Hunger can be taught: Hunger Recognition regulates eating and improves energy balance

Abstract

A set of spontaneous hunger sensations, Initial Hunger (IH), has been associated with low blood glucose concentration (BG). These sensations may arise pre-meal or can be elicited by delaying a meal. With self-measurement of BG, subjects can be trained to formally identify and remember these sensations (Hunger Recognition). Subjects can then be trained to ensure that IH is present pre-meal for most meals and that their pre-meal BG is therefore low consistently (IH Meal Pattern). IH includes the epigastric Empty Hollow Sensation (the most frequent and recognizable) as well as less specific sensations such as fatigue or light-headedness which is termed inanition. This report reviews the method for identifying IH and the effect of the IH Meal Pattern on energy balance. In adults, the IH Meal Pattern has been shown to significantly decrease energy intake by one-third, decrease preprandial BG, reduce glycosylated hemoglobin, and reduce insulin resistance and weight in those who are insulin resistant or overweight. Young children as well as adults can be trained in Hunger Recognition, giving them an elegant method for achieving energy balance without the stress of restraint-type dieting. The implications of improving insulin sensitivity through improved energy balance are as wide as improving immune activity.

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International Journal of General Medicine 2013:6 465–478
International Journal of General Medicine
Hunger can be taught: Hunger Recognition
regulates eating and improves energy balance
Mario Ciampolini
1
H David Lovell-Smith
2
Timothy Kenealy
3
Riccardo Bianchi
4
1
Unit of Preventive Gastroenterology,
Department of Pediatrics, Università
di Firenze, Florence, Italy;
2
Department of General Practice,
University of Otago, Christchurch,
New Zealand;
3
Department
of General Practice and Primary
Health Care, University of Auckland,
Auckland, New Zealand;
4
Department
of Physiology and Pharmacology, State
University of New York Downstate
Medical Center, Brooklyn, NY, USA
Correspondence: Mario Ciampolini
Unit of Preventive Gastroenterology,
Department of Pediatrics, Università di
Firenze, Florence 50132, Italy
Tel +39 055 215744
Email mlciampolini@fastwebnet.it
Abstract: A set of spontaneous hunger sensations, Initial Hunger (IH), has been associated
with low blood glucose concentration (BG). These sensations may arise pre-meal or can be
elicited by delaying a meal. With self-measurement of BG, subjects can be trained to formally
identify and remember these sensations (Hunger Recognition). Subjects can then be trained
to ensure that IH is present pre-meal for most meals and that their pre-meal BG is therefore
low consistently (IH Meal Pattern). IH includes the epigastric Empty Hollow Sensation (the
most frequent and recognizable) as well as less specific sensations such as fatigue or light-
headedness which is termed inanition. This report reviews the method for identifying IH and
the effect of the IH Meal Pattern on energy balance. In adults, the IH Meal Pattern has been
shown to significantly decrease energy intake by one-third, decrease preprandial BG, reduce
glycosylated hemoglobin, and reduce insulin resistance and weight in those who are insulin
resistant or overweight. Young children as well as adults can be trained in Hunger Recognition,
giving them an elegant method for achieving energy balance without the stress of restraint-type
dieting. The implications of improving insulin sensitivity through improved energy balance are
as wide as improving immune activity.
Keywords: energy intake, hunger, energy balance, food intake regulation, prevention, insulin
resistance, obesity, diabetes, inflammation, risks
Introduction
This review outlines the authors’ perspective on the current status and promising
avenues for future research and clinical application of the recognition of hunger
validated by pre-meal low blood glucose concentration (BG). The authors’ work so far
on low BG-associated hunger, the effect of such recognition on food intake regulation,
and its clinical implications as a non-restraint dietary method in managing insulin
resistance and obesity is reviewed.
The theory
Hypothesis: Food intake regulation improves when BG-validated hunger is
recognized.
Prediction: Recognition of BG-validated hunger should lead to improved intake
regulation and homeostatic energy balance as evidenced by improved insulin resistance
and loss of weight in the overweight (OW).
Research strategies
The authors’ investigations have taken the following course:
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International Journal of General Medicine 2013:6
1. Subjective assessment of hunger in infants by trained
carers (MC).
2. Correlation of identified hunger with low BG concentration
in infants (MC).
3. Self-identification of hunger sensations in adults
(DLS, TK).
4. Correlation of identified hunger with low BG concentra-
tion in adults (MC, RB, DLS).
5. Identification of a meal pattern in which hunger and low
BG is present pre-meal for most meals (the Initial Hunger
[IH] Meal Pattern) (MC, RB, DLS).
6. Correlation of the IH Meal Pattern with loss of weight
in the OW and with improved insulin sensitivity (MC,
RB, DLS).
Background
The effects of positive energy balance are well known and
underlie the great scourges of Western industrialized nations
including obesity, diabetes, and heart disease. More than
1.1 billion adults worldwide are OW, and 312 million of
them are obese;
1
obesity has been shown prospectively to be
associated with dietary and lifestyle factors.
2
Dieters’ inability
to lose weight long term by restraining food intake (dietary
restraint) is well known.
3
During dietary restraint-induced
weight loss, appetite-associated blood hormone concentrations
change. These changes are mostly in the direction of appetite
stimulation and persist for at least 12 months.
4
The adverse
effects of excessive nutrient intake extend not only to the
obese. Insulin resistance secondary to positive energy
balance can affect normal-weight (NW) people leading to
cardiovascular disease, type-2 diabetes, hypertension, and
immune disorders. A system for regulating nutrient intake
that does not involve dietary restraint is called for.
Historical perspective on the role
of hunger in food intake regulation
Hunger is an internal stimulus that is influenced by food
intake. Eating in response to hunger has been regarded
as homeostatic and an intermediary step in the process of
food regulation.
5
Workers in psychiatry, psychology, and
pediatrics have independently observed that many people
eat in response to stimuli that are not influenced by food
intake. Stimuli that are not influenced by food intake may
override or obscure hunger and include compelling extrinsic
factors such as highly palatable and heavily marketed food,
6
social factors such as eating in the presence of others,
7
and
intrinsic factors such as emotions.
8–11
Furthermore, people
often interpret a wide range of nonspecific body sensations
as “hunger.”
12
These sensations, poorly identified as an
undifferentiated unpleasant feeling, could include nausea,
pain, or thirst. They can be particularly confusing since they
may temporarily disappear after food intake giving the false
notion that they represent hunger.
Debate continues as to whether the significance of the
hunger sensation must be learned from parents or others, or
whether it is instinctive. Thus “eating in the absence of
hunger” is thought by some workers to result from imperfect
parental instruction.
12–14
Others regard hunger as instinctive
(“intuitive eating”) but forestalled by too frequent eating
and therefore unrecognized, not reinforced, and eventually
forgotten during childhood development.
15,16
Whatever may
be the cause, confusion derived from early childhood about
the perception of hunger is prevalent. In the authors’ view,
this is exacerbated by the widespread practice of imposing
scheduled meals in disregard of infants’ food-seeking
behavior. Habits of food intake, once laid down in infancy,
tend to persist and the habit of eating at set times without
evaluation of current energy availability becomes “normal”
behavior. Thus, even though it may prima facie seem self-
evident that adults know whether they are hungry or not,
in practice many people assume they are hungry when
physiologic hunger is not present, do not perceive physiologic
hunger when it is present, or they may confuse it with some
other experience such as nausea, anxiety, pain, or thirst. The
authors’ investigations indicate that hunger corresponds to a
different physiological condition to that of appetite (the desire
to eat) alone. The desire to eat may occur in the absence of
hunger, but hunger alone represents a state of physiological
preparedness to digest.
Identifying hunger
To help people recognize whether they are indeed
physiologically hungry, two complementary lines of
enquiry were independently followed. Lovell-Smith et al
sought to define the subjective hunger experience precisely
and hence help people to differentiate between hunger
and other experiences.
17
Building on the early work of
Cannon and his contemporaries, hunger was identified as
two sets of subjective experiences. The first is the Empty
Hollow Sensation (EHS). This corresponds to Cannon and
Washburn’s hunger pang, is a physical sensation experienced
in the epigastrium, and indicates readiness to digest.
18
This
physical epigastric sensation is associated with Phase III
contractions of stomach and duodenum.
19
During the interdigestive period the distal stomach is
involved in a recurrent pattern of contractions known as the
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migrating motor complex.
20
Phase III contractions, the final
phase, are complex powerful constrictive and propulsive
movements that occur in the distal stomach and duodenum
during the intermeal interval. It has been suggested that
these contractions have a “housekeeping” effect in clearing
the stomach and small intestine of undigested food particles,
secretions, debris, and microbes thus readying the subject for
food intake. Phase III contractions are likely to be regulated
by gut hormones somatostatin and motilin.
The second subjective physical experience often
associated with hunger is termed inanition. This includes
fatigue, light-headedness, and general weakness. Inanition
is taken to indicate the need for nutrition, but not necessarily
readiness to digest. As indicated above, both the EHS and
inanition are accompanied by, but are distinct from, appetite,
the desire to eat. The desire to eat, when it occurs in the
absence of EHS or inanition may be prompted by any of
the confounding intrinsic or extrinsic stimuli alluded to in
the above introduction. The term IH was coined by author
MC and is either EHS or inanition at their first appearance.
IH correlates well with BG below about 81.8 mg/dL
(4.54 mmol/L).
21
These two approaches to the study of
hunger, subjective clarification, and the discovery of an
objective marker overlap and are mutually supportive.
The relationship between
hunger and BG
Transient declines in BG pre-meal are well recognized,
22–24
and BG decline is associated with hunger.
25
Glucose has
long been considered a prime candidate in the regulation of
energy metabolism, being an exclusive energy source for
the central nervous system and having limited storage, high
turnover rate, and tight regulation.
The initiation of hunger
and eating behavior is the result of a complex interplay
between genetic, psychological, neurological, biochemical,
and hormonal factors. Early single factor depletion models
such as the glucostatic hypothesis of Mayer
26
in which it is
assumed that all physiology and behaviors seek to maintain
a stable glucose have given way to models that recognize
this interplay. Nevertheless, BG is a useful metabolic marker
in training subjects to recognize hunger. BG is taken to
indicate the body’s supply of readily available nutrients
and their ability to quickly provide energy to body tissues.
In a physiologically normal, nondiabetic population, BG
therefore indicates the dynamic state of energy balance. High
BG indicates immediate positive energy balance, while low
BG indicates immediate negative energy balance. It should be
noted that subjects can be trained to recognize hunger without
BG measurement. This method has been successfully used
clinically by one author (DLS) in treating obesity, improving
BG control in diabetes mellitus,
27
and in the management
of some autoimmune diseases (see Implications and Future
Directions, below); however, further work needs to be done
to establish its effectiveness in comparison to concurrent
BG measurement. Training without BG measurement is
simpler to arrange and does not subject the patient to invasive
finger pricks. On the other hand, individuals respond in a
multitude of ways to the question: “What do you feel when
you are hungry?” Interpretation of these responses requires
considerable skill from the trainer/therapist. Thus, although
protocols are under development, this method has the
disadvantage that training is more difficult to standardize.
Concurrent BG measurement provides an objective standard
against which subject and trainer/therapist can assess the
correspondence of future interoceptive sensations. This
is helpful in building confidence in those sensations that
subjects are learning to interpret as hunger, it helps “slow
learners” to find the relevant sensations more readily, it
gives the trainer/therapist an objective “window” into the
subject’s internal world, it helps the trainer/therapist assess
compliance, and helps subjects to correct occasional errors
of perception even months or years after training. All formal
studies reported here have used the concurrent BG method
of training.
Pediatric studies: signicant
reduction in infant diarrhea
Subjective assessment of hunger by carers
The initial impetus for these studies was to identify feeding
patterns that might assist infants in recovering from
malnutrition.
28
Later studies were directed to infants with
troublesome diarrhea. MC questioned whether perhaps
infants were being overfed or fed at scheduled times, not
necessarily when hungry, and were therefore frequently
in positive energy balance. In early attempts (pre-1984) to
recognize hunger in infants, carers were trained to recognize
characteristic signals such as crying (in the first months of
life), mood changes including loss of enthusiasm for playing,
and gestural or verbal requests for food, or searching for food
without any external stimulus. Meals were initiated only
when such signals were exhibited (treated infants). Using this
method, total energy intake, and days with diarrhea among
treated infants decreased significantly, while malnourished
infants recovered body weight.
29
In a further study, compared
with 73 control infants, energy intake and days with diarrhea
among 70 treated infants decreased significantly.
30,31
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Hunger can be taught

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Correlation of identied hunger
with low BG concentration in infants
In the latter study, consent was obtained to gather preprandial
BG measurements in treated infants to ensure that the “on
demand” feeding regime did not put these infants at risk of
hypoglycemia. (It was not considered ethical at that stage
to measure BG in the control infants as no change had been
made to their feeding regimen). It was noted as an incidental
finding that the 70 treated infants showed a significant
decrease in mean pre-meal BG compared to pretreatment.
These preliminary findings argued for a correlation between
food demand and preprandial BG and were the stimulus for
later adult studies in which BG was measured in both treated
and control groups.
Adult studies
Correlation of IH and BG
The method used in all reports is detailed here. Subjects
were asked to withhold food intake for a few hours, and
make note of the physical sensations that they experienced
and which they associated with the need for food intake.
The EHS was the most frequent and recognizable sensation,
followed by inanition. After determining their symptoms,
subjects were trained to measure their own BG by portable
glucometer and thus learned to associate these sensations
with BG concentration. Subjects were encouraged to eat
only when the sensations of IH were present. The principal
investigator phoned each subject at the end of the first day
of training to ascertain any changes made by the subject in
eating pattern. A mean delay of 2 hours (range 0–48 hours)
in meal intake was noted on the first day of training. At
subsequent mealtimes, adults evaluated their physical
sensations according to the BG-correlated experience to help
them assess if their present sensation was indeed hunger or
whether their desire to eat was conditioned by time of day or
other extrinsic factor. Subjects were encouraged to become
familiar with the hunger sensation and to take a meal only
at its first appearance (see Appendix).
The effectiveness of this method in altering eating habits
needs to be spelled out to be fully appreciated. In effect,
subjects stopped eating “automatically.” This means that
they stopped eating according to extrinsic cues and began
eating according to their intrinsic interoceptive awareness of
hunger. The method encourages subjects to make a judgment
on the amount to be eaten such that hunger will appear at
the next mealtime. This is a radically different approach to
other systems of dietary instruction in which emphasis is laid
upon feelings of satiety. In the authors’ experience, subjects
find instructions such as “stop before you feel full” and the
like restrictive and disheartening. Such instructions tend to
be ignored leading to excessive food intake. By contrast the
instruction “start when you feel empty” invites compliance,
since eating when hungry is inherently pleasurable. For
most subjects at the beginning of training, a meal intake of
150 kcal for infants and 300 kcal for adults ensured hunger
at the subsequent mealtime, with adjustments spontaneously
made in either increasing or decreasing energy-dense food
to reach IH at the desired time. In spite of a generally lower
caloric intake subjects reported normal activity and did not
report lowered energy during the intermeal period.
Subjects received information on food energy content,
recommended vegetable intake, and physical activity per
day. The recommended fruit and vegetable amount for adults
was 1 kg/day. The investigators recommended avoiding high
ambient temperatures and wearing excessive clothing as these
tend to slow metabolic rate and delay the appearance of hunger
sensations. They also encouraged normal outdoor and gym
activities. Avoiding snacks was suggested, though earlier than
optimal IH was satisfied with fruit and adequate energy-dense
food if needed. Social obligations such as parties and school
catering were included in planning the intake amount and
timing of the previous and subsequent meals.
Interaction between expert and subject was necessary for
most subjects to interrupt automatic feeding and to stop any
reliance on fullness sensations toward meal end. The process
generally became “second nature” after a few days. The subject
realizes that IH will arise at the desired times when intake is
accurately judged. The intervention may be summarized as an
effortless cessation of automatic feeding and its replacement
by an informed judgment on the amount to be eaten.
Is self-estimation of BG concentration
possible?
If hunger and low BG are correlated, then using the above
method should make it possible for a subject to predict his or
her BG by reference to hunger sensations alone. This was
demonstrated by Ciampolini and Bianchi.
32
In this randomized controlled trial, 158 adults were
randomly assigned to experimental (trained, n = 80) and control
(untrained n = 78) groups. Over 7 weeks the experimental
group were trained to measure pre-meal blood glucose by
glucometer at the earliest feelings of hunger or discomfort
(hence the term “IH”). A 7-week period was chosen to
ensure a high degree of facility in the IH Meal Pattern;
however, the majority of subjects learned the skill within
2 weeks. Subjects were asked to state whether they were or
were not feeling hunger sensations and then estimate on that
basis their pre-meal glucose concentration. Control subjects
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were asked to estimate their glucose levels by referring to a
range of values between the extremes of 60 mg/dL (“intense
hunger”) and 100 mg/dL (“after a satiating meal”). Blood
samples were taken from each group.
Figure 1 shows that even though members of the control
group considered themselves hungry, they were unable to
reliably estimate their blood glucose concentration whereas
members of the trained group, who considered themselves
hungry, were able to do this with remarkable accuracy. The
correlation lines for the “hungry” groups in Figure 1 show
that there was significant correlation between estimated and
measured BG in the trained group (r = 0.92; P = 0.0001) but
not in the control group (r = 0.29; P = 0.06). The subjective
experience of hunger thus appears for most people to be
reliably associated with the objective marker BG, but only
when people are trained to recognize hunger.
Not all subjects reported the EHS in the final session. All
trained and control subjects who did not experience the EHS
estimated their BG to be significantly lower than measured,
with the control subjects performing more poorly than trained
(the estimation errors being 4.8% ± 3.2% and 16.1% ± 11.3%
in the trained and control groups, respectively). The linear
correlation between estimated and measured BG was highly
significant in the trained group that did not experience the
EHS (r = 0.68; P = 0.0001) and not significant in controls
who did not experience the EHS (r = −0.12; P = 0.32). This
difference can be accounted for by trained subjects’ reports
that they were able to recognize subtle cues other than the
EHS, which they found useful in estimating glycemic levels.
These subtle cues included feelings of physical weakness,
difficulty concentrating, impatience, irritability, drowsiness,
and loss of enthusiasm and are the symptoms that are termed
inanition. In other words, recognizing inanition allowed
trained subjects to achieve similar accuracy in estimating
BG as those trained subjects who recognized the EHS
(Figure 2).
Is inanition hunger then? It has been included it in the
definition of IH because the authors consider both the EHS
and inanition are valid signals to start a meal. Do they carry
equal significance physiologically? Probably not, since only
the EHS is accompanied by Phase III gastrointestinal tract
contractions. Although further work is needed to elucidate
the full significance of these signals, it seems likely that the
EHS indicates a readiness to digest that is not necessarily
11010090
Measured blood glucose (mg/dL)
Estimated blood glucose (mg/dL)
80
Control reporting hunger
Trained reporting hunger
7060
40
50
60
70
80
90
100
110
Figure 1 Estimated versus measured blood glucose of trained subjects (hollow
red circles; n = 18) and control (untrained) subjects (hollow black circles; n = 42)
reporting to be hungry at the nal laboratory investigative session.
Notes: Linear correlation was signicant for the trained data (red dashed line;
r = 0.92; P = 0.0001) but not for the control data (black dashed line; r = 0.29, P = 0.06).
Image courtesy of Ciampolini M, Bianchi R. Training to estimate blood glucose and
to form associations with initial hunger. Nutr Metab (Lond). 2006;3:42.
32
85 908075
Measured blood glucose (mg/dL)
Estimated blood glucose (mg/dL)
70
Trained reporting EHS
Trained not reporting EHS
6560
50
60
70
80
90
100
Figure 2 Estimated versus measured blood glucose of trained subjects with
measured blood glucose < 87 mg/dL at the nal session.
Notes: Below this value, 18 subjects reported the EHS (hollow red circles) and
14 subjects reported inanition only but not EHS (lled black squares). These
14 subjects showed an average estimation error of 4.5% ± 3.1% of the measured
blood glucose, which did not signicantly differ from the estimation error of the
18 trained subjects who reported the EHS (3.2% ± 2.4%; P = 0.20). Linear regression
was signicant for the hungry subjects reporting EHS (dashed red line; r = 0.92;
P = 0.0001) but not for those not reporting EHS (solid black line; r = 0.18; P = 0.54).
Image courtesy of Ciampolini M, Bianchi R. Training to estimate blood glucose and
to form associations with initial hunger. Nutr Metab (Lond). 2006;3:42.
32
Abbreviation: EHS, Empty Hollow Sensation.
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indicated by inanition. In the clinical setting, DLS has found
it advantageous to recommend light meals in response to
inanition.
To the authors’ knowledge, this study on the relationship
between BG and hunger is the first in over 60 years to refer
research subjects to their specific subjective symptoms.
Intervening studies, such as that by Bernstein and Grossman,
that appear to show a lack of correlation between low pre-
meal blood glucose and hunger used hunger questionnaires
and hunger rating scales and were therefore subject to all the
limitations of subjects’ untrained interoceptive perception.
33
In the authors’ experience in untrained subjects, adults’
hunger is related to a particular metabolic condition in only
a small number of people. Such studies led to a general
perception that while the brain might be able to detect gross
changes in BG (eg, many diabetic patients can perceive
extreme hypoglycemia), it is unable to detect more subtle
changes.
34
By contrast, this study demonstrates that with
training, people can estimate their pre-meal blood glucose
with accuracy and hence estimate their current energy
availability and energy requirement.
Establishment of a hunger-based
meal pattern
Once the subjective sensation of hunger has been recognized,
the measurement of BG functions as an objective marker
against which the subject can check ongoing pre-meal
subjective sensations. It should be noted that subjects are not
asked to wait until BG is low or at its nadir before checking
their hunger sensations. On the contrary, the subject first
notes the subjective experience then checks it against BG.
BG acts to clarify, verify, and validate what might otherwise
remain as undifferentiated interoceptive sensations.
After a few days of trial and error and sometimes irregular
mealtimes, MC found subjects were able to arrange their
meal size and composition to ensure that IH appeared just
prior to the following meal-time with a mean error of half an
hour in 80% of adults and 90% of children. This is the pattern
of food intake that has been called the IH Meal Pattern.
The next step was to investigate the metabolic consequences
of sustained application of this meal pattern. The initial aim
was to see whether by creating immediate blood energy balance
(avoiding food intake in the presence of high BG and taking
food only in the presence of low BG) it would be possible to
balance total body energy intake to energy requirement long
term, ie, to achieve total body energy balance as shown by
neither increase or decrease of body weight in NW subjects
and loss of weight in OW subjects, over a period of months.
35
It was also desired to see whether creating immediate blood
energy balance would improve insulin sensitivity.
36
Recognizing hunger before each
meal: metabolic consequences
A total of 181 subjects aged 18–60 years were recruited
between the years 1995 and 2000. All subjects entered a
randomized controlled study in which the primary outcome
was weight.
35
One-hundred and forty-nine subjects completed
the full study. One-hundred and forty-three subjects were
included in a second study whose primary outcome was insulin
sensitivity.
36
All subjects were trained in Hunger Recognition
over a 7-week period then followed for a further 3 months.
Weight
Hunger Recognition was associated with signif icant
decreases in body weight and body mass index (BMI) in OW
subjects compared to controls after 7 weeks of training and
after 3 further months of application. BMI decreased from
28.7 ± 3.5 to 26.5 ± 3.5 in the trained group. The decrease
was significant in comparison to controls (P = 0.004) and
in comparison with baseline values of the same group
(P = 0.0001). Multivariate analysis of variance showed
a significant association between training and both BMI
and weight. Pre-meal BG emerged as the most significant
predictor of variations in BMI and body weight. NW subjects
maintained weight overall; however, those trained NW
subjects whose BG was high at recruitment also lost weight
compared to controls.
Insulin sensitivity
Hunger Recognition was associated with signif icant
decreases in insulin and BG peaks, insulin at 60 minutes and
90 minutes during the glucose tolerance test, glycosylated
hemoglobin, and mean pre-meal BG as well as energy intake
and BMI when compared to controls. Insulin sensitivity
index increased from 7.1 ± 4.1 to 9.4 ± 5.2. The increase
was significant in comparison to controls (P , 0.01) and
in comparison with baseline values of the same group
(P , 0.001).
Post hoc analysis
In the latter study it was noticed that at recruitment mean
pre-meal BG ranged from 64.5 mg/dL to 109.9 mg/dL. This
wide distribution suggested that the overall improvement in
insulin sensitivity at study end could be mostly accounted
for by improvements in those subjects whose pre-meal
BG was high at recruitment. Furthermore, it was noted
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that for the week in which each subject kept a diary of
pre-meal BG, the mean confidence interval (95%) around
that subject’s mean pre-meal BG was only ± 3.84 mg/dL.
Thus, although subjects differed widely from each other in
BG concentration pre-meal, their own individual pre-meal
BG concentration varied little. This suggests that many
people eat at an arbitrary BG, not necessarily according
to homeostasis and more likely associated with habit. For
many subjects, energy intake was habitually high and was
likely leading to positive energy balance. Other subjects were
already eating at low BG concentration and thus probably
already eating more or less according to homeostasis.
To test this, the effect of Hunger Recognition on each of
two subgroups – those who at recruitment were found to
eat habitually at a high blood glucose concentration (high
BG) and those who at recruitment habitually ate at a low
blood glucose concentration (low BG) – was analyzed. The
demarcation point that divided the two groups was a mean
pre-meal BG concentration of 81.8 mg/dL (4.54 mmol/L).
This was the BG value that statistically most significantly
divided the two groups.
Stability of mean pre-meal BG
among control low BG and control
high BG subjects
Pre-meal BG among control subjects did not significantly
change during the study. Thirty-one control subjects,
comprising members of both high BG and low BG groups,
maintained a stable mean pre-meal BG after 5 months (from
85.2 ± 8.1 mg/dL to 85.3 ± 7.6 mg/dL). The absolute pre/
post change (increase or decrease) was 6.0 ± 4.6 mg/dL with
a confidence interval (95%) from 3.1 mg/dL to 8.9 mg/dL.
This confirmed the suspicion that left to their own devices,
untrained subjects continue to eat habitually at a given
pre-meal BG concentration which may or may not be in
accordance with homeostasis.
Variation in mean pre-meal BG among
trained low BG and high BG subjects
High BG trained subjects significantly decreased their
mean pre-meal BG (n = 55; pre: 91.6 ± 7.7 mg/dL; post:
81.0 ± 7.7 mg/dL; P , 0.0001; Figure 3). Among low BG
trained subjects (n = 34) pre-meal BG remained relatively
constant (pre: 76.6 ± 3.7 mg/dL; post: 77.2 ± 4.2 mg/
dL; P = 0.499). Trained high BG but not low BG subjects
showed a cumulative energy balance that was negative over
the 5 months of the study as indicated by measurement of
skin-fold thickness. Furthermore, trained high BG but not
65
−35
−25
−15
−5
5
76 79
Baseline
blood glucose (mg/dL)
Blood glucose
difference (mg/dL)
82 85 89 95 103
HBG
LBG
Figure 3 Difference of mean preprandial BG after training versus BG at recruitment
for each trained subject.
Notes: Column height shows 5 months after pretraining mean BG difference in
each trained subject. Signicant increases are indicated by blue bars, signicant
decreases by red bars, and not signicant changes by black bars. Mean BG is
reported in sequentially increasing order at recruitment, not in linear correlation
with segment length on the X-axis scale. The range of mean blood glucose values
at recruitment is indicated by the minimum and maximum values for the rst and
last subjects (large arrows). The vertical dashed line indicates the most signicant
division between subjects who showed no mean BG decrease after training (low BG
group, n = 34) and those who showed signicant decrease of mean BG (high BG
group, n = 55; Chi-squared analysis: P = 0.00001). This threshold blood glucose at
recruitment (demarcation point) is 81.8 mg/dL (4.5 mmol/L) at recruitment in the
randomized controlled studies. Subjects above this threshold accounted for most of
the improvements in weight and insulin resistance.
35,36
Copyright © 2011, Dove Medical Press Ltd. Reproduced with permission from
Ciampolini M, Sifone M. Differences in maintenance of mean blood glucose (BG)
and their association with response to “recognizing hunger.” Int J Gen Med. 2011;
4:403–412.
21
Abbreviations: BG, blood glucose; HBG, high blood glucose; LBG, low blood
glucose.
low BG subjects showed decreased insulin area under the
curve, an index of whole body insulin resistance, decreased
glycosylated hemoglobin, and increased insulinogenic
index,
37
suggesting that low pre-meal BG is physiologically
appropriate for energy needs. Only those subjects whose
energy intake (and BG) was high at recruitment adjusted
their food intake after training. Those for whom energy intake
was already low made little or no adjustment. These data are
consistent with homeostasis and support the notion that the
observed effects could be accounted for mainly by the effect
of the intervention on the high BG trained subjects.
Variation in weight among trained
low BG and high BG subjects
In post hoc analysis of the study on weight, subjects were
divided into four groups according to weight (OW; NW)
based on BMI and pre-meal BG at recruitment. The four
groups were thus: OW high BG, OW low BG, NW high
BG, and NW low BG. As might be expected, after training
OW high BG and OW low BG subjects lost weight and
NW low BG subjects retained weight, further confirming
the homeostatic nature of Hunger Recognition. However,
NW high BG subjects also lost weight.
35
The distinction
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between NW and OW based on BMI is, after all, arbitrary.
It is concluded that some subjects with pre-meal high BG
but so-called “NW” may, in fulfillment of homeostatic
requirements, need to lose weight. For this situation, the term
“hidden fattening” is suggested. This term is chosen since
it conveys the notion that many of the risks of obesity are,
in reality, the risks of insulin resistance. Thus, NW subjects
with insulin resistance are no less subject to the risks of
obesity than the obese. It follows that mean pre-meal BG
and insulin sensitivity may be better predictors of risk than
weight or BMI calculation.
Limitations
Limitations in the studies
The main limitation in the latter two studies was the high
dropout rate among subjects. However, as detailed in
the reports, sensitivity analysis suggests that the dropout
population did not significantly differ from the population
who completed the study. It is also acknowledged that
owing to the limitations imposed by post hoc analysis, the
conclusions with respect to subgroups are indicative rather
than conclusive.
Limitations to BG–hunger correlation
The statistical analysis suggests that a demarcation point
between homeostatic eating and nonhomeostatic eating occurs
at a BG concentration of around 81.8 mg/dL (4.54 mmol/L).
It is tempting to conclude that hunger always occurs below
this BG and not above, and that homeostatic eating can be
ensured by eating only when one’s BG is below 81.8 mg/dL.
However, there does appear to be possible variation in the
BG at which physical hunger appears and hence variation in
the pre-meal BG that might be considered a correct eating
prompt for a given individual. After 7 weeks of training, 77 of
89 trained subjects recognized hunger at a mean pre-meal BG
of ,81.8 mg/dL and 62 maintained low pre-meal BG at the end
of the investigation. Of the 27 remaining who showed high BG
at the end of the investigation, 15 had shown low BG at the end
of their 7-week training period. Their regression to high BG
could be attributed to fading compliance with their instructions
in the final weeks of investigation. The twelve subjects with
high pre-meal BG reported hunger did not achieve low BG
after training. Of these, six were involved in heavy manual
work for 8–10 hours per day in cold ambient conditions. These
subjects’ reports, their insulin, BG area under the curve, and
insulin sensitivity index at the final examination suggested
they complied with the IH Meal Pattern. They reported hunger,
yet their mean pre-meal BG was 86.4 ± 4.0 mg/dL, higher than
the statistically derived demarcation point of 81.8 mg/dL. The
demarcation between compliance and noncompliance with
Recognizing Hunger is statistically strong at 81.8 mg/dL,
but subjects with high energy expenditure might comply
with Recognizing Hunger and yet show higher pre-meal BG
concentration than 81.8 mg/dL. This conclusion is supported
by the significantly higher insulin sensitivity shown by the
six manual workers when compared to the other 21 subjects
(Table 1). At study end they showed higher insulin sensitivity
than the other 21 subjects in the face of a pre-meal BG at
study end that was statistically no different from that of the
other 21 subjects (86.4 ± 4.0 mg/dL for the six high mean BG
subjects and 87.1 ± 5.3 mg/dL for the 21 high BG subjects;
Table 1). These observations suggest that a similar association
might be found with other physiological conditions such as
fever and snacking (ie, intake of small amounts of food within
an hour of BG measurement).
Implications and future directions
of the work
Weight loss
Avoids restraint
Conventional dieting for weight loss generally involves
restraint in food intake whose long-term efficacy is poor.
In the study on weight, control subjects were encouraged to
lose weight in the conventional way. Control OW high BG
subjects decreased energy intake and had indeed significantly
Table 1 Effects of heavy outdoor work
†
in 27 trained subjects
who remained with high blood glucose at investigation end
6 HBG
†
21 HBG
‡
Mean BG (mg/dL)
86.4 ± 4.0 87.1 ± 5.3
Final insulin AUC (mU L
−1
3h
−1
) 124 ± 26 207 ± 99**
Final BG AUC (mg dL
−1
3h
−1
) 536 ± 56 601 ± 82*
Insulin sensitivity index
11.4 ± 2.9 6.68 ± 4.0***
Beta-cell function index
1.29 ± 0.66 1.43 ± 1.22
Notes: Values are expressed as mean ± standard deviation. *P , 0.05; **P , 0.01;
***P , 0.001 (Student’s t-test);
†
six HBG subjects reported full days of heavy manual
labor in an outdoor environment during a cold winter season. Their reports and
measurements suggested that they had complied with the Initial Hunger Meal
Pattern. There were no signicant differences in the ve above parameters at study
end from recruitment (mean BG at recruitment = 86.9 ± 5.3 mg/dL). At study end
they showed higher insulin sensitivity than the other 21 subjects in the face of a
pre-meal BG at study end that was statistically no different from that of the other
21 subjects (87.1 ± 5.3 mg/dL for the 21 subjects);
‡
the 21 HBG subjects included
15 that were low BG after 7 weeks training (at clinical assessment) and six who had
higher mean BG than 100 mg/dL at recruitment.
Copyright © 2011, Dove Medical Press Ltd. Reproduced with permission from
Ciampolini M, Sifone M. Differences in maintenance of mean blood glucose (BG)
and their association with response to “recognizing hunger.” Int J Gen Med. 2011;
4:403–412.
21
Abbreviations: AUC, area under the curve; BG, blood glucose; HBG, high blood
glucose.
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International Journal of General Medicine 2013:6
lost weight at study end from 77.1 ± 16.2 kg to 72.8 ± 15.3
(7 weeks) to 73.7 ± 15.9 kg (5 months). However, all sig-
nificant weight loss took place in the first 7 weeks in these
subjects. Their energy intake during the final weeks of the
study rose significantly (from 1082 ± 291 kcal/day at 7 weeks
to 1343 ± 467; P = 0.02 at 5 months), suggesting dietary
disinhibition.
Not onerous
It is well recognized that food tastes delicious when one
is hungry.
38
This provides positive reinforcement for
compliance with the IH Meal Pattern. Subjects report that it
is not onerous. Compliance is good. OW subjects reported
their hunger was of no greater intensity nor was it more
prolonged than NW subjects. These findings suggest that
Hunger Recognition is effective in promoting weight loss
and provides an appealing alternative to dietary restraint. In
contrast to most dietary systems, this method eliminates the
need to identify sensations of fullness at meal end, a process
that is disheartening and also deceptive, especially for OW
subjects who have high insulin release during meals in the
first weeks of intake limitation and in whom feelings of satiety
are therefore delayed.
Meal by meal adjustment of food intake
In attempting to lose weight, rather than seeking an arbitrary
and often daunting goal weight, subjects following the IH
Meal Pattern receive immediate meal-by-meal feedback
on food intake from their physiological hunger signals.
Food intake is adjusted to accommodate hourly changes in
energy need. Subjects thus eat only when food is required
for energy. Subjects are protected from overconsumption
but are also protected from taking insufficient energy for
day-to-day body functioning as may occur with restraint
diets of ,900 kcal per day. The guilty temptation to eat
more while “on a diet” is removed, which helps provide a
stress-free approach to eating. Subjects are also able to find
their own physiological NW rather than pursue an arbitrary
statistical norm.
Solution to hunger rating
scale woes
The difficulty that untrained subjects have in recognizing
hunger calls into serious question these subjects’
ability to provide accurate or useful data in completing
traditional hunger rating scales. This casts doubt on the
findings of the many studies in which such rating scales
have been used. It must be questioned whether hunger
rating scales have been either sensitive (hunger might be
present but missed as in anorexia) or specific (hunger is
frequently not present but reported).
39–41
After Hunger
Recognition training, the response to the question “Are
you hungry?” is more likely to be a reflection of the
underlying physiological state than before training,
and thus of greater use to the investigator. It should be
noted that in training people to recognize the subjective
symptoms EHS and inanition, supported by objective BG
measurement, no rating scales or visual analog scales are
used. Subjects do not rate hunger, but rather recognize
it. A person either experiences the EHS or does not. This
“either/or” response is, in the authors’ experience, more
useful than the degree to which it is experienced. EHS
arises as a threshold phenomenon, although inanition
arises gradually.
New approach to diabetes
prevention and treatment
Type 2 diabetes mellitus is a devastating outcome of
maintaining positive energy balance. Hunger Recogni-
tion suggests an innovative approach to diabetes pre-
vention and control. In a longitudinal investigation of
13,163 subjects, a fasting plasma glucose of $87 mg/dL
(3.9 mmol/L) was found to be associated with an increased
risk of noninsulin-dependent diabetes mellitus in men
compared to those whose fasting plasma glucose was
,81 mg/dL (4.5 mmol/L).
42
It is interesting that this lat-
ter figure corresponds closely to the demarcation point
which separated the current study’s low BG and high
BG groups. By recognizing hunger pre-meal and eating
only when hunger is present, most of the subjects were
eating at a BG of ,81 mg/dL. The finding that the high
BG control subgroup showed a decreased insulinogenic
index of beta-cell function whereas the high BG trained
subgroup showed an increase in this index supports the
use of Hunger Recognition in diabetes prevention and
treatment. The difference in insulinogenic index between
the two groups was significant, implying higher insulin
production and preservation of beta-cell function in the
trained group. It should be noted that the IH Meal Pat-
tern is diametrically opposite to the prevailing treatment
of diabetes which calls for unvarying caloric intake at
prescribed times during the day. Diabetes control using
this rigid method is notoriously difficult. It is suggested
that the meal-by-meal feedback furnished by the IH Meal
Pattern is a more physiologic approach to this widespread
and difficult disorder.
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Implications of improved
insulin sensitivity
Resolution of the proinammatory state
It is a clinical commonplace that healing is poor in
uncontrolled diabetes. However, prediabetic glucose
metabolism derangement is also associated with immune
disruption and low-degree inflammatory activity. This has
been variously termed the proinflammatory state or subclinical
inflammation,
43–46
and is characterized by the development of
bacterial biofilms (including Helicobacter pylori) inside the
alimentary canal. Subclinical inflammation is implicated in
the gradual development of cardiovascular disease, cancer,
autoimmune diseases, and other disorders.
47
In a randomized
controlled study, Ciampolini et al studied the direct effect of
Hunger Recognition on H. pylori gastrointestinal disease.
48
They trained a group of children and adults (n = 24) aged
60 months to 25 years known to have H. pylori serum
antibodies to recognize hunger (recovery study). Twenty-
three subjects of similar age and serum antibodies formed the
control group. The outcome was assessed after about 1 year.
They also trained another group of healthy children (n = 43)
aged 6–60 months in comparison with 43 healthy control
subjects of the same age (prevention study). Both groups
were assessed at 4, 8, and 12 years postintervention.
The diagnosis of H. pylori gastrointestinal disease is
supported by the presence of serum antibodies whose titer
decreases after successful treatment. In the recovery study,
15 of 24 trained subjects (62.5%) had lost seropositivity for
H. pylori compared to only three of 23 (13%) control subjects
(P = 0.002). In the prevention study, 13 of 43 control subjects
showed seropositivity at study end compared to just two
positive (plus one transient) conversions to seropositivity
among the intervention group. This difference was highly
significant and corresponded to one infection every 176 years
under intervention compared to one infection every 25.6 years
in control subjects.
Gastric emptying and upper gastrointestinal secretions
are known to increase with increasing insulin sensitivity
and are inhibited by high glycemic concentrations.
49–51
Although H. pylori thrive at pH 6–7 (ie, lower than most
bacteria), it cannot survive in the extreme acidity commonly
found, for example, in the fundus of the stomach. In
these conditions, its acid-buffering strategies (such as the
production of ammonia by urease) are overcome. H. pylori
therefore seek a niche in which pH and other factors are
optimal for its survival.
52
Reference has already been made
to the “housekeeping” effect of Phase III contractions
associated with the EHS. Approximately 20% of H. pylori
in the stomach adheres to the surfaces of mucus epithelial
cells partly to inflict cellular damage and inflammation
but also to avoid mechanical clearance.
53
Gastric and
duodenal “sweeping” combined with lowered gastric pH
may account for the inhibition of H. pylori proliferation
found by Ciampolini et al.
H. pylori is just one of a number of intestinal bacteria
that may proliferate when high glycemic concentrations
inhibit gastric motility. Ciampolini et al have shown that in
children with irritable bowel syndrome and celiac disease, the
bacteria count (mainly streptococci and staphylococci) per
gram of mucosa for all subjects was 24 times higher after a
20-hour fast than after a 26-hour fast and for celiac sufferers,
39 times higher. In these subjects, bacteria persisted longer
than the intermeal interval.
54
Other immunogenic bacteria
are implicated in irritable bowel syndrome,
55
colorectal
cancer, and obesity.
56
By helping to avoid glycemic peaks,
clearing the bowel of unwanted bacteria, and preventing the
proinflammatory state, Hunger Recognition may help prevent
a wide range of disorders.
These disorders may extend to the autoimmune diseases.
Fasting has long been recognized as beneficial in rheumatoid
arthritis,
57
but dismissed as an “impractical management
strategy”
58,59
since it is not possible to fast indefinitely.
The IH Meal Pattern is, in effect, a controlled fasting in
which the subject fasts just long enough to allow hunger
to appear. This yields the benefits of fasting without the
disadvantages. The inflammatory marker C-reactive protein
is one indication of the proinflammatory state and shows a
strong positive correlation with insulin resistance. One of
the authors (DLS) has noted dramatic and sustained clinical
improvement, supported by reversion of C-reactive protein
to normal concentrations, among patients suffering from
rheumatoid arthritis
60
and Crohn’s disease after training in
Hunger Recognition as well as sustained improvement in a
case of Graves’ disease.
61
Further work is indicated to further
investigate the role of recognizing hunger in treating these
autoimmune disorders.
May help with psychological stress
Hormones that allow the body to meet stress such as cortisol,
cortisol releasing factor, and serotonin together raise blood
glucose concentration, activate mast cells, monocytes, and
macrophages, increase intestinal permeability, and contribute
to subclinical inflammation – essentially the same effects
as eating in the absence of IH. Recognizing hunger may
therefore help to reverse the deleterious physiological effects
of psychological stress by loss of one or two meals.
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Training should begin early
Training in Hunger Recognition should begin in infancy and
continue through childhood. Young children are commonly
enjoined to “eat everything on their plate” at closely scheduled
mealtimes with no regard to whether the child is actually
feeling hunger. Based on the current findings, this instruction,
often given simply for reasons of social convenience, has
disastrous implications for the health of the child. Habits of
eating learned early tend to persist. It becomes “normal” for
the child to be unable to recognize hunger and hence unable
to evaluate current energy availability. Food choices tend
to be conditioned by external stimuli or emotional internal
stimuli and are made “without full conscious awareness.”
62
To manage the weight gain that ensues, the child may then
be subjected to the stress of restraint-based dieting. Insulin
resistance syndromes have reached pandemic proportions.
63
They are at the root of the most serious illnesses in Western
culture. Early training in Hunger Recognition has the
potential to sidestep habitual overconsumption, the root cause
of most Western illnesses.
Conclusion
The last 60 years have seen huge effort towards teasing out
the physical, neurological, and biochemical pathways that
regulate food intake and energy balance. The motivation
generally is to discover drugs that will help foster energy
balance. While unraveling physiological complexities has
its own fascination, the solution to achieving energy balance
may be as simple as asking people to wait before they eat
until they experience objectively validated hunger.
Resume
What was already known
The role of hunger in regulating food intake for energy bal-
ance had been arrived at by a number of disciplines working
independently.
What had been overlooked
Many people are confused about the perception of hunger.
People cannot be relied upon to recognize hunger without
training. There was a need for greater clarity about the
subjective experience of hunger and an objective “hunger
marker.”
What could not be known
“What it is like to be hungry” could not be known so
long as subjective experience was largely excluded from
the scientific domain. Hunger self-report scales were an
attempt to “objectify” hunger that has enjoyed only limited
success. Returning to hunger as a subjective experience, the
authors suggest that subjective hunger can be well defined
and recognized using blood glucose concentration as an
objective marker of a recurrent physiological condition.
What the authors’ studies have added
Hunger has been differentiated from other misleading and
confounding experiences by clarity of definition and by
association with an objective marker. An association between
the experience of Initial Hunger and low blood glucose has
been demonstrated. It has also been demonstrated that Hunger
Recognition yields improvements in insulin sensitivity in both
normal-weight and overweight subjects and loss of weight
in overweight subjects.
Implications
Hunger Recognition could help people regulate their food
intake and thereby achieve energy balance. Hunger-promoted
energy balance could help alleviate obesity, diabetes, heart
disease, autoimmune disorders, and stress – the great
scourges of Western industrialized societies.
Abbreviations
BMI: body mass index (body weight in kg/height in square
meters); BG: blood glucose concentration; EHS: empty
hollow sensation. The epigastric hunger “pang”; High BG:
high mean pre-meal BG (> 81.8 mg/dL); IH: initial hunger.
Low BG-associated hunger. The EHS and/or inanition at
their first appearance; IH Meal Pattern: a meal pattern in
which IH and low BG is present pre-meal for most meals;
Low BG: low mean pre-meal BG (< 81.8 mg/dL); NW:
normal weight; OW: overweight.
Disclosure
The authors report no conflicts of interest in this work.
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Appendix
Glossary
Appetite The desire to eat
Blood glucose estimation
During training
After training and validation
Writing the expected blood glucose value immediately before measuring the blood sample
by glucometer
Evaluating one’s own current blood glucose value without measurement
Hunger Recognition The meal pattern whereby initial hunger is recognized
Initial hunger Low blood glucose-associated hunger: the empty hollow sensation and/or inanition at their
rst appearance
Initial hunger meal pattern A meal pattern in which initial hunger and low blood glucose is present pre-meal for most
meals
Inanition Fatigue or light-headedness associated with lack of food: “A condition of exhaustion resulting
from lack of nourishment” (denition from: New Shorter Oxford English Dictionary, 1993)
Migrating motor complex A cycle of quiescence and contractions of the stomach and small intestine
Phase III contractions A series of high-amplitude contractions, which form part of the migrating motor complex
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