Review Paper Final Stage_6614452

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Running head: CHANGES IN OLFACTORY HEDONIC APPRAISAL IN PREGNANCY
Etiology of Changes in Hedonic Appraisal of Olfactory Stimuli in First Trimester
Pregnancy
Chalice Walker (6614452)
Judith Fortier (7445393)
University of Ottawa
CHANGES IN OLFACTORY HEDONIC APPRAISAL IN PREGNANCY
Abstract
Changes in olfactory sensitivity during early pregnancy have been theorized to be
linked to changes in olfactory processing at a sensory level. Evolutionary theories have
proposed that phenomena such as nausea and vomiting during pregnancy are due to
heightened objective olfactory sensitivity. Recent research has suggested that this is not
the case, but in fact, olfactory perception decreases in sensitivity during early pregnancy.
Objective olfactory sensitivity does not increase in pregnant women, though their hedonic
odor ratings and strong food aversions indicate a change in subjective olfactory
processing at a cognitive level (Köbel N. et al., 2001). Endocrine changes and its effect
on neurological structures linked to cognitive olfactory processing linked to hedonic
appraisal of odors are discussed.
Keywords: hyperemesis gravidarum, hedonic appraisal, human chorionic
gonadotrophin.
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Etiology of Changes in Hedonic Appraisal
of Olfactory Stimuli in First Trimester of Pregnancy
An astonishing number of physical and physiological changes occur while women
are pregnant. These changes are the most obvious to women in early pregnancy as a
result of the critical development that occurs during this period (Profet, 1988).
Perceptual changes that occur in pregnancy are widely accepted to have adaptive roles in
limiting the number of teratogens that the fetus is exposed to, which may limit or affect
its development. The olfactory perceptual system is one of the systems that are altered
due to physiological changes that occur during pregnancy. Olfactory sensitivity and
processing has been thoroughly studied in pregnant women and changes that onset in
pregnancy have been observed. Research on olfactory perceptual changes is relevant
because of the connection that it has with hyperemesis gravidarum, also known as nausea
and vomiting during pregnancy. The aim of this review paper is to evaluate the literature
concerning the olfactory perceptual changes that occur during early pregnancy and the
etiology of these changes.
Literature Review
Hyperemesis gravidarum symptoms are observed in 50% to 80% of women
across cultures during the first trimester of pregnancy (Swallow, 2005). To investigate
this phenomenon further, researchers have focused mainly on the changes in
chemosensory perceptual sensitivity namely taste and smell. Much of the research done
before and during the 1990’s suggested that nausea and vomiting during pregnancy were
mechanisms of defense against teratogens, which are defined as toxins and dangerous
substances that could be harmful for the fetus during the critical period of development in
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the first trimester (Profet, 1988). Consequently, it was proposed that pregnant women
experience a modification of their olfactory sensitivity in order to detect a lower
threshold of chemical toxins in their environment. An example of this kind of research
found that olfactory aversion is stronger towards specific odours such as rum, coffee and
cigarette smoke (Nordin, 2004). Pregnant woman perceive these smells as particularly
stronger than normal. It is broadly accepted that the chemicals in cigarette smoke and
alcohol may endanger the fetus, thus it was believed the heightened olfactory aversion to
these odours is an adaptive process that encourages women to avoid these substances
during pregnancy (Kölble, 2001).
Objective versus Subjective Olfactory Perceptual Changes
It should be noted again that pregnant women considered themselves as more
sensitive to odours during early pregnancy (Hummel, 2002). Current research conflicts
with this report, as results show that objective olfactory sensitivity appears unchanged
and may even decrease in pregnant compared to non-pregnant women (Hummel, 2002;
Kölble, 2001; Swallow, 2005). This phenomenon can be observed in Figure 1. Swallow
(2005) demonstrates only a slight decrease in perception of the pleasantness of both safe
and unsafe odours. This raises the question of how women can “feel” as though they have
become more sensitive to olfactory stimuli, when their objective olfactory sensitivity
remains unchanged, These results bring into question theories concerning the adaptive
nature of perceptual changes that occur in early pregnancy.
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Figure 1. Ratings of pleasantness of odors for safe and potentially harmful
compounds. [- - - - -] non-pregnant women; [— - —] men; ——pregnant women.
Increasing pleasantness = low scores, decreasing pleasantness = high scores. (Swallow,
2005, p. 60).
The key to the conflict mentioned above, lies in whether objective or subjective
perception is assessed. Odour discrimination and odour identification are objective,
quantitative methodologies used to assess objective olfactory sensitivity. Hedonic
questionnaires using Likert scales assess subjective olfactory experiences and qualitative
olfactory sensitivity (Hummel, 2002 & Kölble, 2001). Leslie Cameron’s study (2007) on
olfactory hedonics, or pleasantness, found that “pregnant women in their first trimester
rated odours as more intense than non-pregnant women” and “pregnant women in their
first trimester rated odours as less pleasant than non-pregnant women”. Hedonic
questionnaires involve the presentation of an odour after which the subject rates the
pleasantness (the highest score on the Likert Scales) or unpleasantness (the lowest score)
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of the odour (Hummel, 2002). The sensitivity of olfactory system can be problematic to
test and measure since it is such a highly subjective system; odours are linked to the
subject’s internal thoughts and feelings about the odour. The subjectivity of such methods
are criticized as being unreliable given that individuals often have varying appraisals of
the hedonics of certain odours (Powell, 2013).
The above findings, concerning the variances in hedonic appraisal and not in
objective sensitivity between pregnant and non-pregnant subjects, led researchers to
investigate the causes of olfactory perceptual changes in pregnancy. Data suggests that
the major difference between pregnant and non-pregnant women’s olfactory perception is
the hedonic ratings of odours, not olfactory sensitivity differences. This research
indicates that the changes must occur in mechanisms of perceptual processing rather than
the olfactory sensory receptors, and that this change occurs significantly more in the first
trimester (Leslie Cameron, 2007).
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Figure 2 . Hedonic rating of coffee (mean±SD) in 46 non- pregnant controls and
38 pregnant women. Measurements were taken at sessions 1 (12th week), 2 (21st week),
and 3 (36th week) during pregnancy, and 7 weeks after delivery (session 4). Significant
differences are only observed between the first trimester of pregnant women and their
non-pregnant counterparts (Ochsenbein-Kölble et al., 2007, p.12).
Hedonic assessments are highly subjective and subjective appraisal is linked to
cognitive processing. This indicates that olfactory perceptual changes in pregnant women
may be the result of changes in the cognitive information processing systems (Hummel,
2002 & Nordin, 2005). Studies by Kölble (2001) and Leslie Cameron (2007) suggest that
changes in cognitive olfactory processing in pregnancy result from strengthened
connections between the olfactory system and the limbic system, the neurological
structure responsible for processing emotional information.
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Discussion
As explained above, there is no objective increase in the ability to detect olfactory
stimulus in pregnant women in their first trimester. In fact, their ability to detect and
identify olfactory stimulation may decrease in early pregnancy. They do however selfreport from their experience an increased ability to detect olfactory stimuli than before
they became pregnant (Ochsenbein-Kölble et al., 2007). This may be for a number of
reasons. Most likely, they have stronger reactions to detected olfactory stimuli than their
non-pregnant counterparts, particularly stronger aversive reactions to adverse stimuli
(Zald and Pardo, 1997). This increase in the emotional component to olfaction may lead
women to believe that their objective olfactory perceptual abilities increased in
sensitivity.
If the olfactory change in women is not at the sensory level of olfactory
perception (for example, an increase of olfactory receptor density), what neurological
changes in pregnant subjects lead to their altered perceptual experience? This is a
difficult question to answer, due to the number of endocrine changes that correlate with
the beginning of pregnancy. It is most likely that endocrine changes, due to pregnancy,
affect the olfactory processing network in a way that alters the perceptual experience of
the individual. A case will be built for a possible mechanism behind these changes in the
remainder of this paper.
Nature of Olfactory Neurological Pathways and Structures
Olfactory processing involves a complex network of neurological structures. In
order to understand the effect that the changes in hormone balances have on olfactory
processing, it is critical to identify structures that are involved. The sensory pathway of
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the olfactory system runs through the olfactory bulb, which projects the olfactory tract to
a variety of structures. These structures include the anterior olfactory nucleus, the
olfactory tubercle, the piriform cortex, the entorhinal cortex and the amygdala. The
entorhinal cortex sends projections to the hippocampus, which relays information further
on to the orbitofrontal cortex (Chaudhuri, 2011). For the purposes of this review, we will
focus solely on changes in a number of these structures that belong to the limbic system,
particularly the amygdala and hippocampus, due to these structures’ particular roles in
hedonic appraisal.
The amygdala is highly connected to the processing of the hedonic valence of
olfactory stimuli. Zald and Pardo (1997) conducted a study using PET neuroimaging to
observe amygdala activity under conditions of varying olfactory adhesiveness. This study
showed that as hedonic valence ratings decreased (i.e. as olfactory stimuli became more
aversive in nature), amygdala activity increased significantly. This demonstrates
significant relationship between hedonic assessment of olfactory stimuli and the limbic
system. This also supports the claim that if hormonal changes due to pregnancy influence
changes in amygdala activity, the hedonic appraisal of olfactory stimuli must necessarily
also change.
Correlations in Endocrine and Olfactory Hedonic Appraisal Changes
Pregnancy is associated with a vast number of hormonal changes, which
undoubtedly are related to changes in perceptual processing. The first major change in
pregnancy is a great increase in Human Chorionic Gonadotropin (HCG), which peaks at
around eight weeks gestation and decreases slowly over the course of pregnancy. This
increase is highly correlated with the first trimester, indicating that it likely that changes
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that occur only in the first trimester are at least partially due to the increase in HCG
levels. There is slow gradual increases in estrogen and progesterone levels throughout the
course of pregnancy, progesterone decreasing slightly near the time of parturition.
Figure 3. Relative levels of Human Chorionic Gonadotropin,
Estrogen and Progesterone throughout the course of pregnancy
(Marghescu, 2014).
Galea et al. (2008) have conducted extensive research on endocrine influence on
cognitive processing. They demonstrate the effects of estradiol, one of the three
circulating forms of estrogen, on the limbic system, specifically the hippocampus. It was
observed that estrogen has a great effect on neurogenesis and proliferation in the
hippocampus, increasing neural density and activation in this structure. Increases in
estrogen, like those associated with the progression of pregnancy, are also known to
facilitate an increase in amygdala activity (Innes, 1970). This result is interesting because
since estrogen increases consistently through the course of pregnancy, necessitating that
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amygdala activity also increases through the course of pregnancy. Thus, it cannot be
estrogen or the amygdala activity that are solely responsible for the changes in hedonic
appraisal in first term pregnancy, because their levels and activity increase past the first
trimester. More likely it is endocrine changes that are isolated to the first trimester that
cause the subjective changes in olfactory sensitivity that occur in the first trimester.
Avenues for Future Research
Human Chorionic Gonadotropin (HCG) is a hormone that increases and decreases
dramatically in the first trimester, with its peak being at 12 weeks (Furneaux, 2001); the
same week that hedonic sensitivity is at its peak (Ochsenbein-Kölble et al., 2007).
Furneaux et al. (2001) demonstrate that higher HCG levels are positively correlated with
hyperemesis gravidarum (2001). The etiology of this process, and the relationship
between HCG and hedonic appraisal is still unknown (Furneaux et al., 2001). Due to the
known relationship between hedonic sensitivity and the limbic system, a valuable avenue
for future research is the relationship between HCG and the limbic system. This
relationship could be studied by a neuroimaging study that assessed limbic system
activity in pregnant individuals with varying serum HCG levels. Also limbic system
activity at experimentally induced increases in HCG could provide valuable information
to neuroscientists concerning the causational effects of endocrine changes in limbic
activity. This study could also be paired with hedonic assessment of various foods under
differing serum levels of HCG. These are excellent avenues for future investigation.
Conclusion
In conclusion, research shows that it is not an increase in objective olfactory
perception that occurs in pregnant women in their first trimester, but a change in
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subjective olfactory response mechanisms and hedonic appraisal. Changes in the neural
networks that process olfactory information, like the limbic system, occur due to major
endocrine changes that occur in pregnancy, and it is these neural changes that lead to the
changes in hedonic appraisal. The changes in hedonic appraisal are the most dramatic
during first term pregnancy, leading us to investigate endocrine changes that are isolated
to first term pregnancy. Human Chorionic Gonadotropin levels are significantly increased
during first trimester pregnancy, making it a likely contributor to changes in limbic
activity and hedonic appraisal during pregnancy. The etiology of the changes in hedonic
assessments is still unknown, though it is likely related to an increase in HCG levels.
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