Skip to main content
SpringerLink
Log in

Immunological Consequences of Nursery Rearing

  • Chapter
Nursery Rearing of Nonhuman Primates in the 21st Century

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR))

Abstract

The concept of rearing primate infants in a nursery fell out of favor over the past two decades, after research showed the detrimental behavioral effects of restricted rearing and raised concerns about how best to care for animals with these abnormalities (Harlow and Harlow, 1969; Ruppenthal and Sackett, 1979; Capitanio, 1985). In addition to behavioral effects, several investigators have described physiological differences between mother-reared (MR) and nursery-reared (NR) infants (Sackett et al., 1973; Champoux et al., 1989; Kraemer et al., 1989). Some of these differences were resolved as the infants grew older, while others persisted (Novak and Harlow, 1975; Mason et al., 1991). Today, however, many institutions have changed or expanded their research focus and once again require some degree of nursery rearing. In some cases, nursery rearing is needed either to keep maternal variables from interfering with certain aspects of the infant’s development, such as in AIDS research, or to keep the animals free from specific pathogens (Marthas et al., 1995; Lindberg et al., 1997).

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abel, K., Alegeria-Hartman, M.J., Zanotto, K., McChesney, M.B., Marthas, M.L., and Miller, C.J. (2001). Anatomic site and immune function correlate with relative cytokine mRNA expression levels in lymphoid tissues of normal macaques. Cytokine 16:191–204.

    Article  CAS  PubMed  Google Scholar 

  • Abo, T., Kawate, T., Itoh, K., and Kumagai, K. (1981). Circadian rhythms of human T, B, and K cell traffic in the peripheral blood. J. Immunol. 126:1360–1363.

    CAS  PubMed  Google Scholar 

  • Ackerman, S.H., Hofer, M.A., and Wiener, H. (1978). Early maternal separation increases gastric ulcer risk in rats by producing a latent thermoregulatory disturbance. Science 201:373–376.

    Article  CAS  PubMed  Google Scholar 

  • Ader, R. (1983). Developmental psychoneuroimmunology. Dev. Psychobiol. 16:251–267.

    Article  CAS  PubMed  Google Scholar 

  • Alberts, J.R., and Brunjes, P.C. (1978). Ontogeny of thermal and olfactory determinants of huddling in the rat. J. Comp. Physiol. Psychol. 92:897–906.

    Article  CAS  PubMed  Google Scholar 

  • Alberts, J.R., and May, B. (1984). Non-nutritive, thermotactile induction of olfactory preferences for huddling in rat pups. Dev. Psychobiol. 17:161–181.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, J.H. (1986). Rearing and intensive care of neonatal and infant nonhuman primates. In: Benirschke, K. (ed.), Primates: The Road to Self-Sustaining Populations. Springer-Verlag, New York, pp. 747–762.

    Google Scholar 

  • Aschoff, J., and von Goetz, C. (1986). Effects of feeding cycles on circadian rhythms in squirrel monkeys. J. Biol. Rhythms 1:267–276.

    Article  CAS  PubMed  Google Scholar 

  • Bailey, M.T., and Coe, C.L. (1999). Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev. Psychobiol. 35:146–155.

    Article  CAS  PubMed  Google Scholar 

  • Bailey, M.T., Lubach, G.R., and Coe, C.L. (2004). Prenatal stress alters bacterial colonization of the gut in infant monkeys. J. Pediatr. Gastroenterol. Nutr. 38:414–421.

    Article  PubMed  Google Scholar 

  • Baroncelli, S., Panzini, G., Geraci, A., Pardini, S., Corrias, F., Iale, E., Varano, F., Turillazzi, P.G., Titti, F., and Verani, P. (1997). Longitudinal characterization of CD, CD8 T-cell subsets and of haematological parameters in healthy newborns of cynomolgus monkeys. Vet. Immunol. Immunopathol. 59:141–150.

    Article  CAS  PubMed  Google Scholar 

  • Bernt, K.M., and Walker, W.A. (1999). Human milk as a carrier of biochemical messages. Acta Paediatr. Suppl. 430:27–41.

    Google Scholar 

  • Bertotto, A., Vagliasindi, C., Gerli, R., Spinozzi, F., Castellucci, G., Fabietti, G., Crupi, S., Radicioni, M., Cozzali, R., Ferraro, L., Niccoli, A., De Rosa, O., Lupi, C., Brunelli, R., Merluzzi, A., Guadalupi, D., Prente, C., Pertici, L.

    Google Scholar 

  • Serra, M., and Vaccaro, R. (1997). Soluble CD30 antigen in human colostrum. Biol. Neonate 71:69–74.

    PubMed  Google Scholar 

  • Bleavins, M., and de la Iglesia, F.A. (2000). Preclinical immune function testing. An approach using the cynomolgus monkey (Macaca fascicularis). In: Korte, R., and Weinbauer, G.F. (eds.), Towards New Horizons in Primate Toxicology. Waxmann Munster, New York, pp. 127–141.

    Google Scholar 

  • Blomquist, A.J., and Harlow, H.F. (1961). The infant rhesus monkey program at the University of Wisconsin Primate Laboratory. Proc. Anim. Care Panel 11:57–64.

    Google Scholar 

  • Burbacher, T.M., and Grant, K.S. (2000). Methods for studying nonhuman primates in neurobehavioral toxicology and teratology. Nerotoxicol. Teratol. 22:475–486.

    Article  CAS  Google Scholar 

  • Buse, E., Habermann, G., Osterburg, I., Korte, R., and Weinbauer, G.F. (2003). Reproductive/developmental toxicity and immunotoxicity assessment in the nonhuman primate model. Toxicology 221:221–227.

    Article  Google Scholar 

  • Butte, N.F., Wong, W.W., Ferlic, L., Smith, E.O., Klein, P.D., and Garza, C. (1990). Energy expenditure and deposition of breast-fed and formula-fed infants during early infancy. Pediatr. Res. 28:631–640.

    Article  CAS  PubMed  Google Scholar 

  • Capitanio, J.P. (1985). Early experience and social processes in rhesus macaques (Macaca mulatta): II. Complex social interaction. J. Comp. Psychol. 99: 133–144.

    Article  CAS  PubMed  Google Scholar 

  • Capitanio, J.P., and Lerche, N.W. (1991). Psychosocial factors and disease progression in simian AIDS: A preliminary report. AIDS 5:1103–1106.

    Article  CAS  PubMed  Google Scholar 

  • Cauchi, M.N. (1981). Obstetric and Perinatal Immunology. Edward Arnold Publishers, London.

    Google Scholar 

  • Champoux, M., Coe, C.L., Schanberg, S.M., Kuhn, C.M., and Suomi, S.J. (1989). Hormonal effects of early rearing conditions in the infant rhesus monkey. Am. J. Primatol. 19:111–117.

    Article  Google Scholar 

  • Cleary, T.G., Winsor, D.K., Reich, D., Ruiz-Palacios, G., and Calva, J.J. (1989). Human milk immunoglobulin A antibodies to Shigella virulence determinants. Infect. Immun. 57:1675–1679.

    CAS  PubMed  Google Scholar 

  • Coe, C.L., and Erickson, C.M. (1997). Stress decreases lymphocyte cytolytic activity in the young monkey even after blockade of steroid and opiate hormone receptors. Dev. Psychobiol. 30:1–10.

    Article  CAS  PubMed  Google Scholar 

  • Coe, C.L., Lubach, G.R., Ershler, W.B., and Klopp, R.G. (1989). Influence of early rearing on lymphocyte proliferation responses in juvenile rhesus monkeys. Brain Behav. Immun. 3:47–60.

    Article  CAS  PubMed  Google Scholar 

  • Coe, C.L., Lubach, G.R., Schneider, M.L., Dierschke, D.J., and Ershler, W.B. (1992). Early rearing conditions alter immune responses in developing infant primates. Pediatrics 90:505–509.

    CAS  PubMed  Google Scholar 

  • Coe, C.L., Lubach, G.R., and Izard, K.M. (1994). Progressive improvement in the transfer of maternal antibody across the Order Primates. Am. J. Primatol. 32:51–55.

    Article  Google Scholar 

  • Dahlgren, U.I., Hanson, L.A., and Telemo, E. (2001). Maturation of immuno-competence in breast-fed vs. formula-fed infants. In: Woodward, B., and Draper, H.H. (eds.), Advances in Nutritional Research, Vol. 10, Kluwer Academic/Plenum Publishers, New York, pp. 311–325.

    Google Scholar 

  • Davidson, L.A., and Lonnerdal, B. (1986). Isolation and characterization of rhesus monkey lactoferritin. Pediatr. Res. 20:197–201.

    Article  CAS  PubMed  Google Scholar 

  • DeMaria, M.A., Casto, M., O’Connell, M., Johnson, R.P., and Rosenzweig, M. (2000). Characterization of lymphocyte subsets in rhesus macaques during the first year of life. Eur. J. Haematol. 65:245–257.

    Article  CAS  PubMed  Google Scholar 

  • de Vries, E., de Bruin-Versteeg, S., Comans-Bitter, W.M., de Groot, R., Hop, W.C.J., Boerma, G.J.M., Lotgering, F.K., and van Dongen, J.J.M. (2000). Longitudinal survey of lymphocyte subpopulations in the first year of life. Pediatr. Res. 47:528–537.

    Article  PubMed  Google Scholar 

  • Dewey, K., Heinig, M.J., and Nommsen-Rivers, L.A. (1995). Differences in morbidity between breast-fed and formula-fed infants. J. Pediatr. 126: 696–702.

    Article  CAS  PubMed  Google Scholar 

  • Duffy, L. (2000). Interactions mediating bacterial translocation in the immature intestine. J. Nutr. 130:432S–436S.

    CAS  PubMed  Google Scholar 

  • Dykhuizen, M., Ceman, J., Mitchen, J., Zayas, M., MacDougall, A., Helgeland, J., Rakasz, E., and Pauza, C.D. (2000). Importance of the CD3 marker for evaluating changes in rhesus macaque CD4/CD8 T-cell ratios. Cytometry 40:69–75.

    Article  CAS  PubMed  Google Scholar 

  • Ershler, W.B., Coe, C.L., Gravenstein, S., Schultz, K.T., Klopp, R.G., Meyer, M., and Houser, W.D. (1988). Aging and immunity in nonhuman primates: I. Effects of age and gender on cellular immune function in rhesus monkeys (Macaca mulatta). Am. J. Primatol. 15:181–188.

    Article  Google Scholar 

  • Foerster, M., Delgado, I., Abraham, K., Gerstmayr, S., and Neubert, R. (1997). Comparative study on age-dependent development of surface receptors on peripheral blood lymphocytes in children and young nonhuman primates (marmosets). Life Sci. 60:773–785.

    Article  CAS  PubMed  Google Scholar 

  • Folkerts, G., Walzl, G., and Openshaw, J.M. (2000). Do common childhood infections ‘teach’ the immune system not to be allergic. Immunol. Today 21:118–120.

    Article  CAS  PubMed  Google Scholar 

  • Ganschow, R., Broering, D.C., Nolkemper, D., Albani, J., Kemper, M.J., Rogiers, X., and Burdelski, M. (2001). Th2 cytokine profile in infants predisposed to improved graft acceptance after liver transplantation. Transplantation 72:929–934.

    Article  CAS  PubMed  Google Scholar 

  • Glimcher, L.H., and Murphy, K.M. (2000). Lineage commitment in the immune system: The T helper lymphocyte grows up. Genes Dev. 14:1693–1711.

    CAS  PubMed  Google Scholar 

  • Goldman, A.S. (2000). Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J. Nutr. 130:426S–431S.

    CAS  PubMed  Google Scholar 

  • Goldman, A.S. (2002). Evolution of the mammary gland defense system and the ontogeny of the immune system. J. Mammary Gland Biol. Neoplasia 7:277–289.

    Article  PubMed  Google Scholar 

  • Goldman, A.S., Chheda, S., and Garofalo, R. (1998). Evolution of immunologic functions of the mammary gland and the postnatal development of immunity. Pediatr. Res. 43:155–162.

    Article  CAS  PubMed  Google Scholar 

  • Granot, E., Rabinowitz, R., and Schlesinger, M. (1999). Lymphocyte subset profile of young healthy children residing in a rural area: Possible role of recurrent gastrointestinal infections. J. Pediatr. Gastroenterol. Nutr. 28:147–151.

    Article  CAS  PubMed  Google Scholar 

  • Gust, D.A., Gordon, T.P., Wilson, M.E., Ahmed-Ansari, A., Brodie, A.R., and McClure, H.M. (1991). Formation of a new social group of unfamiliar rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav. Immun. 5:296–307.

    Article  CAS  PubMed  Google Scholar 

  • Hannet, I., Erkeller-Yuksel, F., Lydyard, P., Denys, V., and DeBruyere, M. (1992). Developmental and maturational changes in human blood lymphocyte subpopulations. Immunol. Today. 13:215–218.

    Article  CAS  PubMed  Google Scholar 

  • Hanson, L.A. (1998). Breastfeeding provides passive and likely long-lasting active immunity. Ann. Allergy Asthma Immunol. 81:523–533.

    Article  CAS  PubMed  Google Scholar 

  • Harlow, H.F., and Harlow, M.K. (1969). Effects of various mother-infant relationships on rhesus monkey behaviors. In: Foss, B.M. (ed.), Determinants of Infant Behavior, Vol. 4. Methuen, London, pp. 15–36.

    Google Scholar 

  • Hasselbalch, H., Jeppesen, D.L., Engelmann, M.D., Michaelsen, K.F., and Nielsen, M.B. (1996). Decreased thymus size in formula-fed infants compared with breastfed infants. Acta Paediatr. 85:1029–1032.

    Article  CAS  PubMed  Google Scholar 

  • Hasselbalch, H., Engelmann, M.D., Ersboll, A.K., Jeppesen, D.L., and Fleischer-Michaelsen, K. (1999). Breast-feeding influences thymic size in late infancy. Eur. J. Pediatr. 158:964–967.

    Article  CAS  PubMed  Google Scholar 

  • Hayward, A.R., and Kurnick, J. (1981). Newborn T cell suppression: Early appearance, maintenance in culture, and lack of growth factor suppression. J. Immunol. 126:50–53.

    CAS  PubMed  Google Scholar 

  • Heird, W.C. (2001). The role of polyunsaturated fatty acids in term and preterm infants and breastfeeding mothers. Pediatr. Clin. North Am. 48:173–188.

    Article  CAS  PubMed  Google Scholar 

  • Hird, D.W., Anderson, J.H., and Bielitzki, J.B. (1984). Diarrhea in nonhuman primates: A survey of primate colonies for incidence rates and clinical opinion. Lab. Anim. Sci. 34:465–470.

    CAS  PubMed  Google Scholar 

  • Hiroshige, T., and Honma, K. (1987). Comparative Aspects of Circadian Clocks. Hokkaido University Press, Sapporo, Japan.

    Google Scholar 

  • Hofer, M.A. (1983). The mother-infant interaction as a regulator of infant physiology and behavior. In: Rosenblum, L.A., and Moltz, H. (eds.), Symbiosis in Parent-Offspring Interactions. Plenum Press, New York, pp. 61–75.

    Google Scholar 

  • Holt, P.G., and Macaubas, C. (1997). Development of long term tolerance versus sensitization to environmental allergens during the perinatal period. Curr. Opin. Immunol. 9:782–787.

    Article  CAS  PubMed  Google Scholar 

  • Hooper, L.V., Xu, J., Falk, P.G., Midtvedt, T., and Gordon, J.I. (1999). A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc. Natl. Acad. Sci. USA 96:9833–9838.

    Article  CAS  PubMed  Google Scholar 

  • Hooper, L.V., Wong, M.H., Thelin, A., Hansson, L., Falk, P.G., and Gordon, J.I. (2001). Molecular analysis of commensal host-microbial relationship in the intestine. Science 291:881–884.

    Article  CAS  PubMed  Google Scholar 

  • Illi, S., von Mutius, E., Lau, S., Bergmann, R., Niggemann, B., Sommerfeld, C., Wahn, C., and MAS Group. (2001). Early childhood infectious diseases and the development of asthma up to school age: A birth cohort study. BMJ 322:390–395.

    Article  CAS  PubMed  Google Scholar 

  • Jeppesen, D., Hasselbalch, H., Ersboll, A.K., Heilmann, C., and Valerius, N.H. (2003). Thymic size in uninfected infants born to HIV-positive mothers and fed with pasteurized human milk. Acta Paediatr. 92:679–683.

    Article  CAS  PubMed  Google Scholar 

  • Johnston, S.L., and Openshaw, P.J.M. (2001). The protective effect of childhood infections. BMJ 322:376–377.

    Article  CAS  PubMed  Google Scholar 

  • Jones, C.A., and Warner, J.O. (2000). Breast milk as an alternative source of cytokines for offspring. Clin. Exp. Allergy 30:599–601.

    Article  CAS  PubMed  Google Scholar 

  • Juto, P., Moller, C., Engberg, S., and Bjorksten, B. (1982). Influence of type of feeding on lymphocyte function and development of infantile allergy. Clin. Allergy 12:409–416.

    Article  CAS  PubMed  Google Scholar 

  • Kelleher, S., and Lonnerdal, B. (2001). Immunological activities associated with milk. In: Woodward, B., and Draper, H.H. (eds.), Advances in Nutritional Research, Vol. 10. Kluwer Academic/Plenum Publishers, New York, pp. 39–65.

    Google Scholar 

  • Kelleher, S., Casas, I., Carbajal, N., and Lonnerdal, B. (2002). Supplementation of infant formula with the probiotic Lactobacillus reuteri and zinc: Impact on enteric infection and nutrition in infant rhesus monkeys. J. Pediatr. Gastroenterol. Nutr. 35:162–168.

    Article  PubMed  Google Scholar 

  • Kelleher, S.L., Chatterton, D., Nielsen, K., and Lonnerdal, B. (2003). Glycomacropeptide and alpha-lactalbumin supplementation of infant formula affects growth and nutritional status in infant rhesus monkeys. Am. J. Clin. Nutr. 77:1261–1268.

    CAS  PubMed  Google Scholar 

  • Kelley, K.W. (1980). Stress and immune function: A bibliographic review. Ann. Rech. Vet. 11:445–478.

    CAS  PubMed  Google Scholar 

  • Kelley, K.W., Mertsching, H.J., and Salmon, H. (1984). Immunity changes in confined animals: A route to disease? Ann. Rech. Vet. 15:201–204.

    CAS  PubMed  Google Scholar 

  • Kleessen, B., Bunke, H., Tovar, K., Noack, J., and Sawatzki, G. (1995). Influence of two infant formulas and human milk on the development of the faecal flora in newborn infants. Acta Paediatr. 84:1347–1356.

    Article  CAS  PubMed  Google Scholar 

  • Klein, R.B., Fisher, T.J., Gard, S.E., Biberstien, M., Rich, K.C., and Stiehm, E.R. (1977). Decreased mononuclear and polymorphonuclear chemotaxis in human newborns, infants, and young children. Pediatrics 60:467–472.

    CAS  PubMed  Google Scholar 

  • Kovarik, J., and Siegrist, C-A. (1998). Immunity in early life. Immunol. Today 19:150–152.

    Article  CAS  PubMed  Google Scholar 

  • Kraemer, G.W., Ebert, M.H., Schmidit, D.E., and McKinney, W.T. (1989). A longitudinal study of the effect of different rearing conditions on cerebrospinal fluid norepinephrine and biogenic amine metabolites in rhesus monkeys. Neuropsychopharmacology 2:175–189.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn, C.M., Park, J., and Schanberg, S.M. (1990). Endocrine responses to mother-infant separation in developing rats. Dev. Psychobiol. 23:395–410.

    Article  CAS  PubMed  Google Scholar 

  • Lejeune, C., Bourrillon, A., Boussougant, Y., and de Paillerets, F. (1984). Sequential development of the intestinal flora in newborn infants: A quantitative differential analysis. Dev. Pharmacol. Ther. 7:138–143.

    PubMed  Google Scholar 

  • Le Souef, P.N., Goldblat, J., and Lynch, N.R. (2000). Evolutionary adaptation of inflammatory immune responses in human beings. Lancet 356:242–244.

    Article  PubMed  Google Scholar 

  • Lindberg, T., Engberg, S., Jakobsson, I., and Lonnerdal, B. (1997). Digestion of proteins in human milk, human milk fortifier, and preterm formula in infant rhesus monkeys. J. Pediatr. Gastroenterol. Nutr. 24:537–543.

    Article  CAS  PubMed  Google Scholar 

  • Lonnerdal, B., Keen, C., Glazier, C.E., and Anderson, J. (1984). A longitudinal study of rhesus monkey (Macaca mulatta) milk composition: Trace elements, minerals, protein, carbohydrate, and fat. Pediatr. Res. 18:911–914.

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Alarcon, M., Garza, C., Habicht, J-P., Martinez, L., Pegueros, V., and Villalpando, S. (2002). Breastfeeding attenuates reductions in energy intake induced by a mild immunologic stimulus represented by DPTH immunization: Possible roles of interleukin-1 beta, tumor necrosis factor-alpha and leptin. J. Nutr. 132:1293–1298.

    CAS  PubMed  Google Scholar 

  • Losonsky, G.A., and Ogra, P.L. (1981) Maternal-neonatal interactions and human breast milk. In: Gleicher, N. (ed.), Reproductive Immunology. Alan R. Liss, Inc., New York, pp. 171–182.

    Google Scholar 

  • Lubach, G.R., Kittrell, E.M., and Coe, C.L. (1992). Maternal influences on body temperature in the infant primate. Physiol. Behav. 51:987–994.

    Article  CAS  PubMed  Google Scholar 

  • Lubach, G.R., Coe, C.L., and Ershler, W.B. (1995). Effects of early rearing environment on immune responses of infant monkeys. Brain Behav. Immun. 9:31–46.

    Article  CAS  PubMed  Google Scholar 

  • Makori, N., Tarantal, A.F., Lu, F.X., Rourke, T., Marthas, M.L., McChesney, M.B., Hendrickx, A.G., and Miller, C.J. (2003). Functional and morphological development of lymphoid tissues and immune regulatory and effector function in rhesus monkeys: Cytokine-secreting cells, immunoglobulinsecreting cells, and CD5+ B-1 cells appear early in fetal development. Clin. Diagn. Lab. Immunol. 10:140–153.

    PubMed  Google Scholar 

  • Marthas, M.L., Van Rompay, K.K.A., Otsyula, M., Miller, C.J., Canfield, D.R., Pedersen, N.C., and McChesney, M.B. (1995). Viral factors determine progression to AIDS in simian immunodificiency virus-infected newborn rhesus monkeys. J. Virol. 69:4198–4205.

    CAS  PubMed  Google Scholar 

  • Martin, D.P., McGowan, M.J., and Loeb, W.F. (1973). Age related changes of hematologic values in infant Macaca mulatta. Lab. Anim. Sci. 23:194–200.

    CAS  PubMed  Google Scholar 

  • Mason, W.A., Mendoza, S.P., and Moberg, G.P. (1991). Persistent effects of early social experience on physiological responsiveness. In: Ehara, A., Kimura, T., Takenaka, O., and Iwamoto, M. (eds.), Primatology Today. Elsevier, New York, pp. 469–471.

    Google Scholar 

  • Mata, L.J., and Wyatt, R.G. (1971). Host resistance to infection. Am. J. Clin. Nutr. 24:976–986.

    CAS  PubMed  Google Scholar 

  • Matricardi, P.M., Rosmini, F., Riondino, S., Fortini, M., Ferrigano, L., Rapicetta, M., and Bonini, S. (2000). Exposure to foodborn and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: Epidemiological study. BMJ 320:412–417.

    Article  CAS  PubMed  Google Scholar 

  • Miller, M.E. (1980). The immunodeficiencies of immaturity. In: Steihm, E.R., and Fulginiti, V.A. (eds.), Immunologic Disorders in Infants and Children. W.B. Saunders, Co., Philadelphia, pp. 219–238.

    Google Scholar 

  • Murayama, Y., Fukao, K., Noguchi, A., and Takenaka, O. (1986). Epitope expression on primate lymphocyte surface antigens. J. Med. Primatol. 15:373–387.

    Google Scholar 

  • Nam, K.-H., Akari, H., Terao, K., Itagaki, S., and Yoshikawa, Y. (1998). Agerelated changes in major lymphocyte subsets in cynomolgus monkeys. Exp. Anim. 47:159–166.

    Article  CAS  PubMed  Google Scholar 

  • Neubert, R., Delgado, I., Abraham, K., Schuster, C., and Helge, H. (1998). Evaluation of the age-dependent development of lymphocyte surface receptors in children. Life Sci. 62:1099–1110.

    Article  CAS  PubMed  Google Scholar 

  • Novak, M.A., and Harlow, H.F. (1975). Social recovery of monkeys isolated for the first year of life: I. Rehabilitation and therapy. Dev. Psychol. 11:453–465.

    Article  Google Scholar 

  • Osburn, B.I., MacLachlan, N.J., and Terrel, T.G. (1982). Ontogeny of the immune system. J. Am. Vet. Med. Assoc. 181:1049–1052.

    CAS  PubMed  Google Scholar 

  • Pabst, H.F., Spady, D.W., Pilarski, L.M., Carson, M.M., Beeler, J.A., and Krezolek, M.P. (1997). Differential modulation of the immune response by breast-or formula-feeding of infants. Acta Paediatr. 86:1–7.

    Article  Google Scholar 

  • Packard, V.S. (1982). Human Milk and Infant Formula. Academic Press, New York.

    Google Scholar 

  • Prescott, S.L., Macaubas, C., Holt, B.J., Smallacombe, T.B., Loh, R., Sly, P.D., and Holt, P.G. (1998). Transplacental priming of the human immune system to environmental allergens: Universal skewing of initial T cell responses toward the Th2 cytokine profile. J. Immunol. 160:4730–4737.

    CAS  PubMed  Google Scholar 

  • Reite, M., Seiler, C., Crowley, T.J., Hydinger-MacDonald, M., and Short, R. (1982). Circadian rhythm changes following maternal separation. Chronobiologia 9:1–11.

    CAS  PubMed  Google Scholar 

  • Reyes, T.M., and Coe, C.L. (1997). Prenatal manipulations reduce the proinflammatory response to a cytokine challenge in juvenile monkeys. Brain Res. 769:29–35.

    Article  CAS  PubMed  Google Scholar 

  • Rook, G.A.W., and Stanford, J.L. (1998). Give us this day our daily germs. Immunol. Today 19:113–116.

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg, Y.J., and Reimann, K.A. (2000). Immunophenotypic and functional properties of lymphoid cells from nonhuman primates. In: Korte, R., and Weinbauer, G.F. (eds.), Towards New Horizons in Primate Toxicology. Waxmann Munster, New York, pp. 111–126.

    Google Scholar 

  • Rowe, J., Macaubas, C., Monger, T.M., Holt, B.J., Harvey, J., Poolman, J.T., Sly, P.D., and Holt, P.G. (2000). Antigen-specific responses to diphtheria-tetanus-acellular pertussis vaccine in human infants are initially Th2 polarized. Infect. Immun. 68:3873–3877.

    Article  CAS  PubMed  Google Scholar 

  • Ruppenthal, G.C. and Reese, D.J. (eds.) (1979). Nursery Care of Nonhuman Primates. Plenum Press, New York.

    Google Scholar 

  • Ruppenthal, G.C., and Sackett, G.P. (1979). Experimental and husbandry procedures: Their impact on development. In: Ruppenthal, G.C., and Reese, D.J. (eds.), Nursery Care of Nonhuman Primates. Plenum Press, New York, pp. 269–284.

    Google Scholar 

  • Russell, R.G., Rosenkranz, S.L., Lee, A.L., Howard, H., DiGiacomo, R.F., Bronsdon, M.A., Blakely, G.A., Tsai, C.-C., and Morton, W.R. (1987). Epidemiology and etiology of diarrhea in colony-born Macaca nemestrina. Lab. Anim. Sci. 37:309–316.

    CAS  PubMed  Google Scholar 

  • Sackett, G.P., Bowman, R.E., Meyer, J.S., Tripp, R.L., and Grady, S.S. (1973). Adrenocortical and behavioral reactions by differentially raised rhesus monkeys. Physiol. Psychol. 1:209–212.

    Google Scholar 

  • Sackett, G.P., Ruppenthal, G.C., and Davis, A.E. (2002). Survival, growth, health and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina). Am. J. Primatol. 56:165–183.

    Article  PubMed  Google Scholar 

  • Schiffrin, E.J., Carter, E.A., Walker, W.A., Frieberg, E., Benjamin J., and Israel, E.J. (1993). Influence of prenatal corticosteroids on bacterial colonization in the newborn rat. J. Pediatr. Gastroenterol. Nutr. 17:271–275.

    Article  CAS  PubMed  Google Scholar 

  • Smolensky, M.H., Reinberg, A., and McGovern, J.P. (eds.) (1980). Recent Advances in the Chronobiology of Allergy and Immunology. Pergamon Press, New York.

    Google Scholar 

  • Sopper, S., Stahl-Hennig, C., Demuth, M., Johnston, I.C.D., Dorries, R., and ter Meulen, V. (1997). Lymphocyte subsets and expression of differentiation markers in blood and lymphoid organs of rhesus monkeys. Cytometry 29:351–362.

    Article  CAS  PubMed  Google Scholar 

  • Stevens, S., Kennedy, C.R., Lakhani, P.K., and Brenner, M.K. (1984). In-vivo immune responses of breast-fed and bottle-fed infants to tetanus toxoid antigen and to normal gut flora. Acta Paediatr. Scand. 73:426–432.

    Article  Google Scholar 

  • Stone, E.A., Bonnet, K.A., and Hofer, M.A. (1976). Survival and development of maternally deprived rats: Role of body temperature. Psychosom. Med. 38:242–249.

    CAS  PubMed  Google Scholar 

  • Sulzman, F.M., Fuller, C.A., and Moore-Ede, M.C. (1977). Feeding time synchronizes primate circadian rhythms. Physiol. Behav. 18:775–779.

    Article  CAS  PubMed  Google Scholar 

  • Suomi, S.J., and Harlow, H.F. (1972). Social rehabilitation of isolate-reared monkeys. Dev. Psychol. 6:487–496.

    Article  Google Scholar 

  • Terao, K., Suzuki, J., and Ohkura, S. (2002). Circadian rhythm in circulating CD16-positive natural killer (NK) cells in macaque monkeys, implication of plasma cortisol levels. Primates 43:329–338.

    Article  PubMed  Google Scholar 

  • Van Rompay, K.K.A., Greenier, J.L., Cole, K.S., Earl, P., Moss, B., Steckbeck, J.D., Pahar, B., Rourke, T., Montelaro, R.C., Canfield, D.R., Tarara, R.P., Miller, C., McChesney, M.B., and Marthas, M.L. (2003). Immunization of newborn rhesus macaques with simian immunodeficiency virus (SIV) vaccines prolongs survival after oral challenge with virulent SIVmac251. J. Virol. 77:179–190.

    Article  PubMed  CAS  Google Scholar 

  • Vigano, A., Esposito, S., Arienti, D., Zagliani, A., Massironi, E., Principi, N., and Clerici, M. (1999). Differential development of Type 1 and Type 2 cytokines and beta-chemokines in the ontogeny of healthy newborns. Biol. Neonate 75:1–8.

    Article  CAS  PubMed  Google Scholar 

  • Woodward, B., and Draper, H.H. (eds.) (2001). Advances in Nutritional Research, Vol. 10. Kluwer Academic/Plenum Publishers, New York.

    Google Scholar 

  • Yoshino, N., Ami, Y., Terao, K., Tashiro, F., and Honda, M. (2000). Upgrading of flow cytometric analysis for absolute counts, cytokines and other antigenic molecules of cynomolgus monkeys (Macaca fascicularis) by using anti-human cross-reactive antibodies. Exp. Anim. 49:97–110.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X.-L., Komada, Y., Chipeta, J., Li, Q.-S., Inaba, H., Azuma, E., Yamamoto, H., and Sakurai, M. (2000). Intracellular cytokine profile of T cells from children with acute lymphoblastic leukemia. Cancer Immunol. Immunother. 49:165–172.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Harlow Primate Laboratory, University of Wisconsin, Madison, WI, 53715, USA

    Gabriele R. Lubach

  2. Harlow Primate Laboratory, University of Wisconsin, Madison, WI, 53715-1239, USA

    Christopher L. Coe

Authors
  1. Gabriele R. Lubach
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher L. Coe
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Washington National Primate Research Center, University of Washington, Seattle, WA, USA

    Gene P. Sackett , Gerald C. Ruppentahal  & Kate Elias ,  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer Science+Business Media, Inc.

About this chapter

Cite this chapter

Lubach, G.R., Coe, C.L. (2006). Immunological Consequences of Nursery Rearing. In: Sackett, G.P., Ruppentahal, G.C., Elias, K. (eds) Nursery Rearing of Nonhuman Primates in the 21st Century. Developments in Primatology: Progress and Prospects. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-25640-5_9

Download citation

Publish with us

Policies and ethics

Search

Navigation