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971

REVIEW
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Nutrients, satiety, and control of energy intake1


Angelo Tremblay and France Bellisle

Abstract: In the context of the worldwide epidemic of obesity affecting men and women of all ages, it is important to understand
the mechanisms that control human appetite, particularly those that allow the adjustment of energy intake to energy needs.
Satiety is one important psycho-biological mechanism whose function is to inhibit intake following the ingestion of a food or a
beverage. According to the classical theories of appetite control, satiety is influenced by macronutrient intake and/or metabo-
lism. Satiety also seems to be modified by micronutrients, non-nutrients, and some bioactive food constituents. Under optimal
conditions, satiety should be well connected with hunger and satiation in a way that spontaneously leads to a close match
between energy intake and expenditures. However, the current obesity epidemic suggests that dysfunctions often affect satiety
and energy intake. In this regard, this paper presents a conceptual integration that hopefully will help health professionals
address satiety issues and provide the public with informed advice to facilitate appetite control.

Key words: appetite, satiation, obesity, weight loss.

Résumé : Dans le contexte de l’épidémie mondiale de l’obésité touchant les femmes et les hommes de tous âges, il est important
de comprendre les mécanismes de contrôle de l’appétit humain et particulièrement ceux des ajustements de l’apport énergé-
tique aux besoins énergétiques. La satiété est un important mécanisme psychobiologique dont la fonction est d’inhiber l’apport
alimentaire consécutivement à la consommation d’un aliment ou d’une boisson. D’après les théories classiques du contrôle de
l’appétit, la satiété subit l’influence de l’apport en macronutriments et/ou du métabolisme. La satiété semble aussi sous
l’influence des micronutriments, des ingrédients non nutritifs et de quelques constituants alimentaires bioactifs. Dans des
For personal use only.

conditions optimales, la satiété devrait être bien connectée à la faim et à la sensation de plénitude de manière à installer
spontanément une connexion nette entre l’apport et la dépense énergétique. Toutefois, l’épidémie actuelle d’obésité indique
une dysfonction de la satiété et de l’apport énergétique. Dans cette optique, cet article présente une intégration conceptuelle qui
devrait aider, on l’espère, les professionnels de la santé à aborder la question de la satiété et à communiquer au public de sages
conseils pour faciliter le contrôle de l’appétit. [Traduit par la Rédaction]

Mots-clés : appétit, rassasiement, obésité, perte de poids.

Introduction ories of appetite control to recently proposed conceptual paradigms.


In the context of the worldwide epidemic of obesity affecting Other sections are devoted to the role of micronutrients in satiety
men and women of all ages, it is important to understand the and the contribution of non-nutrients and bioactive food constitu-
mechanisms that control human appetite, particularly those that ents. The developing field of satiety induced by the gut microflora
allow the adjustment of energy intake to energy needs. While and its diet-induced variations is also addressed. Finally, we discuss
hunger and numerous environmental cues stimulate eating, sati- the conceptual transfer that can be offered to health professionals.
ety is one important psycho-biological mechanism whose func-
Satiation and satiety: definitions and current
tion is to inhibit intake following the ingestion of a food or a
beverage. The intensity and duration of this post-ingestive inhibi- knowledge
tion are determined by several factors, including the nutrient In mammals, including humans, eating is a patterned activity.
composition of the foods or drinks consumed. Depending on its Under ethological conditions, eating patterns are often deter-
nutrient content, a food exerts a certain “satiating power”; in mined by the intermittent availability of food sources. In many
other words, it has a particular “satiating efficiency”. Enhancing human societies, and particularly in developed areas of the world,
the specific “satiating power” of foods might be a way to increase the supply of food has ceased to be uncertain and food is now
the intensity and duration of the post-meal inhibition of appetite easily available at any time. Even under circumstances of constant
and, perhaps, facilitate the control of energy intake. access to food, however, humans as well as laboratory animals do not
The present review examines classic notions and recent develop- eat continuously. Periodic signals trigger meal onset, whereas other
ments in the field of satiety research. Definitions and methods used signals bring consumption to an end and then inhibit further intake
for the assessment of satiety are presented in the first section. Then, for a certain time before the cycle starts again. Much research in the
we address the role of macronutrients in satiety, from classical the- field of appetite has been devoted to the identification of critical

Received 11 December 2014. Accepted 25 March 2015.


A. Tremblay.* Department of Kinesiology, PEPS, Room 0234, Université Laval, Quebec City, QC G1V 0A6, Canada.
F. Bellisle. Department of Kinesiology, PEPS, Room 0234, Université Laval, Quebec City, QC G1V 0A6, Canada; Unité d’Épidémiologie Nutritionnelle,
UMR U557 INSERM, U1125 INRA, CNAM, Université Paris 13, 74 rue Marcel Cachin, 93017 Bobigny, France.
Corresponding author: Angelo Tremblay (e-mail: angelo.tremblay@kin.ulaval.ca).
*All editorial decisions for this paper were made by Wendy Ward and Terry Graham.
1This paper is the first recipient of the Award for Nutrition Translation, which was granted by the Canadian Nutrition Society in conjunction with Canadian

Science Publishing and the Editorial Staff of APNM.

Appl. Physiol. Nutr. Metab. 40: 971–979 (2015) dx.doi.org/10.1139/apnm-2014-0549 Published at www.nrcresearchpress.com/apnm on 13 May 2015.
972 Appl. Physiol. Nutr. Metab. Vol. 40, 2015

Fig. 1. The Satiety Cascade. CCK, cholecystokinin; GLP-1, glucagon-like peptide-1; PYY, peptide YY. (From Blundell 2010, reproduced with
permission of Academic Press, © 1987 Elsevier.)
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signals that trigger and inhibit intake. It has become obvious, partic- scribed more than 25 years ago (Blundell et al. 1987) and subse-
ularly in the human situation, that such signals are the result of quently modified to integrate new findings (Fig. 1) (Blundell 2010).
complex processes involving physiological as well as sensory, cogni- Sensory factors such as taste, smell, and texture of foods stimulate
tive, environmental, and social factors. intake at the onset of an eating episode; as eating progresses,
Pioneer studies of animal behavior postulated the existence of sensory-specific habituation develops to the ingested foods
two related mechanisms that contribute to the inhibition of food (Hetherington and Havermans 2013; Rolls et al. 1981), while signals
intake: satiation and satiety (Le Magnen 1971). Satiation was de- from the gastrointestinal tract (gastric distention, drop in stomach
fined as a set of complex processes that progressively inhibit the ghrelin, release of hormones and peptides, and others) and the rise
motivation to eat during an eating event. At the beginning of a in glycemia progressively undermine the motivation to eat and bring
meal, eating occurs under the combined stimulatory influences of eating to an end. After satiation is reached for the specific sensory
physiological factors (hunger), sensory cues (olfactory, gustatory, characteristics of a particular food, other foods with different sen-
visual, somesthetic), and numerous other factors linked to the sory aspects retain their stimulatory power and maintain consump-
environment, such as time of day and the social situation (de tion until satiation signals are sufficiently powerful to counter the
Castro 2010). Progressively, as food is ingested, internal inhibitory sensory appeal of all food options. Palatability antagonizes satiation:
influences (sensory, cognitive, gastric, hormonal, neural) develop highly palatable meals in free-living subjects can be 44% larger than
and finally bring ingestion to an end. This mechanism, satiation, neutral or unpalatable meals (de Castro et al. 2000).
determines meal size (Le Magnen 1992). Other factors such as cognitive influences (expectations about the
Satiety is the inhibitory mechanism that takes place after the satiating effects of the foods, beliefs, attention or distraction at the
end of an eating episode and prevents the return of hunger for a time of eating) also contribute to satiation (Bellisle and Dalix 2001;
variable duration. In animal models with constant access to food Bellisle et al. 2004; Brunstrom 2011; Mitchell and Brunstrom 2005).
sources, satiety is recognized as a powerful mechanism that al- Even non-food-related cognitions play a role. For example, a demand-
lows the matching of intake to energy needs via the adjustment of ing cognitive task carried out before a meal has been shown to in-
the postprandial interval to the energy content of the previous crease energy intake at mealtime without increasing perceived
meal (Le Magnen 1992). In the human situation, however, meal- hunger (Chaput and Tremblay 2007). In this context, preprandial
times are set by cultural norms, and satiety mechanisms cannot mental work increases glycemic instability and cortisolemia, which
adjust intake to needs through the modulation of postprandial can disturb satiating effects (Chaput et al. 2008). Evidence of impair-
intervals, although they could do so by inhibiting intake at the ments in satiation has also been observed in short sleepers who
next socially determined eating occasion. In efficient appetite display hormonal adaptations (Chaput et al. 2007; Spiegel et al. 2004)
control, hunger, satiation, and satiety occur in succession and that likely allow increased energy intake to occur before the devel-
allow the adjustment of energy intake to energy needs. The pres- opment of satiation signals (Brondel et al. 2010).
ent epidemic of obesity shows that many things can go wrong in Following the end of a meal, numerous influences contribute to
appetite control when powerful and ubiquitous stimulatory influ- the inhibition of further intake for a certain time (de Castro 2010).
ences override inhibitory mechanisms. The intensity and duration of post-intake satiety depend on the
weight, volume, energy and nutrient content, and energy density
The Satiety Cascade of the meal, among other factors (Keller et al. 2013). Cognitions,
The interplay of post-consumption factors that contribute to the for example beliefs about the satiety value or the energy load of
inhibition of intake is illustrated in the Satiety Cascade, first de- the last meal, also contribute to the modulation of satiety (Cassady

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Tremblay and Bellisle 973

et al. 2012; Wansink et al. 2005). “Sensory-specific satiety” inhibits observation of food intake patterns in laboratory rats whose epi-
the intake of any food sharing the sensory characteristics (the sodic meal intake suggested an alternating hunger/satiety cycle
smell, the taste, and even the shape and the color) of ingested (Le Magnen 1971). The onset and cessation of meal intake clearly
foods in the hours or days following consumption (Hetherington required specific explanatory hypotheses, whereas the observa-
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et al. 1989). Caloric beverages often induce less post-intake inhibi- tion of inter-meal intervals of variable duration suggested the
tion of subsequent intake than comparable solid energy loads, influence of distinct underlying factors.
a satiety deficit that can induce “passive overconsumption” Clearly, some influences are limited to the time of eating, for
(Almiron-Roig et al. 2013; Mattes 2006). example the early responses of the “cephalic phase of digestion”,
Sensory and cognitive factors exert an inhibitory influence after the drop in gastric ghrelin, and environmental cues (social con-
the end of a meal, in parallel with a succession of physiological text, distraction), while others develop well after meal termina-
post-ingestive and post-absorptive signals. Eating with attention tion (post-absorptive metabolic effects). Nevertheless, many satiety
reinforces post-meal satiety (Bellisle et al. 2004), and so does the factors are present at the time of consumption and continue to
cued recall of the foods consumed earlier on the same day (Higgs affect behavior in the hours that follow meal termination: cogni-
et al. 2008). The volume of the previous meal exerts satiety effects tive and sensory factors, the rise and later decline of glycemia,
in the early phase of satiety (owing to gastric distension signals), gastric and hormonal responses, etc.
whereas nutrient contents exert their influence during the post- Despite a certain degree of overlap between satiation and sati-
absorptive phase. Although in humans the duration of the post- ety influences, the distinction of the two concepts is useful. First,
prandial interval cannot be solely determined by the energy load it allows consideration of the specific factors that actually inhibit
ingested at the previous meal, food intake diaries obtained over ongoing consumption as opposed to preventing or delaying inges-
7 consecutive days revealed how previous intake inhibits later tive responses. Second, as the recent literature on claims suggests,
consumption: the weight of food remaining in the stomach at the satiety and satiation processes can be manipulated independently
time of meal onset (in other words, at the end of the satiety cas- by various means to influence total intake and body weight con-
cade of events) is one significant influence determining the size of trol (Blundell 2010). Two approaches or strategies can be envis-
the next meal (de Castro 2010). aged. In the “satiation strategy”, a food can be tailored to provide
As illustrated in the Satiety Cascade, many metabolic satiety less energy for a given weight or volume, for example by the use of
factors originate from the periphery of the organism (Woods ingredients with reduced energy density (Blundell 2010). This
2013). Such signals can be neural, for example when the nutrient strategy would decrease the energy load of meals. An alternative
chemoreceptors and stretch receptors in the gastrointestinal tract “satiety” strategy would aim to strengthen the satiety efficiency of
respond to the presence of food and send signals to the brain. foods via the use of satiety-enhancing ingredients such as fibres
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Hormonal signals such as leptin, insulin, glucagon, and ghrelin and proteins (Blundell 2010).
modulate appetite and satiety. Numerous other “satiety peptides”
and “satiety hormones” are secreted in the gastrointestinal tract Measuring satiety effects
following food consumption: cholecystokinin (CCK), glucagon- The inhibition of intake that follows an eating event can be
like peptide-1 (GLP-1), gastric inhibitory peptide (GIP), and peptide quantified in different ways. One classic approach, used in many
YY (PYY), among others. pioneer studies of free feeding in laboratory animals, consists of
The Satiety Cascade also illustrates how the brain receives and measuring the duration of the spontaneous interval that sepa-
integrates various signals from the periphery of the organism, the rates one meal from the beginning of the next one; satiety is then
“internal milieu”. The brain integrates signals reflecting energy quantified as a duration (Le Magnen 1971). The duration of post-
input and energy expenditures and acts as a “homeostatic regula- meal intervals has also been assessed in human studies of satiety
tor”, adjusting intake to needs to maintain the body energy bal- (Himaya et al. 1997; Melanson et al. 1999). Satiety can also be
ance (Berthoud 2002). One of the key features of the homeostatic measured as the decrease in intake observed at the next eating
regulator is the alternation between hunger and satiety states. occasion following an inter-meal interval of fixed duration. This
Recent data suggest that the homeostatic adjustment of energy approach is typical of the preload paradigm, widely used in both
intake and expenditure becomes more difficult to achieve when animal and human studies (Kissileff 1985). It presents the inhibi-
energy expenditure is significantly decreased by interventions tion of intake in terms of a reduction of amounts consumed rela-
such as a weight-reducing program. Indeed, the management of tive to a control condition. In human consumers, satiety can also
this homeostatic process represents a significant challenge for be assessed as changes in the intensity of various subjective sen-
weight-reduced individuals whose energy expenditure may be de- sations that follow eating, for example hunger, fullness, desire to
creased much below the level predicted by normal variations in eat, or prospective consumption; satiety is then presented as a
body weight (Doucet et al. 2001; Leibel et al. 1995). In this regard, score (Flint et al. 2000). Typically, ratings of hunger, fullness, etc.
we have reported a significant positive relationship between ther- are obtained at regular intervals during the postprandial interval,
mogenic adaptation in post-obese individuals and the increase in from 30 min up to 5 h or more, and reflect the time-related
their hunger level (Tremblay et al. 2013), suggesting that the pre- changes in post-meal appetite.
cise alternation between hunger and satiety states may be more A “Satiety Index” can be computed based on the model of the
difficult after a substantial weight loss. As discussed in the follow- glycemic index (GI) (Holt et al. 1995): the area under the curve
ing sections, a decrease in energy expenditure is also associated (AUC) of satiety ratings (rather than glycemic values) following the
with other biological adaptations influencing satiety. ingestion of a food is measured and compared with the AUC of
satiety ratings obtained following the consumption of a reference
Satiation and satiety: one or two processes? food. The “Satiety Quotient” corresponds to the difference in hun-
Many of the inhibitory influences active in satiety are also pres- ger ratings before and after consumption of a food, divided by the
ent in satiation. It is then legitimate to ask how distinct these weight or the energy load of the food ingested (Drapeau et al.
processes are. There is one obvious behavioral reason to distin- 2007). In many studies, different indices of satiety are used in
guish satiation from satiety: satiation inhibits an ongoing intake combination.
behavior, whereas satiety inhibits all potential ingestive re- For all these aspects of satiety, rigorous measurement princi-
sponses for a certain time. Satiation processes occur while inges- ples have been established (Chapelot 2013). The reliability and
tion is taking place, whereas satiety processes prevent ingestion. validity of experimental tools to assess satiety have been con-
Satiation and satiety processes were originally inferred from the firmed. Both the Satiety Index and the Satiety Quotient have been

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974 Appl. Physiol. Nutr. Metab. Vol. 40, 2015

shown to predict future consumption (Drapeau et al. 2005, 2007). nutrient-specific hierarchy of satiating power, with protein show-
Under controlled laboratory conditions, the reproducibility of satiety ing the highest potency (protein > CHO > fats) (Veldhorst et al.
effects on further ad libitum energy intake is high (Gregersen et al. 2008). This conception finds an echo in current works on the high
2008). The Visual Analogue Scales (VAS) classically used to assess satiating value of protein-rich functional foods (Lluch et al. 2010).
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the intensity of satiety sensations can generate highly reproduc- Several mechanisms could contribute to the high satiating value
ible satiety profiles over repeated presentations of the same meal of dietary proteins. Gastrointestinal responses to dietary proteins
conditions (Flint et al. 2000). A recent analysis of 23 randomized reach the brain via an indirect neural pathway (mainly via the vagus
controlled studies showed that VAS scores recorded for 30 min to nerve) and a direct humoral pathway (Johnstone 2013). The pres-
5 h following the intake of a preload significantly predict energy ence of amino acids in the gastrointestinal tract induces the re-
intake at the next meal (Sadoul et al. 2014). Electronic devices, lease of the satiating hormone CCK, which is released before the
such as the validated hand-held Electronic Appetite Rating System end of the meal and could therefore contribute to both satiation
(Gibbons et al. 2011), now facilitate the acquisition of repeated and satiety (Tomé et al. 2009; Woods 2013). In addition, the gas-
ratings over the postprandial period. Taken together, these obser- trointestinal tract responds to the presence of amino acids by
vations suggest that even if there is no standardized clinical best releasing other anorexigenic substances such as GLP-1 and PYY
practice for the measurement of satiety, the use of VAS scores has (Lejeune et al. 2006; Moran and Dailey 2011).
high relevance. Indeed, as indicated above, it offers a simple and The lipostatic theory (Kennedy 1953) proposes that body weight,
valid tool to predict variations in energy intake in different con- or more precisely the body fat mass, is the regulated parameter.
texts, for example in the management of a diet-based weight- This theory was reinforced by the discovery of the hormone lep-
reducing program. tin, which is secreted by the body adipose tissue and informs the
brain of the current body adiposity (Zhang et al. 1994). A homeo-
Macronutrients and satiety: from classical theories static regulation of the body fat mass by the brain would explain
of appetite to recent conceptual paradigms why attempts at weight loss are often followed by a return to the
pre-dieting body weight.
Early theories of appetite control were built around the notion Experimental and clinical evidence in support of all these the-
of “homeostasis”, or in other words, the stability of the organism’s ories has accumulated. These approaches seem to offer comple-
internal milieu. According to these early perspectives, homeo- mentary perspectives on the control of food intake rather than
static mechanisms trigger and then inhibit intake to ensure that mutually exclusive options.
the intake of energy or nutrients matches bodily needs. These In a more recent paradigm proposed by Flatt (1996), the orga-
theories postulated that some regulated physiological parameter nism’s CHO stores (in the form of liver and muscle glycogen) are
would be actively maintained within a narrow range by the brain.
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the regulated parameter. According to this model, the body’s reg-


Such regulation requires that a signaling mechanism informs the ulatory functions strive to maintain nutrient balance rather than
brain of the current status of the regulated parameter. The brain, energy balance, since “energy” is an abstract notion without phys-
in turn, via a feedback loop, corrects the fluctuations of the regu- iological equivalent. While the fat and protein (muscle) reserves
lated factor by generating the states of hunger or satiety that are abundant in the body, the glycogen reserve varies between
trigger or inhibit consumption. 1.0 and 1.5 times the amount of CHO consumed and oxidized
Many of the classic theories of appetite control have focused on during a typical day, representing about 1000–2000 kcal. Given its
the bodily status of one macronutrient. The glucostatic theory small size in relation to its turnover and the importance of main-
(Mayer 1953) posits that eating is triggered by a decrease in the taining adequate blood glucose levels, the glycogen reserve is reg-
availability of glucose to tissues. Glucosensitive neurons in the ulated within narrow limits by potent mechanisms (key enzyme
brain monitor the blood glucose level and generate signals that activity and hormonal signals) to adjust glucose oxidation to CHO
stimulate or inhibit food intake. According to this view, the in- availability. Glycogen is maintained at levels sufficient to prevent
crease in the blood glucose level after a meal is the critical factor hypoglycemia and maintain usual physical activity. Glycogen
underlying satiety. Experimental manipulations of glycemia in stores vary between individuals and also in response to environ-
human subjects confirmed this hypothesis (Gielkens et al. 1998). mental conditions. For example, they tend to be higher on high-
In contrast to the notion that hyperglycemia induces satiety, en- CHO diets than on low-CHO diets. When the range within which
hanced satiety sensations (van Amelsvoort and Weststrate 1992), glycogen levels are maintained rises, daily fat oxidation is likely to
delayed onset of hunger (Benini et al. 1995), and/or decreased ad decrease, promoting fat accumulation and contributing to the
libitum energy intake (Ludwig et al. 1999) have been reported development of overweight or obesity (Flatt 2004).
following the intake of low-GI foods or meals that induce modest In this regard, the Respiratory Quotient-Food Quotient (RQ-FQ)
post-intake rises in glycemia (Brand-Miller et al. 2002). This field concept described by Flatt (1987) represents an interesting integra-
remains controversial, and conflicting reports suggest that the GI tion of the glucostatic and lipostatic theories of appetite control.
is not a reliable predictor of satiety effects (Geliebter et al. 2013). Accordingly, we have found that after obese individuals have lost
Many factors could potentially account for the diverging results, enough body weight to reach a state of resistance to further loss of
such as the difficulty of predicting the GI of a meal from the GI of body fat, mild hypoglycemia is observed (Tremblay et al. 1999).
its food components (Dodd et al. 2011) or the concurrent influence Moreover, this hypoglycemia is a significant predictor of body
of other nutrients or hormonal responses (Chapman et al. 1998). weight regain in weight-reduced obese patients followed over
Resolving the controversy is beyond the scope of the present re- 1.5 years after weight loss (Boulé et al. 2008). This suggests that the
view, but it is mentioned here as an illustration of the present-day altered glycemia–body fat relationship may make the achieve-
relevance of the glucostatic theory. The impact of carbohydrate ment of satiety more difficult in weight-reduced obese individuals
(CHO) intake on satiety is not limited to the effects of available reaching a lower energy balance status. Even if the RQ-FQ concept
CHO but also depends on the presence of fibre (soluble and insol- is based on substrate (protein, lipid, CHO) gradient effects, its
uble), which has been shown to enhance satiety (Holt et al. 1992). clinical implications are consistent with studies documenting an
The aminostatic theory (Mellinkoff et al. 1956) holds that amino impact of fat loss on hormonal and neural factors influencing
acids and their metabolites are the crucial agents determining satiety and energy balance. For instance, Rosenbaum et al. (2010)
satiety. Early experimental tests showed that the intake of pro- showed that a substantial fat loss promotes a decrease in leptine-
tein, which elevates serum amino acid concentrations, reduced mia and sympathetic nervous system (SNS) activity associated
hunger sensations and food intake in human subjects (Mellinkoff with an increase in hunger. Thus, fat loss modifies appetite con-
et al. 1956). Over the years, evidence has accumulated suggesting a trol via biological effects that must be counteracted if one wishes

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Tremblay and Bellisle 975

to postpone the occurrence of resistance to further loss of body peptides and neurotransmitters that control food intake. Further-
weight/fat. As discussed further in this paper, a major challenge more, beyond a possible calcium-specific appetite control effect, it
for health professionals and food producers is the development of is realistic to hypothesize that the intake of other micronutrients
foods, beverages, and menus favoring appetite-reducing effects could be controlled to permit the maintenance of essential func-
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that can at least partly compensate for the opposite effects in- tions of body homeostasis.
duced by weight loss. Globally, these observations suggest that changes in appetite
Under isoenergetic conditions, the macronutrient content of and food intake can reflect a strategy to maintain homeostasis
foods modulates satiety effects. A hierarchy of satiating power has under conditions of suboptimal micronutrient intake. For obese
been documented (Poppitt et al. 1998). Protein induces the maxi- individuals with an inadequate micronutrient intake, vitamin
mum satiety, followed by CHO and then by fat, for which a rela- and/or mineral supplementation may thus facilitate appetite con-
tive “satiety deficit” has been documented. For example, Lawton trol and compliance with a targeted energy deficit.
et al. (1993) showed that obese individuals displayed significant
overconsumption when exposed to a high-fat meal compared Non-nutrients and bioactive food constituents
with a high-CHO meal. The weak satiety efficiency of dietary fats Some food ingredients cannot be considered nutrients because
could be accounted for by their high energy density and/or their they are not essential to body homeostasis, but they nevertheless
palatability-enhancing effects: in many foods, taste, aroma, and have the potential to influence appetite control. They can act
texture are improved by fat, which stimulates overconsumption peripherally, for example in the stomach or the gut, where they
with relatively poor post-intake satiety. In addition, hormonal affect fullness or transit responses. This is the case with fibres,
factors contribute to the hierarchy of nutrient-associated satiat- which promote satiety at a reduced energy intake level, particu-
ing potency. For example, the hormone ghrelin, an appetite- larly in the context of weight loss programs. In this category of
stimulating substance, is present in high concentrations in the non-nutrients, glucomannan fibres seem to have the best potency
stomach before a meal and drops to a low level at the end of the to affect energy balance, presumably because of their ability to
meal while hunger feelings are totally suppressed. The postpran- bind water and thus promote satiety, inducing a decrease in en-
dial drop in ghrelin is more profound after a CHO-rich meal than ergy intake that results in a substantial weight loss over time
after ingesting dietary fats (Gibbons et al. 2013). (Drapeau and Tremblay 2000).
Alcohol induces lower satiety than food macronutrients, per- Non-nutrient food constituents also include ingredients that
haps because of its liquid form and its disinhibiting effect (Mattes produce centrally mediated effects on energy intake and expen-
1996). In fact, in the context of ad libitum food intake, alcohol diture that resemble psychoactive drug effects. Caffeine can pro-
calories simply add to the energy intake from solids, suggesting duce a substantial decrease in energy intake when administered
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that alcohol intake exerts no inhibitory effect on the ingestion of as a preload in a pre-breakfast decaffeinated coffee beverage
food (Tremblay and St-Pierre 1996; Tremblay et al. 1995). (Tremblay et al. 1988). When combined with catechins, caffeine
significantly increases energy expenditure while also increasing
Micronutrients: a potential role in satiety ambulatory blood pressure (Bérubé-Parent et al. 2005).
Classical theories of appetite control are based on mechanisms Capsaicin is another non-nutrient food constituent that has
related to macronutrient and energy metabolism. However, there been shown to reduce post-intake appetite sensations and subse-
is no reason to exclude a role for micronutrients in the control of quent energy intake (Yoshioka et al. 1999). The measurement of
appetite and energy intake. This viewpoint is consistent with the heart rate variability revealed an association between an increase
existence of a calcium-specific appetite control mechanism (Tordoff in SNS activity and the satiating effects induced by capsaicin
2001): calcium-deprived animals display a preferential calcium in- (Yoshioka et al. 1999). In a more recent study, preprandial intake
take when given the opportunity. Following a 6-week low-calcium of capsaicin, whether in capsules or diluted in tomato juice, in-
diet, rats were able to selectively ingest calcium-containing bev- creased satiety and reduced energy intake (Westerterp-Plantenga
erages to compensate for the imposed deficiency (Paradis and et al. 2005). When tested in combination with caffeine, capsaicin
Cabanac 2005). produced the same effects as when used alone to influence energy
The existence of a calcium-specific appetite is more difficult to intake (Yoshioka et al. 2001). Capsaicin and green tea decrease
demonstrate in human subjects than in animals. This may be due hunger and increase satiety to a greater extent during negative
to the confounding factors that influence feeding behaviors in than during positive energy balance (Reinbach et al. 2009). This is
humans and/or sensory acuity, which might be less pronounced in consistent with the observation that following the completion of
humans than in other animals. As a first attempt to test the valid- a 4-week, very low-energy diet, post-weight-loss fat oxidation was
ity of a calcium appetite in humans, obese individuals with very better sustained during a 3-month observation period with capsaicin
low calcium intake participated in a weight loss program with or supplementation compared with a placebo condition (Lejeune et al.
without calcium plus vitamin D supplementation. The mean weight 2003).
loss over 15 weeks was 5.8 and 1.4 kg in supplemented and placebo
controls, respectively (Major et al. 2009). The use of a buffet-type Gut microbiota and satiety
meal to measure ad libitum energy intake before and after the Beyond their direct digestive effects, macro- and micronutri-
study revealed that most of the between-group difference in en- ents can have an indirect but powerful influence on satiety via
ergy balance was explained by variations in energy/lipid intake. their action on the gut microbiota. In animal models, a high-fat
More recently, Jones et al. (2013) showed that the supplementa- diet induces alterations in the composition of the gut microbiota
tion of calcium in obese low-calcium consumers significantly in- that favor the development of obesity (Neyrinck et al. 2011). Alter-
creased the plasma concentration of the anorexigenic hormone ations in the gut microbiota are also observed when the diet varies
PYY. in its content of many micronutrients and elements. Prebiotics, a
Other micronutrients might exert inhibitory influences on ap- class of nondigestible/fermentable CHO likely to increase bifido-
petite. Obese women on a weight loss program displayed favor- bacteria, decrease food intake in different animal models of obe-
able changes in their appetite sensations when receiving a sity. For example, a 3-week treatment on a standard diet enriched
multivitamin supplement compared with their placebo controls with the prebiotic oligofructose (OFS), which is rapidly and exten-
(Major et al. 2008). As discussed by these investigators, the appetite- sively fermented in the proximal part of the colon, induced a
related effects of multivitamin supplementation might be related decrease in energy intake, leading to a significant decrease in
to the role of some vitamins and minerals in the synthesis of epidydimal fat, in parallel with an increase in the anorexigenic

Published by NRC Research Press


976 Appl. Physiol. Nutr. Metab. Vol. 40, 2015

peptides PYY and GLP-1 and a decrease in the orexigenic hormone Table 1. Impact of a satiating meal course (chicken stir-fry) and a
ghrelin (Cani et al. 2004). control food (fettucine carbonara) on energy intake.
Recently, experimental evidence has been obtained in human Mean energy intake (kJ) Chicken Fettucine Difference
subjects of consistent links between nutrient intake, the gut mi-
Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by DIRECTORATE OF COLDWATER FISHERIES RES on 09/27/15

crobiota, and satiety. Evening meals rich in dietary fibres contain- Energy content of the standardized 2090 2090 0
ing nondigestible/fermentable CHO, such as whole-grain barley meal course
Ad libitum energy intake for the rest 2362 3106 744
kernel, reduce appetite on the following day (Johansson et al.
of the meal (dessert)
2013) in parallel with an increase in the satiety peptide GLP-1 and
Energy intake for the rest of the day 4932 5961 1029
a decrease in fasting serum free fatty acids. These effects are hy-
pothesized to be mediated by gut microbial fermentation of the Note: Adapted from Poortvliet et al. (2007).
indigestible CHO. Consistent with this hypothesis, a fructan pre-
biotic treatment over 2 weeks increased breath-hydrogen excre- gurts), cereals, ready-to-eat meals, and even snack foods (choco-
tion (a marker of gut microbiota fermentation) 3-fold, lowered late bars). Satiety claims may suggest a reduction in hunger or an
hunger ratings, and increased anorexigenic gut peptide concen- increase in the duration of satiety following consumption. Such
trations (GLP-1 and PYY) (Cani et al. 2009). Administration of OFS claims raise a number of issues. First, it is important to assess the
supplements to men and women increased satiety sensations fol- consumer’s understanding of satiety claims, or even satiety itself.
lowing breakfast and dinner and reduced overall energy intake Second, the long-term benefits that can be reasonably expected
(Cani et al. 2006). In a 12-week randomized study, overweight from the use of these products must be ascertained.
adults received either 21 g of OFS per day or a maltodextrin pla- In a focus group study, British consumers described fullness as
cebo (Parnell and Reimer 2009). A decrease in self-reported energy having physical (perception of gastric signals arising from the
intake coincided with a reduction in ghrelin and an increase in presence of food) and psychological (satisfaction, lack of desire to
PYY in the prebiotic group. Accordingly, over the course of the eat) aspects (Murray and Vickers 2009). These notions reflect an
intervention, the OFS group lost weight, whereas control subjects awareness of some important features of the Satiety Cascade, al-
gained weight. Some evidence exists that prebiotic effects on gut though the participants in the study did not spontaneously use
peptide release and appetite might be dose-dependent. In a cross- the term “satiety”. Consequently, it is likely that consumers could
over study carried out in adults receiving a supplement of either correctly understand enhanced satiety claims that have to do with
10 or 16 g of OFS versus placebo for 13 days, a significant effect of post-meal fullness and absence of hunger. A concern has been
OFS on energy intake and gut PYY and GLP-1 responses appeared expressed in the literature about the potential misinterpretation
of satiety claims as slimming claims (Booth and Nouwen 2010).
only with the 16-g dose (Verhoef et al. 2011).
For personal use only.

Indeed, changes in experienced satiety do not necessarily trans-


Our own experience reinforces the idea of a potential role of
late into decreased intake and weight loss. Satiety enhancement is
probiotic bacteria on gut microbiota and energy intake. Specifically,
one influence that could favor weight loss, but it should not be
obese women receiving a supplement of Lactobacillus rhamnosus dur-
equated with it. A study of consumers’ understanding (Bilman
ing weight loss exhibited a decrease in Lachnospiraceae, an im-
et al. 2012) showed sensible expectations in most people, who
portant subclass of Firmicutes (Sanchez et al. 2014). This change
understand that such products can only play a part in weight
was related to a better capacity to adhere to a reduced-energy diet
management and that personal efforts are required. However, the
and achieve significant body weight and fat losses. In a recent
same study also revealed that restrained eaters appear more in-
study, probiotic intake resulted in lower energy intake without
clined to over-interpret satiety claims than peers with lower levels
subjective changes in appetite sensations in humans (Bjerg et al.
of dietary restraint, suggesting a particular vulnerability in cer-
2014).
tain groups of consumers.
At this time, the links between the gut microbiota and satiety
Enhanced satiety can also have potential indirect benefits such
remain controversial. The field is young and it is premature to
as improved hunger management, reduced opportunistic eating
provide recommendations or advice based on the existing evi-
in dieters, reduced hunger dysphoria, and improved compliance
dence, particularly in human subjects.
with goal-directed behaviors, for example the dietary aspects of a
weight loss program (Hetherington et al. 2013). Indeed, it has been
Satiety and potential benefits for consumers
confirmed that higher ratings of appetite are associated with
The short-term effects of nutrients on satiety are well docu- lower weight loss in dieters (Drapeau et al. 2007) and higher levels
mented. At least in the context of one meal or one day, satiety can of perceived hunger predict a poor outcome of weight loss inter-
be influenced significantly by modifying the nutrient content of ventions (Womble et al. 2001) and weight loss maintenance (Pasman
foods or beverages. For example, the appetite-reducing effects of et al. 1999).
an innovative low-fat yogurt enriched with protein (8 g/serving) Enhanced satiety should endure over time and not be counter-
and fibre (2.6–2.9 g/serving) were assessed using a preload para- acted by energy compensation. In a recent note about the substan-
digm under laboratory conditions (Lluch et al. 2010). The test yo- tiation of satiety claims, the European Food Safety Authority
gurt reduced appetite ratings for 2 h after consumption and (EFSA 2012) stated that evidence for a sustained effect on appetite
decreased energy intake at the next ad libitum lunch. Poortlviet ratings with continuous consumption of the food (to exclude ad-
et al. (2007) demonstrated that calorie for calorie, a meal course aptation) should be provided. The long-term maintenance of sati-
focusing on optimal nutrient composition acutely promoted a ety effects is a clear condition for satiety-related weight effects.
substantial decrease in daily energy intake without compromis- However, the maintenance of a satiety effect should be inter-
ing satiety and palatability (Table 1). preted with caution following weight loss in obese individuals.
Less is known, however, about how satiety manipulations Indeed, substantial weight loss favors numerous metabolic changes
might affect intake over the long term and, critically, how the such as mild hypoglycemia (Tremblay et al. 1999), a decrease in
modulation of satiety via nutritional or other factors might affect leptinemia and SNS activity (Rosenbaum et al. 2010), an increase
body weight changes. Would it be possible to use the satiating in hunger (Doucet et al. 2000), and a greater than predicted de-
power of existing foods, or to engineer novel foods to optimize crease in energy expenditure (Doucet et al. 2001; Leibel et al. 1995).
their satiating efficiency, to enhance satiety over the long term Under these conditions, it is clear that the decreased satiety pro-
and facilitate body weight control (Blundell 2010)? Many func- file of weight-reduced obese individuals may be strong enough to
tional foods have been developed to maximize satiety effects counteract the chronic satiating effect of a functional food. This
(Hetherington et al. 2013). Such foods include dairy products (yo- does not imply that the satiety effect of the functional food is not

Published by NRC Research Press


Tremblay and Bellisle 977

Fig. 2. Weight loss maintenance over 26 weeks under 5 diet conditions. Conclusions
At the end of follow-up, a diet with higher protein content and lower
The scientific study of satiety and its determinants is of great
glycemic index significantly improved weight loss maintenance
importance both for the basic understanding of the mechanisms
compared with diets with lower protein content or higher glycemic
of appetite and for applied purposes, particularly in the context of
Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by DIRECTORATE OF COLDWATER FISHERIES RES on 09/27/15

index. The number of participants in each diet condition at each time


the global epidemic of obesity. Beyond the well-established immediate
point is indicated below the figure. LP, low protein; HP, high protein;
effects, the direct and indirect (e.g., via gut microbiota) satiety
LGI, low glycemic index; HGI, high glycemic index. (From Larsen et al.
effects of nutrients should now be investigated over sufficiently
2010, reproduced with permission of N. Engl. J. Med., vol. 363, p. 2109,
long periods of time to determine under what conditions a
© 2010 Massachusetts Medical Society.)
nutrient-induced enhancement of satiety can affect health or
body weight control. Weight loss, the maintenance of a previous
weight loss, and the prevention of weight gain are all legitimate
but very ambitious targets. Clearly, nutrient composition is one
among many factors that affect satiety, and satiety is but one of
the numerous influences that determine energy intake and body
weight. One important challenge for researchers is to establish
how the nutrient-induced modulation of satiety can contribute to
a multidimensional strategy that can ultimately facilitate body
weight control.

Conflict of interest statement


There is no conflict of interest related to the content of this
paper.

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