Simultaneous measurement of endogenous steroid hormones and their metabolites with LC-MS/MS in faeces of a New World primate species, Cebus capucinus

Physiology and Behavior

Volumn 105, Issue 2, 2012, Pages 510-521

  Weltring, Anja ^a   Schaebs, Franka S ^a   Perry, Susan E ^b   Deschner, Tobias ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Feces; LC MS MS; New World primates; Steroids; Validation; White faced capuchins

Indexed keywords

DRUG METABOLITE; ESTRONE; HYDROCORTISONE; MATRIX PROTEIN; METHANOL; PROGESTERONE; STEROID HORMONE; TESTOSTERONE;

ACCURACY; ARTICLE; CEBUS; CONJUGATE; CONTROLLED STUDY; ELECTROSPRAY; EXTRACTION; FECES; FEMALE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOASSAY; LIMIT OF QUANTITATION; LIQUID CHROMATOGRAPHY; LIQUID LIQUID EXTRACTION; MALE; MEASUREMENT; METABOLITE; NONHUMAN; PRIORITY JOURNAL; PURIFICATION; SOLID PHASE EXTRACTION; SOLVOLYSIS; TANDEM MASS SPECTROMETRY; VALIDATION PROCESS;

ANIMALS; CALLITHRIX; CHROMATOGRAPHY, LIQUID; ESTRONE; FECES; FEMALE; HYDROCORTISONE; MALE; PROGESTERONE; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SOLID PHASE EXTRACTION; STEROIDS; TANDEM MASS SPECTROMETRY; TESTOSTERONE;

EID: 80053930785     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.09.004     Document Type: Article

References (87)

1. Möstl E., Palme R. Hormones as indicators of stress. Domest Anim Endocrinol 2002, 23:67-74.
2. Risler L., Wasser S.K., Sackett G.P. Measurement of excreted steroids in Macaca nemestrina. Am J Primatol 1987, 12:91-100.
3. Schwarzenberger F. The many uses of non-invasive faecal steroid monitoring in zoo and wildlife species. Int Zoo Yb 2007, 41:52-74.
4. Pugeat M.M., Chrousos G.P., Nisula B.C., Loriaux D.L., Brandon D., Lipsett M.B. Plasma cortisol transport and primate evolution. Endocrinology 1984, 115:357-361.
5. Hubler T.R., Denny W.B., Valentine D.L., Cheung-Flynn J., Smith D.F., Scammell J.G. The FK506-binding immunophilin FKBP51 is transcriptionally regulated by progestin and attenuates progestin responsiveness. Endocrinology 2003, 144:2380-2387.
6. Scammell J.G., Denny W.B., Valentine D.L., Smith D.F. Overexpression of the FK506-binding immunophilin FKBP51 is the common cause of glucocorticoid resistance in three New World primates. Gen Comp Endocrinol 2001, 124:152-165.
7. Cassorla F.G., Albertson B.D., Chrousos G.P., Booth J.D., Renquist D., Lipsett M.B., et al. The mechanism of hypercortisolemia in the squirrel monkey. Endocrinology 1982, 111:448-451.
8. Siiteri P.K., Murai J.T., Hammond G.L., Nisker J.A., Raymoure W.J., Kuhn R.W. The serum transport of steroid hormones. Recent Prog Horm Res 1982, 38:457-503.
9. Scammell J.G., Westberry J.M., Sadosky P.W., Hubler T.R., Williams L.E., Gibson S.V., et al. Cortisol metabolism in the bolivian squirrel monkey (Saimiri boliviensis boliviensis). Comp Med 2006, 56:128-135.
10. Cristóbal-Azkarate J., Chavira R., Boeck L., Rodríguez-Luna E., Vea J.J. Glucocorticoid levels in free ranging resident mantled howlers: a study of coping strategies. Am J Primatol 2007, 69:866-876.
11. Heistermann M., Tari S., Hodges J.K. Measurement of faecal steroids for monitoring ovarian function in New World primates, Callitrichidae. J Reprod Fert 1993, 99:243-251.
12. Romano M.C., Rodas A.Z., Valdez R.A., Hernández S.E., Galindo F., Canales D., et al. Stress in wildlife species: noninvasive monitoring of glucocorticoids. Neuroimmunomodulation 2010, 17:209-212.
13. Touma C., Palme R. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 2005, 1046:54-74.
14. Whitten P.L., Brockman D.K., Stavisky R.C. Recent advanced in noninvasive techniques to monitor hormone-behavior interactions. Yearbk Phys Anthropol 1998, 41:1-23.
15. Carnegie S.D., Fedigan L.M., Ziegler T.E. Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus). Am J Primatol 2005, 67:51-68.
16. Carosi M., Heistermann M., Visalberghi E. Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys. Horm Behav 1999, 36:252-265.
17. Lynch J.W., Ziegler T.E., Strier K.B. Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm Behav 2002, 41:275-287.
18. Poelmans S., De Wasch K., Noppe H., Van Hoof N., Van De Wiele M., Courtheyn D., et al. Androstadienetrione, a boldenone-like component, detected in cattle faeces with GC-MSn and LC-MSn. Food Addit Contam 2005, 22:798-807.
19. Van de Wiele M., De Wasch K., Vercammen J., Courtheyn D., De Brabander H., Impens S. Determination of 16beta-hydroxystanozolol in urine and faeces by liquid chromatography-multiple mass spectrometry. J Chromatogr A 2000, 904:203-209.
20. Möstl E., Maggs J.L., Schrötter G., Besenfelder U., Palme R. Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 2002, 26:127-139.
21. Hauser B., Deschner T., Boesch C. Development of a liquid chromatography-tandem mass spectometry method for the determination of 23 endogenous steroids in small quantities of primate urine. J Chromatogr B 2008, 862:100-112.
22. Ganswindt A., Palme R., Heistermann M., Borragan S., Hodges J.K. Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol 2003, 134:156-166.
23. Heistermann M., Palme R., Ganswindt A. Comparison of different enzymeimmunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am J Primatol 2006, 68:257-273.
24. Möhle U., Heistermann M., Palme R., Hodges J.K. Characterisation of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Gen Comp Endocrinol 2002, 129:135-145.
25. Schatz S., Palme R. Measurement of faecal cortisol metabolites in cats and dogs: a non-invasive method for evaluating adrenocortical function. Vet Res Commun 2001, 25:271-287.
26. Preis A, Mugisha L, Hauser B, Weltring A, Deschner T. Androgen and androgen metabolite levels in serum and urine of east African chimpanzees (Pan troglodytes schweinfurthii). Comparison of EIA and LC-MS analyses. J Comp Endocrinol in press.
27. Kutsukake N., Ikeda K., Honma S., Teramoto M., Mori Y., Hayasaka I., et al. Validation of salivary cortisol and testosterone assays in chimpanzees by liquid chromatography-tandem mass spectrometry. Am J Primatol 2009, 71:696-706.
28. Gesquiere L.R., Onyango P.O., Alberts S.C., Altmann J. Endocrinology of year-round reproduction in a highly seasonal habitat: environmental variability in testosterone and glucocorticoids in baboon males. Am J Phys Anthropol 2011, 144:169-176.
29. Girard-Buttoz C., Heistermann M., Krummel S., Engelhardt A. Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiol Behav 2009, 98:168-175.
30. Mehta P.H., Josephs R.A. Testosterone and cortisol jointly regulate dominance: evidence for a dual-hormone hypothesis. Horm Behav 2010, 58:898-906.
31. Chame M. Terrestrial mammal feces: a morphometric summary and description. Mem Inst Oswaldo Cruz 2003, 98(Suppl. 1):71-94.
32. Jacobsen R., Lorenzen J.K., Toubro S., Krog-Mikkelsen I., Astrup A. Effect of short-term high dietary calcium intake on 24-h energy expenditure, fat oxidation, and fecal fat excretion. Int J Obes 2005, 29:292-301.
33. Meillet D., Raichvarg D., Tallet F., Savel J., Yonger J., Gobert J.G. Measurement of total, monomeric and polymeric IgA in human faeces by electroimmunodiffusion. Clin Exp Immunol 1987, 69:142-147.
34. Lin D.S., Connor W.E. Fecal steroids of the coprolite of a Greenland Eskimo mummy, AD 1475: a clue to dietary sterol intake. Am J Clin Nutr 2001, 74:44-49.
35. Taylor W. The excretion of steroid hormone metabolites in bile and feces. Vitam Horm 1971, 29:201-285.
36. MacDonald I.A., Bokkenheuser V.D., Winter J., McLernon A.M., Mosbach E.H. Degradation of steroids in the human gut. J Lipid Res 1983, 24:675-700.
37. Heistermann M. Non-invasive monitoring of endocrine status in laboratory primates: methods, guidelines and applications. Adv Sci Res 2010, 1:1-9.
38. Ziegler T.E., Scheffler G., Wittwer D.J., Schultz-Darken N., Snowdon C.T., Abbott D.H. Metabolism of reproductive steroids during the ovarian cycle in two species of callitrichids, Saguinus oedipus and Callithrix jacchus, and estimation of the ovulatory period from fecal steroids. Biol Reprod 1996, 54:91-99.
39. Wasser S.K., Monfort S.L., Southers J., Wildt D.E. Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J Reprod Fert 1994, 101:213-220.
40. Ziegler T.E., Wittwer D.J. Fecal steroid research in the field and laboratory: improved methods for storage, transport, processing, and analysis. Am J Primatol 2005, 67:159-174.
41. Bahr N.I., Palme R., Möhle U., Hodges J.K., Heistermann M. Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen Comp Endocrinol 2000, 117:427-438.
42. Volin P. High-performance liquid chromatographic analysis of corticosteroids. J Chromatogr B 1995, 671:319-340.
43. Heistermann M., Finke M., Hodges J.K. Assessment of female reproductive status in captive-housed hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am J Primatol 1995, 37:275-284.
44. Hennion M.-C. Solid-phase extraction: method development, sorbents, and coupling with liquid chromatography. J Chromatogr A 1999, 856:3-54.
45. MacDougall D., Crummett W.B. Guidelines for data acquisition and data quality evaluation in environmental chemistry. Anal Chem 1980, 52:2242-2249.
46. Wasser S.K., Papageorge S., Foley C., Brown J.L. Excretory fate of estradiol and progesterone in the African elephant (Loxodonta africana) and patterns of fecal steroid concentrations throughout the estrous cycle. Gen Comp Endocrinol 1996, 102:255-262.
47. Fedigan L.M., Rose L.M., Avila R.M. See how they grow. Tracking capuchin monkey (Cebus capucinus) populations in a regenerating Costa Rican dry forest. Adaptive Radiations of Neotropical Primates 1996, 289-307. Plenum Press, New York. M.A. Norconk, A.L. Rosenberger, P.A. Garber (Eds.).
48. Castro D.C., Sousa M.B.C. Fecal androgen levels in common marmoset (Callithrix jacchus) males living in captive family groups. Braz J Med Biol Res 2005, 38:65-72.
49. Raminelli J.L.F., de Sousa M.B.C., Cunha M.S., Barbosa M.F.V. Morning and afternoon patterns of fecal cortisol excretion among reproductive and non-reproductive male and female common marmosets, Callithrix jacchus. Biol Rhythm Res 2001, 32:159-167.
50. Sousa M.B.C., Ziegler T.E. Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. Am J Primatol 1998, 46:105-117.
51. Albuquerque A.C.S.R., Sousa M.B.C., Santos H.M., Ziegler T.E. Behavioral and hormonal analysis of social relationships between oldest females in a wild monogamous group of common marmosets (Callithrix jacchus). Int J Primatol 2001, 22:631-645.
52. Beehner J.C., Gesquiere L., Seyfarth R.M., Cheney D.L., Alberts S.C., Altmann J. Testosterone related to age and life-history stages in male baboons and geladas. Horm Behav 2009, 56:472-480.
53. Coe C.L., Chen J., Lowe E.L., Davidson J.M., Levine S. Hormonal and behavioral changes at puberty in the squirrel monkey. Horm Behav 1981, 15:36-53.
54. Hauser B., Mugisha L., Preis A., Deschner T. LC-MS analysis of androgen metabolites in serum and urine from east African chimpanzees (Pan troglodytes schweinfurthii). Gen Comp Endocrinol 2011, 170:92-98.
55. French J.A., Koban T., Rukstalis M., Ramirez S.M., Bardi M., Brent L. Excretion of urinary steroids in pre- and postpartum female baboons. Gen Comp Endocrinol 2004, 137:69-77.
56. Hodgen G.D., Stouffer R.L., Barber D.L., Nixon W.E. Serum estradiol and progesterone during pregnancy and the status of the corpus luteum at delivery in cynomolgus monkeys (Macaca fascicularis). Steroids 1977, 30:295-301.
57. Bales K.L., French J.A., Hostetler C.M., Dietz J.M. Social and reproductive factors affecting cortisol levels in wild female golden lion tamarins (Leontopithecus rosalia). Am J Primatol 2005, 67:25-35.
58. Saltzman W., Maestripieri D. The neuroendocrinology of primate maternal behavior. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:1192-1204.
59. Smith T.E., French J.A. Social and reproductive conditions modulate urinary cortisol excretion in black tufted-ear marmosets (Callithrix kuhli). Am J Primatol 1997, 42:253-267.
60. Ziegler T.E., Scheffler G., Snowdon C.T. The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Horm Behav 1995, 29:407-424.
61. Kromidas S. Validierung in der Analytik 1999, Wiley-VCH, Weinheim.
62. Zondek B. Mass excretion of oestrogenic hormone in the urine of the stallion. Nature 1934, 133:209-210.
63. Velle W. Urinary oestrogens in the male. J Reprod Fert 1966, 12:65-73.
64. Nunes S., Brown C., French J.A. Variation in circulating and excreted estradiol associated with testicular activity in male marmosets. Am J Primatol 2002, 56:27-42.
65. Ziegler T.E., Carlson A.A., Ginther A.J., Snowdon C.T. Gonadal source of testosterone metabolites in urine of male cotton-top tamarin monkeys (Saguinus oedipus). Gen Comp Endocrinol 2000, 118:332-343.
66. Hodges J.K., Eastman S.A.K. Monitoring ovarian function in marmosets and tamarins by the measurement of urinary estrogen metabolites. Am J Primatol 1984, 6:187-197.
67. Ziegler T.E., Peterson L.J., Sosa M.E., Barnard A.M. Differential endocrine responses to infant odors in common marmoset (Callithrix jacchus) fathers. Horm Behav 2011, 59:265-270.
68. Sohl C.D., Guengerich F.P. Kinetic analysis of the three-step steroid aromatase reaction of human cytochrome P450 19A1. J Biol Chem 2010, 285:17734-17743.
69. Goddard P., Hill M.J. Degradation of steroids by intestinal bacteria: IV. The aromatisation of ring A. Biochim Biophys Acta 1972, 280:336-342.
70. Hodges J.K., Gulick B.A., Czekala N.M., Lasley B.L. Comparison of urinary oestrogen excretion in South American primates. J Reprod Fert 1981, 61:83-90.
71. Abbott D.H., Bird I.M. Nonhuman primates as models for human adrenal androgen production: function and dysfunction. Rev Endocr Metab Disord 2009, 10:24-33.
72. Pattison J.C., Saltzman W., Abbott D.H., Hogan B.K., Nguyen A.D., Husen B., et al. Gender and gonadal status differences in zona reticularis expression in marmoset monkey adrenals: cytochrome b5 localization with respect to cytochrome P450 17,20-lyase activity. Mol Cell Endocrinol 2007, 265-266:93-101.
73. Seraphin S.B., Whitten P.L., Reynolds V. The influence of age on fecal steroid hormone levels in male Budongo Forest chimpanzees (Pan troglodytes schweinfurthii). Am J Primatol 2008, 70:661-669.
74. Remer T., Maser-Gluth C., Boye K.R., Hartmann M.F., Heinze E., Wudy S.A. Exaggerated adrenarche and altered cortisol metabolism in Type 1 diabetic children. Steroids 2006, 71:591-598.
75. Wudy S.A., Hartmann M.F., Remer T. Sexual dimorphism in cortisol secretion starts after age 10 in healthy children: urinary cortisol metabolite excretion rates during growth. Am J Physiol Endocrinol Metab 2007, 293:E970-E976.
76. Adlercreutz H., Järvenpää P. Assay of estrogens in human feces. J Steroid Biochem 1982, 17:639-654.
77. Eriksson H., Gustafsson J.-A. Excretion of steroid hormones in adults. Eur J Biochem 1971, 18:146-150.
78. Ziegler T.E., Sholl S.A., Scheffler G., Haggerty M.A., Lasley B.L. Excretion of estrone, estradiol, and progesterone in the urine and feces of the female cotton-top tamarin (Saguinus oedipus oedipus). Am J Primatol 1989, 17:185-195.
79. Commission Decision 2002/657/EC implementing Council Directive 96/23/EC concerning the performance of analytical methods and the interpretation of results (notified under document number C(2002) 3044). Off J Eur Communities 2002, L221:8-36.
80. Horwitz W. Evaluation of analytical methods used for regulation of foods and drugs. Anal Chem 1982, 54:67A-76A.
81. Hunt K.E., Wasser S.K. Effect of long-term preservation methods on fecal glucocorticoid concentrations of Grizzly bear and African elephant. Physiol Biochem Zool 2003, 76:918-982.
82. Kahn M.Z., Altmann J., Isani S.S., Yu J. A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen Comp Endocrinol 2002, 128:57-64.
83. Yalkowsky S.H. Solubility and solubilization in aqueous media 1999, American Chemical Society & Oxford University Press, Washington, D. C.
84. Terio K.A., Brown J.L., Moreland R., Munson L. Comparison of different drying and storage methods on quantifiable concentrations of fecal steroids in the cheetah. Zoo Biol 2002, 21:215-222.
85. Wasser S.K., Risler L., Steiner R.A. Excreted steroids in primate feces over the menstrual cycle and pregnancy. Biol Reprod 1988, 39:862-872.
86. Groh H., Schade K., Hörhold-Schubert C. Steroid metabolism with intestinal microorganisms. J Basic Microbiol 1993, 33:59-72.
87. Wallner B., Möstl E., Dittami J., Prossinger H. Fecal glucocorticoids document stress in female Barbary macaques (Macaca sylvanus). Gen Comp Endocrinol 1999, 113:80-86.