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“We are what we eat.” In a way, this quote by the German philosopher Ludwig Feuerbach (1804–1872) also applies to what we feed our offspring: the aroma profile of breast milk reflects a mother's eating habits [1, 2] and can thus influence the preferences of her children for different foods [3–7].

The molecular foundation of what might be sensory imprinting in early childhood was investigated by means of a curry dish, in a recently published intervention study. It was conducted at the Chair of Aroma and Smell Research at the Friedrich-Alexander University Erlangen-Nürnberg (FAU), headed by Professor A. Buettner, in cooperation with the Chair of Food Chemistry and Molecular Sensory Science at the Technical University of Munich (TUM), headed by Professors T. Hofmann and C. Dawid [8, 9]. The study investigated the transfer of odor- and taste-active compounds and analyzed how metabolic processes influence the composition of breast milk. This could shed light on processes of early childhood imprinting and, possibly, the resulting preferences of individuals, which in turn may be associated with health advantages or disadvantages (e.g. [10]). Such research projects also enable in-depth investigation of human digestive, metabolic and excretory processes that are closely health-related (e.g., [11]).

Previous studies have already shown the transfer of specific aroma compounds and their metabolites into breast milk, as in the case of sulfur-containing substances in garlic [12], ramson [13] and terpenes such as 1,8-cineole which is also called eucalyptol due to its eucalyptus-like odor [14]. Based on these findings, the aim of the consumption study presented here, was to comprehensively study the spectrum of compounds and metabolites that may influence sensory development in infants. Due to its complex odor and taste profile a curry dish was selected for this purpose. This allowed the investigation of a wide range of chemosensorially active target compounds in breast milk.

Chemosensorially active target compounds and aim of the study

Chemosensorially active substances include odor- and taste-active substances as well as so-called trigeminally active compounds. The volatile odor-active compounds reach the olfactory mucosa either orthonasally, i.e. via the nose, or retronasally via the throat when food is consumed. In the olfactory mucosa their interaction with G-protein coupled receptors evokes an olfactory perception. In contrast to odor compounds, there are many non-volatiles among tastants, for example elemental ions, amino acids, sugars and alkaloids. Our salty and sour senses of taste are caused by interaction with ion channels, whereas sweet, bitter and umami are caused by interaction with G-protein coupled receptors. Trigeminal compounds, on the other hand, are perceived by the trigeminal nerve (Nervus trigeminus) and evoke cooling, pungent or similar sensory perceptions. A compound may, for example, elicit an odor and taste perception while seeming to be cooling, hot or pungent, i.e. it is perceived multisensorially.

Fig. 1 Study design. After consumption of a curry dish, donated milk and urine samples were analyzed for chemosensorially active compounds and their metabolites. Additional excretion may occur via breath and the skin (not shown here).

Sensory-analytical methods can be used to characterize chemosensorially active compounds in foods as well as their transition into breast milk. Chemosensorially active compounds can be distinguished from other compounds by combining chemical and human sensory analysis. In both gas chromatography-olfactometry/mass spectrometry (GC-O/MS) and liquid chromatography-taste dilution analysis/mass spectrometry (LC-TDA/MS), the human nose and tongue, respectively, act as a detector.

Odor- and taste-active substances are mostly metabolized along their path through the human body. Odorants are excreted via urine, skin and breath in addition to breast milk, tastants primarily via urine. These excretions can be used to identify metabolites and thus to characterize metabolic processes of chemosensorially active compounds in the body. For example, 1,8-cineole is excreted via diverse body fluids that contain distinct metabolic products [14–16]. Functionalization and conjugation are two of the biochemical processes that odor compounds can undergo during metabolization [17]. In the study presented here, metabolites in urine were examined in direct comparison with breast milk. This serves to elucidate differences in metabolism and excretion of individual chemosensorially active compounds from the curry dish (Fig. 1).

Standardization and characterization of the curry dish

Initially, a standardized curry dish was established and characterized. The curry spice powder used, contained coriander seeds, cumin seeds, turmeric, dried red chili peppers, fenugreek seeds, black pepper, cinnamon sticks, green cardamon, curry leaves and cloves. A sauce was prepared from the curry spice, which was served with rice [8]. The sensory properties of the curry spice powder were described by a sensory panel as coriander-like/soapy, lovage-like, citrus-like, clove-like, pepper-like, ginger-like, eucalyptus-like, turmeric-like, cooling, cinnamon-like and pungent. The aroma compounds 1,8-cineole, linalool, cuminaldehyde, furaneol, eugenol, sotolone, vanillin and cinnamaldehyde were identified and quantified as major constituents using isotope dilution analysis and solvent assisted flavor evaporation (SAFE) with subsequent GC-O/MS analysis. Capsaicin, piperine and 6-gingerol, identified as the major agents of the pungent sensory impression, were quantified on an LC-MS/MS instrument [9].

Detection of linalool, 1,8-cineole and piperine

Fig. 2 Molecular structures of compounds detected in breast milk

Significant sensory changes were perceived in the breast milk up to two hours after the intervention, even though the overall aroma intensities were very low. In particular, a bergamot-like odor was noticed, which could be attributed to linalool passing over into the milk. To our knowledge, this study is the first report of its transfer into breast milk. In addition, low concentrations of 1,8-cineole and piperine were detected throughout the sampling period (see Fig. 2). None of the other constituents showed significant transitioning into breast milk. Estimations of the transition rates into breast milk of nursing mothers ranged from 2 to 4 x 10–4% for linalool, 0.4 to 8 x 10–2% for 1,8-cineole and 0.5 to 2 x 10–2% for piperine. The amounts varied greatly between individuals and showed compound-specific transition patterns. This indicates disparate metabolization of the substances by the different participants, as well as distinct metabolic processing of the individual compounds themselves.

The answer to the question of whether an infant perceives chemosensorially active compounds at all is determined primarily by the concentration of these compounds in the breast milk. Odor and taste threshold concentrations for the individual constituents, as determined by the study’s sensory test panel, suggest a stimulation of sensory impressions in the infant to only be conceivable for linalool and 1,8-cineole. Piperine remained below the threshold for sensory perception at all times. Nevertheless, it cannot be excluded that infants sensorially perceive piperine, since the thresholds were determined by adult panelists, and infants might have a more sensitive sensory perception [18, 19]. Moreover, the interference between different chemosensorially active compounds might enhance the perceptibility of a compound beyond its individual threshold [20].

Conclusion and outlook

Infants might sensorially perceive chemosensorially active substances in milk. This could be the basis for early childhood imprinting by odor and taste impressions and their multisensory connection. Chemosensorially active compounds can also have physiological (e.g., anti-inflammatory or antioxidant) effects. Therefore, it is important to characterize active compounds and their metabolites in subsequent studies to understand their mechanisms of action in the maternal metabolism and as constituents of breast milk. Chemosensorially active compounds may elicit bioactivity beyond odor and taste.

Acknowledgement

This study was funded by the German Research Foundation (DFG) as part of a collaborative project between the Friedrich-Alexander-Universität Erlangen-Nürnberg and the Technical University of Munich. We thank all participants for their cooperation in the study. ________________________________________________________________________________________

Category: Food Chemistry | Aroma and Smell Research

Literature:
[1] Mennella JA, Beauchamp GK. Maternal Diet Alters the Sensory Qualities of Human Milk and the Nursling’s Behavior. Pediatrics. 1991 Oct;88(4):737-44
[2] Forestell CA, Mennella JA. The Relationship Between Infant Facial Expressions and Food Acceptance. Curr Nutr Rep., 2017 Jun;6(2):141-147. DOI:10.1007/s13668-017-0205-y
[3] Mennella JA. Mother´s Milk: A Medium for Early Flavor Experiences. J Hum Lact. 1995;11(1):39-45
[4] Mennella JA. Daniels LM, Reiter AR. Learning to like vegetables during breastfeeding: a randomized clinical trial of lactating mothers and infants. Am J Clin Nutr. Jul. 2017;106(1):67-76. DOI:10.3945/ajcn.116.143982
[5] Hausner H, Bredie WLP, Mølgaard C, Petersen MA, Møller P. Differential transfer of dietary flavour compounds into human breast milk. Physiol Behav. 2008 Sep 3;95(1-2):118-24. DOI:10.1016/j.physbeh.2008.05.007
[6] Maier AS, Chabanet C, Schaal B, Leathwood PD, Issanchou SN. Breastfeeding and experience with variety early in weaning increase infants’ acceptance of new foods for up to two months. Clin Nutr. 2008 Dec;27(6):849-857. DOI:10.1016/j.clnu.2008.08.002
[7] Denzer MY, Kirsch F, Buettner A. Are Odorant Constituents of Herbal Tea Transferred into Human Milk? J Agric Food Chem. 2015 Jan;63(1):104-111. DOI:10.1021/jf504073d
[8] Debong MW et al. Dietary Linalool is Transferred into the Milk of Nursing Mothers. Mol Nutr Food Res. 2021 Dec;65(23):2100507. DOI:10.1002/mnfr.202100507
[9] Diaye KN et al. Dietary Piperine is Transferred into the Milk of Nursing Mothers. Mol Nutr Food Res. 2021 Dec;65(23):2100508, DOI:10.1002/mnfr.202100508
[10] Ross AC, Caballero BH, Cousins RJ, Tucker KL, Ziegler TR. Modern nutrition in health and disease: Eleventh edition. Wolters Kluwer Health, 2012
[11] Moszak M, Szulińska M, Bogdański P. You Are What You Eat – The Relationship between Diet, Microbiota, and Metabolic Disorders – A Review. Nutrients. 2020 Apr;12(4):1096. DOI:10.3390/nu12041096
[12] Scheffler L. Characterization of biotransformation and excretion processes if garlic and ramson volatiles in humans: Influence on the aroma and metabolite profile of breast milk and urine. Dissertation, FAU. 2019. https://nbn-resolving.org/urn:nbn:de:bvb:29-opus4-111761
[13] Scheffler L, Sharapa C, Amar T, Buettner A. Identification and Quantification of Volatile Ramson-Derived Metabolites in Humans. Front Chem. 2018 Sep; 6:410. DOI:10.3389/fchem.2018.00410
[14] Kirsch F, Buettner A. Characterisation of the Metabolites of 1,8-Cineole Transferred into Human Milk: Concentrations and Ratio of Enantiomers. Metabolites. 2013 Jan;3(1):47-71. DOI:10.3390/metabo3010047
15] Horst K, Rychlik M. Quantification of 1,8-cineole and of its metabolites in humans using stable isotope dilution assays. Mol Nutr Food Res. 2010 Oct;54(10):1515-1529. DOI:10.1002/mnfr.200900528
[16] Schaffarczyk M, Balaban TS, Rychlik M, Buettner A. Syntheses of Chiral 1,8-Cineole Metabolites and Determination of Their Enantiomeric Composition in Human Urine After Ingestion of 1,8-Cineole-Containing Capsules. ChemPlusChem. 2013;78(1):77-85. DOI:10.1002/cplu.201200253
[17] Rychlik M. Metabolism of odorants in humans. In: Andrea Buettner (eds) Springer Handbook of Odor. Springer International Publishing Switzerland 2017:75-76
[18] Loos HM et al. Responsiveness of Human Neonates to the Odor of 5α-Androst-16-en-3-one: A Behavioral Paradox? Chem Senses. 2014 Oct;39(8):693-703. DOI:10.1093/chemse/bju041
[19] Loos HM et al. Responses of Human Neonates to Highly Diluted Odorants from Sweat. J Chem Ecol. 2017 Jan;43(1):106-117. DOI:10.107/s10886-016-0804-x
[20] Delwiche JF, Heffelfinger,A.L. Cross-Modal Additivity of Taste and Smell. J Sens Stud. 2005 Dec;20(6):512-525. DOI:10.1111/j.1745-459X.2005.00047.x

Date of publication: 19-Jul-2022

Facts, background information, dossiers

  • sensory sciences
  • early childhood imprinting
  • odor-active substances
  • taste-active substances
  • breast milk
  • metabolites
  • metabolic processes
  • chemosensorially ac…
  • trigeminally active…
  • GC-O/MS
  • LC-TDA/MS
  • isotope dilution analysis
  • solvent assisted fl…
  • sensory panel

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