Neonatal animal testing paradigms and their suitability for testing infant formula

Toxicology Mechanisms and Methods

Volumn 23, Issue 2, 2013, Pages 57-67

  Flamm, Edwin G ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

"pup in a cup"; Autosow; Colostrum; Gavage

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTIFICIAL MILK; EXPERIMENTAL DOG; EXPERIMENTAL GUINEA PIG; EXPERIMENTAL MODEL; EXPERIMENTAL MONKEY; EXPERIMENTAL PIG; EXPERIMENTAL RABBIT; FOOD AND DRUG ADMINISTRATION; INTERNET; LAMB; METHODOLOGY; MOUSE; NEWBORN; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RAT; REVIEW; SEARCH ENGINE;

ANIMALS; ANIMALS, LABORATORY; ANIMALS, NEWBORN; DOGS; FOOD ADDITIVES; FOOD SAFETY; HAPLORHINI; HUMANS; INFANT FORMULA; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; INFANT, NEWBORN; MICE; MODELS, ANIMAL; RATS; RISK ASSESSMENT; SWINE; TOXICITY TESTS;

EID: 84873822739     PISSN: 15376516     EISSN: 15376524     Source Type: Journal    
DOI: 10.3109/15376516.2012.725108     Document Type: Review

References (69)

1. Aalinkeel R, Srinivasan M, Kalhan SC, Laychock SG, Patel MS. 1999. A dietary intervention (high carbohydrate) during the neonatal period causes islet dysfunction in rats. Am J Physiol 277: E1061-E1069.
2. Arbuckle LD, MacKinnon MJ, Innis SM. 1994. Formula 18: 2(n-6) and 18: 3(n-3) content and ratio influence long-chain polyunsaturated fatty acids in the developing piglet liver and central nervous system. J Nutr 124: 289-298.
3. Beierle EA, Chen MK, Hartwich JE, Iyengar M, Dai W, Li N, Demarco V, Neu J. 2004. Artificial rearing of mouse pups: development of a mouse pup in a cup model. Pediatr Res 56: 250-255.
4. Book SA, Bustad LK. 1974. The fetal and neonatal pig in biomedical research. J Anim Sci 38: 997-1002.
5. Butchbach ME, Edwards JD, Schussler KR, Burghes AH. 2007. A novel method for oral delivery of drug compounds to the neonatal SMNDelta7 mouse model of spinal muscular atrophy. J Neurosci Methods 161: 285-290.
6. Butler JE, Sun J, Weber P, Ford SP, Rehakova Z, Sinkora J, Lager K. 2001. Antibody repertoire development in fetal and neonatal piglets. IV. Switch recombination, primarily in fetal thymus, occurs independent of environmental antigen and is only weakly associated with repertoire diversification. J Immunol 167: 3239-3249.
7. Butler JE, Lager KM, Splichal I, Francis D, Kacskovics I, Sinkora M, Wertz N, Sun J, Zhao Y, Brown WR, DeWald R, Dierks S, Muyldermans S, Lunney JK, McCray PB, Rogers CS, Welsh MJ, Navarro P, Klobasa F, Habe F, Ramsoondar J. 2009. The piglet as a model for B cell and immune system development. Vet Immunol Immunopathol 128: 147-170.
8. Champoux M, Hibbeln JR, Shannon C, Majchrzak S, Suomi SJ, Salem N Jr, Higley JD. 2002. Fatty acid formula supplementation and neuromotor development in rhesus monkey neonates. Pediatr Res 51: 273-281.
9. Clarke DO, Connelly CS, Hall RL, Leedle RA, Miller EM, Williams JM, Sarazan RD, Ponsler GD, Sauer JM, Tizzano JP. 2001. Nonclinical pediatric testing of tomoxetine: Toxicity study in young beagle dogs. (abstract) Neurotoxicol Teratol 23: 294-295.
10. Craig-Schmidt MC, Stieh KE, Lien EL. 1996. Retinal fatty acids of piglets fed docosahexaenoic and arachidonic acids from microbial sources. Lipids 31: 53-59.
11. Dorman DC, Struve MF, Vitarella D, Byerly FL, Goetz J, Miller R. 2000. Neurotoxicity of manganese chloride in neonatal and adult CD rats following subchronic (21-day) high-dose oral exposure. J Appl Toxicol 20: 179-187.
12. Eriksson P, Viberg H, Jakobsson E, Örn U, Fredriksson A. 2002. A brominated flame retardant, 2,2',4,4',5-pentabromodiphenyl ether: uptake, retention, and induction of neurobehavioral alterations in mice during a critical phase of neonatal brain development. Toxicol Sci 67: 98-103.
13. FDA/CDER. 2006. Guidance for Industry Nonclinical Safety Evaluation of Pediatric Drug Products. [Online] Available at: http://www.fda.gov/downloads/ Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm079247.pdf (Last accessed in YAHOO (07/16/2012).
14. Fernandez ML. 2001. Guinea pigs as models for cholesterol and lipoprotein metabolism. J Nutr 131: 10-20.
15. Flores CA, Hu C, Edmond J, Koldovsky O. 1996. Milk carnitine affects organ carnitine concentration in newborn rats. J Nutr 126: 1673-1682.
16. Fukuda N, Ito Y, Yamaguchi M, Mitumori K, Koizumi M, Hasegawa R, Kamata E, Ema M. 2004. Unexpected nephrotoxicity induced by tetrabromobisphenol A in newborn rats. Toxicol Lett 150: 145-155.
17. Garthoff LH, Henderson GR, Sager AO, Sobotka TJ, O'Dell R, Thorpe CW, Trotter WJ, Bruce VR, Dallas HL, Poelma PL, Solomon HM, Bier JW, O'Donnell MW Jr, Chi RK, Chirtel SJ, Barton CN, Brown LH, Frattali VP, Khan MA. 2002a. The Autosow raised miniature swine as a model for assessing the effects of dietary soy trypsin inhibitor. Food Chem Toxicol 40: 487-500.
18. Garthoff LH, Henderson GR, Sager AO, Sobotka TJ, Gaines DW, O'Donnell MW Jr, Chi R, Chirtel SJ, Barton CN, Brown LH, Hines FA, Solomon T, Turkleson J, Berry D, Dick H, Wilson F, Khan MA. 2002b. Pathological evaluation, clinical chemistry and plasma cholecystokinin in neonatal and young miniature swine fed soy trypsin inhibitor from 1 to 39 weeks of age. Food Chem Toxicol 40: 501-516.
19. Gomez GG, Sandler RS, Seal E Jr. 1995. High levels of inorganic sulfate cause diarrhea in neonatal piglets. J Nutr 125: 2325-2332.
20. Gomez GG. 1997. The colostrum-deprived, artificially-reared, neonatal pig as a model animal for studying rotavirus gastroenteritis. Frontiers in Bioscience 2: 471-481.
21. Grainger S, Blakey S. 2000. Safety assessment studies in neaonatal dogs. (abstract). Toxicol Lett 116: 88.
22. Hall WG. 1975. Weaning and growth of artificially reared rats. Science 190: 1313-1315.
23. Hrboticky N, MacKinnon MJ, Innis SM. 1990. Effect of a vegetable oil formula rich in linoleic acid on tissue fatty acid accretion in the brain, liver, plasma, and erythrocytes of infant piglets. Am J Clin Nutr 51: 173-182.
24. Hsiao SH, Acevedo JL, DuBois DW, Smith KR, West JR, Frye GD. 2001. Early postnatal ethanol intubation blunts GABA(A) receptor up-regulation and modifies 3alpha-hydroxy-5alpha-pregnan-20-one sensitivity in rat MS/DB neurons. Brain Res Dev Brain Res 130: 25-40.
25. IOM. 2004. Infant formula evaluating the safety on new ingredients. (Chapter 5) Testing ingredients with Preclinical studies. PP 70-97.
26. Isaacson RE, Dean EA, Morgan RL, Moon HW. 1980. Immunization of suckling pigs against enterotoxigenic Escherichia coli-induced diarrheal disease by vaccinating dams with purified K99 or 987P pili: antibody production in response to vaccination. Infect Immun 29: 824-826.
27. Ismail-Beigi F, Catalano PM, Hanson RW. 2006. Metabolic programming: fetal origins of obesity and metabolic syndrome in the adult. Am J Physiol Endocrinol Metab 291: E439-E440.
28. Jeffrey BG, Mitchell DC, Hibbeln JR, Gibson RA, Chedester AL, Salem N Jr. 2002. Visual acuity and retinal function in infant monkeys fed long-chain PUFA. Lipids 37: 839-848.
29. Jones EE, Coalson JA, Lecce JG. 1977. Soy flour as a source of protein for baby pigs. J Anim Sci 45: 1073-1078.
30. Jones SA, Langille BL, Frise S, Adamson SL. 1993. Nonadrenergic noncholinergic autonomic mediation of pressor response to feeding in lambs. Am J Physiol 265: R530-R536.
31. Kansagra K, Stoll B, Rognerud C, Niinikoski H, Ou CN, Harvey R, Burrin D. 2003. Total parenteral nutrition adversely affects gut barrier function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 285: G1162-G1170.
32. Kinirons SA, Shall MS, McClung JR, Goldberg SJ. 2003. Effect of artificial rearing on the contractile properties and myosin heavy chain isoforms of developing rat tongue musculature. J Neurophysiol 90: 120-127.
33. Kraehenbuhl JP, Campiche MA. 1969. Early stages of intestinal absorption of specific antibiodies in the newborn. An ultrastructural, cytochemical, and immunological study in the pig, rat, and rabbit. J Cell Biol 42: 345-365.
34. Lavoie JC, Rouleau T, Chessex P. 2004. Interaction between ascorbate and light-exposed riboflavin induces lung remodeling. J Pharmacol Exp Ther 311: 634-639.
35. Lecce JG. 1969. Rearing colostrum-free pigs in an automatic feeding device. J Anim Sci 28: 27-33.
36. Lecce JG. 1971. Rearing neonatal piglets of low birth weight with an automatic feeding device. J Anim Sci 33: 47-51.
37. Lecce JG. 1975. Rearing piglets artificially in a farm environment: a promise unfulfilled. J Anim Sci 41: 659-666.
38. Lecce JG, Coalson JA. 1976. Diets for rearing colostrum-free piglets with an automatic feeding device. J Anim Sci 42: 622-629.
39. Lecce JG, Armstrong WD, Crawford PC, Ducharme GA. 1979. Nutrition and management of early weaned piglets: liquid vs dry feeding. J Anim Sci 48: 1007-1014.
40. Lecce JG, Balsbaugh RK, Clare DA, King MW. 1982. Rotavirus and hemolytic enteropathogenic Escherichia coli in weanling diarrhea of pigs. J Clin Microbiol 16: 715-723.
41. Lee DJ, Drongowski RA, Coran AG, Harmon CM. 2000. Evaluation of probiotic treatment in a neonatal animal model. Pediatr Surg Int 16: 237-242.
42. Li N, Liboni K, Fang MZ, Samuelson D, Lewis P, Patel R, Neu J. 2004. Glutamine decreases lipopolysaccharide-induced intestinal inflammation in infant rats. Am J Physiol Gastrointest Liver Physiol 286: G914-G921.
43. Miller ER, Ullrey DE. 1987. The pig as a model for human nutrition. Annu Rev Nutr 7: 361-382.
44. Morgan RL, Isaacson RE, Moon HW, Brinton CC, To CC. 1978. Immunization of suckling pigs against enterotoxigenic Escherichia coli-induced diarrheal disease by vaccinating dams with purified 987 or K99 pili: protection correlates with pilus homology of vaccine and challenge. Infect Immun 22: 771-777.
45. Moser VC, Walls I, Zoetis T. 2005. Direct dosing of preweaning rodents in toxicity testing and research: deliberations of an ILSI RSI Expert Working Group. Int J Toxicol 24: 87-94.
46. Pan HZ, Chen HH. 2007. Hyperalgesia, low-anxiety, and impairment of avoidance learning in neonatal caffeine-treated rats. Psychopharmacology) 191: 119-125.
47. Patel MS, Srinivasan M. 2002. Metabolic programming: causes and consequences. J Biol Chem 277: 1629-1632.
48. Pollack PF, Goda T, Colony PC, Edmond J, Thornburg W, Korc M, Koldovský O. 1987. Effects of enterally fed epidermal growth factor on the small and large intestine of the suckling rat. Regul Pept 17: 121-132.
49. Pond WG, Snyder W, Walker EF Jr, Stillings BR, Sidwell V. 1971. Comparative utilization of casein, fish protein concentrate and isolated soybean protein in liquid diets for growth of baby pigs. J Anim Sci 33: 587-591.
50. Potsic B, Holliday N, Lewis P, Samuelson D, DeMarco V, Neu J. 2002. Glutamine supplementation and deprivation: effect on artificially reared rat small intestinal morphology. Pediatr Res 52: 430-436.
51. Ramirez CG, Miller ER, Ullrey DE, Hoefer JA. 1963. Swine hematology from birth to maturity. III. Blood volume of the nursing pig. J Anim Sci 22: 1068-1074.
52. Rhoads JM, Keku EO, Bennett LE, Quinn J, Lecce JG. 1990. Development of L-glutamine-stimulated electroneutral sodium absorption in piglet jejunum. Am J Physiol 259: G99-107.
53. Rhoads JM, Keku EO, Woodard JP, Bangdiwala SI, Lecce JG, Gatzy JT. 1992. L-glutamine with D-glucose stimulates oxidative metabolism and NaCl absorption in piglet jejunum. Am J Physiol 263: G960-G966.
54. Sand S, von Rosen D, Eriksson P, Fredriksson A, Viberg H, Victorin K, Filipsson AF. 2004. Dose-response modeling and benchmark calculations from spontaneous behavior data on mice neonatally exposed to 2,2',4,4',5- pentabromodiphenyl ether. Toxicol Sci 81: 491-501.
55. Sawada T, Karaki K, Hayashi T, Yoneyama S, Mizushima Y, Moriyama T, Nishimura K, Kimura Y, Nakano M, Kato I. 2001. [Toxicity study of cefmatilen hydrochloride hydrate (S-1090) (7)-Three-month repeated oral dose toxicity study in juvenile dogs]. J Toxicol Sci 26 Suppl 1: 135-147.
56. Srinivasan M, Aalinkeel R, Song F, Lee B, Laychock SG, Patel MS. 2000. Adaptive changes in insulin secretion by islets from neonatal rats raised on a high-carbohydrate formula. Am J Physiol Endocrinol Metab 279: E1347-E1357.
57. Srinivasan M, Laychock SG, Hill DJ, Patel MS. 2003. Neonatal nutrition: metabolic programming of pancreatic islets and obesity. Exp Biol Med (Maywood) 228: 15-23.
58. Stegink LD, Brummel MC, Boaz DP, Filer LJ Jr. 1973. Monosodium glutamate metabolism in the neonatal pig: conversion of administered glutamate into other metabolites in vivo. J Nutr 103: 1146-1154.
59. Stegink LD, Reynolds WA, Filer LJ Jr, Pitkin RM, Boaz DP, Brummel MC. 1975. Monosodium glutamate metabolism in the neonatal monkey. Am J Physiol 229: 246-250.
60. Ulshen MH, Lecce JG, Stiles AD, Lyn-Cook LE. 1991. Effects of nursing on growth and development of small bowel mucosa in newborn piglets. Pediatr Res 30: 337-341.
61. USDA. 2000. Information resources on swine in biomedical research 1990-2000. Smith CP (Eds.) [Online] Available at: www.nal.usda.gov/awic/pubs/ swine/swine.htm (Last accessed in YAHOO 07/16/2012).
62. Viberg H, Johansson N, Fredriksson A, Eriksson J, Marsh G, Eriksson P. 2006. Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions of adult mice. Toxicol Sci 92: 211-218.
63. Wainwright PE, Xing HC, Ward GR, Huang YS, Bobik E, Auestad N, Montalto M. 1999. Water maze performance is unaffected in artificially reared rats fed diets supplemented with arachidonic acid and docosahexaenoic acid. J Nutr 129: 1079-1089.
64. Weaver LT, Laker MF, Nelson R, Lucas A. 1987. Milk feeding and changes in intestinal permeability and morphology in the newborn. J Pediatr Gastroenterol Nutr 6: 351-358.
65. Wedig J, Christian MS, Hoberman A, Diener RM, Thomas-Wedig R. 2002. A study to develop methodology for feeding 24-hour-old neonatal swine for 3 weeks. Int J Toxicol 21: 361-370.
66. West DB, Diaz J, Woods SC. 1982. Infant gastrostomy and chronic formula infusion as a technique to overfeed and accelerate weight gain of neonatal rats. J Nutr 112: 1339-1343.
67. West JR. 1993. Use of pup in a cup model to study brain development. J Nutr 123: 382-385.
68. Wykes LJ, Ball RO, Pencharz PB. 1993. Development and validation of a total parenteral nutrition model in the neonatal piglet. J Nutr 123: 1248-1259.
69. Zoetis T, Walls I. (Eds.) 2003. Principles and practices for direct dosing of pre-weaning mammals in toxicity testing and research. A report of the ILSI Risk Science Institute expert working group.