosis progression. The American Journal of Pathology, 175(1), 225–234. https://doi.org/10.2353/ajpath.2009.080804
- Nishikawa, Y., & Baba, T. (1985). Effects of ovarian hormones on manifestation of purulent endometritis in rat uteruses infected with Escherichia coli. Infection and Immunity, 47(1), 311–317.
- Roberts, R. A., Laskin, D. L., Smith, C. V., Robertson, F. M., Allen, E. M. G., Doorn, J. A., & Slikker, W. (2009). Nitrative and oxidative stress in toxicology and disease. Toxicological Sciences, 112(1), 4–16. https://doi.org/10.1093/toxsci/kfp179
- Salah, N., & Yimer, N. (2017). Cytological endometritis and its agreement with ultrasound examination in postpartum beef cows. Veterinary World, 10(6), 605–609. https://doi.org/10.14202/vetworld.2017.605-609
- Sarrazin, S., Adam, E., Lyon, M., Depontieu, F., Motte, V., Landolfi, C., Lortat-Jacob, H., Bechard, D., Lassalle, P., & Delehedde, M. (2006). Endocan or endothelial cell specific molecule-1 (ESM-1): A potential novel endothelial cell marker and a new target for cancer therapy. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, 1765(1), 25–37. https://doi.org/10.1016/j.bbcan.2005.08.004
- Sheldon, I. M., Cronin, J., Goetze, L., Donofrio, G., & Schuberth, H.-J. (2009). Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction, 81(6), 1025–1032.
- Sheldon, I. M., & Dobson, H. (2004). Postpartum uterine health in cattle. Animal Reproduction Science, 82–83, 295–306. https://doi.org/10.1016/j.anireprosci.2004.04.006
- Sheldon, I., Noakes, D., Rycroft, A., Pfeiffer, D., & Dobson, H. (2002). Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction (Cambridge, England), 123, 837–845. https://doi.org/10.1530/rep.0.1230837
- Ten Dijke, P., Goumans, M.-J., & Pardali, E. (2008). Endoglin in angiogenesis and vascular diseases. Angiogenesis, 11(1), 79–89.
- Tiwari, A., Singh, P., Jaitley, P., Sharma, S., Prakash, A., Mandil, R., Choudhury, S., Gangwar, N. K., & Garg, S. K. (2018). Eucalyptus robusta leaves methanolic extract suppresses inflammatory mediators by specifically targeting TLR4/TLR9, MPO, COX2, iNOS and inflammatory cytokines in experimentally-induced endometritis in rats. Journal of Ethnopharmacology, 213, 149–158. https://doi.org/10.1016/j.jep.2017.10.035
- Wiesenfeld, H., & Paavonen, J. (2010). 6—Pelvic Inflammatory Disease. In S. A. Morse, R. C. Ballard, K. K. Holmes, & A. A. Moreland (Eds.), Atlas of Sexually Transmitted Diseases and AIDS (Fourth Edition) (pp. 94–110). W.B. Saunders. https://doi.org/10.1016/B978-0-7020-4060-3.00006-5
- Xiao, H.-B., Sui, G.-G., Lu, X.-Y., & Sun, Z.-L. (2018). Elevated levels of ADMA are associated with lower DDAH2 and higher PRMT1 in LPS-Induced endometritis rats. Inflammation, 41(1), 299–306. https://doi.org/10.1007/s10753-017-0687-1
- Yoshioka, T., Kawada, K., Shimada, T., & Mori, M. (1979). Lipid peroxidation in maternal and cord blood and protective mechanisms. Am J Obstet Gynecol, 135, 972–976.
Year 2022,
Volume: 7 Issue: 3, 366 - 375, 31.12.2022
Mustafa Makav
,
Mushap Kuru
,
Hatice Beşeren
,
Yasemen Adalı
,
Mustafa Reha Coşkun
,
Hüseyin Avni Eroğlu
Project Number
2022-TS-13
References
- Adnane, M., Kaidi, R., Hanzen, C., & England, G. C. W. (2017). Risk factors of clinical and subclinical endometritis in cattle: A review. Turkish Journal of Veterinary & Animal Sciences, 41, 1–11.
- Afsar, B., Takir, M., Kostek, O., Covic, A., & Kanbay, M. (2014). Endocan: A new molecule playing a role in the development of hypertension and chronic kidney disease? The Journal of Clinical Hypertension, 16(12), 914–916. https://doi.org/10.1111/jch.12440
- Balta, S., Mikhailidis, D. P., Demirkol, S., Ozturk, C., Celik, T., & Iyisoy, A. (2015). Endocan: A novel inflammatory indicator in cardiovascular disease? Atherosclerosis, 243(1), 339–343. https://doi.org/10.1016/j.atherosclerosis.2015.09.030
- Baydın, P. Ö., & Akbulut, H. (2013). Designing gene therapy vectors targeting tumor cell endothelium. TURKISH JOURNAL OF ONCOLOGY, 28(4), 179–186.
- Beutler, E., Duron, O., & Kelly, B. (1963). Improved method for the determination of blood glutathione. J. Lab. Clin. Med., 61, 882–888.
Cicinelli, E., De Ziegler, D., Nicoletti, R., Colafiglio, G., Saliani, N., Resta, L., Rizzi, D., & De Vito, D. (2008). Chronic endometritis: Correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertility and Sterility, 89(3), 677–684. https://doi.org/10.1016/j.fertnstert.2007.03.074
- Cicinelli, E., Ziegler, D. D., Nicoletti, R., Tinelli, R., Saliani, N., Resta, L., Bellavia, M., & Vito, D. D. (2009). Poor reliability of vaginal and endocervical cultures for evaluating microbiology of endometrial cavity in women with chronic endometritis. Gynecologic and Obstetric Investigation, 68(2), 108–115. https://doi.org/10.1159/000223819
- Cohen, C. R., Manhart, L. E., Bukusi, E. A., Astete, S., Brunham, R. C., Holmes, K. K., Sinei, S. K., Bwayo, J. J., & Totten, P. A. (2002). Association between mycoplasma genitalium and acute endometritis. The Lancet, 359(9308), 765–766. https://doi.org/10.1016/S0140-6736(02)07848-0
- Cora, M. C., Kooistra, L., & Travlos, G. (2015). Vaginal cytology of the laboratory rat and mouse: Review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicologic Pathology, 43(6), 776–793. https://doi.org/10.1177/0192623315570339
- Demirel, M. A., Han, S., Tokmak, A., Gokay, N. E., Uludag, M. O., Ustun, T. Y., & Cicek, A. F. (2019). Therapeutic effects of resveratrol in Escherichia coli-induced rat endometritis model. Naunyn-Schmiedeberg’s Archives of Pharmacology, 392(12), 1577–1589.
- Franco, R., Schoneveld, O., Pappa, A., & Panayiotidis, M. (2007). The central role of glutathione in the pathophysiology of human disease. Archives of Physiology and Biochemistry, 113, 234–258. https://doi.org/10.1080/13813450701661198
- Garcia, L. (n.d.). Preparation of routine media and reagents used in antimicrobial susceptibility testing. In Clinical Microbiology Procedures Handbook (3rd Edition, p. p 181-201). ASM Press.
- Güralp, O., Acikgöz, S., Tüten, N., Ekmekci, H., Schild-Suhren, M., Malik, E., & Tüten, A. (2020). Evaluation of serum endocan levels in endometriosis: A case-control study: Evaluation of serum endocan levels in endometriosis: A case-control study. La Clinica Terapeutica, 171(6).
- Hawinkels, L. J. A. C., Kuiper, P., Wiercinska, E., Verspaget, H. W., Liu, Z., Pardali, E., Sier, C. F. M., & Dijke, P. ten. (2010). Matrix metalloproteinase-14 (MT1-MMP)–mediated endoglin shedding inhibits tumor angiogenesis. Cancer Research, 70(10), 4141–4150. https://doi.org/10.1158/0008-5472.CAN-09-4466
- He, C., Wu, R., Li, L., Wang, X., Wang, J., Wang, S., Liu, W., & Yang, K. (2008). Establishment of a rat model of endometritis and its treatment with a Chinese-Western medicine emulsion. Acta Laboratorium Animalis Scientia Sinica, 3.
- Herath, S., Lilly, S. T., Fischer, D. P., Williams, E. J., Dobson, H., Bryant, C. E., & Sheldon, I. M. (2009). Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin F2α to prostaglandin E2 in bovine endometrium. Endocrinology, 150(4), 1912–1920.
- Kaygusuzoglu, E., Caglayan, C., Kandemir, F. M., Yıldırım, S., Kucukler, S., Kılınc, M. A., & Saglam, Y. S. (2018). Zingerone ameliorates cisplatin‐induced ovarian and uterine toxicity via suppression of sex hormone imbalances, oxidative stress, inflammation and apoptosis in female wistar rats. Biomedicine & Pharmacotherapy, 102, 517–530. https://doi.org/10.1016/j.biopha.2018.03.119
- Kitaya, K., Matsubayashi, H., Takaya, Y., Nishiyama, R., Yamaguchi, K., Takeuchi, T., & Ishikawa, T. (2017). Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure. American Journal of Reproductive Immunology, 78(5), e12719. https://doi.org/10.1111/aji.12719
- Kitaya, K., Takeuchi, T., Mizuta, S., Matsubayashi, H., & Ishikawa, T. (2018). Endometritis: New time, new concepts. Fertility and Sterility, 110(3), 344–350. https://doi.org/10.1016/j.fertnstert.2018.04.012
- Kiviat, N. B., Wølner-Hanssen, P., Eschenbach, D. A., Wasserheit, J. N., Paavonen, J. A., Bell, T. A., Critchlow, C. W., Stamm, W. E., Moore, D. E., & Holmes, K. K. (1990). Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis. The American Journal of Surgical Pathology, 14(2), 167–175.
- Kuru, M., Öğün, M., Kulaksız, R., Kükürt, A., & Oral, H. (2018). Comparison of oxidative/nitrosative stress, leptin and progesterone concentrations in pregnant and non-pregnant abaza goats synchronized with controlled internal drug release application. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(6), 887–892.
- Laloglu, E., Kumtepe, Y., Aksoy, H., & Yilmaz, E. P. T. (2017). Serum endocan levels in endometrial and ovarian cancers. Journal of Clinical Laboratory Analysis, 31(5), e22079. https://doi.org/10.1002/jcla.22079
- Mazaheri-Tirani, M., & Madadkar Haghjou, M. (2019). Reactive oxygen species (ROS), Total antioxidant capacity (AOC) and Malondialdehyde (MDA) make a triangle in evaluation of Zinc stress extension. Journal of Animal and Plant Sciences, 29.
- McQueen, D. B., Perfetto, C. O., Hazard, F. K., & Lathi, R. B. (2015). Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss. Fertility and Sterility, 104(4), 927–931. https://doi.org/10.1016/j.fertnstert.2015.06.044
- Mitsui, H., Shibata, K., Mano, Y., Suzuki, S., Umezu, T., Mizuno, M., Yamamoto, E., Kajiyama, H., Kotani, T., Senga, T., & Kikkawa, F. (2013). The expression and characterization of endoglin in uterine leiomyosarcoma. Clinical & Experimental Metastasis, 30(6), 731–740. https://doi.org/10.1007/s10585-013-9574-9
- Mohammed, Z. A., Mann, G. E., & Robinson, R. S. (2019). Impact of endometritis on post-partum ovarian cyclicity in dairy cows. The Veterinary Journal, 248, 8–13. https://doi.org/10.1016/j.tvjl.2019.03.008
- Ness, R., & Brooks-nelson, D. (2000). 29—Pelvic Inflammatory Disease. In M. B. Goldman & M. C. Hatch (Eds.), Women and Health (pp. 369–380). Academic Press. https://doi.org/10.1016/B978-012288145-9/50033-4
- Ngô, C., Chéreau, C., Nicco, C., Weill, B., Chapron, C., & Batteux, F. (2009). Reactive oxygen species controls endometriosis progression. The American Journal of Pathology, 175(1), 225–234. https://doi.org/10.2353/ajpath.2009.080804
- Nishikawa, Y., & Baba, T. (1985). Effects of ovarian hormones on manifestation of purulent endometritis in rat uteruses infected with Escherichia coli. Infection and Immunity, 47(1), 311–317.
- Roberts, R. A., Laskin, D. L., Smith, C. V., Robertson, F. M., Allen, E. M. G., Doorn, J. A., & Slikker, W. (2009). Nitrative and oxidative stress in toxicology and disease. Toxicological Sciences, 112(1), 4–16. https://doi.org/10.1093/toxsci/kfp179
- Salah, N., & Yimer, N. (2017). Cytological endometritis and its agreement with ultrasound examination in postpartum beef cows. Veterinary World, 10(6), 605–609. https://doi.org/10.14202/vetworld.2017.605-609
- Sarrazin, S., Adam, E., Lyon, M., Depontieu, F., Motte, V., Landolfi, C., Lortat-Jacob, H., Bechard, D., Lassalle, P., & Delehedde, M. (2006). Endocan or endothelial cell specific molecule-1 (ESM-1): A potential novel endothelial cell marker and a new target for cancer therapy. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, 1765(1), 25–37. https://doi.org/10.1016/j.bbcan.2005.08.004
- Sheldon, I. M., Cronin, J., Goetze, L., Donofrio, G., & Schuberth, H.-J. (2009). Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction, 81(6), 1025–1032.
- Sheldon, I. M., & Dobson, H. (2004). Postpartum uterine health in cattle. Animal Reproduction Science, 82–83, 295–306. https://doi.org/10.1016/j.anireprosci.2004.04.006
- Sheldon, I., Noakes, D., Rycroft, A., Pfeiffer, D., & Dobson, H. (2002). Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction (Cambridge, England), 123, 837–845. https://doi.org/10.1530/rep.0.1230837
- Ten Dijke, P., Goumans, M.-J., & Pardali, E. (2008). Endoglin in angiogenesis and vascular diseases. Angiogenesis, 11(1), 79–89.
- Tiwari, A., Singh, P., Jaitley, P., Sharma, S., Prakash, A., Mandil, R., Choudhury, S., Gangwar, N. K., & Garg, S. K. (2018). Eucalyptus robusta leaves methanolic extract suppresses inflammatory mediators by specifically targeting TLR4/TLR9, MPO, COX2, iNOS and inflammatory cytokines in experimentally-induced endometritis in rats. Journal of Ethnopharmacology, 213, 149–158. https://doi.org/10.1016/j.jep.2017.10.035
- Wiesenfeld, H., & Paavonen, J. (2010). 6—Pelvic Inflammatory Disease. In S. A. Morse, R. C. Ballard, K. K. Holmes, & A. A. Moreland (Eds.), Atlas of Sexually Transmitted Diseases and AIDS (Fourth Edition) (pp. 94–110). W.B. Saunders. https://doi.org/10.1016/B978-0-7020-4060-3.00006-5
- Xiao, H.-B., Sui, G.-G., Lu, X.-Y., & Sun, Z.-L. (2018). Elevated levels of ADMA are associated with lower DDAH2 and higher PRMT1 in LPS-Induced endometritis rats. Inflammation, 41(1), 299–306. https://doi.org/10.1007/s10753-017-0687-1
- Yoshioka, T., Kawada, K., Shimada, T., & Mori, M. (1979). Lipid peroxidation in maternal and cord blood and protective mechanisms. Am J Obstet Gynecol, 135, 972–976.