Review Article
Highlights on artificial insemination (AI) technology in the pig
Tarek Khalifa * ,
Constantinos Rekkas ,
Foteini Samartzi ,
Aristotelis Lymberopoulos ,
Kostas Kousenidis ,
Toni Dovenski

Mac Vet Rev 2014; 37 (1): 5 - 34

10.14432/j.macvetrev.2014.09.022

Received: 07 September 2013

Received in revised form: 12 July 2019

Accepted: 30 September 2013

Available Online First: 15 September 2013

Published on: 15 March 2014

Correspondence: Tarek Khalifa, drtarekkhalifa@gmail.com
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Abstract

Over the past decade, there has been a tremendous increase in the development of field AI services in the majority of countries concerned with pig production. The objective of this paper is to review: (a) the current status of swine AI in the world, (b) significance and limitation of AI with liquid and frozen semen, (c) the biological traits of porcine semen in relation to in-vitro sperm storage, (d) the criteria used for selection of a boar stud as a semen supplier, (e) how to process boar semen for liquid and frozen storage in the commercial settings and (f) how to improve fertility and prolificacy of boar semen. More than 99% of the inseminations conducted worldwide are made with liquid-stored semen. AI with frozen semen is used only for upgrading the genetic base in a particular country or herd. Determining the initial quality of semen ejaculates along with the selection of the optimum storage extender has a profound effect on the quality and fertility of AI doses. Different procedures have been used for improving the fertility of preserved spermatozoa including colloidal centrifugation of the semen, intrauterine insemination and modulation of the uterine defense mechanism after AI. Development of an efficient protocol for synchronizing the time of ovulation in sows and gilts coupled with improving uterine horn insemination technique will make a breakthrough in the commercial use of frozen boar semen.

Keywords: boar; semen storage; artificial insemination; fertility


References

1. Broekhuijse, M.L., Feitsma, H., Gadella B.M. (2012). Artificial insemination in pigs: predicting male fertility. Vet Q 32: 151-157.
2. Johnson, L.A., Weitze K.F., Fiser, P., Maxwell, W.M.C. (2000). Storage of boar semen. Anim Reprod Sci 62: 143-172.
3. Riesenbeck, A. (2011). Review on international trade with boar semen. Reprod Domest Anim 46 (Suppl. 2): 1-3.
4. Sigleton, W.L. (2001). State of the art in artificial insemination of pigs in the United States. Theriogenology 56: 1305-1310.
5. Knox, R., Levis, D., Safranski, T., Singleton, W. (2008). An update on North American boar stud practices. Theriogenology 70: 1202-1208.
6. Feitsma, H. (2009). Artificial insemination in pigs, research and developments in The Netherlands, a review. Acta Scientiae Veterinariae 37 (Suppl. 1): 61-71.
7. Broekhuijse, M.L.W.J., Feitsma, H., Gadella, B.M. (2011). Field data analysis of boar semen quality. Reprod Domest Anim 46 (Suppl. 2): 59-63.
8. Vyt, P., Maes, D., Rijsselaere, T., Dewulf, J., De Kruif, A., Van Soom, A. (2007). Semen handling in porcine AI centers: the Belgian situation. Vlaams Diegeneeskundig Tijdschrift 76: 195-199.
9. López Rodríguez, A., Rijsselaere, T., Vyt, P., Van Soom, A., Maes, D. (2012). Effect of dilution temperature on boar semen quality. Reprod Domest Anim 47: 63-66.
10. Martinez, E.A., Vazquez J.M., Roca, J., Cuello, C., Gil, M.A., Parrilla, I., Vazquez, J.L. (2005). An update on reproductive technologies with potential short-term application in pig production. Reprod Domest Anim 40: 300-309.
11. Roca, J., Parrilla, I., Rodriguez-Martinez, H., Gil, M.A., Cuello, C., Vazquez J.M., Martinez, E.A. (2011). Approaches towards efficient use of boar semen in the pig industry. Reprod Domest Anim 46 (Suppl. 2): 79-83.
12. Gadea, J. (2003). Review: semen extenders used in the artificial insemination of swine. Spanish J Agric Res 1 (2): 17-27.
13. Waberski, D., Henning, H., Petrunkina, A.M. (2011). Assessment of storage effects in liquid preserved boar semen. Reprod Domest Anim 46 (Suppl. 2): 45-48.
14. Goldberg, A.M., Argenti, L.E., F accin, J.E., Linck, L., Santi, M., Bernardi, M.L., Cardoso, M.R., Wentz, I., Bortolozzo, F.P. (2013). Risk factors for bacterial contamination during boar semen collection. Res Vet Sci (In press). https://doi.org/10.1016/j.rvsc.2013.06.022
15. Dziuk, P.J., Henshaw, G. (1958). Fertility of boar semen artificially inseminated following in vitro storage. J Anim Sci 17: 554-558.
16. First, N.L., Stratman, F.W., Casida, L.E. (1963). Effect of sperm age on embryo survival in swine. J Anim Sci 22: 135-138.
17. Pursel, V.G., Johnson, L.A., Schulman, L.L. (1973). Fertilizing capacity of boar semen stored at 15oC. J Anim Sci 37: 532-535.
18. Bailey, J.L., Lessard, C., Jacques, J., Bréque, C., Dobrinski, I., Zeng, W., Galantino-Homer, H.L. (2008). Cryopreservation of boar semen and its future importance to the industry. Theriogenology 70: 1251-1259.
19. Großfeld, R., Sieg, B., Struckmann, C., Franzel, A., Maxwell, W.M.C., Rath, D. (2008). New aspects of boar semen freezing strategies. Theriogenology 70: 1225-1233.
20. Knox, R.V. (2011). The current value of frozen-thawed boar semen for commercial companies. Reprod Domest Anim 46 (Suppl. 2): 4-6.
21. Khalifa, T.A.A., Tsakmakidis, I.A. (2012). A preliminary study on preservability of porcine semen in INRA-96 extender. Proceeding of the 17th International Congress on Biotechnology in Animal Reproduction (ICBAR), 12th to 14th September, Leipzig, Anhalt University of Applied Sciences, Germany.
22. Mozo-Martín, R., Gil, L., Gómez-Rincón, C.F., Dahmani, Y., García-Tomás, M., Úbeda, J.L., Grandía, J. (2012). Use of a novel double uterine deposition artificial insemination technique using low concentrations of sperm in pigs. Vet J 193: 251-256.
23. AAlbers, J.G., Mann, T., Polge, C. (1961). Metabolism of boar semen in relation to sperm motility and survival. J Reprod Fertil 2: 42-53.
24. Shelby, D.R., Foley, C.W. (1971). Influence of atmosphere and incubation temperature on the metabolism of washed boar spermatozoa. J Anim Sci 32: 103-106.
25. Jones, A.R. (1997). Metabolism of lactate by mature boar spermatozoa. Reprod Fertil Dev 9: 227-232.
26. Jones, A.R. (1997). Triosephosphate metabolism by mature boar spermatozoa. Reprod Fertil Dev 9: 577-581.
27. Jones, A.R., Connor, D.E. (2000). Fructose metabolism by mature boar spermatozoa. Reprod Fertil Dev 12: 355-359.
28. Marin, S., Chiang, K., Bassilian, S., Lee, W-N.P., Boros, L.G., Fernández-Novell, J.M., Centelles, J.J., Medrano, A., Rodriguez-Gil, J.E., Cascante, M. (2003). Metabolic strategy of boar spermatozoa revealed by a metabolomic characterization. FEBS Letters 554: 342-346.
29. Medrano, A., Fernández-Novell, J.MA., Ramió, L., Alvarez, J., Goldberg, E., Rivera, MA. M., Guinovart, J.J., Rigau, T., Rodríguez-Gil, J.E. (2006). Utilization of citrate and lactate through a lactate dehydrogenase and ATP-regulated pathway in boar spermatozoa. Mol Reprod Dev 73: 369-378.
30. White, I.G. (1993). Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod Fertil Dev 5: 639-658.
31. Galantino-Homer, H.L., Zeng, W-X., Omgee, S.O., Dallmeyer, M., Voelkl, D., Dobrinski, I. (2006). Effects of 2-hydroxypropyl-β-cyclodextrin and cholesterol on porcine sperm viability and capacitation status following cold shock or incubation. Mol Reprod Dev 73: 638-650.
32. Blanch, E., Tomás, C., Graham, J.K., Mocé, E. (2012). Response of boar sperm to the treatment with cholesterol-loaded cyclodextrins added prior to cryopreservation. Reprod Deomest Anim 47: 959-964.
33. Tomás, C., Blanch, E., Cebián, B., Mocé, E. (2013). In vivo fertilizing ability of frozen-thawed boar sperm treated with cholesterol-loaded cyclodextrins prior to cryopreservation. Anim Reprod Sci 140: 77-82.
34. Mann, T., Lutwak-Mann, C. (1981). Male reproductive function and semen. Themes and trends in physiology, biochemistry and investigative andrology. Springer-Verlag, Berlin, Heildelberg, New York.
35. Rodríguez-Martínez, H., Kvist, U., Saravia, F., Wallgren, M., Johannisson, A., Sanz, L., Peña, F.J., Martínez, E.A., Roca, J., Vázquez, J.M., Calvete, J.J. (2009). The physiological roles of the boar ejaculate. Soc Reprod Fertil Suppl. 66: 1-21.
36. Pursel, V.G., Johnson, L.A., Rampacek, G.B. (1972). Acrosome morphology of boar spermatozoa incubated before cold shock. J Anim Sci 34: 278-283.
37. Pursel, V.G., Johnson, L.A., Schulman, L.L. (1973). Effect of dilution, seminal plasma and incubation period on cold shock susceptibility of boar spermatozoa. J Anim Sci 37: 528-531.
38. Juarez, J.D., Parrilla, I., Vazquez, J.M., Martinez, E.A., Roca, J. (2011). Boar semen can tolerate rapid cooling rates prior to freezing. Reprod Fertil Dev 23: 681-690.
39. Althouse, G.C., Wilson, M.E., Kuster,C., Parsley, M. (1998). Characterization of lower temperature storage limitations of fresh-extended porcine semen. Theriogenology 50: 535-543.
40. Paulenz, H., Kommisrud, E., Hofmo, P.O. (2000). Effect of long-term storage at different temperatures on the quality of liquid boar semen. Reprod Domest Anim 35: 83-87.
41. Mann, T. (1964). The biochemistry of semen and of the male reproductive tract. London: Mathuen & Co LTD, New York: John Wiley & Sons Inc.
42. Althouse, G.C., Pierdon, M.S., Lu, K.G. (2008). Thermotemporal dynamics of contaminant bacteria and antimicrobials in extended porcine semen. Theriogenology 70: 1317-1323.
43. Schilling, E., Vengust, M. (1987). Frequency of semen collection in boars and quality of ejaculates as evaluated by the osmotic resistance of acrosomal membranes. Anim Reprod Sci 12: 283-290.
44. Arkins, S., Thomposon, L.H., Giles, J.R., Camacho, T., Hosmon, B.D. (1988). The effect of collection procedure on the sperm output and copulatory behavior of AI stud boars. Anim Reprod Sci 16: 277-283.
45. Frangež, R., Gider,T., Kosec, M. (2005). Frequency of boar ejaculate collection and its influence on semen quality, pregnancy rate and litter size. Acta Vet Brno 74: 265-273.
46. Aneas, S.B., Gary, B.G., Bouvier, B.P. (2008). Collectis® automated boar collection technology. Theriogenology 70: 1368-1373.
47. Thacker, B.J., Larsen, R.E., Joo, H.S., Leman, A.D. (1984). Swine diseases transmissible with artificial insemination. J Am Vet Med Assoc 185: 511-516.
48. Althouse, G.C., Kuster, C.E., Clark, S.G., Weisiger, R.M. (2000). Field investigations of bacterial contaminants and their effects on extended porcine semen. Theriogenology 53: 1167-1176.
49. Althouse, G.C., Kristina, G. Lu. (2005). Bacteriospermia in extended porcine semen. Theriogenology 63: 573-584.
50. Martín, L.O.M., Muñoz, , E.C., De Cupere, F., Van Driessche, E., Echemendia-Blanco, D., Rodríguez, J.M.M., Beeckmans, S. (2010). Bacterial contamination of boar semen affects the litter size. Anim Reprod Sci 120: 95-104.
51. Bussalleu, E., Yeste, M., Sepúlveda, L., Torner, E., Pinart, E., Bonet, S. (2011). Effects of different concentrations of enterotoxigenic and verotoxigenic E. coli on boar sperm quality. Anim Reprod Sci 127: 176-182.
52. Schautteet, K., De Clercq, E., Miry, C., Van Groenweghe, F., Delava, P., Kalmar, I., Vanrompay, D. (2013). Tetracycline-resistant Chlamydia suis in cases of reproductive failure on Belgian, Cypriote and Israeli pig production farms. J Med Microbiol 62 (Pt 2): 331-334.
53. Bamba, K., Sone, M. (1981). Factors affecting the quality of boar semen stored by means of dialysis. J Reprod Fert 62: 193-197.
54. Sone, M., Ohmura, K., Bamba, K. (1982). Effects of various antibiotics on the control of bacteria in boar semen. Vet Rec 111: 11-14.
55. Okazaki, T., Mihara, T., Fujita, Y., Yoshida, S., Teshima, H., Shimada, M. (2010). Polymixin B neutralizes bacteria-released endotoxin and improves the quality of boar sperm during liquid storage and cryopreservation. Theriogenology 74: 1691-1700.
56. Waberski, D., Weitze, K.F., Meding, S., Leiding, C., Weiskopf, S. (1990) Examination on sperm and fertility compatibility of Lincospectin® sterile solution as antibiotic additive in liquid boar semen. Reprod Domest Anim 25: 291-295.
57. Morrell, J.M., Wallgren, M. (2011). Removal of bacteria from boar ejaculates by single layer centrifugation can reduce the use of antibiotics in semen extenders. Anim Reprod Sci 123: 64-69.
58. Morrell, J.M., Wallgren, M. (2011). Colloid centrifugation of boar semen. Reprod Domest Anim 46 (Suppl. 2): 18-22.
59. Rigau, T., Piedrafita, J., Reverter, A., Canal, M., Rodríguez-Gil, J.E. (1996). The rate of L-lactate production: a feasible parameter for the fresh boar semen quality analysis. Anim Reprod Sci 43: 161-172.
60. Kamp, G., Büsselmann, G., Jones, N., Wiesner, B., Lauterwein, J. (2003). Energy metabolism and intracellular pH in boar spermatozoa. Reproduction 126: 517-525.
61. Ford, W.C.L. (2006). Glycolysis and sperm motility: does a spoon of sugar help the flagellum go round? Hum Reprod Update 12: 269-274.
62. Vyt, P., Maes, D., Sys, S.U., Rijsselaere, T., Van Soom, A. (2007). Air contact influences the pH of extended porcine semen. Reprod Domes Anim 42: 218-220.
63. Storey, B.T. (2008). Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 52: 427-437.
64. Bucci, D., Isani, G., Spinaci, M., Tamanini, C., Mari, G., Zambelli, D., Galeati, G. (2010). Comparative immunolocalization of GLUTs 1, 2, 3 and 5 in boar, stallion and dog spermatozoa. Reprod Doest Anim 45: 365.
65. Bucci, D., Rodriguez-Gil, J.E., Vallorani, C., Spinaci, M.,Galeati, G., Tamanini, C. (2011). GLUTs and mammalian sperm metabolism. J Androl 32: 348-355.
66. Purdy, P.H., Tharp, N., Stewart, T., Spiller, S.F., Blackburn, H.D. (2010). Implications of the pH and temperature of diluted, cooled boar semen on fresh and frozen-thawed sperm motility characteristics. Theriogenology 74: 1304-1310.
67. Bonet, S. (1990). Immature and aberrant spermatozoa in the ejaculate of Sus domesticus. Anim Reprod Sci 22: 67-80.
67. Briz, M.D., Bonet, S., Pinart, B., Egozcue, J., Camps, R. (1995). Comparative study of boar sperm coming from the caput, corpus, and cauda regions of the epididymis. J Androl 16: 175-187.
69. Harayama, H., Shibukawa, T., Miyake, M., Kannan, Y., Kato, S. (1996). Fructose stimulates shedding of cytoplasmic droplets from epididymal boar spermatozoa. Reprod Fertil Dev 8: 1039-1043.
70. Vyt, P., Maes, D., Dejonckheere, E., Castryck, F., Van Soom, A. (2004). Comparative study on five different commercial extenders for boar semen. Reprod Domest Anim 39: 8-12.
71. Gilmore, J.A., Du, J., Tao, J., Peter, A.T., Critser, J.K. (1996). Osmotic properties of boar spermatozoa and their relevance to cryopreservation. J Reprod Fertil 107: 87-95.
72. Fraser, L., Gorszczaruk, K., Strzeźek, J. (2001). Relationship between motility and membrane integrity of boar spermatozoa in media varying in osmolality. Reprod Domest Anim 36: 325-329.
73. Yeste, M., Briz, M., Pinart, E., Sílvia, S., Bussalleu, E., Bonet, S. (2010). The osmotic tolerance of boar spermatozoa and its usefulness as sperm quality parameter. Anim Reprod Sci 119: 265-274.
74. Marcos, C.P., Sanchez, R., Palacio, M., Pursel, V.G., Garcia, T.P., Rillo, S.M. (1991). Effects of dilution rate on the motility and acrosome morphology of boar spermatozoa stored at 15oC. Reprod Domest Anim 26: 112-116.
75. Maxwell, W.M.C., Johnson, L.A. (1999). Physiology of spermatozoa at high dilution rates: the influence of seminal plasma. Theriogenology 52: 1353-1362.
76. Harrison, R.A.P., Dott, H.M., Foster, G.C. (1978). Effect of ionic strength, serum albumin and other macromolecules on the maintenance of motility and the surface of mammalian spermatozoa in a simple medium. J Reprod Fert 52: 65-73.
77. Waberski, D., Meding, S., Dirksen, G., Weitze, K.F., Leiding, C., Hahn, R. (1994). Fertility of long-term-stored boar semen: influence of extender (Androhep and Kiev), storage time and plasma droplets in the semen. Anim Reprod Sci 36: 145-151.
78. Dziuk, P.J., Henshaw, G. (1959). Fertility of boar semen artificially inseminated following in vitro storage. J Anim Sci 17: 554-558.
79. Baker, R.D., Dziuk, P.J., Norton, H.W. (1968). Effect of volume of semen, number of sperm and drugs on transport of sperm in artificially inseminated gilts. J Anim Sci 27: 88-93.
80. Johnson, L.A., Aalbers, J.G., Willems, C.M.T., Rademaker, J.H.M., Rexroad, C.E. Jr. (1982). Use of boar spermatozoa for artificial insemination III. Fecundity of boar spermatozoa stored in Beltsville liquid and Kiev extenders for three days at 18oC. J Anim Sci 54: 132-136.
81. Johnson, L.A., Aalbers, J.G., Grooten, H.J.G. (1988). Artificial insemination of swine: fecundity of boar semen stored in Beltsville TS (BTS), modified modina (MM), or MA-A and inseminated on one, three and four days after collection. Zuchthyg 23: 49-55.
82. Waberski, D., Weitze, K.F., Lietmann, C., Lübbert zur Large, W., Bortolozzo, F.P., Willmen, T., Petzoldt, R. (1994). The initial fertilizing capacity of long term-stored liquid boar semen pre- and postovulatory insemination. Theriogenology 41: 1367-1377.
83. Soede, N.M., Wetzels, C.C.H., Zondag, W., de Koning, M.A.I., Kemp, B. (1994). Effects of time of insemination relative to ovulation, as determined by ultrasonography, on fertilization rate and accessory sperm count in sows. J Reprod Fertil 104: 99-106.
84. Soede, N.M., Wetzels, C.C.H., Zondag, W., Hazeleger, W., Kemp, B. (1994). Effects of a second insemination after ovulation on fertilization rate and accessory sperm count in sows. J Reprod Fertil 105: 135-140.
85. Nissen, A.K., Soede, N.M., Hyttel, P., Schmidt, M., D’Hoore, L. (1997). The influence of time of insemination relative to time of ovulation on farrowing frequency and litter size in sows, as investigated by ultrasonography. Theriogenology 47: 1571-1582.
86. Steverink, D.W. B., Soede, N.M., Bouwman, E.G., Kemp, B. (1998). Semen backflow after insemination and its effect on fertilization results in sows. Anim Reprod Sci 54: 109-119.
87. Kuster, C.E., Althouse, G.C. (1999). The fecundity of porcine semen stored for 2 to 6 days in Androhep® and X-CellTM extenders. Theriogenology 52: 365-376.
88. Foote, R.H. (2002). Within-herd use of boar semen at 5oC, with a note on electronic monitoring of estrus. Reprod Domest Anim 37: 61-63.
89. Watson, P.F., Behan, J.R. (2002). Intrauterine insemination of sows with reduced sperm numbers: results of a commercially based field trial. Theriogenology 57: 1683-1693.
90. Haugan, T., Gaustad, A.H., Reksen, O., Gröhn, Y.T., Hofmo, P.O. (2007). Fertility results of artificial inseminations performed with liquid boar semen stored in X-CellTM vs. BTS extender. Reprod Domest Anim 42: 94-99.
91. Wolf, J., Smital, J. (2009). Quantification of factors affecting semen traits in artificial insemination boars from animal model analyses. J Anim Sci 87: 1620-1627.
92. Stančić, B., Radović, I., Stančić, I., Dragin, S., Boźić, A., Gvozdić, D. (2010). Fertility of sows after intracervical or intrauterine insemination with different spermatozoa number in reduced volume doses. Acta Veterinaria (Beograd) 60: 257-262.
93. Weitze, K.F., Wagner-Rietschel, H., Waberski, D., Richter, L., Krieter, J. (1994). The onset of heat after weaning, heat duration, and ovulation as major factors in AI timing in sows. Reprod Domest Anim 29: 433-443.
94. Koketsu, Y., Dial, G.D., King, V.L. (1997). Returns to service after mating and removal of sows for reproductive reasons from commercial swine farms. Theriogenology 47: 1347-1363.
95. de Kruif, A. (2003). Fertility and sterility in domestic animals. Verh K Geneeskd Bleg 65: 189-202.
96. Sancho, S., Pinart, E., Briz, M., Garcia-Gil, N., Badia, E., Bassols, J., Kádár, E., Pruneda, A., Bussalleu, E., Yeste, M., Coll, M.G., Bonet, S. (2004). Semen quality of postpubertal boars during increasing and decreasing natural photoperiods. Theriogenology 62: 1271-1282.
97. Einarsson, S., Brandt,Y., Lundeheim, N., Madej, A. (2008). Stress and its influence on reproduction in pigs: a review. Acta Vet Scand 50:48. doi: 10.1186/1751-0147-50-48 (http://www.actavetscand.com/content/50/1/48).
98. Sonderman, J.P., Luebbe, J.J. (2008). Semen production and fertility issues related to differences in genetic lines of boars. Theriogenology 70: 1380-1383.
99. Huang, Y.H., Lo, L.L., Liu, S.H., Yang, T.S. (2010). Age-relating changes in semen quality characteristics and expectations of reproductive longevity in Duroc boars. Anim Sci J 81: 432-437.
100. Tsakmakidis, I.A., Khalifa, T.A.A., Boscos, C.M. (2012). Age-related changes in quality and fertility of porcine semen. Biol Res 45: 381-386.
101. Khalifa, T., Rekkas, C., Tsakmakidis, I., Zdragas, A., Samartzi, F., Lymberopulos, A. (2012). Long-term storage of porcine spermatozoa in chemically defined extenders. Reprod Domest Anim 47 (Suppl. 5): 91 (abstract P83).
102. Hood, R.D., Foley, C.W., Martin, T.G. (1970). Effects of cold shock, dilution, glycerol and dimethyl sulfoxide on cation concentrations in porcine spermatozoa. J Anim Sci 30: 91-94.
103. Watson, P.F. (1995). Recent development and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod Fertil Dev 7: 871-891.
104. Bamba, K., Cran, D.G. (1985). Effect of rapid warming of boar semen on sperm morphology and physiology. J Reprod Fert 75: 133-138.
105. Bamba, K., Cran, D.G. (1988). Further studies on rapid dilution and warming of boar semen. J Reprod Fert 82: 509-518.
106. Safranski, T.J., Ford, J.J., Rohrer, G.A., Guthrie, H.D. (2011). Genetic selection for freezability and its controversy with selection for performance. Reprod Domest Anim 46 (Suppl. 2): 31-34.
107. Benson, R.W., Pickett, B.W., Komarek, R.J., Lucas, J.J. (1967). Effect of incubation and cold shock on motility of boar spermatozoa and their relationship to lipid content. J Anim Sci 35: 580-584.
108. Pursel, V.G., Johnson, L.A., Schulman, L.L. (1972). Interaction of extender composition and incubation period on cold shock susceptibility of boar spermatozoa. J Anim Sci 35: 580-584.
109. Tamuli, M.K., Watson, P.F. (1994). Cold resistance of live boar spermatozoa during incubation after ejaculation. Vet Rec 135: 160-162.
110. Eriksson, B.M., Vazquez, J.M., Martinez, E.A., Roca, J., Lucas, X., Rodriguez-Martinez, H. (2001). Effects of holding time during cooling and of type of package on plasma membrane integrity, motility and in vitro oocyte penetration ability of frozen-thawed boar spermatozoa. Theriogenology 55: 1593-1605.
111. Casas, I., Althouse, G.C. (2013). The protective effect of a 17oC holding time on boar sperm plasma membrane fluidity after exposure to 5oC. Cryobiology 66: 69-75.
112. Berger, T., Clegg, E.D. (1985). Effect of male accessory gland secretions on sensitivity of porcine sperm acrosomes to cold shock, initiation of motility and loss of cytoplasmic droplets. J Anim Sci 60: 1295-1302.
113. Saravia, F. (2008). Cryopreservation of boar semen: impact of the use of specific ejaculate portions, concentrated packaging, and simplified freezing procedures on sperm cryosurvival and potential fertilizing capacity. Doctoral Thesis No. 2008:98, Swedish University of Agricultural Sciences, Faculty of Veterinary Medicine and Animal Science, Division of Reproduction, Department of Clinical Sciences, Uppsala, Sweden.
114. Guthrie, H.D., Welch, G.R. (2005). Impact of storage prior to cryopreservation on plasma membrane function and fertility of boar sperm. Theriogenology 63: 396-410.
115. Garcia, J.C., Dominquez, J.C., Pena, F.J., Alegre, B., Gonzalez, R., Castro, M.J., Habing, G.G., Kirkwood, R.N. (2010). Thawing boar semen in the presence of seminal plasma: effects on sperm quality and fertility. Anim Reprod Sci 119: 160-165.
116. Leahy, T., Gadella, B.M. (2011). Capacitation and capacitation-like sperm surface changes induced by handling boar semen. Reprod Domest Anim 46 (Suppl. 2): 7-13.
117. Gómez-Fernández, J., Gómez-Izquierdo, E., Tomás, C., González-Bulnes, A., Sánchez- Sánchez, R., de Mercado, E. (2012). Inclusion of seminal plasma in sperm cryopreservation of Iberian pig. Anim Reprod Sci 130: 82-90.
118. Okazaki, T., Akiyoshi, T., Kan, M., Mori, M., Teshima, H., Shimada, M. (2012). Artificial insemination with seminal plasma improves the reproductive performance of frozen-thawed boar epididymal spermatozoa. J Androl 33: 990-998.
119. Okazaki, T., Shimada, M. (2012). New strategies of boar sperm cryopreservation: development of novel freezing and thawing methods with a focus on the roles of seminal plasma. Anim Sci J 83: 623-629.
120. Fernández-Gago, R., Domínguez, J.C., Martínez-Pastor, F. (2013). Seminal plasma applied post-thawing affects boar sperm physiology: a flow cytometry study. Theriogenology 80: 400-410.
121. Khalifa, T.A.A., Tsakmakidis, I.A., Michos, I.A., Rekkas, C.A. (2011). Effect of semen processing procedures on quality of cooled boar spermatozoa. Reprod Domest Anim 46 (Suppl. 2): 95-96 (abstract P15).
122. Batellier, F., Magistrini, M., Fauquant, J., Palmer, E. (1997). Effect of milk fractions on survival of equine spermatozoa. Theriogenology 48 : 391-410.
123. Vishwanath, R., Shannon, P. (2000). Storage of bovine semen in liquid and frozen state. Anim Reprod Sci 62: 23-53.
124. Salamon, S., Maxwell, W.M.C. (2000). Storage of ram semen. Anim Reprod Sci 62: 77-111.
125. Leboeuf, B., Restall, B., Salamon, S. (2000). Production and storage of goat semen for artificial insemination. Anim Reprod Sci 62: 113-141.
126. Gutiérrez-Cepeda, L., Fernández, Á., Crespo, F., Ramírez, M. Á., Gosálvez, J., Serres, C. (2012). The effect of two pre-cryopreservation single layer colloidal centrifugation protocols in combination with different freezing extenders on the fragmentation dynamics of thawed equine sperm DNA. Acta Vet Scand 54: 72. https://doi.org/10.1186/1751-0147-54-72.
127. Butler, W.J., Roberts, T.K. (1975). Effects of some phosphatidyl compounds on boar spermatozoa following cold shock or slow cooling. J Reprod Fert 43: 183-187.
128. Pursel, V.G., Johnson, L.A. (1975). Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure. J Anim Sci 40: 99-102.
129. Pursel, V.G., Schulman, L.L., Johnson, L.A. (1978). Effect Orvus ES Paste on acrosome morphology. motility and fertilizing capacity of frozen-thawed boar sperm. J Anim Sci 47: 198-202.
130. Graham, E.F., Crabo, B.G., Pace, M.M. (1978). Current status of semen preservation in the ram, boar and stallion. J Anim Sci 47 (Suppl. 2): 80-119.
131. Pursel, V.G., Schulman, L.L., Johnson, L.A. (1978). Effect of glycerol concentration on frozen boar sperm. Theriogenology 9: 305-312.
132. Pursel, V.G. (1979). Effect of cold shock on boar sperm treated with butylated hydroxytoluene. Biol Reprod 21: 319-324.
133. Bamba, K., Cran, D.G. (1992). Effects of treatment with butylated hydroxytoluene on the susceptibility of boar spermatozoa to cold stress and dilution. J Reprod Fert 95: 69-77.
134. Bamba, K., Miyagawa, N. (1992). Protective action of aromatic compounds against cold-shock injuries in boar spermatozoa. Cryobiology 29: 533-536.
135. Roca, J., Gil, M.A., Hernandez, M., Parrilia, I., Vazquez, J.M., Martinez, E.A. (2004). Survival and fertility of boar spermatozoa after freeze-thawing in extender supplemented with butylated hydroxytoluene. J Androl 25: 397-405.
136. Khalifa, T.A.A., El-Saidy, B.E. (2006). Pellet-freezing of Damascus goat semen in a chemically defined extender. Anim Reprod Sci 93: 303-315.
137. Khalifa, T.A.A., Lymberopoulos, A.G., El-Saidy, B.E. (2008). Testing usability of butylated hydroxytoluene in conservation of goat semen. Reprod Domest Anim 43 : 525-530.
138. Hammerstedt, R.H., Keith, A.D., Snipes, W., Amann, R.P., Arruda, D., Griel, L.C. (1978). Use of spin labels to evaluate effects of cold shock and osmolality on sperm. Biol Reprod 18: 686-696.
139. Parks, J.E., Graham, J.K. (1992). Effects of cryopreservation procedures on sperm membranes. Theriogenology 38: 209-222.
140. Demianowicz, W., Strzezek, J. (1995). The effect of lipoprotein fraction from egg yolk on some of the biological properties of boar spermatozoa during storage of the semen in liquid state. Reprod Domest Anim 31: 279-280.
141. Jiang, Z-I., Li, Q-w., Hu, J-h., W-y., Zhao, H-w., Zhang, S-s. (2007). Improvement of the quality of boar cryopreservation semen by supplementing with low density lipoprotein in diluents. Cryobiology 54: 301-304.
142. Hu, J-h., Li, Q-w., Jiang, Z-I., Li, W-y. (2008). Effects of different extenders on DNA integrity of boar spermatozoa following freezing-thawing. Cryobiology 57: 257-262.
143. Yamauchi, S., Nakamura, S., Lay, K.M., Azuma, T., Yakabi, T., Muto, N., Nakada, T., Ashizawa, K., Tatemoto, H. (2009). Characteristics of Okinawan native Agu pig spermatozoa after addition of low-density lipoprotein to freezing extender. J Reprod Dev 55: 558-565.
144. Wang, P., Wang, Y.F., Wang, C.W., Bu, S.H., Li, Q.W., Pang, W.J., Yang, G.S. (2012). Effects of low-density lipoproteins extracted from different avian yolks on boar spermatozoa quality following freezing-thawing. Zygote 30: 1-7.
145. Zhang, S-S., Hu, J-H., Li, Q-W., Jiang, Z-L., Zhang, X-Y. (2009). The cryoprotective effects of soybean lecithin on boar spermatozoa quality. African J Biotech 8: 6476-6480.
146. Namula, Z., Sato, Y., Kodama, R., Morinaga, K., Luu, V.V., Taniguchi, M., Nakai, M., Tanihara, F., Kikuchi, K., Nagai, T., Otoi, T. (2013). Motility and fertility of boar semen after liquid preservation at 5oC for more than 2 weeks. Anim Sci J 84: 600-606.
147. Almlid, T., Johnson, L.A. (1988). Effect of glycerol concentration, equilibration time and temperature of glycerol addition on post-thaw viability of boar spermatozoa frozen in straws. J Anim Sci 66: 2899-2905.
148. Fiser, P.S., Fairfull, R.W., Panich, P.L. (1996). Glycerol equilibration time revisited. Reprod Domest Anim 31 (1): 141-146.
149. Fiser, P.S., Fairfull, R.W. (1990). Combined effect of glycerol concentration and cooling velocity on motility and acrosomal integrity of boar spermatozoa frozen in 0.5 ml straws. Mol Reprod Dev 25: 123-129.
150. Morris, G.J., Acton, E., Murray, B.J., Fonseca, F. (2012). Freezing injury: the special case of the sperm cell. Cryobiology 64: 71-80.
151. Mazur, P. (1985). Basic concepts in freezing cells. Proceeding of the 1st International Conference on Deep Freezing of Boar Semen. Swedish University of Agriculture Sciences, Uppsala, Sweden, pp. 91-111.
152. Mazur, P., Leibo, S.P., Seidel Jr., E. (2008). Cryopreservation of the germplasm of animals used in biological and medical research: importance, status, and future implications. Biol Reprod 78: 2-12.
153. Wessel, M.T., Ball, B.A. (2004). Step-wise dilution for removal of glycerol from fresh and cryopreserved equine spermatozoa. Anim Reprod Sci 84: 147-156.
154. Burnaugh, L., Ball, B.A., Sabeur, K., Thomas, A.D., Meyers, S.A. (2010). Osmotic stress stimulates generation of superoxide anion by spermatozoa in horses. Anim Reprod Sci 117: 249-260.
155. Baumber, J., Vo, A., Sabeur, K., Ball, B.A. (2002). Generation of reactive oxygen species by equine neutrophils and their effect on motility of equine spermatozoa. Theriogenology 57: 1025-1033.
156. Broekhuijse, M.L.W.J., Feitsma, H., Gadella, B.M. (2012). Field data analysis of boar semen quality. Reprod Domest Anim 46 (Suppl. 2): 59-63.
157. Young, L.G., King, G.L. (1986). Low concentrations of zearalenone in diets of boars for a prolonged period of time. J Anim Sci 63: 1197-1200.
158. Solti, L., Pécsi, T., Barna-Vetró, I., Szász, F.Jr., Biró, K., Szabó, E. (1999). Analysis of serum and seminal plasma after feeding ochratoxin A with breeding boars. Anim Reprod Sci 56: 123-132.
159. Biró, K., Barna-Vetró, I., Pécsi, T., Szabó, E., Winkler, G., Fink-Gremmels, J., Solti, L. (2003). Evaluation of spermatological parameters in ochratoxin A-challenged boars. Theriogenology 60: 199-207.
160. Tsakmakidis, I.A., Lymberopoulos, A.G., Alexopoulos, C., Boscos, C.M., Kyriakis, S.C. (2006). In vitro effect of zearalenone and alpha-zearalenone on boar sperm characteristics and acrosome reaction. Reprod Domest Anim 41: 394-401.
161. Tsakmakidis, I.A., Lymberopoulos, A.G., Vainas, E., Boscos, C.M., Kyriakis, S.C., Alexopoulos, C. (2007). Study on the in vitro effect of zearalenone and alpha-zearalenone on boar sperm-zona pellucida interaction by hemizona assay application. J Appl Toxicol 27: 498-505.
162. Tsakmakidis, I.A., Lymberopoulos, A.G., Khalifa, T.A.A., Boscos, C.M., Saratsi, A., Alexopoulos, C. (2008). Evaluation of zearalenone and alpha-zearalenone toxicity on boar sperm DNA integrity. J Appl Toxicol 28: 681-688.
163. Thibier, M., Guerin, B. (2000). Hygienic aspects of storage and use of semen for artificial insemination. Anim Reprod Sci 62: 233-251.
164. Bielanski, A. (2007). Disinfection procedures for controlling microorganisms in the semen and embryos of humans and farm animals. Theriogenology 68: 1-22.
165. Althouse, G.C., Rossow, K. (2011). The potential risk of infectious disease dissemination via artificial insemination in swine. Reprod Domest Anim 46 (Suppl. 2): 64-67.
166. Bussalleu, E., Pinart, E., Rivera, M.M., Arias, X., Briz, M., Sancho, S., García-Gil, N., Bassols, J., Pruneda, A., Yeste, M., Casas, I., Rigau, T., Rodriguez-Gil, J.E., Bonet, S. (2008). Effects of filtration of semen doses from subfertile boars through neuter sephadex columns. Reprod Domest Anim 43: 48-52.
167. Morrell, J.M., Saravia, F., Van Wienen, M., Wallgren, M., Rodriguez-Martinez, H. (2009). Selection of boar spermatozoa using centrifugation on a glycidoxypropyltrimethoxysilane-coated silica colloid. J Reprod Dev 55: 547-552.
168. Morrell, J.M., Saravia, F., Van Wienen, M., Wallgren, M., Rodriguez-Martinez, H. (2009). Sperm survival following colloid centrifugation varies according to the part of the sperm-rich fraction used. Soc Reprod Fertil Suppl 66: 85-86.
169. Ramió-LIuch, L., Balasch, S., Bonet, S., Briz, M., Pinart, E., Rodríguez-Gil, J. E. (2009). Effects of filtration through sephadex columns improve overall quality parameters and “in vivo” fertility of subfertile refrigerated boar-semen. Anim Reprod Sci 115: 189-200.
170. Blomqvist, G., Persson, M., Wallgren, M., Wallgren, P., Morrell, J.M. (2011). Removal of virus from boar semen spiked with porcine circovirus type 2. Anim Reprod Sci 126: 108-114.
171. Holt, W.V., Van Look, K.J.W. (2004). Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127: 527-535.
172. Pertoft, H., Laurent, T.C., Låås, T., Kågedal, L. (1978). Density gradients prepared from colloidal silica particles coated by polyvinylpyrrolidone (Percoll). Anal Biochem 88: 271-282.
173. Rodriguez-Martinez, H., Larsson, B., Pertoft, H. (1997). Evaluation of sperm damage and techniques for sperm clean-up. Reprod Fertil Dev 9: 297-308.
174. Mortimer, D. (2000). Sperm preparation methods. J Androl 21: 357-366.
175. Henkel, R.R., Schill, W-B. (2003). Sperm preparation for ART. Reprod Biol Endocrinol 1: 108 (http://www.rbej.com/content/1/1/108).
176. Morrell, J.M., Rodriguez-Martinez, H. (2009). Biomimetic techniques for improving sperm quality in animal breeding: a review. The Open Andrololgy Journal 1: 1-9 (Bentham open access).
177. Morrell, J.M., Rodriguez-Martinez, H. (2010). Practical applications of sperm selection techniques as a tool for improving reproductive efficiency. Veterinary Medicine International, volume 2011, article ID 894767, SAGE-Hindawi access to research (doi: 10.4061/2011/894767).
178. Vanderwall, D.K. (2008). How to process a dilute ejaculate of semen for cooled-transported insemination. Proceedings of the 54th Annual Convention of the American Association of Equine Practitioners, Dec 6-10, San Diego, California, Vol. 54, pp. 369-373.
179. Matthijs, A., Harkema, W., Engel, B., Woelders, H. (2000). In vitro phagocytosis of boar spermatozoa by neutrophils from peripheral blood of sows. J Reprod Fertil 120: 265-273.
180. Matthijs, A., Engel, B., Woelders, H. (2003). Neutrophil recruitment and phagocytosis of boar spermatozoa after artificial insemination of sows, and the effects of inseminate volume, sperm dose and specific additives in the extender. Reproduction 125: 357-367.
181. Oh, S.A., Park, Y.J., You, Y.A., Mohamed, E. A., Pang, M.G. (2010). Capacitation status of stored boar spermatozoa is related to litter size of sows. Anim Reprod Sci 121:131-138.
182. Horrigan, L.A.,Kelly, J.P., Connor, T.J. (2004). Caffeine suppresses TNF-α production via activation of the cyclic AMP/protein kinase A pathway. Int J Immunopharmacol 4: 1409-1417.
183. Horrigan, L.A.,Kelly, J.P., Connor, T.J. (2009). Immunomodulatory effects of caffeine: Friend or foe? Pharmacol Ther 111: 877-892.
184. Yeste, M., Briz, M., Pinart, E., Sancho, S., Garcia-Gil, N., Badia, E., Bassols, J., Pruneda, A., Bussalleu, E., Casas, I., Bonet, S. (2008). Hyaluronic acid delays boar sperm capacitation after 3 days of storage at 15oC. Anim Reprod Sci 109: 236-250.
185. Martecikova, S., Hulinska, P., Reckova, Z., Pavlik, A., Jeseta, M., Machatkova, M. (2010). Effect of acrosome reaction progress in frozen-thawed boar spermatozoa on the efficiency of in vitro oocyte fertilization. Veterinarni Medicina, 55: 429-437.
186. Yamaguchi, S., Suzuki, C., Noguchi, M., Kasa, S., Mori, M., Isozaki, Y., Ueda, S., Funahashi, H., Kikuchi, K., Nagai, T., Yoshioka, K. (2013). Effects of caffeine on sperm characteristics after thawing and inflammatory response in the uterus after artificial insemination with frozen-thawed boar semen. Theriogenology 79: 87-93.
187. Li, J.-C., Yamaguchib, S., Kondoa, Y., Funahashia, H. (2011). Caffeine, dibutyryl cyclic-AMP and heparin affect the chemotactic and phagocytotic activities of neutrophils for boar sperm in vitro. Theriogenology 75:1336–1345.
188. Li, J.-C., Yamaguchib, S., Kondoa, Y., Funahashia, H. (2012). Boar seminal plasma or hen’s egg yolk decrease the in vitro chemotactic and phagocytotic activities of neutrophils when co-incubated with boar or bull sperm. Theriogenology 77: 73-80.
189. Jiwakanon, J., Persson, E., Berg, M., Dalin, A.M. (2011). Influence of seminal plasma, spermatozoa and semen extender on cytokine expression in the porcine endometrium after insemination. Anim Reprod Sci 123:210-220.
190. Katila, T. (2012). Post-mating inflammatory responses of the uterus. Reprod Domest Anim 47 (Suppl. 5): 31-41.
191. Langendijk, P., Soede, N.M., Kemp, B. (2005). Uterine activity, sperm transport, and the role of boar stimuli around insemination in sows. Theriogenology 63: 500-513.
192. Yamaguchi, S., Funahashi, H., Murakami, T. (2009). Improved fertility in gilts and sows after artificial insemination of frozen-thawed boar semen by supplementation of semen extender with caffeine and CaCl2. J Reprod Dev 55: 645-649.
193. Yamaguchi, S., Funahashi, H. (2012). Effect of the addition of beta-mercaptoethanol to a thawing solution supplemented with caffeine on the function of frozen-thawed boar sperm and on the fertility of sows after artificial insemination. Theriogenology 77: 926-932.
194. Vazquez, J.M., Roca, J., Gil, M.A., Cuello, C., Parrilla, I., Vazquez, J.L., Martínez, E.A. (2008). New developments in low-dose insemination technology. Theriogenology 70: 1216-1224.
195. Watson, P.F., Behan, J.R. (2006). A field investigation of intra-cervical insemination with reduced sperm numbers in gilts. Theriogenology 66:338-343.
196. Martinez, E.A.,Vazquez, J.M., Roca, J., Lucas, X., Gil, M.A., Parrilla, I., Vazquez, J.L., Day, B.N. (2001). Successful non-surgical deep intrauterine insemination with small numbers of spermatozoa in sows. Reproduction 122: 289-296.
197. Martinez, E.A.,Vazquez, J.M., Roca, J., Lucas, X., Gil, M.A., Parrilla, I., Vazquez, J.L., Day, B.N. (2002). Minimum number of spermatozoa required for normal fertility after deep intrauterine insemination in non-sedated sows. Reproduction 123: 163-170.
198. Vazquez, J.M., Roca, J., Gil, M.A., Cuello, C., Parrilla, I., Vazquez, J.L., Martínez, E.A. (2008). Low-dose insemination in pigs: problems and possibilities. Reprod Domes Anim 43 (Suppl. 2): 347-354.
199. Spencer, K.W. (2010). Factors affecting fertility of frozen-thawed boar sperm. M.S. Thesis, University of Illinois at Urbana-Champaign, Illinois, USA (http://hdl.handle.net/2142/16492).
200. Vazquez, J.M., Martínez, E.A., Roca, J., Gil, M.A., Parrilla, I., Cuello, C., Carvajal, G., Lucas, X., Vazquez, J.L. (2005). Improving the efficiency of sperm technologies in pigs: the value of deep intrauterine insemination. Theriogenology 63: 536-547.
201. Spencer, K.W., Purdy, P.H., Blackburn, H.D., Spiller, S.F., Stewart, T.S., Knox, R.V. (2010). Effect of number of motile, frozen-thawed boar sperm and number of fixed-time inseminations on fertility in estrous-synchronized gilts. Anim Reprod Sci 121: 259–266.


Copyright

© 2014 Khalifa T. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Acknowledgment

This work was supported by Nidacon International AB, Flöjelbergsgatan 16B, SE-431 37 Mölndal, Sweden (Project # 1003-P; 2011-2012) and by the Veterinary Research Institute, Hellenic Agricultural Organization, 57001 NAGREF Campus, Thermi, P.O. Box 60272, Thessaloniki, Greece.

Conflict of Interest Statement

The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 37, Issue 1, Pages 5-34, p-ISSN 1409-7621, e-ISSN 1857-7415, DOI: 10.14432/j.macvetrev.2014.09.022, 2014