|Year : 2017 | Volume
| Issue : 5 | Page : 610-615
Comparison between olfactory function of pregnant women and non-pregnant women in reproductive age group in Ibadan, Nigeria
U Nwankwo1, AJ Fasunla1, A Oladokun2, OG Nwaorgu1
1 Department of Otorhinolaryngology, College of Medicine, University of Ibadan and University College Hospital, Ibadan, Nigeria
2 Department of Obstetrics and Gynaecology, College of Medicine, University of Ibadan and University College Hospital, Ibadan, Nigeria
|Date of Acceptance||15-Nov-2016|
|Date of Web Publication||17-May-2017|
A J Fasunla
Department of Otorhinolaryngology, College of Medicine, University College Hospital, PMB, Ibadan
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Pregnant women require normal olfactory function in order to develop good appetite for healthy living and normal fetal development. This study was carried out to investigate and compare olfactory function of pregnant women with non-pregnant women. Methods: This was a case control study of women in reproductive age group at the University College Hospital, Ibadan, Nigeria from July 2014 to February 2015. Consecutive 70 pregnant women and 70 non-pregnant women (controls) without rhinologic symptoms were studied. A structured questionnaire was administered to obtain participants' information on socio-demographics, pregnancy history, and ability to perceive smell. They subjectively rated their olfactory function on a visual analogue scale of 0 – 100. Olfactory threshold (OT), discrimination (OD), identification (OI) scores and TDI of both groups were determined with“Sniffin' sticks”kits and compared. The level of significance was P<0.05. Results: The mean age of the pregnant women was 30.5±3.9years and control was 28.5±6.6years. There were more pregnant women (7.1%) with hyposmia than the non-pregnant women (2.9%). The subjective rating of olfactory function was 68.2±24.9 (median 70) and 72.3±21.6 (median 69) in pregnant women and controls respectively. The mean OT, OD, OI, TDI scores were higher in pregnant women than the controls. However, it was only in OI (P=0.000) and TDI (P=0.012) that the differences were significant. Conclusions: Pregnant women have olfactory dysfunction more than the non-pregnant women of reproductive age group. Also, they have tendency to develop loss of cognitive olfactory information more than the non-pregnant women.
Keywords: Odor, Olfaction, Olfactory perception, Pregnancy, Smell, “Sniffin sticks”
|How to cite this article:|
Nwankwo U, Fasunla A J, Oladokun A, Nwaorgu O G. Comparison between olfactory function of pregnant women and non-pregnant women in reproductive age group in Ibadan, Nigeria. Niger J Clin Pract 2017;20:610-5
|How to cite this URL:|
Nwankwo U, Fasunla A J, Oladokun A, Nwaorgu O G. Comparison between olfactory function of pregnant women and non-pregnant women in reproductive age group in Ibadan, Nigeria. Niger J Clin Pract [serial online] 2017 [cited 2021 Jul 27];20:610-5. Available from: https://www.njcponline.com/text.asp?2017/20/5/610/206367
| Introduction|| |
Pregnancy is a normal physiologic process that is associated with a change in estrogen and progesterone levels. This change increases the vascularity of nasal mucosa with resultant nasal congestion and has been reported to affect odor perception and recognition. Olfactory responses vary depending on the chemical nature of the stimuli. Olfactory thresholds depend on the level of inhibitory activity, which is generated by higher centers. Changes in nasal mucosa and its pH will alter olfactory perception. Human beings are better at detecting the pleasantness of an odor rather than recognizing it. During the pregnancy period, first trimester is significant in the proper growth and development of the unborn babies and the health behavior of pregnant mothers. Hyperemesis gravidarum, a clinical condition characterized by frequent episodes of nausea, excessive salivation, and vomiting, is more associated with first trimester and first pregnancy.,,,, Certain odorous substance cause nausea during pregnancy, thereby influencing dietary type and intake. It is hypothesized that olfactory dysfunction may play a role in this process, hence the absence of this clinical condition in some pregnant women. Olfactory function has been reportedly better in women but decreases with an increasing age.,
Rapid growth and development of unborn babies occurs throughout the pregnancy period. Therefore, pregnant mothers need to eat well for maintenance of good health and, normal growth and development of their unborn babies. Normal olfactory function has been documented as an important factor for good appetite. It may also protect against exposure to and accidental ingestion of spoilt, contaminated food which may predispose them to food poisoning and its effects such as miscarriage, premature labor, and the other conditions. Olfactory dysfunction may cause a change in the dietary behavior of an individual. The change in the level of reproductive hormone at the different trimesters of pregnancy has been documented to produce a significant change in olfactory function of pregnant mothers. Cognitive processing of odors appears to change in early pregnancy.,,, A few studies have documented on olfactory function of pregnant women; however, there is none from Nigeria. Although some of these studies on pregnant women reported an increase in olfactory sensitivity,,,,, the finding could not be confirmed by other similar studies.,,,, A study reported on a decrease in olfactory sensitivity and anosmia in the pregnant women. Environmental odor, which varies from place to place, may influence olfactory sensitivity to some substances due to odor desensitization. This study was therefore conducted to investigate and compare the olfactory function of pregnant women with that of non-pregnant women in Ibadan, Nigeria.
| Methods|| |
This was a case-control olfactory study involving 70 pregnant women and 70 non-pregnant women without rhinologic diseases at the University College Hospital, Ibadan. They were instructed to refrain from smoking, drinking, and eating for at least 1 hour before the olfactory tests were performed. Ethical approval was obtained from University of Ibadan/University College Hospital review board for the conduct of the study. Informed consent was also obtained from the participants in the study. Women with clinical history of rhinosinusitis, nasal tumor, previous nasal surgery, and head trauma were excluded from the study. Urine pregnancy test was done to rule out cyesis in the non-pregnant women.
A structured questionnaire was administered to obtain participants' information on sociodemographics, occupation, age of pregnancy, presence of nasal disease, head injury, and ability to perceive smell or not.
Ear, Nose, Throat Examination
The participants had their noses, oral cavities, and throats examined to exclude the presence of nasal pathologies such as discharge, polyps, or tumors.
Subjective assessment of smell
Participants were asked to specify if their perception of odor was reduced, increased, or unchanged at first trimester of pregnancy.
The participants had olfactory identification, discrimination, and threshold tests done using the validated“Sniffin sticks”test battery (Burghart Messtechnik GmbH, Wedel, Germany). Odors were presented in felt-tip pens. The cap was removed and the tip of the pen was positioned approximately 2 cm in front of the participants' nasal cavities for about 3s to prevent adaptation.
Odor identification (OI) testing
Each of the 16 pens already impregnated with 16 different familiar odors were placed close to the anterior nares of each participant for about 3s. The odor pens were presented at interval of 30s to prevent olfactory desensitization., They were then asked to select the source substance that matched the presented odor from four different items in a forced choice procedure (four alternative forced choice). The number of correctly selected source substance by the participant was then recorded. The minimum point that could be scored by a participant was zero and the maximum score was 16.
Odor discrimination (OD) testing
The kit for OD contains 48 pens that were arranged in 16 triplets. In each triplet, two of the pens contained the same odor while the third contained another odor. The participant was presented with these three pens and expected to identify the pen with a different odor (three alternative forced choice). They were allowed to sample each odor only once, to minimize the test duration. The triplets were presented at intervals of at least 30s and the individual odor pens at intervals of approximately 3s. When the participant correctly identified the pen with a different odor she was given a point score and when she missed it, she scored zero. The process was repeated for the 16 triplet pens. The minimum point that could be scored by a participant was zero and the maximum score was 16.
Odor threshold (OT) testing
The kit also contains 48 pens which were arranged in 16 triplets. In each triplet, two of the pens contained no odor, whereas the third stick was impregnated with different concentrations of n-butanol solution in an increasing fashion from the lowest to the highest (4%–16%). The three odor pens were presented in a randomized fashion and the task was for the participants to identify the pen with a different smell. After the correct recognition of the pen with n-butanol odor in a triplet, the triplet pens were then re-shuffled and represented in a randomized fashion. If she correctly recognized the pen with n-butanol in a triplet the second time, a reversal of the staircase was started with the triplet pens from the highest concentration of n-butanol until she was no longer able to identify the pen which contains n-butanol. The staircase was then reversed and the process repeated. The threshold is the mean of the last four of seven staircase reversal points. Thus, the value of the threshold will range from 1 to 16.
The sum of OT, discrimination and identification values is referred to as threshold, discrimination, and identification (TDI) score. Each of these three different tests allowed for a maximum score of 16 points and together, a total maximum score of 48 points
(TDI score). In this study, anosmia was defined as TDI scores of <15 whereas hyposmia was defined as TDI scores of ≤30.5, OT scores of ≤6.5, olfactory discrimination scores of ≤10, and olfactory identification scores of ≤11 were suggestive of hyposmia.
Data obtained were analyzed using IBM SPSS (Statistical Package for Social Sciences) version 20 manufactured in Armonk, New-York, USA. Demographic variables were represented using tables while summary statistics was done using means and proportions. The comparison of mean olfactory scores between pregnant and non-pregnant women was done using the independent samples t test. The difference in olfactory perception between pregnant women and controls was tested using the analysis of variance. The odd ratio was calculated to detect a potential association between pregnancy and hyposmia. Level of statistical significance was set at P value of <0.05, two-tailed level at 95% confidence interval (CI) and correlation coefficient (r).
| Results|| |
The age of the pregnant women ranged from 22 to 38 years, mean of 30.5 ± 3.9 while that of non-pregnant women ranged from 20 to 40 years, mean of 28.5 ± 6.6. Forty (57.1%), 28 (40%), and 2 (2.9%) of the pregnant women were in the third, second, and first trimester, respectively.
Subjective olfactory perception of pregnant and non-pregnant women
Thirty four (48.6%) pregnant women had increased perception of smell in pregnancy, three (4.3%) reported reduction, and 33 (47.1%) reported no change in the first trimester of pregnancy.
Objective olfactory testing of pregnant and non-pregnant women
The mean OI, OD, OT, and TDI of both the pregnant and non-pregnant women were within the scores of the 10th percentile for 16–35-year-old individuals defined by Hummel et al. However, the mean OI and TDI were significantly higher in pregnant women. The comparison of the mean OI, OD, OT, and TDI values of pregnant women and the controls are shown in [Table 1].
|Table 1: Comparison of mean olfactory test values of pregnant women with the control group|
Click here to view
There was no significant correlation between the gestational age of pregnancy and OI (r = -0.088; P = 0.470), OD (r = 0.097; P = 0.427), OT (r = -0.219; P = 0.069), and TDI (r = 0.117; P = 0.335). There was also no significant difference in olfactory test values in the three trimesters of pregnancy—OI (P = 0.655), OD (P = 0.525), OT (P = 0.472), and TDI (P = 0.388). There was no significant correlation between the subjective assessment of olfaction and OI (r = 0.169; P = 0.162), OD (r = -0.039; P = 0.749), OT (r = -0.230; P = 0.055), and TDI (r = 0.020; P = 0.866).
The mean OI, OD, OT, and TDI scores in both the pregnant and non-pregnant women are within the normosmic values. However, the values are lower in the pregnant women than the non-pregnant women [Table 1].
TDI score revealed that five (7.1%) pregnant women and two (2.9%) non-pregnant women were hyposmic. The pregnant women had twice the tendency to develop hyposmia more than the non-pregnant women [Table 2]. However, the observation was not statistically significant (P > 0.05).
|Table 2: Comparison of hyposmic pregnant women with hyposmic non-pregnant women|
Click here to view
| Discussion|| |
Objectively, this study showed that majority of the pregnant and non-pregnant women had normal olfactory function and, only in mean OI and TDI score that there was a significant difference between the groups. This is similar to the report by Kolble et al. who reported no major pregnancy related changes in olfactory sensitivity of pregnant women at first trimester when compared with non-pregnant women. The subjective increased perception of smell noted in about 49% of the pregnant women during the first trimester in pregnancy in this study is similar to the report from similar studies.,,,,,,,,, Self-report has shown that the largest changes in olfactory perception occur in early pregnancy. Human chorionic gonadotropin level peaks during the first trimester and match the profile of self-reported changes. In this study, the prevalence of hyposmia in pregnant women was higher than in the non-pregnant women. Although the participants in this study were not progressively monitored in pregnancy, the five hyposmic pregnant women were identified at their second trimester of pregnancy. This supports evidence that the change in smell sensitivity occurs in the early phase of pregnancy and may normalize in the course of pregnancy and after delivery. Studies have reported that effect of pregnancy on olfaction occurs during the first trimester and declines with increasing gestational age.,,,,
OT reflects peripheral processing of olfactory information., This present study did not find any difference between the OT scores of pregnant and non-pregnant women. Disease of the nose and olfactory nerve that were excluded from this study might have contributed to the finding on OT in this study. This finding agrees with what has been previously reported in the literature.,, Few studies have reported decreased OT in the last trimester of pregnancy and during postpartum period.,, It is only longitudinal studies that investigated olfaction of pregnant women across the three trimesters that can correctly report the trend in pregnancy. The levels of circulating gonadal hormones have been implicated in the observed olfactory changes in pregnancy. Estrogen levels rise throughout pregnancy. Thus one would expect that olfactory function should improve across pregnancy if estrogen alone was involved but measures of olfactory function and self-report do not support this.
OI reflects the central processing of olfactory information. In this study, mean OI score in pregnant women was found to be significantly higher than that of the controls. This is in contrast with findings in other studies that documented no significant difference in OI scores between pregnant and non-pregnant women.,, [12,,,,, Ochsenbein-Kolble et al., reported that OI scores tended to be lower in pregnant women than controls. Pregnant women have been reported to identify some odors better than the controls.,,, Pregnant women in this study identified the odor of smoked meat, peppermint, ginger, garlic, apple, orange, grass, fish, chocolate, and lemon better than the controls. This supports the idea that olfactory changes during pregnancy appear to relate mostly to changes of the cognitive processing of olfactory information rather than in olfactory acuity.
OD reflects central processing of olfactory information. There is no significant difference in OD between pregnant women and the control group in this study, which is similar to findings in other studies.,
TDI score is the summation of measurement of both the peripheral and central processing of olfactory function. TDI score of pregnant women in this study was significantly higher than that of non-pregnant women which is similar to findings in other similar studies.,,,,,,3 This shows that pregnancy may have an effect on olfaction. Some studies have failed to demonstrate a significant effect of pregnancy on olfaction., This varied finding in olfaction in pregnancy may be due to the fact that the effect is more cognitive (central) than sensory (peripheral)., It may also be because the effect of pregnancy on olfaction is little and may vary with individuals, hence more sensitive tests are required to reveal any appreciable change in olfaction. Olfaction is linked to important cognitive and emotional domains such as the orbitofrontal cortex and the dorsomedial nucleus of the thalamus in the brain.
Olofsson et al. measured odor event-related potentials (OERP) in pregnant women and non-pregnant women. He reported no significant difference in the amplitude and latency of N1 and P1 components (which reflect sensory processing), but reported a tendency for shorter latency and higher amplitude of the more cognitive P3 component in pregnant women. Therefore, the change in olfactory perception experienced by some women during pregnancy is due to psychological changes, possibly explaining the largely negative sensitivity test results. Such a high-level change in odor processing may not be detected by some standard tests of olfactory function. Olfactory-induced nausea appears to be due to cognitive processing of olfactory information but not changes in olfactory acuity. The heightened sense of smell in pregnancy induces aversions to certain foods that contain teratogenic and abortifacient chemicals by causing pregnant women to avoid these food.,
| Conclusions|| |
The prevalence of hyposmia is more in pregnant women than the non-pregnant women and there was tendency for pregnant women to develop loss of smell than the non-pregnant women. Awareness should be created among the pregnant women on the possible change in olfactory perception in pregnancy. They should also be educated on how to cope with it for better quality of life and maternal nutrition.
The authors acknowledge with appreciation all the participants of this study.
Financial support and sponsorship
Conflicts of interest
There is no conflict of interest.
| References|| |
Worthington-Roberts B, William SR. Physiology of pregnancy. In: Nutrition in pregnancy and lactation. 1993;5th St Louis, MO:Mosby;64-86.
Drake-Lee A. Physiology of the nose and paranasal sinuses. In: Scott-Brown's Otorhinolaryngology, Head and neck surgery. 7th
Ed ward Arnold 2008;1367.
Swallow BL, Lindow SW, Masson EA, Hay DM. Development of an instrument to measure nausea and vomiting in pregnancy. J Obstet Gynaecol 2002;22:481-5.
Gadsby R, Barnie-Adshead AM, Jagger C. A prospective study of nausea and vomiting during pregnancy. Br J Gen Pract 1993;43:245-8.
Bashiri A, Neumann L, Maymon E, Katz M. Hyperemesis gravidarum: Epidemiologic features, complications and outcome. Eur J Obstet Gynecol Reprod Biol 1995;63:135-8.
Boyce RA. Enteral nutrition in hyperemesis gravidarum: A new development. J Am Diet Assoc 1992;92:733-6.
de-Graft Aikins A. Food beliefs and practices during pregnancy in Ghana: Implications for maternal health interventions. Health Care Women Int 2014;35:954-72.
Faas MM, Melgert BN, de Vos P. A brief review on how pregnancy and sex hormones interfere with taste and food intake. Chemosens Percept 2010;3:51-6.
Ferdenzi C, Roberts SC, Schirmer A, Delplanque S, Cekic S, Porcherot C, et al.
Variability of affective responses to odours: Culture, gender, and olfactory knowledge. Chem Senses 2013;38:175-86.
Doty RL, Shaman P, Applebaum SL, Giberson R, Siksorski L, Rosenberg L. Smell identification ability: Changes with age. Science 1984;226:1441-3.
Doty RL, Cameron EL. Sex differences and reproductive hormone influences on human odor perception. Physiol Behav 2009;97:213-28.
Croy I, Landis BN, Meusel T, Seo HS, Krone F, Hummel T. Patient adjustment to reduced olfactory function. Arch Otolaryngol Head Neck Surg 2011;137:377-82.
Hummel T, Barz S, Pauli E, Kobal G. Chemosensory event-related potentials change with age. Electroencephalogr Clin Neurophysiol 1998;108:208-17.
Nordin S, Murphy C, Davidson TM, Quinonez C, Jalowayski AA, Ellison DW. Prevalence and assessment of qualitative olfactory dysfunction in different age groups. Laryngoscope 1996;106:739-44.
Hummel T, Kobal G, Gudziol H, Mackay-Sim A. Normative data for the“sniffin sticks”including tests of odour identification, odour discrimination and olfactory thresholds: An upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol 2007;264:237-43.
Simsek G, Bayar Muluk N, Arikan OK, Ozcan Dag Z, Simsek Y, Dag E. Marked changes in olfactory perception during early pregnancy: A prospective case-control study. Eur Arch Otorhinolaryngol 2015;272:627-30.
Cameron EL. Pregnancy does not affect human olfactory detection thresholds. Chem Senses 2014;39:143-50.
Hummel T, Knecht M, Kobal G. Peripherally obtained electrophysiological responses to olfactory stimulation in man: Electro-olfactograms exhibit a smaller degree of desensitization compared with subjective intensity estimates. Brain Res 1996;717:160-4.
Hummel T, Gollisch R, Wildt G, Kobal G. Changes in olfactory perception during the menstrual cycle. Experientia 1991;47:712-5.
Hummel T, von Mering R, Huch R, Kolble N. Olfactory modulation of nausea during early pregnancy?. BJOG 2002;109:1394-7.
Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL. Olfactory dysfunction in schizophrenia: A qualitative and quantitative review. Neuropsychopharmacology 1999;21:325-40.
Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G. 'Sniffin sticks': Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 1997;22:39-52.
Gudziol H, Schubert M, Hummel T. Decreased trigeminal sensitivity in anosmia. ORL J Otorhinolaryngol Relat Spec 2001;63:72-5.
Kolble N, Hummel T, von Mering R, Huch A, Huch R. Gustatory and olfactory function in the first trimester of pregnancy. Eur J Obstet Gynecol Reprod Biol 2001;99:179-83.
Nordin S, Broman DA, Olofsson JK, Wulff M. A longitudinal descriptive study of self-reported abnormal smell and taste perception in pregnant women. Chem Senses 2004;29:391-402.
Festin M. Nausea and vomiting in early pregnancy. Am Fam Physician 2015;92:516-7.
Jones-Gotman M, Zatorre RJ. Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia 1988;26:387-400.
Lee NM, Saha S. Nausea and vomiting of pregnancy. Gastroenterol Clin North Am 2011;40:309-34.
Laska M, Koch B, Heid B, Hudson R. Failure to demonstrate systemic changes in olfactory perception in the course of pregnancy: A longitudinal study. Chem Senses 1996;21:567-71.
Cameron EL. Measures of human olfactory perception during pregnancy. Chem Senses 2007;32:775-82.
Wohlgemuth C, Beinder E, Ochsenbein-Kolble N, Hummel T. Changes in olfactory function with several pregnancies? Swiss Med Wkly 2008;138:466-9.
Ochsenbein-Kolble N, von Mering R, Zimmerman R, Hummel T. Changes in olfactory function in pregnancy and postpartum. Int J Gynaecol Obstet 2007;97:10-4.
Cameron EL. Pregnancy and olfaction: A review. Front Psychol 2014;5:67.
Wysocki CJ, Gilbert AN. National geographic smell survey. Effects of age are heterogenous.. Ann N
Y Acad Sci 1989;61:12-28.
Olofsson JK, Broman DA, Wulff M, Martinkauppi M, Nordin S. Olfactory and chemosomatosensory function in pregnant women assessed with event-related potentials. Physiol Behav 2005;86:252-7.
Nyaruhucha CN. Food cravings, aversions and pica among pregnant women in Dar es Salaam, Tanzania. Tanzan J Health Res 2009;11:29-34.
Wijewardene K, Fonseka P, Goonaratne C. Dietary cravings and aversions during pregnancy. Indian J Public Health 1994;38:95-8.
[Table 1], [Table 2]