Theriogenology
Volume 73, Issue 6 , Pages 758-767 , 1 April 2010

Sampling techniques for oviductal and uterine luminal fluid in cattle

  • M.A. Velazquez

      Affiliations

    • Department of Biotechnology, Institute of Farm Animal Genetics, Friedrich-Loeffler-Institute (FLI), Höltystrasse 10 Mariensee, 31535 Neustadt, Germany
    • Escuela Superior de Ciencias Agropecuarias, Universidad Autónoma de Campeche, Calle 53s/n, C.P. 24350, Escárcega, Campeche, Mexico
  • ,
  • I. Parrilla

      Affiliations

    • Department of Animal Medicine and Surgery, Faculty of Veterinary Science, University of Murcia, E-30071 Murcia, Spain
  • ,
  • A. Van Soom

      Affiliations

    • Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium
  • ,
  • S. Verberckmoes

      Affiliations

    • Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium
  • ,
  • W. Kues

      Affiliations

    • Department of Biotechnology, Institute of Farm Animal Genetics, Friedrich-Loeffler-Institute (FLI), Höltystrasse 10 Mariensee, 31535 Neustadt, Germany
  • ,
  • H. Niemann

      Affiliations

    • Department of Biotechnology, Institute of Farm Animal Genetics, Friedrich-Loeffler-Institute (FLI), Höltystrasse 10 Mariensee, 31535 Neustadt, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 5034 871136; fax: +49 5034 871143.

Received 28 March 2009 ,Accepted 28 April 2009.

References 

  1. Wolf E, Arnold GJ, Bauersachs S, Beier HM, Blum H, Einspanier R, et al. Embryo-maternal communication in bovine-strategies for deciphering a complex cross-talk. Reprod Domest Anim. 2003;38:276–289
  2. Leese HJ, Hugentobler SA, Gray SM, Morris DG, Sturmey RG, Whitear SL, et al. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev. 2008;20:1–8
  3. Inskeep EK, Dailey RA. Embryonic death in cattle. Vet Clin North Am Food Anim Pract. 2005;21:437–461
  4. Diskin MG, Morris DG. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim. 2008;43(Suppl. 2):260–267
  5. Looney CR, Nelson JS, Schneider HJ, Forrest DW. Improving fertility in beef cow recipients. Theriogenology. 2006;65:201–209
  6. Martin JL, Vonnahme KA, Adams DC, Lardy GP, Funston RN. Effects of dam nutrition on growth and reproductive performance of heifer calves. J Anim Sci. 2007;85:841–847
  7. Vonnahme KA, Zhu MJ, Borowicz PP, Geary TW, Hess BW, Reynolds LP, et al. Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome. J Anim Sci. 2007;85:2464–2472
  8. Han H, Hansen TR, Berg B, Hess BW, Ford SP. Maternal undernutrition induces differential cardiac gene expression in pulmonary hypertensive steers at high elevation. Am J Physiol Heart Circ Physiol. 2008;295:H382–H389
  9. McMillen IC, MacLaughlin SM, Muhlhausler BS, Gentili S, Duffield JL, Morrison JL. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol. 2008;102:82–89
  10. Gardner DS, Lea RG, Sinclair KD. Developmental programming of reproduction and fertility: what is the evidence?. Animal. 2008;2:1128–1134
  11. Brown JR. A chronology of major events in obstetrics and gynaecology. Br J Obstet Gynaecol. 1964;71:302–309
  12. In:  Hafez ESE, Blandau RJ  editor. The Mammalian Oviduct. University of Chicago Press; 1969;
  13. Talbot P, Shur BD, Myles DG. Cell adhesion and fertilization: steps in oocyte transport, sperm-zona pellucida interactions, and sperm egg fusion. Biol Reprod. 2003;68:1–9
  14. Rodriguez-Martinez H. Role of the oviduct in sperm capacitation. Theriogenology. 2007;68(Suppl. 1):138–146
  15. Hunter RHF. Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles. Mol Reprod Dev. 2008;75:167–174
  16. Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121:339–346
  17. Killian GJ. Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim Reprod Sci. 2004;82–83:141–153
  18. Hunter RHF. The fallopian tubes in domestic mammals: how vital is their physiological activity?. Reprod Nutr Dev. 2005;45:281–290
  19. Olds D, Vandemark NL. The behavior of spermatozoa in luminal fluids of bovine female genitalia. Am J Vet Res. 1957;18:603–607
  20. Olds D, Vandemark NL. Composition of luminal fluids in bovine female genitalia. Fertil Steril. 1957;8:345–354
  21. Carlson D, Black DL, Howe GR. Oviduct secretion in the cow. J Reprod Fertil. 1970;22:549–552
  22. Stanke DF, Deyoung DW, Sikes JD, Mather EC. Collection of bovine oviduct secretions. J Reprod Fertil. 1973;32:535–537
  23. Roberts GP, Parker JM, Symonds HW. Proteins in the luminal fluid from the bovine oviduct. J Reprod Feril. 1975;45:301–313
  24. Kavanaugh JF, Killian GJ. Bovine oviductal cannulations. J Invest Surg. 1988;1:201–208
  25. Kavanaugh JF, Grippo AA, Killian GJ. Cannulation of the bovine ampullary and isthmic oviduct. J Invest Surg. 1992;5:11–17
  26. Greve T, Schmidt M, Høst Hansen T. Collection of oviduct fluid in heifers. Dtsch Tierarztl Wochenschr. 1996;103:291–293
  27. Bergqvist A-S, Killian G, Erikson D, Hoshino Y, Båge R, Sato E, et al. Detection of Fas ligand in the bovine oviduct. Anim Reprod Sci. 2005;86:71–88
  28. Bergqvist A-S, Rodríguez-Martínez H. Sulphated glycosaminoglycans (S-GAGs) and syndecans in the bovine oviduct. Anim Reprod Sci. 2006;93:46–60
  29. Hunter RHF. Have the fallopian tubes a vital role in promoting fertility?. Acta Obstet Gynecol Scand. 1998;77:475–486
  30. Kenny DA, Humpherson P, Leese HJ, Morris DG, Tomos AD, Diskin MG, et al. Effect of elevated systemic concentrations of ammonia and urea on the metabolite and ionic composition of oviductal fluid in cattle. Biol Repro. 2002;66:1797–1804
  31. Hugentobler SA, Diskin MG, Leese HJ, Humpherson PG, Watson T, Sreenan JM, et al. Amino acids in the oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Mol Reprod Dev. 2007;74:445–454
  32. Hugentobler SA, Morris DG, Sreenan JM, Diskin MG. Ion concentrations in oviduct and uterine fluid and blood serum during the oestrous cycle in the bovine. Theriogenology. 2007;68:538–548
  33. Hugentobler SA, Humpherson PG, Leese HJ, Sreenan JM, Morris DG. Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Mol Reprod Dev. 2008;75:496–503
  34. Gonçalves RF, Staros AL, Killian GJ. Oviductal fluid proteins associated with the bovine zona pellucida and the effect of in vitro sperm-egg binding, fertilization and embryo development. Reprod Domest Anim. 2008;43:720–729
  35. Souza CEA, Moura AA, Monaco E, Killian GJ. Binding patterns of bovine seminal plasma proteins A1/A2, 30 kDa and osteopontin on ejaculated sperm before and after incubation with isthmic and ampullary oviductal fluid. Anim Reprod Sci. 2008;105:72–89
  36. Klaritsch P, Albert K, Van Mieghem T, Gucciardo L, Done’ E, Bynens B, et al. Instrumental requirements for minimal invasive fetal surgery. BJOG. 2009;116:188–197
  37. Haga Y, Matsunaga T, Makishi W, Totsu K, Mineta T, Esashi M. Minimally invasive diagnostics and treatment using micro/nano machining. Minim Invasive Ther Allied Technol. 2006;15:218–225
  38. Heap RB, Lamming GE. Studies on the uterine secretion of different species. Proc IV Int Congr Anim Reprod, The Hague. 1961;pp. 300–11
  39. Beier HM. The discovery of uteroglobin and its significance for reproductive biology and endocrinology. Ann NY Acad Sci. 2000;923:9–24
  40. Hamilton WJ, Laing JA. Development of the egg of the cow up to the stage of blastocyst formation. J Anat. 1946;80:194–204
  41. El-Banna AA, Hafez ESE. Egg transport in beef cattle. J Anim Sci. 1970;30:430–432
  42. Eytan O, Elad D. Analysis on intra-uterine fluid motion induced by uterine contractions. Bull Math Biol. 1999;61:221–238
  43. Bauersachs S, Mitko K, Ulbrich SE, Blum H, Wolf E. Transcriptome studies of bovine endometrium reveal molecular profiles characteristics for specific stages of estrous cycle and early pregnancy. Exp Clin Endocrinol Diabetes. 2008;116:371–384
  44. Robinson RS, Hammond AJ, Wathes DC, Hunter MG, Mann GE. Corpus luteum-endometrium-embryo interactions in the dairy cow: underlying mechanisms and clinical relevance. Reprod Domest Anim. 2008;43(Suppl. 2):104–112
  45. Spencer TE, Sandra O, Wolf E. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction. 2008;135:165–179
  46. Eytan O, Jaffa AJ, Har-Toov J, Dalach E, Elad D. Dynamics of the intrauterine fluid-wall interface. Ann Biomed Eng. 1999;27:372–379
  47. Morris D, Diskin M. Effect of progesterone on embryo survival. Animal. 2008;2:1112–1119
  48. Gupta HC, Branton C, Evans DL, Waters WH. Chemical and physiological properties of the cervical and uterine fluids of repeat and normal breeding cows during estrus. J Dairy Sci. 1962;45:668–669
  49. Fahning ML, Schultz RH, Graham EF. A technique for the collection of uterine fluids from the live cow. Vet Rec. 1966;79:230–233
  50. Lamothe P, Gual P. Electrolytes des sécrétions intra-utérines bovines lors d’infertilité sine materia. Can J Comp Med. 1970;34:167–176
  51. Jordan ER, Chapman TE, Holtan DW, Swanson LV. Relationship of dietary crude protein to composition of uterine secretions and blood in high-producing postpartum dairy cows. J Dairy Sci. 1983;66:1854–1862
  52. Hammond DS, Holyoak GR, Dhiman TR. Association between blood plasma urea nitrogen levels and reproductive fluid urea nitrogen and ammonia concentrations in early lactation dairy cows. Anim Reprod Sci. 2005;86:195–204
  53. Menino AR, Cheek HK, O’Claray JL. The effects of bovine serum albumin, bovine uterine fluid, and heat-treated bovine serum on in vitro mouse embryo development. Theriogenology. 1985;23:461–472
  54. Guise MB, Gwazdauskas FC. Profiles of uterine protein in flushings and progesterone in plasma of normal and repeat-breeding dairy cattle. J Dairy Sci. 1987;70:2635–2641
  55. Segerson EC, Libby DW. Interaction of bovine uterine luminal protein with interleukin-2 and the interleukin-2 receptor of T lymphocytes. Biol Reprod. 1990;43:619–628
  56. Keller ML, Roberts AJ, Seidel GE. Characterization of insulin-like growth factor-binding proteins in the uterus and conceptus during early conceptus elongation in cattle. Biol Reprod. 1998;59:632–642
  57. Rhoads ML, Gilbert RO, Lucy MC, Butler WR. Effects of urea infusion on the uterine luminal environment of dairy cows. J Dairy Sci. 2004;87:2896–2901
  58. Tsiligianni T, Amiridis GS, Vainas E. Activity of glycosidases (β-N-acetyloglucosaminidase, α-mannosidase, and β-galactosidase) in the uterine luminal fluid of cows after multiple ovulation. Can J Vet Res. 2007;71:300–304
  59. Villaseñor M, Coscioni AC, Galvão KN, Chebel RC, Santos JEP. Gossypol disrupts embryo development in heifers. J Dairy Sci. 2008;91:3015–3024
  60. Elsden RP, Hasler JF, Seidel GE. Non-surgical recovery of bovine eggs. Theriogenology. 1976;6:523–532
  61. Verberckmoes S, Van Soom A, De Pauw I, Dewulf J, Verbaet C, de Kruif A. Assessment of a new utero-tubal junction insemination device in dairy cattle. Theriogenology. 2004;61:103–115
  62. Aguilar J, Reyley M. The uterine tubal fluid: secretion, composition and biological effects. Anim Reprod. 2005;2:91–105
  63. Elhassan YM, Wu G, Leanez AC, Tasca RJ, Watson AJ, Westhusin ME. Amino acid concentrations in fluids from the bovine oviduct and uterus and in KSOM-based culture media. Theriogenology. 2001;55:1907–1918
  64. Alavi-Shoushtari SM, Asri-Rezai S, Abshenas J. A study of the uterine protein variations during the estrus cycle in the cow: a comparison with the serum proteins. Anim Reprod Sci. 2006;96:10–20
  65. Robinson RS, Mann GE, Gadd TS, Lamming GE, Wathes DC. The expression of the IGF system in the bovine uterus throughout the oestrous cycle and early pregnancy. J Endocrinol. 2000;165:231–243
  66. Meikle A, Sahlin L, Ferraris A, Masironi B, Blanc JE, Rodríguez-Irazoqui M, et al. Endometrial mRNA expression of oestrogen receptor α, progesterone receptor and insulin-like growth factor-I (IGF-I) throughout the bovine oestrous cycle. Anim Reprod Sci. 2001;68:45–56
  67. Velazquez MA, Hadeler KG, Beckers JF, Remy B, Niemann H. Effects of intraovarian application of insulin-like growth factor-1 (IGF-1) on the superovulatory response of dairy cattle. Reprod Domest Anim. 2009;44(Suppl. 1):38;[abstract 111]
  68. de Feu MA, Patton J, Evans ACO, Lonergan P, Butler ST. The effect of strain of Holstein-Friesian cow on size of ovarian structures, periovulatory circulating steroid concentrations, and embryo quality following superovulation. Theriogenology. 2008;70:1101–1110
  69. Sales JNS, Dias LMK, Viveiros ATM, Pereira MN, Souza JC. Embryo production and quality of Holstein heifers and cows supplemented with β–carotene and tocopherol. Anim Reprod Sci. 2008;106:77–89
  70. van der Gaast MH, Beier-Hellwig K, Fauser BCJM, Beier HM, Macklon NS. Endometrial secretion aspiration prior to embryo transfer does not reduce implantation sites. Reprod Biomed Online. 2003;7:105–109
  71. Boomsma CM, Kavelaars A, Eijkemans MJC, Amarouchi K, Teklenburg G, Gutknecht D, et al. Cytokine profiling in endometrial secretions: a non-invasive window on endometrial receptivity. Reprod Biomed Online. 2009;18:85–94
  72. Heap RB. Some chemical constituents of uterine washings: a method of analysis with results from various species. J Endocrinol. 1962;24:367–378
  73. Bischof P, Schindler AM, Urner F, Mensi N, Herrmann WL, Sizonenko PC. Pregnancy-associated plasma protein-A (PAPP-A): concentration in uterine fluid and immunohistochemical localization in the endometrium. Br J Obstet Gynaecol. 1984;91:863–869
  74. Martin L. On the source of uterine ‘luminal fluid’ proteins in the mouse. J Reprod Fertil. 1984;71:73–80
  75. Milligan SR, Martin L. The resistance of the mouse uterine lumen to flushing and possible contamination of samples by plasma and interstitial fluid. J Reprod Dev. 1984;71:81–87
  76. Foresman KR. Uterine luminal proteins during the preimplantation period in the ferret. J Exp Zool. 1987;243:103–109
  77. Einspanier R, Gabler C, Kettler A, Kloas W. Characterization and localization of ß2-adrenergic receptors in the bovine oviduct:indication for progesterone-mediated expression. Endocrinology. 1999;140:2679–2684
  78. Gao H, Wu G, Spencer TE, Johnson GA, Li X, Bazer FW. Select nutrients in the ovine uterine lumen. I. Amino Acids, glucose, and ions in uterine lumenal flushings of cyclic and pregnant ewes. Biol Reprod. 2009;80:86–93
  79. MacLaughlin DT, Santoro NF, Bauer HH, Lawrence D, Richardson GS. Two-dimensional gel electrophoresis of endometrial protein in human uterine fluids: qualitative and quantitative analysis. Biol Reprod. 1986;34:579–585
  80. Paula-Lopes FF, De Moraes AAS, Hansen PJ. The presence of interleukin-1β in the bovine reproductive tract. J Interferon Cytokine Res. 1999;19:279–285
  81. Parmar T, Sachdeva G, Savardekar L, Katkam RR, Nimbkar-Joshi S, Gadkar-Sable S, et al. Protein repertoire of human uterine fluid during the mid-secretory phase of the menstrual cycle. Hum Reprod. 2008;23:379–386
  82. Carrasco LC, Coy P, Avilés M, Gadea J, Romar R. Glycosidase determination in bovine oviductal fluid at the follicular and luteal phases of the oestrus cycle. Reprod Fertil Dev. 2008;20:808–817
  83. Coy P, Cánovas S, Mondéjar I, Saavedra MD, Romar R, Grullón L, et al. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci USA. 2008;105:15809–15814
  84. Okada H, Hirose Y, Ito M, Sandai T. Aspiration method to collect epithelial cells from mouse, rat, and monkey oviducts. Contemp Top Lab Anim Sci. 2003;42:46–51
  85. Welsh AO. Uterine cell death during implantation and early placentation. Microsc Res Tech. 1993;25:223–245
  86. Fahey JV, Schaefer TM, Wira CR. Sex hormone modulation of human uterine epithelial cell immune responses. Integr Comp Biol. 2006;46:1082–1087
  87. Steffl M, Schweiger M, Sugiyama T, Amselgruber WM. Review of apoptotic and non-apoptotic events in non-ciliated cells of the mammalian oviduct. Ann Anat. 2008;190:46–52
  88. Salleh N, Baines DL, Naftalin RJ, Milligan SR. The hormonal control of uterine fluid secretion and absorption. J Membr Biol. 2005;206:17–28
  89. Casslén B, Kobayashi TK, Stormby N. Cyclic variation of the cellular components in human uterine fluid. J Reprod Fertil. 1982;66:213–218
  90. Müller-Schöttle F, Classen-Linke I, Alfer J, Krusche C, Beier-Hellwig K, Sterzik K, et al. Expression of uteroglobin in the human endometrium. Mol Hum Reprod. 1999;5:1155–1161
  91. Niklasson O, Skude G, Lingman G, Casslén B, Maršál K. Transvaginal ultrasound and lactate dehydrogenase isoenzyme activity profile in uterine aspirate for diagnosis of endometrial carcinoma in women with postmenopausal bleeding. Int J Gynecol Cancer. 2007;17:1322–1326
  92. Ametzazurra A, Matorras R, García-Velasco JA, Prieto B, Simón L, Martínez A, et al. Endometrial fluid is a specific and non-invasive biological sample for protein biomarker identification in endometriosis. Hum Reprod. 2009;24:954–965
  93. Boomsma CM, Kavelaars A, Eijkemans MJ, Lentjes EG, Fauser BC, Heijnen CJ, et al. Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF. Hum Reprod. 2009;24:1427–1435
  94. Olds D. Buffering capacity of bovine female reproductive tract fluids. J Dairy Sci. 1959;42:529–532
  95. Kim M, Hong M, Kim J, Kim H, Lee S-J, Kang SG, et al. Bovine follicular fluid and serum share a unique isoform of matrix metalloproteinase-2 that is degraded by the oviductal fluid. Biol Reprod. 2001;65:1726–1731
  96. Boice ML, Geisert RD, Blair RM, Verhage HG. Identification and characterization of bovine oviductal glycoproteins synthesized at estrus. Biol Reprod. 1990;43:457–465
  97. Abe H, Numazawa C, Abe M, Hoshi H, Oikawa T. Production and characterization of monoclonal antibodies specific for bovine oviductal glycoproteins. J Exp Zool. 1993;265:77–83
  98. Lapointe S, Sirard M-A. Importance of calcium for the binding of oviductal fluid proteins to the membranes of bovine spermatozoa. Mol Reprod Dev. 1996;44:234–240
  99. Roberts GP, Parker JM. Macromolecular components of the luminal fluid from the bovine uterus. J Reprod Fertil. 1974;40:291–303
  100. Laster DB. A pregnancy-specific protein in the bovine uterus. Biol Reprod. 1977;16:682–690
  101. Manns JG, Nkuuhe JR, Bristol F. Prostaglandin concentrations in uterine fluid of cows with pyometra. Can J Comp Med. 1985;49:436–438
  102. Kazemi M, Malathy PV, Keisler DH, Roberts RM. Ovine trophoblast protein-1 and bovine trophoblast protein 1 are present as specific components of uterine flushings in pregnant ewes and cows. Biol Reprod. 1988;39:457–463
  103. Lucy MC, Thatcher WW, Collier RJ, Simmen FA, Ko Y, Savio JD, et al. Effects of somatotropin on the conceptus, uterus, and ovary during maternal recognition of pregnancy in cattle. Domest Anim Endocrinol. 1995;12:73–82
  104. Bilby TR, Guzeloglu A, Kamimura S, Pancarci SM, Michel F, Head HH, et al. Pregnancy and bovine somatotropin in nonlactating diary cows: I. Ovarian, conceptuses, and insulin-like growth factor system responses. J Dairy Sci. 2004;87:3256–3267
  105. Ledgard AM, Lee RS-F, Peterson AJ. Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus. Mol Reprod Dev. 2009;76:65–74

PII: S0093-691X(09)00289-1

doi: 10.1016/j.theriogenology.2009.07.004

Theriogenology
Volume 73, Issue 6 , Pages 758-767 , 1 April 2010