SAES-422 Multistate Research Activity Accomplishments Report

Status: Approved

Basic Information

Participants

Dave Miller (University of Illinois), Jason Ross (Iowa State University), Jean Feugang (Mississippi State University), Tim Safranski (University of Missouri), Brett White (University of Nebraska - Lincoln), Beth Hines (Penn State University), Kara Stewart (Purdue University), Lea Rempel (USMARC) and John Parrish (University of Wisconsin)

Brief Minutes of the NCERA-57 Multistate Committee on Swine Reproduction Meeting

Mississippi State University, Starkville, MS

May 20 – 21, 2019

May 20, 2019

The meeting, held at the Mississippi Agriculture and Forestry Extension Service (MAFES) Conference Center (Bull Barn), was called to order at 8:44 am on May 20th by Committee Chair, Kara Stewart (Purdue).  In attendance were:  Dave Miller (Illinois), Jason Ross (Iowa), Jean Feugang (Mississippi), Tim Safranski (Missouri), Brett White (Nebraska), Beth Hines (Pennsylvania), Kara Stewart (Purdue), Lea Rempel (USMARC) and John Parrish (Wisconsin).  Jean Feugang provided an overview of the schedule for the 2-day meeting.

Opening remarks were provided by Dr. George Hoffer (Dean and Director of the Agricultural Experiment Station).  First, Dr. Hoffer sent regards from Deb Hamernik (Administrative Advisor) who was unable to attend the meeting this year.  Next, he provided an overview of the student demographics at Mississippi State University as well as within the Department of Animal and Dairy Sciences and the Department of Poultry Science.  Dr. Wes Berger (Associate Director for Research) described the breakdown of research funding from partners, extramural granting agencies and commodity groups.  Finally, Dr. John Blanton (Head of the Department of Animal and Dairy Sciences) discussed the make-up of the Department of Animal Science including their four primary focus areas:  1) Teaching; 2) Reproductive Physiology; 3) Growth and Development; and 4) Nutrition. Dr. Blanton also presented additional information regarding the student population in the Department of Animal and Dairy Sciences.  The meeting agenda was reviewed and approved.  Brett White (Nebraska) made a motion to approve the minutes from the previous meeting as read and Tim Safranski (Missouri) seconded the motion.  The minutes were unanimously approved.

At 9:40 am, station reports were presented and discussed for USMARC, Wisconsin and Iowa.  Lea Rempel (USMARC) discussed her work on the relationship between piglet growth and lactation in sows as parities increase as well as investigations of the metabolome and microbiome of milk from sows.  John Parrish (Wisconsin) briefly described the changing paradigm in graduate education and a discussion ensued regarding whether the committee could become involved in a multi-institutional online course related to swine reproduction.  Dr. Parrish also provided an overview of his research studies examining:  1) the effects of scrotal insulation on histology of the testis; 2) activation of heat shock transcription factor 1 in somatic and meiotic cells; and 3) whether PG-600 could offset the effects of heat stress in the boar.  Jason Ross (Iowa) described studies examining estrous synchronization and stress stimuli during the follicular and luteal phases of the estrous cycle in gilts, the intraovarian heat shock protein response to heat stress, and health factors associated with vaginal prolapses in sows.  The committee suspended activities to take a lunch break at 12:30 pm.

In the afternoon, the first order of business was the election of new officers. Brett White (Nebraska), current secretary, will become the new chair of the committee.  John Parrish (Wisconsin) made a motion to elect Beth Hines (Pennsylvania) as secretary and Kara Stewart (Indiana) seconded the motion.  The motion passed unanimously.  Next, we proceeded with additional station reports.  Dave Miller (Illinois) discussed his recent work on sperm storage and binding in the porcine oviduct including: 1) ABHD2, a non-genomic receptor for progesterone on sperm; 2) evaluation of proximal and distal droplets on sperm within the epididymis; and 3) the core transcriptome of sperm storage organs.  Jean Feugang (Mississippi) described studies with metal and carbon-based nanoparticles for sperm selection, potential use of nanoparticles (based on lysosomes) for delivery in live animals and intrafollicular injection of nanoparticles.  

At 3:00 pm, members of the committee were provided an enjoyable tour of the new Meat Lab as well as the animal facilities at Mississippi State University.  The group returned for dinner at the MAFES Conference Center.  Following dinner, the committee discussed details of the 2020 biennial symposium.  Kara Stewart (Indiana) volunteered to host the 2020 meeting.  Potential topics for the symposium including technology, gilt development and sow productivity/longevity were debated.  Members agreed that “managing the high-performance sow” would be an appropriate topic and sow farm decision makers would be the target audience for the 2020 biennial symposium in Indiana.  Additional details will be discussed via email or video conferencing.  At 7:30 pm, the meeting was adjourned for the day.

May 21, 2019

The committee resumed its annual meeting at 8:30 am on May 21, 2019.  The remaining station reports were presented.  Tim Safranski (Missouri) discussed a project he was developing to provide research and training opportunities to undergraduate students at the University of Missouri.  This included the acquisition of funds for students to attend both scientific and producer meetings.  Next, Kara Stewart (Purdue) presented results of a reproductive technology survey sent to swine producers, especially regarding the adoption of post-cervical AI on sow farms.  She also discussed the lipidome profiles from vaginal smears in Day 2 piglets may have biomarkers of colostrum intake.  Brett White (Nebraska) provided an overview of his work utilizing a swine line with reduced endogenous levels of the porcine GnRH-II receptor (GnRHR-II KD). Results from experiments examining the luteal phase of the estrous cycle in gilts were reported. The last station report was presented by our new member, Beth Hines (Pennsylvania). Details of the swine facilities available at Penn State University as well as the programmatic goals of Dr. Hines were described.

The committee thanked Jean Feugang (Mississippi) for graciously hosting the meeting and the wonderful hospitality. John Parrish (Wisconsin) was recognized for his excellent efforts in preparing the recent rewrite for the NCERA-57 Committee. In addition, thanks were given to Dr. Wes Berger (Associate Dean for Research) for providing funding support for the meals. Lastly, the members thanked the Meat Laboratory (supervised by Tim Armstrong and Joseph Mangano) for the superb meals provided throughout the meeting. The meeting was adjourned at 11:15 am.

Respectively Submitted,

Brett White – Secretary

NCERA-57 Technical Committee on Swine Reproduction

Accomplishments

1) Committee members have been highly productive in terms of publications related to reproduction in swine. Only peer-reviewed manuscripts (53 accepted or published) are provided in the current report. In addition, 32 abstracts were presented at various professional and scientific meetings.

2) A survey of U.S. swine breeding herds regarding pelvic organ prolapse in sows identified several different risk factors needing further investigation.

3) Determined that producers can administer OvuGel to sows in proestrus or estrus on d 4 post-weaning, followed by a single insemination 24 hours later, and achieve similar performance as sows inseminated multiple times upon detection of estrus.

4) Demonstrated that the secretions of cumulus oocyte complexes can trigger the release of sperm from oviduct epithelial cells and that release of sperm from the sperm reservoir within the oviduct is induced by progesterone action through CatSper channels.

5) A survey of swine producers to determine their likeliness to adopt reproductive technologies such as post-cervical artificial insemination (PCAI), indicated that cost was the most important factor.

6) Illustrated that high concentrations of circulating progesterone during early gestation influences within-litter birth weight variation in pigs.

7) Identified several putative metabolites that change within the uterine milieu as porcine embryos transition between spherical, ovoid, and tubular conceptuses.

8) Determined that if a heat stress event was detected or predicted, administration of PG600 to boars could mitigate the impact on spermatogenesis.

9) Ovulation rate was reduced in GnRH-II receptor knockdown compared to littermate control gilts, despite no difference in weight of the ovaries between lines.

10) On Day 10 of the estrous cycle, circulating progesterone concentrations were lower in GnRH-II receptor knockdown vs. littermate control gilts.

 

Impacts

  1. A better understanding of the mechanisms associated with pelvic organ prolapses could result in new mitigation strategies to reduce sow mortality.
  2. Reducing the number of sperm required to produce a litter can allow boars of higher genetic merit to influence more piglets and therefore, increase profitability of swine producers.
  3. An improved understanding of the role that zinc ions play in sperm fertilization competency may allow more accurate fertility assessment of boars.
  4. Analysis of lipidome profiles from vaginal smears of piglets at 2 days of age may reveal economically important biomarkers of colostrum intake.
  5. Identification of critical molecular factors within the porcine uterus that delay embryo elongation will improve embryonic survival and conception rates.
  6. Development of methods to reduce within-litter birth weight variation will improve piglet viability and survivability.
  7. Novel methods to mitigate heat stress in boars will improve reproductive efficiency and thus, increase the profitability and sustainability of pork production.
  8. Identification of subfertile boars at a younger age would allow producers to focus resources on reproductively superior animals and market subfertile males prior to sexual maturity, significantly increasing their value.
  9. Novel factors may be determined to improve semen extenders in swine, extending the lifespan of sperm and decreasing the cost of semen doses.

Publications

Publications (citations in bold are from more than one station):

Boar Performance (IL, IN, NE, USMARC, WI)

Gruhot, T.R., L.A. Rempel, M.L. Spangler, S.D. Kachman, and B.E. Mote. 2019. The heritability of pampiniform plexus vessel size and varicocele in boars. Reprod. Dom. Anim. 54:270-274.

Hufana-Duran D., P.G. Duran, R. Monson, J.J. Parrish. 2017. Motility and membrane integrity of ejaculated bovine spermatozoa extended and cryopreserved in L-Carnitine Tris-Egg yolk extender. J. International Society for Southeast Asian Agriculture Sciences 23:56-67.

Lugar, D.W., J.A. Proctor, T.J. Safranski, M.C. Lucy, and K.R. Stewart. 2018. In utero heat stress causes reduced testicular area at puberty, reduced total sperm production, and increased sperm abnormalities in boars. Anim. Repro. Sci. 192:126-135.

Rempel L.A., M.M. Krautkramer, T.M. Loether, J.J. Parrish, and J.R. Miles. 2018. Season of collection and sperm head shape impacts expression of CARHSP and FTL from motile-rich boar sperm. Agri Gene 7:1-6.

Rempel, L.A., M.M. Krautkramer, J.J. Parrish, and J.R. Miles. 2019. Impact of seasonality, storage of semen, and sperm head-shape on whole tissue methylation and expression of methylation responsive candidate genes in swine placenta and fetal livers from summer and winter breedings. Mol. Reprod. Dev. 86:465-475.

Winters R.A., D. Hamilton, A. Bhatnagar, R. Fitzgerald, N. Bovin, and D.J. Miller. 2018. Porcine sperm binding to oviduct cells and glycans as supplements to traditional laboratory semen analysis. J. Anim. Sci. 96:5265-5275.

Winters R.A., L.M. Nettenstrom, D.G. Lopez, K.L. Willenburg, R. Vishwanath, and D.J. Miller. 2018. Effect of sorting porcine spermatozoa by sex chromosomes on oviduct cell binding. Theriogenology 108:22-28.

Sow and Gilt Performance (IA, IL, IN, USMARC)

Chapel, N.M., J.S. Radcliffe, K.R. Stewart, J.R. Lucas, and D.C. Lay Jr. 2018. The impact of farrowing room noise on sows’ reactivity to piglets.  Translational Anim. Sci. 3:175-184.

Dickson, M., C.L. Hager, A. Al-Shaibi, P. Thomas, L.H. Baumgard, J.W. Ross, and A.F. Keating, 2018 Impact of heat stress during the follicular phase on porcine ovarian steroidogenic and phosphatidylinositol-3 signaling. J. Anim. Sci. 96:2162-2174.

George, A.F., T. Ho, N. Prasad, B.N. Keel, J.R. Miles, J.L. Vallet, F.F. Bartol, and C.A. Bagnell. 2019. Neonatal lactocrine deficiency affects the adult porcine endometrial transcriptome at pregnancy day 13. Biol. Reprod. 100:71-85.

Graves, K.L., J.T. Seibert, A.F. Keating, L.H. Baumgard, and J.W. Ross. 2018. Characterizing the acute heat stress response in gilts: II. Assessing repeatability and association with fertility. J. Anim. Sci. 96:2419-2426.

Knox, R.V. Physiology and Endocrinology Symposium: Factors influencing follicle development in gilts and sows and management strategies used to regulate growth for control of estrus and ovulation. J. Anim. Sci. 97:1433-45.

Knox, R.V., K.R., Stewart, W.L. Flowers, M.E. Swanson, S.K. Webel, and R.R. Kraeling. 2018. Design and biological effects of a vaginally administered gel containing the GnRH agonist, triptorelin, for synchronizing ovulation in swine. Theriogenology 112:44-52.

Rempel L.A., M.M. Krautkramer, J.J. Parrish, and J.R. Miles. 2019. Impact of seasonality, storage of semen, and sperm head‐shape on whole tissue methylation and expression of methylation responsive candidate genes in swine placenta and fetal livers from summer and winter breedings. Mol. Reprod. Dev. 86:465-475.

Seibert, J.T., K.L. Graves, B.J. Hale, A.F. Keating, L.H. Baumgard, and J.W. Ross, 2018.  Characterizing the acute heat stress response in gilts: I. Thermoregulatory and production variables.  J. Anim. Sci. 96:941-949.

Ulguim R.R., F.P. Bortolozzo, I. Wentz, M. Johnston, S.K. Webel, L. Arend, and R.V. Knox. 2018. Ovulation and fertility responses for sows receiving once daily boar exposure after weaning and OvuGel® followed by a single fixed time post cervical artificial insemination. Theriogenology. 105: 27-33.

Growth, Development, Physiology (IA, IL, MO, USMARC, WI)

Bidne, K.L., M.J. Dickson, J.W. Ross, L.H. Baumgard, and A.F. Keating, 2018. Disruption of reproductive function by gut permeability to endotoxins.   Reproduction 155:R169-R181.

Chen, P.R., B.K. Redel, L.D. Spate, T. Ji, S.R. Salazar, and R.S. Prather. 2018. Glutamine supplementation enhances development of in vitro-produced porcine embryos and increases leucine consumption from the culture medium. Biol. Reprod. 99:938-948.

Kerns, K., M. Zigo, E.Z. Drobnis, M. Sutovsky, and P. Sutovsky. 2018. Zinc ion flux during mammalian sperm capacitation. Nat. Commun. 9:2061.

Kerns, K., M. Zigo, and P. Sutovsky. 2018. Zinc: A necessary ion for mammalian sperm fertilization competency. Int. J. Mol Sci. 19(12).

Knox, R.V., D.J. Miller. 2018. Male ART in Animal Species. In:  M. K. Skinner (Ed.), Encyclopedia of Reproduction (2nd Ed.). Vol. 1, pp. 547–552. Academic Press: Elsevier.

Mayorga E.J., S.K. Kvidera, E.A. Horst, M. Al-Qaisi, M.J. Dickson, J.T. Seibert, S. Lei, A.F. Keating, J.W. Ross, R.P. Rhoads, Z.J. Rambo, M.E. Wilson, and L.H. Baumgard. Effects of zinc amino acid complex on biomarkers of gut integrity and metabolism during and following heat stress or feed restriction in pigs.  J. Anim. Sci. 96:4173-4185.

Meyer, A.E., C.A Pfeiffer, K.E. Brooks, L.D. Spate, J.A. Benne, R. Cecil, M.S. Samuel, C.N. Murphy, S. Behura, M.K. McLean, L.A. Ciernia, M.F. Smith, T.E. Spencer, R.S. Prather, and R.D. Geisert. 2019. New perspective on the role of conceptus estrogens in conceptus development, maternal recognition and establishment of pregnancy in the pig. Biol. Reprod. 101:148-161.

Miller D.J.  2018.  The epic journey of sperm through the female reproductive tract.  Animal 12(Suppl. s1):110-120.

Mordhorst, B.R., J.A. Benne, R.F. Cecil, K.M. Whitworth, M.S. Samuel, L.D. Spate, C.N. Murphy, K.D. Wells, J.A. Green, and R.S. Prather. 2019. Improvement of in vitro and early in utero porcine clone development after somatic donor cells are cultured under hypoxia. Mol. Reprod. Dev. 86:558-565.

Mordhorst, B.R., S.L. Murphy, M. Schaufliner, S. Rojas Salazar, T. Ji, S.K. Behura, K.D. Wells, J.A. Green, and R.S. Prather. 2018. Porcine fetal-derived fibroblast cells alter gene expression and mitochondria to compensate for hypoxic stress during culture. Cell. Reprogram. 20:225-235.

Mordhorst, B.R., S.L. Murphy, R.M. Ross, J. A. Benne, M.S. Samuel, R.A. Cecil, B.K. Redel, L.D. Spate, C.N. Murphy, K.D. Wells, J. A. Green, and R. S. Prather. 2018. Pharmacologic treatment of donor cells induced to have a Warburg effect-like metabolism does not alter embryonic development in vitro or survival during early gestation when used in somatic cell nuclear transfer in pigs. Mol. Reprod. Dev. 85:290-302.

Mordhorst, B.R., S.L. Murphy, R.M. Ross, M.S. Samuel, T. Ji, S. Rojas Salazar, S.K. Behura, K.D. Wells, J.A. Green, and R.S. Prather. 2018. Pharmacologic reprogramming designed to induce a Warburg Effect in porcine fetal fibroblasts alters gene expression and quantities of spent media metabolites without increased cell proliferation. Cell. Reprogram. 20:38-48.

Parrish, J.J. 2019. Spermatogenesis, heat stress and male infertility, In: Molecular Mechanisms In Spermatogenesis And Male Infertility. Ed: Rajender Singh. CRC Press, Boca Raton, FL, USA. (in press)

Seelenbinder K.M., L.D. Zhao, M.D. Hanigan, M.W. Hulver, R.P. McMillan, L.H. Baumgard, J.T. Selsby, J.W. Ross, N.K. Gabler, and R.P. Rhoads, 2018.  Effects of heat stress during porcine reproductive and respiratory syndrome virus infection on metabolic responses in growing pigs. J. Anim. Sci. 96:1375-1387.

Seibert J.T., M. Abuajamieh, M.V. Sanz Fernandez, J.S.Johnson, S.K.Kvidera, E.A. Horst, E.J. Mayorga, S. Lei, J.F. Patience, J.W. Ross, R.P. Rhoads, R.C. Johnson, S.M. Lonergan, J.W. Perfield, 2nd, and L.H Baumgard.  2018.  Effects of heat stress and insulin sensitizers on pig adipose tissue. J. Anim. Sci. 96:510-520.

Smith M.F., R.D. Geisert, and J.J. Parrish. 2018. Reproduction in domestic ruminants during the past 50 years: discovery to application. J. Anim. Sci. 96:2952-2970

Sutovsky, P. 2018. Pig overview (male reproduction) In:  M. K. Skinner (Ed.), Encyclopedia of Reproduction (2nd Ed.). Vol. 1, pp. 501–507. Academic Press: Elsevier.

Whyte, J.J., A.E. Meyer, L.D. Spate, J.A. Benne, R. Cecil, M.S. Samuel, C.N. Murphy, R.S. Prather, and R.D. Geisert. 2018. Inactivation of interleukin-1B (IL1B2) results in failure of rapid conceptus elongation. Proc. Natl. Acad. Sci. U.S.A. 115:307-312.

Zhao, L., R. McMillan, G. Xie, S. Giridhar, L.H. Baumgard, S. El-Kadi, J.T. Selsby, J.W. Ross, N.K. Gabler, M. Hulver, and R. Rhoads. 2018.  Heat stress decreases metabolic flexibility in skeletal muscle of growing pigs. Am J Physiol Regul Integr Comp Physiol. 315:R1096-R1106.

Basic Science and Technology (IA, IL, MO, NE, USMARC)

Abuajamieh, M., S.K. Kvidera, E.J. Mayorga, A. Kaiser, S.M. Lei, J.T. Seibert, E.A. Horst, M.V. Sanz Fernandez, J.W. Ross, J.T. Selsby, A.F. Keating, R.P. Rhoads, and L.H.  Baumgard. 2018 The effect of recovery from heat stress on circulating bioenergetics and inflammatory biomarkers.  J. Anim. Sci. 96:4599-4610.

Bidne K.L., S.S. Kvidera, J.W. Ross, L.H. Baumgard, and A.F. Keating. 2018. Impact of repeated lipopolysaccharide administration on ovarian signaling during the follicular phase of the estrous cycle in post-pubertal pigs.  J. Anim. Sci. 96:3622-3634.

Li, Y., M.K. Adur, B.J. Hale, and J.W. Ross. 2018.  Regulation of oogenesis by noncoding RNAs.  In:  M. K. Skinner (Ed.), Encyclopedia of Reproduction (2nd Ed.). Vol. 3, pp. 190–196. Academic Press: Elsevier.

Manca, S., B. Upadhyaya, E. Mutai, A.T. Desaulniers, R.A. Cederberg, B.R. White and J. Zempleni. 2018. Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Sci. Rep. 8:11321.

Mao, J., C. O’Gorman, M. Sutovsky, M. Zigo, K.D. Wells, and P. Sutovsky. 2018. Ubiquitin A-52 residue ribosomal protein fusion product 1 (Uba52) is essential for preimplantation embryo development. Biol. Open 7(10).

Powell, E.J., S. Charley, A. Boettcher, L. Varley, J. Brown, M. Schroyen, M.K. Adur, S. Dekkers, D. Isaacson, M. Sauer, J. Cunnick, N.M. Ellinwood, J.W. Ross, J.C.M. Dekkers, and C.K.  Tuggle. 2018.  Creating effective biocontainment facilities and maintenance protocols for raising specific pathogen free, severe combined immunodeficient (SCID) swine.  Lab Anim. 52:402-412.

Redel, B.K., B.P. Beaton, J.A. Benne, S.L. Murphy, C.W. O’Gorman, A.M. Spate, R.S. Prather, and K.D. Wells. 2018. Single step production of Cas9 mRNA for zygote injection. BioTechniques, 64:118-124.

Ryu J., R.S. Prather, and K. Lee. 2018. Use of gene-editing technology to introduce targeted modifications in pigs. J. Anim. Sci. Biotechnol. 9:5.

Sutovsky, P., and W. Song. 2018. Post-fertilization sperm mitophagy: The tale of mitochondrial Eve and Steve. Reprod. Fert. Dev. 30:56-63.

Thorson, J.F., L.D. Prezotto, H. Adams, S.L. Petersen, J.A. Clapper, E.C. Wright, W.T. Oliver, B.A. Freking, A.P. Foote, E.D. Berry, D.J. Nonneman, and C.A. Lents. 2018. Energy balance affects pulsatile secretion of luteinizing hormone from the adenohypophesis and expression of neurokinin B in the hypothalamus of ovariectomized gilts. Biol. Reprod. 99:433-445.

Whitworth, K.M., R. Cecil, J.A. Benne, B.K. Redel, L.D. Spate, M.S. Samuel, K.D. Wells, and R.S. Prather. 2018. Zygote injection of RNA encoding Cre recombinase results in efficient removal of LoxP flanked neomycin cassettes in pigs. Transgenic Res. 27:167-178.

Whitworth, K.M., R.R.R. Rowland, V. Petrovan, M. Sheahan, A.G. Cino-Ozuna, J. Nietfeld, Y, Fang, R. Hesse, A. Mileham, M.S. Samuel, K.D. Wells, and R.S. Prather. 2019. Resistance to coronavirus infection in amino peptidase N-deficient pigs. Transgenic Res. 28:21-32.

Zigo, M., K. Kerns, M. Sutovsky, and P. Sutovsky. 2018. Modifications of the 26S proteasome during boar sperm capacitation. Cell Tissue Res. 372:591-601.

Genetics and Genomics (IA, IL, USMARC)

Beiki, H., H. Liu, N. Manchanda, D.J. Nonneman, T.P.L. Smith, J. Reecy, and C. Tuggle. 2019. Improved annotation of the domestic pig genome through integration of Iso-Seq and RNA-seq data. BMC Genomics. 20:344-362.

Fu YR, R. Knox, L. Li, and S. Ren. 2018. Differential gene expression of Eph-ephrin A1 and LEPR-LEP with high or low number of embryos in pigs during implantation. Reprod. Dom. Anim.

Keel, B.N., D.J. Nonneman, A.K. Lindholm-Perry, W.T. Oliver, and G.A. Rohrer. 2018. Porcine single nucleotide polymorphisms and their functional effect: an update. BMC Research Notes 11:860.

Kim, K.S., J.T. Seibert, Z. Edea, K.L. Graves, E.-S. Kim, A.F. Keating, L.H. Baumgard, J.W. Ross, and M.F. Rothschild. 2018. Characterizing the acute heat stress response in gilts: III. Identification of underlying genomic control. J. Anim. Sci. 96:2074-2085.

Teaching and Extension (NE)

McFee, R.M., A.S. Cupp and J.R. Wood. 2018. Use of case-based or hands-on laboratory exercises with physiology lectures improves knowledge retention, but veterinary medicine students prefer case-based activities. Adv Physiol Educ. 42:182-191.

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