Skip to main content

Advertisement

SpringerLink
Log in

Early-Life Intervention of Lactoferrin and Probiotic in Suckling Piglets: Effects on Immunoglobulins, Intestinal Integrity, and Neonatal Mortality

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

The aim of this study was to determine the effects of early-life bovine lactoferrin and host specific probiotic interventions on growth performance, mortality, and concentrations of immunoglobulin A and immunoglobulin G and transforming growth factor beta 1 (a marker of intestinal integrity) in serum of neonatal piglets. A total of eight piglet litters from parity matched sows were randomly divided into four groups and assigned to one of the four interventions: control (sterile normal saline), bovine lactoferrin (100 mg bovine lactoferrin), probiotic (1 × 109 colony forming unit (cfu) of swine origin Pediococcus acidilactici FT28 probiotic), and bovine lactoferrin + probiotic (100 mg bovine lactoferrin and 1 × 109 CFU of P. acidilactici FT28 probiotic). All the interventions were given once daily through oral route for first 7 days of life. The average daily gain (p = 0.0004) and weaning weight (p < 0.0001) were significantly improved in the probiotic group. The piglet survivability was significantly higher in bovine lactoferrin and probiotic groups than control group in Log-rank (Mantel-Cox) test. The concentrations of immunoglobulin A on day 21 in bovine lactoferrin, probiotic, and bovine lactoferrin + probiotic groups increased significantly (p < 0.05). Immunoglobulin G concentrations on day 7 and 15 in bovine lactoferrin and bovine lactoferrin + probiotic groups and on day 15 in probiotic group were significantly (p < 0.05) elevated, whereas, the concentration of transforming growth factor-β1 was significantly (p < 0.05) increased from day 7 to 21 in all the supplemented groups. In conclusion, the early-life bovine lactoferrin and P. acidilactici FT28 probiotic interventions reduced the mortality in the suckling piglets by promoting the systemic immunity and enhancing the intestinal integrity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Sell-Kubiak E (2021) Selection for litter size and litter birthweight in Large White pigs: maximum, mean and variability of reproduction traits. Animal 15:100352. https://doi.org/10.1016/j.animal.2021.100352

    Article  Google Scholar 

  2. Cabrera RA, Lin X, Campbell JM, Moeser AJ, Odle J (2012) Influence of birth order, birth weight, colostrum and serum immunoglobulin G on neonatal piglet survival. J Anim Sci Biotechnol 3:1–10. https://doi.org/10.1186/2049-1891-3-42

    Article  CAS  Google Scholar 

  3. Butler JE, Zhao Y, Sinkora M, Wertz N, Kacskovics I (2009) Immunoglobulins, antibody repertoire and B cell development. Dev Comp Immunol 33:321–333. https://doi.org/10.1016/j.dci.2008.06.015

    Article  CAS  Google Scholar 

  4. Salmon H, Berri M, Gerdts V, Meurens F (2009) Humoral and cellular factors of maternal immunity in swine. Dev Comp Immunol 33:384–393. https://doi.org/10.1016/j.dci.2008.07.007

    Article  CAS  Google Scholar 

  5. Hurley WL, Theil PK (2011) Perspectives on immunoglobulins in colostrum and milk. Nutrients 3:442–474. https://doi.org/10.3390/nu3040442

    Article  CAS  Google Scholar 

  6. Navarro E, Mainau E, de Miguel R, Temple D, Salas M, Manteca X (2021) Oral meloxicam administration in sows at farrowing and its effects on piglet immunity transfer and growth. Front Vet Sci 8:72. https://doi.org/10.3389/fvets.2021.574250

    Article  Google Scholar 

  7. Walker WA (2013) Initial intestinal colonization in the human infant and immune homeostasis. Ann Nutr Metab 63:8–15. https://doi.org/10.1159/000354907

    Article  CAS  Google Scholar 

  8. Isaacson R, Kim HB (2012) The intestinal microbiome of the pig. Anim Health Res Rev 13:100. https://doi.org/10.1017/S1466252312000084

    Article  Google Scholar 

  9. Pajarillo EA, Chae JP, Balolong MP, Kim HB, Kang DK (2014) Assessment of fecal bacterial diversity among healthy piglets during the weaning transition. J Gen Appl Microbiol 60:140–146. https://doi.org/10.2323/jgam.60.140

    Article  CAS  Google Scholar 

  10. Chen X, Xu J, Ren E, Su Y, Zhu W (2018) Co-occurrence of early gut colonization in neonatal piglets with microbiota in the maternal and surrounding delivery environments. Anaerobe 49:30–40. https://doi.org/10.1016/j.anaerobe.2017.12.002

    Article  CAS  Google Scholar 

  11. Bauche D, Marie JC (2017) Transforming growth factor β: a master regulator of the gut microbiota and immune cell interactions. Clin Transl Immunol 6:e136. https://doi.org/10.1038/cti.2017.9

    Article  CAS  Google Scholar 

  12. Stolfi C, Troncone E, Marafini I, Monteleone G (2021) Role of TGF-beta and Smad7 in gut inflammation, fibrosis and cancer. Biomolecules 11:17. https://doi.org/10.3390/biom11010017

    Article  CAS  Google Scholar 

  13. Mei J, Xu RJ (2005) Transient changes of transforming growth factor-β expression in the small intestine of the pig in association with weaning. Br J Nutr 93:37–45. https://doi.org/10.1079/BJN20041302

    Article  CAS  Google Scholar 

  14. Xu R, Wan J, Lin C, Su Y (2020) Effects of early intervention with antibiotics and maternal faecal microbiota on transcriptomic profiling ileal mucosa in neonatal pigs. Antibiotics 9:35. https://doi.org/10.3390/antibiotics9010035

    Article  CAS  Google Scholar 

  15. Bian G, Ma S, Zhu Z, Su Y, Zoetendal EG, Mackie R, Liu J, Mu C, Huang R, Smidt H, Zhu W (2016) Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross-fostering model. Environ Microbiol 18:1566–1577. https://doi.org/10.1111/1462-2920.13272

    Article  CAS  Google Scholar 

  16. Chae JP, Pajarillo EA, Oh JK, Kim H, Kang DK (2016) Revealing the combined effects of lactulose and probiotic enterococci on the swine faecal microbiota using 454 pyrosequencing. Microb Biotechnol 9:486–495. https://doi.org/10.1111/1751-7915.12370

    Article  CAS  Google Scholar 

  17. Hu Q, Liu C, Zhang D, Wang R, Qin L, Xu Q, Che L, Gao F (2020) Effects of low-dose antibiotics on gut immunity and antibiotic resistomes in weaned piglets. Front Immunol 11:903. https://doi.org/10.3389/fimmu.2020.00903

    Article  CAS  Google Scholar 

  18. Paesano R, Berlutti F, Pietropaoli M, Pantanella F, Pacifici E, Goolsbee W, Valenti P (2010) Lactoferrin efficacy versus ferrous sulfate in curing iron deficiency and iron deficiency anemia in pregnant women. Biometals 23:411–417. https://doi.org/10.1007/s10534-010-9335-z

    Article  CAS  Google Scholar 

  19. Comstock SS, Reznikov EA, Contractor N, Donovan SM (2014) Dietary bovine lactoferrin alters mucosal and systemic immune cell responses in neonatal piglets. J Nutr 144:525–532. https://doi.org/10.3945/jn.113.190264

    Article  CAS  Google Scholar 

  20. Elbarbary HA, Ejima A, Sato K (2019) Generation of antibacterial peptides from crude cheese whey using pepsin and rennet enzymes at various pH conditions. J Sci Food Agric 99:555–563. https://doi.org/10.1002/jsfa.9214

    Article  CAS  Google Scholar 

  21. Donker AE, van der Staaij H, Swinkels DW (2021) The critical roles of iron during the journey from fetus to adolescent: developmental aspects of iron homeostasis. Blood Rev 50:100866. https://doi.org/10.1016/j.blre.2021.100866

  22. Zhao X, Zhang X, Xu T, Luo J, Luo Y, An P (2022) Comparative effects between oral lactoferrin and ferrous sulfate supplementation on iron-deficiency anemia: a comprehensive review and meta-analysis of clinical trials. Nutrients 14:543. https://doi.org/10.3390/nu14030543

  23. Majka G, Śpiewak K, Kurpiewska K, Heczko P, Stochel G, Strus M, Brindell MA (2013) A high-throughput method for the quantification of iron saturation in lactoferrin preparations. Anal Bioanal Chem 405:5191–200. https://doi.org/10.1007/s00216-013-6943-9

  24. Oguchi S, Walker WA, Sanderson IR (1995) Iron saturation alters the effect of lactoferrin on the proliferation and differentiation of human enterocytes (Caco-2 cells). Biol Neonate 67:330–339. https://doi.org/10.1159/000244182

    Article  CAS  Google Scholar 

  25. Vega-Bautista A, de la Garza M, Carrero JC, Campos-Rodríguez R, Godínez-Victoria M, Drago-Serrano ME (2019) The impact of lactoferrin on the growth of intestinal inhabitant bacteria. Int J Mol Sci 20:4707. https://doi.org/10.3390/ijms20194707

  26. Hu W, Zhao J, Wang J, Yu T, Wang J, Li N (2012) Transgenic milk containing recombinant human lactoferrin modulates the intestinal flora in piglets. Biochem Cell Biol 90:485–496. https://doi.org/10.1139/o2012-003

    Article  CAS  Google Scholar 

  27. Hering NA, Luettig J, Krug SM, Wiegand S, Gross G, van Tol EA, Schulzke JD, Rosenthal R (2017) Lactoferrin protects against intestinal inflammation and bacteria-induced barrier dysfunction in vitro. Ann N Y Acad Sci 1405:177–188. https://doi.org/10.1111/nyas.13405

    Article  CAS  Google Scholar 

  28. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJM, Wells JM (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 298:G851–G859. https://doi.org/10.1152/ajpgi.00327.2009

    Article  CAS  Google Scholar 

  29. Ahrne S, Hagslatt ML (2011) Effect of lactobacilli on paracellular permeability in the gut. Nutrients 3:104–117. https://doi.org/10.3390/nu3010104

    Article  CAS  Google Scholar 

  30. Davis ME, Parrott T, Brown DC, De Rodas BZ, Johnson ZB, Maxwell CV, Rehberger T (2008) Effect of a Bacillus-based direct-fed microbial feed supplement on growth performance and pen cleaning characteristics of growing-finishing pigs. J Anim Sci 86:1459–1467. https://doi.org/10.2527/jas.2007-0603

    Article  CAS  Google Scholar 

  31. Wang AN, Yi XW, Yu HF, Dong B, Qiao SY (2009) Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing–finishing pigs. J Appl Microbiol 107:1140–1148. https://doi.org/10.1111/j.1365-2672.2009.04294.x

    Article  CAS  Google Scholar 

  32. Galdeano CM, De Leblanc ADM, Vinderola G, Bonet MB, Perdigon G (2007) Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clin Vaccine Immunol 14:485–492. https://doi.org/10.1128/CVI.00406-06

    Article  CAS  Google Scholar 

  33. Dowarah R, Verma AK, Agarwal N, Singh P (2016) Effect of swine-based probiotic on growth performance, nutrient utilization and immune status of early weaned grower-finisher crossbred pigs. Anim Nutr Feed Technol 16:451–461. https://doi.org/10.5958/0974-181X.2016.00042.1

    Article  Google Scholar 

  34. Dowarah R, Verma AK, Agarwal N, Singh P, Singh BR (2018) Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. PLoS ONE 13:e0192978. https://doi.org/10.1371/journal.pone.0192978

    Article  CAS  Google Scholar 

  35. Dowarah R, Verma AK, Agarwal N, Patel BHM, Singh P (2017) Effect of swine-based probiotic on performance, diarrhoea scores, intestinal microbiota and gut health of grower-finisher crossbred pigs. Livest Sci 195:74–79. https://doi.org/10.1016/j.livsci.2016.11.006

    Article  Google Scholar 

  36. Li Y, Hou S, Chen J, Peng W, Wen W, Chen F, Huang X (2019) Oral administration of Lactobacillus delbrueckii during the suckling period improves intestinal integrity after weaning in piglets. J Func Food 63:103591. https://doi.org/10.1016/j.jff.2019.103591

    Article  CAS  Google Scholar 

  37. Li Y, Hou S, Peng W, Lin Q, Chen F, Yang L, Li F, Huang X (2019) Oral administration of Lactobacillus delbrueckii during the suckling phase improves antioxidant activities and immune responses after the weaning event in a piglet model. Oxid Med Cell Longev 2019:6919803. https://doi.org/10.1155/2019/6919803

    Article  CAS  Google Scholar 

  38. Thacker PA (2013) Alternatives to antibiotics as growth promoters for use in swine production: a review. J Anim Sci Biotechnol 4:35. https://doi.org/10.1186/2049-1891-4-35

    Article  CAS  Google Scholar 

  39. Muurinen J, Richert J, Wickware CL, Richert B, Johnson TA (2021) Swine growth promotion with antibiotics or alternatives can increase antibiotic resistance gene mobility potential. Sci Rep 11:1–3. https://github.com/sjmuurine/ZnCu

  40. Vandenplas Y, Benninga M, Broekaert I, Falconer J, Gottrand F, Guarino A, Lifschitz C, Lionetti P, Orel R, Papadopoulou A (2016) Functional gastro-intestinal disorder algorithms focus on early recognition, parental reassurance and nutritional strategies. Acta Paediatr 105:244–252. https://doi.org/10.1111/apa.13270

    Article  Google Scholar 

  41. Wang S, Yao B, Gao H, Zang J, Tao S, Zhang S, Huang S, He B, Wang J (2019) Combined supplementation of Lactobacillus fermentum and Pediococcus acidilactici promoted growth performance, alleviated inflammation, and modulated intestinal microbiota in weaned pigs. BMC Vet Res 15:1–11. https://doi.org/10.1186/s12917-019-1991-9

    Article  CAS  Google Scholar 

  42. Pupa P, Apiwatsiri P, Sirichokchatchawan W, Pirarat N, Maison T, Koontanatechanon A, Prapasarakul N (2021) Use of Lactobacillus plantarum (strains 22F and 25F) and Pediococcus acidilactici (strain 72N) as replacements for antibiotic-growth promotants in pigs. Sci Rep 11:1–12. https://doi.org/10.1038/s41598-021-91427-5

    Article  CAS  Google Scholar 

  43. English EA, Hopkins BA, Stroud JS, Davidson S, Smith G, Brownie C, Whitlow LW (2007) Lactoferrin supplementation to Holstein calves during the preweaning and postweaning phases. J Dairy Sci 90:5276–5281. https://doi.org/10.3168/jds.2007-0361

    Article  CAS  Google Scholar 

  44. Geier MS, Torok VA, GuoP AGE, Boulianne M, Janardhana V, Bean AG, Hughes RJ (2011) The effects of lactoferrin on the intestinal environment of broiler chickens. Br Poult Sci 52:564–572. https://doi.org/10.1080/00071668.2011.607429

    Article  CAS  Google Scholar 

  45. Shan T, Wang Y, Wang Y, Liu J, Xu Z (2007) Effect of dietary lactoferrin on the immune functions and serum iron level of weanling piglets. J Anim Sci 85:2140–2146. https://doi.org/10.2527/jas.2006-754

    Article  CAS  Google Scholar 

  46. Hu P, Zhao F, Zhu W, Wang J (2019) Effects of early-life lactoferrin intervention on growth performance, small intestinal function and gut microbiota in suckling piglets. Food Funct 10:5361–5373. https://doi.org/10.1039/C9FO00676A

    Article  CAS  Google Scholar 

  47. Wajda S, Smiecinska K, Jankowski J, Matusevicius P, Buteikis G (2010) The efficacy of lactic acid bacteria Pediococcus acidilactici, lactose and formic acid as dietary supplements for turkeys. Pol J Vet Sci 13:45. https://www.ncbi.nlm.nih.gov/pubmed/21077430

  48. El Barbary M, Shady NA, Shaaban HA, Shaaban MA, Ahmed OY (2018) Effect of enteral bovine lactoferrin on neonatal iron status. Egypt J Haematol 43:212. https://doi.org/10.4103/ejh.ejh_30_18

    Article  Google Scholar 

  49. Habing G, Harris K, Schuenemann GM, Piñeiro JM, Lakritz J, Clavijo XA (2017) Lactoferrin reduces mortality in preweaned calves with diarrhea. J Dairy Sci 100:3940–3948. https://doi.org/10.3168/jds.2016-11969

    Article  CAS  Google Scholar 

  50. Joysowal M, Saikia BN, Dowarah R, Tamuly S, Kalita D, Choudhury KD (2018) Effect of probiotic Pediococcus acidilactici FT28 on growth performance, nutrient digestibility, health status, meat quality, and intestinal morphology in growing pigs. Vet World 11:1669. https://doi.org/10.14202/2Fvetworld.2018.1669-1676

  51. Hu P, Zhao F, WangJ ZhuW (2020) Early-life lactoferrin intervention modulates the colonic microbiota, colonic microbial metabolites and intestinal function in suckling piglets. Appl Microbiol Biotechnol 104:6185–6197. https://doi.org/10.1007/s00253-020-10675-z

    Article  CAS  Google Scholar 

  52. Washington IM, Van Hoosier G (2012) Clinical biochemistry and hematology. In The laboratory rabbit, guinea pig, hamster, and other rodents, Academic Press, Pp. 57–116. https://doi.org/10.1016/B978-0-12-380920-9.00003-1

  53. Dong X, Zhang N, Zhou M, Tu Y, Deng K, Diao Q (2013) Effects of dietary probiotics on growth performance, faecal microbiota and serum profiles in weaned piglets. Anim Prod Sci 54:616–621. https://doi.org/10.1071/AN12372

    Article  CAS  Google Scholar 

  54. Hu P, Zhao F, Wang J, Zhu W (2021) Metabolomic profiling reveals the effects of early-life lactoferrin intervention on protein synthesis, energy production and antioxidative capacity in the liver of suckling piglets. Food Funct 12:3405–3419. https://doi.org/10.1039/D0FO01747G

    Article  CAS  Google Scholar 

  55. Al-Zubaidi HJ, Falih IB (2018) Immunological and pathological effect of lactoferrin against murine leishmaniasis. J Entomol Zool Stud 6:1108–1111. https://www.entomoljournal.com/archives/2018/vol6issue1/PartP/5-6-345-520.pdf

  56. Sfeir RM, Dubarry M, Boyaka PN, Rautureau M, Tome D (2004) The mode of oral bovine lactoferrin administration influences mucosal and systemic immune responses in mice. J Nutr 134:403–409. https://doi.org/10.1093/jn/134.2.403

    Article  CAS  Google Scholar 

  57. Jang YS, Seo GY, Lee JM, Seo HY, Han HJ, Kim SJ, Jin BR, Kim HJ, Park SR, Rhee KJ, Kim WS, Kim PH (2015) Lactoferrin causes IgA and IgG2b isotype switching through betaglycan binding and activation of canonical TGF-β signaling. Mucosal Immunol 8:906–917. https://doi.org/10.1038/mi.2014.121

    Article  CAS  Google Scholar 

  58. Lee JM, Jang YS, Jin BR, Kim SJ, Kim HJ, Kwon BE, Ko HJ, Yoon SI, Lee GS, Kim WS, Seo GY, Kim PH, (2016) Retinoic acid enhances lactoferrin-induced IgA responses by increasing betaglycan expression. Cell Mol Immunol 13:862–870. https://doi.org/10.1038/cmi.2015.73

  59. Yu LT, Ju CC, Ju J, Wu HL, Yen HT (2004) Effect of probiotics and selenium combination on the immune and blood cholesterol concentration of pigs. J Anim Feed Sci 13:625–634. https://doi.org/10.22358/jafs/67630/2004

  60. Karamese M, Aydin H, Sengul E, Gelen V, Sevim C, Ustek D, Karakus E (2016) The immunostimulatory effect of lactic acid bacteria in a rat model. Iran J Immunol 13:220–228. http://iji.sums.ac.ir/article_33410_0.html

  61. Aiyegoro O, Dlamini Z, Okoh A, Langa1 R (2017) Effects of probiotics on growth performance, blood parameters, and antibody stimulation in piglets. S Afr J Anim Sci 47:766-775. http://dx.doi.org/https://doi.org/10.4314/sajas.v47i6.4

  62. Resendiz-Albor AA, Reina-Garfias H, Rojas-Hernandez S, Jarillo-Luna A, Rivera-Aguilar V, Miliar-Garcia A, Campos-Rodriguez R (2010) Regionalization of pIgR expression in the mucosa of mouse small intestine. Immunol Lett 128:59–67. https://doi.org/10.1016/j.imlet.2009.11.005

    Article  CAS  Google Scholar 

  63. Naqid IA, Owen JP, Maddison BC, Gardner DS, Foster N, Tchórzewska MA, La Ragione RM, Gough KC (2015) Prebiotic and probiotic agents enhance antibody-based immune responses to Salmonella typhimurium infection in pigs. Anim Feed Sci Technol 201:57–65. https://doi.org/10.1016/j.anifeedsci.2014.12.005

    Article  CAS  Google Scholar 

  64. Kim SH, Jeung W, Choi ID, Jeong JW, Lee DE, Huh CS, Kim GB, Hong SS, Shim JJ, Lee, Sim SH, JL, Ahn YT (2016) Lactic acid bacteria improve Peyer's patch cell-mediated immunoglobulin A and tight-junction expression in a destructed gut microbial environment. J Microbiol Biotechnol 26:1035–1045.https://doi.org/10.4014/jmb.1512.12002

  65. Liu H, Wang S, Zhang D, Wang J, Zhang W, Wang Y, Ji H (2020) Effects of dietary supplementation with Pediococcus acidilactici ZPA017 on reproductive performance, fecal microbial flora and serum indices in sows during late gestation and lactation. Asian-Australas J Anim Sci 33:120. https://doi.org/10.5713/2Fajas.18.0764

  66. Vadopalas L, Ruzauskas M, Lele V, Starkute V, Zavistanaviciute P, Zokaityte E, Bartkevics V, Pugajeva I, Reinolds I, Badaras S, Klupsaite D, Bartkiene E (2020) Combination of antimicrobial starters for feed fermentation: influence on piglet feces microbiota and health and growth performance, including mycotoxin biotransformation in vivo. Front Vet Sci 7:528990. https://doi.org/10.3389/2Ffvets.2020.528990

  67. Al-Saiady MY (2010) Effect of probiotic bacteria on immunoglobulin G concentration and other blood components of newborn calves. J Anim Vet Adv 9:604–609. https://doi.org/10.3923/javaa.2010.604.609

    Article  CAS  Google Scholar 

  68. Karamzadeh-Dehaghani A, Towhidi A, Zhandi M, Mojgani N, Fouladi-Nashta A (2021) Combined effect of probiotics and specific immunoglobulin Y directed against Escherichia coli on growth performance, diarrhea incidence, and immune system in calves. Animal 15:100124. https://doi.org/10.1016/j.animal.2020.100124

    Article  CAS  Google Scholar 

  69. Troncone E, Marafini I, Stolfi C, Monteleone G (2018) Transforming growth factor-β1/Smad7 in intestinal immunity, inflammation, and cancer. Front Immunol 9:1407. https://doi.org/10.3389/fimmu.2018.01407

    Article  CAS  Google Scholar 

  70. Gough NR, Xiang X, Mishra L (2021) TGF-β signaling in liver, pancreas, and gastrointestinal diseases and cancer. Gastroenterol 161:434-452.e15. https://doi.org/10.1053/j.gastro.2021.04.064

    Article  CAS  Google Scholar 

  71. Hwang SA, Actor JK (2009) Lactoferrin modulation of BCG-infected dendritic cell functions. Int Immunol 21:1185–1197. https://doi.org/10.1093/intimm/dxp084

    Article  CAS  Google Scholar 

  72. Lönnerdal B, Du X, Jiang R (2021) Biological activities of commercial bovine lactoferrin sources. Biochem Cell Biol 99:35–46. https://doi.org/10.1139/bcb-2020-0182

    Article  CAS  Google Scholar 

  73. Monteleone G, Mann J, Monteleone I, Vavassori P, Bremner R, Fantini M, Del Vecchio BG, Tersigni R, Alessandroni L, Mann D, Pallone F, MacDonald TT (2004) A failure of transforming growth factor-beta1 negative regulation maintains sustained NF-kappaB activation in gut inflammation. J Biol Chem 279:3925–3932. https://doi.org/10.1074/jbc.m303654200

    Article  CAS  Google Scholar 

  74. Sakai F, Hosoya T, Ono-Ohmachi A, Ukibe K, Ogawa A, Moriya T, Kadooka Y, Shiozaki T, Nakagawa H, Nakayama Y, Miyazaki T (2014) Lactobacillus gasseri SBT2055 induces TGF-β expression in dendritic cells and activates TLR2 signal to produce IgA in the small intestine. PLoS ONE 9:e105370. https://doi.org/10.1371/journal.pone.0105370

    Article  CAS  Google Scholar 

  75. Huang IF, Lin IC, Liu PF, Cheng MF, Liu YC, Hsieh YD, Chen JJ, Chen CL, Chang HW, Shu CW (2015) Lactobacillus acidophilus attenuates Salmonella-induced intestinal inflammation via TGF-β signaling. BMC Microbiol 15:203. https://doi.org/10.1186/2Fs12866-015-0546-x

  76. Barigela A, Bhukya B (2021) Probiotic Pediococcus acidilactici strain from tomato pickle displays anti-cancer activity and alleviates gut inflammation in-vitro. 3Biotech 11:1–11. https://doi.org/10.1007/s13205-020-02570-1

  77. Foye OT, Huang IF, Chiou CC, Walker WA, Shi HN (2012) Early administration of probiotic Lactobacillus acidophilus and/or prebiotic inulin attenuates pathogen-mediated intestinal inflammation and Smad 7 cell signaling. FEMS Immunol Med Microbiol 65(3):467–80. https://doi.org/10.1111/2Fj.1574-695X.2012.00978.x

Download references

Acknowledgements

This work was supported by All India Network Programme on Neonatal Mortality project of ICAR. First author (VKS) thanks ICAR-IVRI for granting research fellowship for his research program.

Author information

Authors and Affiliations

  1. Division of Medicine, ICAR-Indian Veterinary Research Institute, Izatnagar, 243122 (UP), India

    Varun Kumar Sarkar, Ujjwal Kumar De, Babul Rudra Paul, Srishti Soni & Jitendra Singh Gandhar

  2. Division of Animal Nutrition, ICAR-Indian Veterinary Research Institute, Izatnagar, 243122 (UP), India

    Anju Kala & Ashok Kumar Verma

  3. Livestock Production and Management Section, ICAR-Indian Veterinary Research Institute, Izatnagar, 243122 (UP), India

    Anuj Chauhan, Manas Kumar Patra & Gyanendra Kumar Gaur

  4. Division of Biological Products, ICAR-Indian Veterinary Research Institute, Izatnagar, 243122 (UP), India

    Pallab Chaudhuri

  5. Department of Veterinary Medicine, College of Veterinary Sciences and Animal Husbandry, Central Agriculture University, Selesih, Aizawl, 796014, Mizoram, India

    Chethan Gollahalli Eregowda

Authors
  1. Varun Kumar Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ujjwal Kumar De
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anju Kala
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ashok Kumar Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anuj Chauhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Babul Rudra Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Srishti Soni
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jitendra Singh Gandhar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pallab Chaudhuri
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Manas Kumar Patra
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chethan Gollahalli Eregowda
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Gyanendra Kumar Gaur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ujjwal Kumar De.

Ethics declarations

Ethics Approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All procedures used during the research were approved by the Institute Animal Ethics Committee, and the research protocol was approved by the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA), Ministry of Fisheries, Animal Husbandry and Dairying, Government of India (approval number V-11–11 (13)/19/2021-CPCSEA-DADF).

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Varun Kumar Sarkar and Ujjwal Kumar De are both first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sarkar, V.K., De, U.K., Kala, A. et al. Early-Life Intervention of Lactoferrin and Probiotic in Suckling Piglets: Effects on Immunoglobulins, Intestinal Integrity, and Neonatal Mortality. Probiotics & Antimicro. Prot. 15, 149–159 (2023). https://doi.org/10.1007/s12602-022-09964-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-022-09964-y

Keywords

Search

Navigation