The influence of nutritional state on the fatty acid composition of circulating lipid fractions: implications for their use as biomarkers of dietary fat intake

Sion A. Parry; Fredrik Rosqvist; Sarah Peters; Rebecca K. Young; Thomas Cornfield; Pamela Dyson; Leanne Hodson

doi:10.48101/ujms.v126.7649

Sion A. Parry Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom https://orcid.org/0000-0002-9037-1619
Fredrik Rosqvist Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom; and Department of Public Health and Caring Sciences, Clinical Nutrition and Metabolism, Uppsala University, Uppsala, Sweden https://orcid.org/0000-0002-8982-6129
Sarah Peters Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom https://orcid.org/0000-0003-0094-8638
Rebecca K. Young Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom
Thomas Cornfield Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom
Pamela Dyson Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom; and National Institute for Health Research Oxford, Biomedical Research Centre, Oxford University, Hospital Trusts, Oxford, United Kingdom https://orcid.org/0000-0001-5391-6301
Leanne Hodson Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom; and National Institute for Health Research Oxford, Biomedical Research Centre, Oxford University, Hospital Trusts, Oxford, United Kingdom https://orcid.org/0000-0002-2648-6526

DOI: https://doi.org/10.48101/ujms.v126.7649

Keywords: Postprandial, fatty acids, biomarker, lipid fractions, fatty acid composition

Abstract

Background: The fatty acid (FA) composition of blood can be used as an objective biomarker of dietary FA intake. It remains unclear how the nutritional state influences the FA composition of plasma lipid fractions, and thus their usefulness as biomarkers in a non-fasted state.

Objectives: To investigate the associations between palmitate, oleate and linoleate in plasma lipid fractions and self-reported dietary FA intake, and assess the influence of meal consumption on the relative abundance of these FA in plasma lipid fractions (i.e. triglyceride [TG], phospholipids [PLs] and cholesterol esters [CEs]).

Design: Analysis was performed in plasma samples collected from 49 (34 males and 15 females) participants aged 26–57 years with a body mass index (BMI) between 21.6 and 34.2 kg/m², all of whom had participated in multiple study visits, thus a pooled cohort of 98 data sets was available for analysis. A subset (n = 25) had undergone nutritional interventions and was therefore used to investigate the relationship between the FA composition of plasma lipid fractions and dietary fat intake.

Results: Significant (P < 0.05) positive associations were observed between dietary polyunsaturated fat and linoleate abundance in plasma CE. When investigating the influence of meal consumption on postprandial FA composition, we found plasma TG palmitate significantly (P < 0.05) decreased across the postprandial period, whereas oleate and linoleate increased. A similar pattern was observed in plasma PL, whereas linoleate abundance decreased in the plasma CE.

Conclusion: Our data demonstrate that the FA composition of plasma CE may be the lipid fraction to utilise as an objective biomarker when investigating recent (i.e. previous weeks-months) dietary FA intakes. In addition, we show that the consumption of a high-fat meal influences the FA composition of plasma TG, PL and CE over the course of the postprandial period, and therefore, suggest that fasting blood samples should be utilised when using FA composition as a biomarker of dietary FA intake.

Downloads

Download data is not yet available.

References

Alter S.E., Simmonds M.P. & Brandon J.R. 2010. Forecasting the consequences of climate-driven shifts in human behavior on cetaceans. Marine Policy 34, 943–954, doi: 10.1016/j.marpol.2010.01.026.

Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour 49, 227–267, doi: 10.1163/156853974X00534.

Araújo J.P., Araújo M.E., Souto A., Parente C.L. & Geise L. 2007. The influence of seasonality, tide and time of activities on the behavior of Sotalia guianensis (Van Bénéden) (Cetacea, Delphinidae) in Pernambuco, Brazil. Revista Brasileira de Zoologia 24, 1122–1130, doi: 10.1590/S0101-81752007000400032.

Baird R.W. 2000. The killer whale: foraging specializations and group hunting. In J. Mannet al. (eds.): Cetacean societies: field studies of dolphins and whales. Pp. 127–153. Chicago, IL: University of Chicago Press.

Bland J.M. & Altman D.G. 1986. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 327, 307–310, doi: 10.1016/S0140-6736(86)90837-8.

Bräger S. 1993. Diurnal and seasonal behavior patterns of bottlenose dolphins (Tursiops truncatus). Marine Mammal Science 9, 434–438, doi: 10.1111/j.1748-7692.1993.tb00477.x.

Buck C.L. & Barnes B.M. 2003. Androgen in free-living Arctic ground squirrels: seasonal changes and influence of staged male–male aggressive encounters. Hormones Behavior 43, 318–326, doi: 10.1016/S0018-506X(02)00050-8.

Caldwell M.C. & Caldwell D.K. 1977. Social interactions and reproduction in the Atlantic bottlenosed dolphin, breeding dolphins: present status, suggestions for the future. Washington, DC: Marine Mammal Commission Report.

Castellotes M., Small R.J., Lammers M.O., Jenniges J., Mondragon J., Garner C.D., Atkinson S., Delevaux J.M.S., Graham R. & Westerholt D. 2020. Seasonal distribution and foraging occurrence of Cook Inlet beluga whales based on passive acoustic monitoring. Endangered Species Research 41, 225–243, doi: 10.3354/esr01023.

Connor R.C., Richards A.F., Smolker R.A. & Mann J. 1996. Patterns of female attractiveness in Indian Ocean bottlenose dolphins. Behaviour 133, 37–69, doi: 10.1163/156853996X00026.

Coscarella M.A., Pedraza S.N. & Crespo E.A. 2010. Behavior and seasonal variation in the relative abundance of Commerson’s dolphin (Cephalorhynchus commersonii) in northern Patagonia, Argentina. Journal of Ethology 28, 463–470, doi: 10.1007/s10164-010-0206-4.

Doan K.H. & Douglas C.W. 1953. Beluga of the Churchill region of Hudson Bay. Bulletin of the Fisheries Research Board of Canada 98, 1–27.

Essapian F.S. 1963. Observations on abnormalities of parturition in captive bottle-nosed dolphins, Tursiops truncatus, and concurrent behavior of other porpoises. Journal of Mammalogy 44, 405–414, doi: 10.2307/1377210.

Frost K. & Lowry L. 1990. Distribution, abundance and movements of beluga whales, Delphinapterus leucas, in coastal waters of western Alaska. Canadian Journal Fisheries and Aquatic Sciences 224, 39–57.

George E.M. & Noonan M. 2014. Respiration rates in captive beluga whales (Delphinapterus leucas): effects of season, sex, age, and body size. Aquatic Mammals 40, 350–356, doi: 10.1578/AM.40.4.2014.350.

Glabicky N., DuBrava A. & Noonan M. 2010. Social–sexual behavior seasonality in captive beluga whales (Delphinapterus leucas). Polar Biology 33, 1145–1147, doi: 10.1007/s00300-010-0790-3.

Gould L. & Ziegler T.E. 2007. Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta). American Journal of Primatology 69, 1325–1339, doi: 10.1002/ajp.20438.

Ham J.R., Lilley M.K. & Manitzas Hill H.M. 2021. Conspecific scarring on wild belugas (Delphinapterus leucas) in Cunningham Inlet. Behaviour, 1–21, doi: 10.1163/1568539X-bja10086.

Heide-Jørgensen M.P., Laidre K.L., Borchers D., Marques T.A., Stern H. & Simon M. 2010. The effect of sea-ice loss on beluga whales (Delphinapterus leucas) in west Greenland. Polar Research 29, 198–208, doi: 10.1111/j.1751-8369.2009.00142.x.

Heide-Jørgensen M.P. & Teilmann J. 1994. Growth, reproduction, age structure and feeding habits of white whales (Delphinapterus leucas) in west Greenland waters. Meddelelser om Grønland, Bioscience 39, 195–212.

Hill H.M. 2009. The behavioral development of two beluga calves during the first year of life. International Journal of Comparative Psychology 22, 234–253.

Hill H.M., Alvarez C.J., Dietrich S. & Lacy K. 2016. Preliminary findings in beluga (Delphinapterus leucas) tactile interactions. Aquatic Mammals 42, 277–291, doi: 10.1578/AM.42.3.2016.277.

Hill H.M. & Campbell C.A. 2014. The frequency and nature of allocare by a group of belugas (Delphinapterus leucas) in human care. International Journal of Comparative Psychology 27, 501–514, doi: 10.46867/ijcp.2014.27.04.08.

Hill H.M., Campbell C., Dalton L. & Osborn S. 2013. The first year of behavioral development and maternal care of beluga (Delphinapterus leucas) calves in human care. Zoo Biology 32, 565–570, doi: 10.1002/zoo.21093.

Hill H.M., Dietrich S., Guarino S., Banda M. & Lacy K. 2019. Preliminary observations of an unusual mouth interaction between beluga calves (Delphinapterus leucas). Zoo Biology 38, 149–156, doi: 10.1002/zoo.21463.

Hill H., Dietrich S., Jantea R.F., Garza S. & Lacy K. 2018. The frequency of contact in beluga (Delphinapterus leucas) calf social interactions. Aquatic Mammals 44, 62–75, doi: 10.1578/AM.44.1.2018.62.

Hill H.M., Dietrich S., Yeater D., McKinnon M., Miller M., Aibel S. & Dove A. 2015. Developing a catalog of socio-sexual behaviors of beluga whales (Delphinapterus leucas). Animal Behavior and Cognition 2, 105–123, doi: 10.12966/abc.05.01.2015.

Hill H. & Ramirez D. 2014. Adults play but not like their young: the frequency and types of play by belugas (Delphinapterus leucas) in human care. Animal Behavior and Cognition 1, 166–185, doi: 10.12966/abc.05.07.2014.

Hobbs R.C., Waite J.M. & Rugh D.J. 2000. Beluga, Delphinapterus leucas, group sizes in Cook Inlet, Alaska, based on observer counts and aerial video. Marine Fisheries Review 62, 46–59.

IBM Corp. 2017. IBM SPSS statistics for Macintosh, Version 25.0. Armonk, NY: IBM Corp.

Krasnova V.V., Bel’kovich V.M. & Chernetsky [Chernetskii] A.D. 2006. Mother–infant spatial relations in wild beluga (Delphinapterus leucas) during postnatal development under natural conditions. Biology Bulletin 33, 53–58, doi: 10.1134/S1062359006010079.

Krasnova V.V., Bel’kovich V.M. & Chernetskii [Chernetsky] A.D. 2009. Formation of behavior in the White Sea beluga calf, Delphinapterus leucas, during early postnatal ontogenesis. Russian Journal of Marine Biology 35, 53–59, doi: 10.1134/S1063074009010088.

Krasnova V.V., Chernetsky [Chernetskii] A.D., Zheludkova A.I. & Bel’kovich V.M. 2014. Parental behavior of the beluga whale (Delphinapterus leucas) in natural environment. Biology Bulletin 41, 349–356, doi: 10.1134/S1062359014040062.

Kuznetsova A., Brockhoff P.B. & Christensen R.H.B. 2017. lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26, doi: 10.18637/jss.v082.i13.

Lenth R.V. 2020. emmeans: estimated marginal means, aka least-squares means. R Package version 1.5.2-1. Accessed on the internet at https://CRAN.R-project.org/package=emmeans

Lilley M.K., Ham J.R. & Hill H.M. 2020. The development of socio-sexual behavior in belugas (Delphinapterus leucas) under human care. Behavioural Processes 171, article no. 104025, doi: 10.1016/j.beproc.2019.104025.

Lomac-MacNair K.S., Smultea M.A., Cotter M.P., Thissen C. & Parker L. 2016. Socio-sexual and probable mating behavior of Cook Inlet beluga whales, Delphinapterus leucas, observed from an aircraft. Marine Fisheries Review 77, 32–39, doi: 10.7755/MFR.77.2.2.

Lydersen C., Martin A.R., Kovacs K.M. & Gjertz I. 2001. Summer and autumn movements of white whales Delphinapterus leucas in Svalbard, Norway. Marine Ecology Progress Series 219, 265–274, doi: 10.3354/meps219265.

McBride A.F. & Hebb D.O. 1948. Behavior of the captive bottle-nose dolphin, Tursiops truncatus. Journal of Comparative and Physiological Psychology 41, 111–123, doi: 10.1037/h0057927.

McBride A.F. & Kritzler H. 1951. Observations on pregnancy, parturition, and postnatal behavior in the bottlenose dolphin. Journal of Mammalogy 32, 251–266, doi: 10.2307/1375657.

McGuire T.L., Himes Boor G.K., McClung J.R., Stephens A.D., Garner C., Shelden K.E.W. & Wright B. 2020. Distribution and habitat use by endangered Cook Inlet beluga whales: patterns observed during a photo-identification study, 2005–2017. Aquatic Conservation: Marine and Freshwater Ecosystems 30, 2402–2427, doi: 10.1002/aqc.3378.

Miller L.J., Solangi M. & Kuczaj S.A. II 2010. Seasonal and diurnal patterns of behavior exhibited by Atlantic bottlenose dolphins (Tursiops truncatus) in the Mississippi Sound. Ethology 116, 1127–1137, doi: 10.1111/j.1439-0310.2010.01824.x.

Möller L.M. & Harcourt R.G. 1998. Social dynamics and activity patterns of bottlenose dolphins, Tursiops truncatus, in Jervis bay, southeastern Australia. Proceedings of the Linnean Society of New South Wales 120, 181–189.

Montano G.A., Robeck T.R., Steinman K.J. & O’Brien J.K. 2017. Circulating anti-Müllerian hormone concentrations in relation to age and season in male and female beluga (Delphinapterus leucas). Reproduction, Fertility and Development 29, 1642–1652, doi: 10.1071/RD15537.

Nakahara F. & Takemura A. 1997. A survey on the behavior of captive odontocetes in Japan. Aquatic Mammals 23, 135–143.

O’Corry-Crowe G., Suydam R., Quakenbush L., Potgieter B., Harwood L., Litovka D., Ferrer T., Citta J., Burkanov V., Frost K. & Mahoney B. 2018. Migratory culture, population structure and stock identity in North Pacific beluga whales (Delphinapterus leucas). PLoS One 13, e0194201, doi: 10.1371/journal.pone.0194201.

O’Corry-Crowe G., Suydam R., Quakenbush L., Smith T.G., Lydersen C., Kovacs K.M., Orr J., Harwood L., Litovka D. & Ferrer T. 2020. Group structure and kinship in beluga whale societies. Scientific Reports 10, article no. 11462, doi: 10.1038/s41598-020-67314-w.

R Core Team 2018. R: a language and environment for statistical computing. Vienna: Society for Statistical Computing.

Richard J.T., Desfosses R., Romano T.A. & Sartini B.L. 2019. Minimally invasive physiological correlates of intersexual behavior in belugas. Paper presented at the Second International Workshop on Beluga Research and Conservation, 12–14 March, Mystic, CT.

Richard J.T., Robeck T.R., Osborn S.D., Naples L., McDermott A., LaForge R., Romano T.A. & Sartini B.L. 2017. Testosterone and progesterone concentrations in blow samples are biologically relevant in belugas (Delphinapterus leucas). General and Comparative Endocrinology 246, 183–193, doi: 10.1016/j.ygcen.2016.12.006.

Rights J.D. & Sterba S.K. 2018. Quantifying explained variance in multilevel models: an integrative framework for defining R‐squared measures. Psychological Methods 24, 309–338, doi: 10.1037/met0000184.

Robeck T.R., Monfort S.L., Calle P.P., Dunn J.L., Jensen E., Boehm J.R., Young S. & Clark S.T. 2005. Reproduction, growth and development in captive beluga (Delphinapterus leucas). Zoo Biology 24, 29–49, doi: 10.1002/zoo.20037.

Samuels A. & Gifford T. 1997. A quantitative assessment of dominance relations among bottlenose dolphins. Marine Mammal Science 13, 70–99, doi: 10.1111/j.1748-7692.1997.tb00613.x.

Sergeant D.E. 1973. Biology of white whales (Delphinapterus leucas) in western Hudson Bay. Journal of the Fisheries Research Board of Canada 30, 1065–1090, doi: 10.1139/f73-178.

Shane S.H., Wells R.S. & Würsig B. 1986. Ecology, behaviour and organization of the bottlenose dolphIn: a review. Marine Mammal Science 2, 34–63, doi: 10.1111/j.1748-7692.1986.tb00026.x.

Shelden K.E.W., Robeck T.R., Goertz C.E.C., McGuire T.L., Burek‐Huntington K.A., Vos D.J. & Mahoney B.A. 2020. Breeding and calving seasonality in the endangered Cook Inlet beluga whale population: application of captive fetal growth curves to fetuses and newborns in the wild. Marine Mammal Science 36, 700–708, doi: 10.1111/mms.12653.

Smith T.G., St. Aubin D.J. & Hammill M.O. 1992. Rubbing behaviour of belugas, Delphinapterus leucas, in a High Arctic estuary. Canadian Journal of Zoology 70, 2405–2409, doi: 10.1139/z92-322.

St. Aubin D.J. & Geraci J.R. 1989. Seasonal variation in thyroid morphology and secretion in the white whale, Delphinapterus leucas. Canadian Journal of Zoology 67, 263–267, doi: 10.1139/z89-038.

St. Aubin D.J., Smith T.G. & Geraci J.R. 1990. Seasonal epidermal molt in beluga whales, Delphinapterus leucas. Canadian Journal of Zoology 68, 359–367, doi: 10.1139/z90-051.

Urian K.W., Duffield D.A., Read A.J., Wells R.S. & Shell E.D. 1996. Seasonality of reproduction in bottlenose dolphins, Tursiops truncatus. Journal of Mammalogy 77, 394–403, doi: 10.2307/1382814.

Vacquié-Garcia J., Lydersen C. & Kovacs K.M. 2019. Diving behaviour of adult male white whales (Delphinapterus leucas) in Svalbard, Norway. Polar Research 38, article no. 3605, doi: 10.33265/polar.v38.3605.

Vermeulen E., Holsbeek L. & Das K. 2015. Diurnal and seasonal variation in the behaviour of bottlenose dolphins (Tursiops truncatus) in Bahía San Antonio, Patagonia, Argentina. Aquatic Mammals 41, 272–283, doi: 10.1578/AM.41.3.2015.272.

Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York: Springer.

Wilson A.P. & Boelkins R.C. 1970. Evidence for seasonal variation in aggressive behaviour by Macaca mulatta. Animal Behaviour 18, 719–724, doi: 10.1016/0003-3472(70)90017-5.

Xia W., Xie H. & Ke C. 2014. Assessing trend and variation of Arctic sea-ice extent during 1979–2012 from a latitude perspective of ice edge. Polar Research 33, article no. 21249, doi: 10.3402/polar.v33.21249.