Influence of gustatory and olfactory perception in the oral phase of swallowing in smokers

Abstracts

Purpose:

To analyze the difference between nonsmokers and smokers on the changes in the perceptions of smell and taste and to verify the influence of these aspects in the emergence of compensatory movements during swallowing.

Methods:

To evaluate these aspects, capabilities of olfactory and gustatory recognition were observed, as well as the compensation swallowing. Twenty-four patients were evaluated in each study group aged from 18 years, grouped in a stratified way. The olfactory evaluation consisted in presenting seven essences and one of three options should be chosen. For the taste test, 16 flavors were offered in a non-sequential and decreasing way in amount of solute. Swallowing solid and liquid was evaluated, in which aspects of compensation perioral muscles were observed.

Results:

Worst performance in olfactory and gustatory tests among smokers (p≤0.01) was found. Through the results of χ² and Fisher's exact tests, it was found that the contraction of the mentalis muscle is less observed in non-smokers, and smokers have an average degree of statistically significant change compared to nonsmokers. Furthermore, through the Spearman correlation coefficient, it was found that the worsening in the sensory tests implies increased compensation during swallowing in smokers.

Conclusion:

These data allowed us to verify that the sensory changes have influence on swallowing pattern, indicating that these changes are aspects that should be considered in the differential diagnosis of changes in swallowing.

Smell; Taste; Deglutition; Smoking; Facial muscles

Objetivo:

Analisar a diferença entre indivíduos não fumantes e fumantes quanto às modificações nas percepções de olfato e paladar e verificar a influência desses aspectos no aparecimento de movimentos compensatórios durante a deglutição.

Métodos:

Para avaliação desses aspectos, foram verificadas as capacidades de reconhecimento olfativo e gustativo, bem como as compensações de deglutição. Foram avaliados 24 indivíduos em cada grupo de estudo com idade a partir de 18 anos, agrupados de forma estratificada. A avaliação olfativa consistiu na apresentação de sete essências, devendo ser escolhida uma entre três opções. Para o teste de paladar, foram oferecidos 16 sabores de forma não sequencial e decrescente em quantidade de soluto. Foi avaliada a deglutição de sólido e líquido na qual se observaram aspectos de compensação da musculatura perioral.

Resultados:

Foi verificado pior desempenho nos testes olfativo e gustativo entre indivíduos tabagistas (p≤0,01). Por meio dos resultados dos testes do χ² e exato de Fisher, foi verificado que a contração da musculatura mentual é menos observada em não fumantes, sendo que fumantes apresentam grau médio de alteração estatisticamente significativo em relação a não fumantes. Além disso, por meio do coeficiente de correlação de Spearman, verificou-se que a piora no desempenho dos testes sensoriais implica aumento de compensações durante a deglutição em indivíduos fumantes.

Conclusão:

Estes dados permitiram verificar que as modificações sensoriais apresentam influência no padrão de deglutição, evidenciando que essas alterações são aspectos que devem ser considerados no diagnóstico diferencial das modificações de deglutição.

Olfato; Paladar; Deglutição; Hábito de fumar; Músculos faciais

INTRODUCTION

Swallowing is one of the functions of the stomatognathic system, responsible for passing the bolus down to the digestive system. With regard to its motor functioning, it can be subdivided into oral preparatory, oral, pharyngeal, and esophageal phase; and, considering that this process is initiated even before contact with food, the anticipatory phase can also be included here. The dynamics of this entire process suffers the influence of intrinsic and extrinsic factors for its occurrence⁽¹⁾. The intrinsic factors are the morphological and functional conditions of the oral, pharyngeal, and esophageal cavity, in addition to central control to perform the movements. Extrinsic factors are those perceived by the somatosensory system, which is responsible for the perception of stimuli from the environment that will directly influence the central commands for motor actions that will pass the bolus down to the digestive system⁽¹⁾.

Although it is a voluntary action, the oral phase of swallowing suffers the interference of reflex actions. It also depends on other structures involved in the process being ready to receive the bolus, thus depending on central commands to perform muscle movements⁽²⁾. In order for this reflex action to occur, the efferent nerves involved in this process must be stimulated. Swallowing, in turn, is initiated by mechanical stimuli through contact with food, and by mechanical stimuli, through olfaction and gustation^(1,2).

Olfactory and gustatory stimulation enable the oral motor system and the gastrointestinal system to prepare for the reception of food by increasing salivary secretion, gastric juice production^(3-5), and the length of time of motor-evoked potentials (motor responses to sensory stimuli)⁽⁵⁾. Furthermore, it favors the adequate positioning of oropharyngeal structures during swallowing and incites nerve and muscle excitability in order to transfer food to the stomach^(2,4).

The sensory stimulation provoked at the presentation of food and the orofacial movements performed during oral preparation for swallowing stimulate cortical pathways and the bulbopontine nuclei of the brainstem, thus generating responses that trigger swallowing according to the time length and the type of stimulus presented^(2,5). The route travelled by the neurons responsible for the swallowing process begins with the arrival of stimuli to the respective nuclei of each nerve involved in this process, located in the nuclear region of the solitary tract (situated in the posterior dorsal region of the bulb in the brainstem) and in the ventral region (which surrounds the nucleus ambiguous), along with neurons in the reticular formation. The reticular formation, located in the central portion of the brainstem, is a highly organized and specialized region, capable of coordinating several stimuli, in addition to being one of the elements responsible for the performance of diverse motor acts. The integration of stimuli that influence feeding behavior and the act of eating is among its functions, and it therefore determines the manner in which this complex process will occur. Regarding this motor action specifically, the pontine reticular and lateral bulb formation is responsible for coordinating motor orofacial responses such as the chewing process (through the motor nucleus of the trigeminal nerve), lip movements (close to the motor nucleus of the facial nerve), and tongue movements (nucleus of the hypoglossal nerve)^(2,5). Little is known about the cortical regions involved in swallowing; however, a region anterior to the sensorimotor cortex is believed to be the integration center that controls this process⁽⁵⁾.

The senses of smell and taste are sensory perceptions easily affected by external agents. When one of these sensory recognition capabilities is altered, it is also generally possible to identify modifications in the other sensitive system, which indicates the influence of one over the other and the possibility of occurrence of simultaneous deficits. Several factors can alter these perception capabilities, such as alterations in nasal and oral function or structure, traumas, and neurological pathologies; even pregnancy can temporarily modify an individual's recognition of smells and flavors. Another factor that can significantly alter the sensibility of olfactory and gustatory receptors is smoking⁽⁶⁾.

Currently, the number of individuals who consume tobacco has been on the rise, especially among young people, despite the efforts made to reduce these rates by means of preventive measures and treatments⁽⁷⁾. The amount and the risk of complication of illnesses related to smoking are alarming and generate considerable economic and social impact, especially in developing countries, such as Brazil⁽⁸⁾. A major part of studies on smoking point to illnesses that greatly impact an individual's health, such as cancer, and few describe other compromised areas of lower impact that can equally inflict harm to the overall health of tobacco consumers. Moreover, it is well known that the main impact caused by smoking is related to a decrease in lung functionality, which causes several illnesses, such as Chronic Obstructive Pulmonary Disease (COPD), which interfere with other systems, such as the ability to swallow^(9,10). In relation to aspects that pertain to speech-language pathology and audiology specifically, it is known that smoking can negatively interfere with the feeding process due to olfactory and gustatory impairments caused by continuous exposure to smoke, which can alter, at the structural and functional level, the capability of these sensory receptors to detect and perceive stimuli ⁽¹¹⁾. This modification occurs not only by the inhalation of smoke by a smoker, but also by inhaling smoke in closed spaces, as is the case with passive smokers⁽¹²⁾.

Based on the aforementioned data, our hypothesis is that smoking alters olfactory and gustatory perception in comparison to the recognition capability of individuals who never smoked, and that these alterations in sensory perception influence the emergence of muscle compensation during the oral phase of swallowing in individuals exposed to this condition. As this relation is not explicitly described in the literature, the conduction of this study is hereby justified.

METHODS

This is a transversal study with descriptive and comparative analysis. The participants who composed the sample were 48 individuals, 24 smokers and 24 who had never consumed tobacco and who did not live with other smokers, and for this reason were not considered passive smokers. The group of smokers was formed by individuals who were under care at the Ambulatory of Pulmonology of Irmandade Santa Casa de Misericórdia in Porto Alegre (ISCMPA). In this study group, we assessed individuals who were being assisted due to pulmonary diseases caused by smoking, namely COPD, pulmonary emphysema, and allergic bronchitis.

The group with non-smokers was composed of individuals who volunteered to participate after the study's conduction was divulged in the researchers' universities. Therefore, we evaluated individuals who manifested interest in being submitted to the assessment battery after seeing the invitation to participate. All participants signed the iInformed Consent Form upon explanation of the purpose and procedures of the study. This research study was approved by ISCMPA's Ethics Committee, report number 3636/11.

In order to compose the sample, we paired the individuals of both groups based on gender and age range. In order to better distribute the sample, four age ranges were determined, in accordance with other studies in the literature: 18-25 years, 26-40 years, 41-60 years, and 61 years and older. Six individuals, three women and three men, were assessed for each age range. Table 1 displays the averages of time and quantity of tobacco consumed by gender and age range, thus demonstrating the characteristics of the smoking habits of the individuals assessed in the group of smokers.

Table 1
Averages of the quantity of cigarettes smoked and time of tobacco consumption among smokers

	Time of tobacco consumption	Quantity of cigarettes smoked per day
Overall average	23.5	19.95
Men	22.41	24.75
Between 18 and 25 years	6.3	16.66
Between 26 and 40 years	18	38
Between 41 and 60 years	26	19
More than 61 years	39.33	25.33
Women	24.58	15.16
Between 18 and 25 years	7.6	26.66
Between 26 and 40 years	18	15.66
Between 41 and 60 years	26	10.33
More than 61 years	46.66	8

Healthy individuals who were within the established age ranges were included in this study. They had no diagnosis of neurodegenerative, systemic, salivary or orofacial anatomic alterations, and no alterations in upper airways. They were not under medication, speech therapy, or pregnant at the moment of assessment. In addition, we excluded individuals who presented, during the orofacial and dental myofunctional evaluation conducted for this study, structural alterations that could interfere with the aspects investigated.

First, we established gustatory and olfactory perception alterations in the group with smokers in comparison to the control group. For the conduction of the tests of these variables, the evaluator had no access to the results during the application, and the order in which they should be tested was described on labels attached to the flasks, so as to minimize a potential interference of the evaluator's knowledge of the answers. The gustatory perception evaluation was carried out with the purpose of verifying the individuals' recognition of each of the main tastes: sweet, salty, bitter, and sour, in accordance with an evaluation protocol described in the literature⁽¹¹⁾. Prior to the test, the participants' mouths were sanitized with water, so as to avoid any taste interferences with the procedure. The evaluator presented the liquid stimuli that contained the four tastes alternately and gradually, in different concentrations, using a dropper. For each taste tested, four different concentrations were presented non-sequentially, totalizing 16 stimuli. Each individual rinsed his/her mouth after each stimulus. The participant had to identify which taste was being tested by pointing to a chart that showed all four possibilities in writing. Thus, each individual could score between 0 and 16 correct answers. The sequence used to present the tastes to all participants was the same in both groups. The material for the test was manipulated with the aid of a technician at the Physiology Laboratory of Universidade Federal de Ciências da Saúde de Porto Alegre, where we conduct our work.

After the gustatory analysis, the individuals' olfactory perception was assessed by means of a standard odor recognition test⁽¹³⁾. Each participant's nose was sanitized before this test so that possible residues could be removed. Once the test was initiated, a stimulus was presented to the individual by opening a container that retained a characteristic odor. Three different images were concomitantly presented, and the individual had to relate one of them to the essence inhaled. In total, seven stimuli were presented with short pauses in between. Each correct answer was worth one point.

Another aspect analyzed was muscle compensation during swallowing. In this evaluation, we sought to analyze the contraction of the orbicularis and mentalis muscle during the deglutition of solid foods, and then liquid foods. For the first food type, we asked each individual to eat a bun as he/she did habitually; and, for the second food type, we asked the participants to drink water from a regular cup. For the analysis of each muscle component, we rated the muscle compensation performed during swallowing as absent, mild, medium, and accentuated. We defined the contraction of the orbicularis muscle as absent when this muscle was not at all moved during swallowing; as mild, when only the lip commissures were contracted; as medium, when the contraction of lip commissures was followed by mild lip contraction; and as accentuated, when the contraction of lip commissures was followed by intense lip contraction. We defined the contraction of the mentalis muscle as absent when this muscle was not at all moved during swallowing; as mild, when it was only lifted; as medium, when contraction was mild; and as accentuated, when contraction was intense. During the assessment of solid food ingestion, we timed how long it took the individuals to chew, given that this transit time can influence bolus formation.

The data collected were analyzed by means of tables, descriptive statistics, and by the following statistical tests: Student's t-test to compare the perception test averages; χ² test and Fisher's exact test to describe and correlate the individuals' swallowing characteristics; and Spearman's correlation coefficient to verify the interference of olfactory and gustatory alterations in compensatory swallowing. The results were considered significant at a maximum significance level of 5%. The statistical software program used to analyze the data was the SPSS version 10.0.

RESULTS

From Table 2, it is possible to verify the scores of the gustatory perception test and the olfactory perception test for both study groups. Through the results obtained with Student's t-test, we found that the variables analyzed differed from one group to the other, and that the average of correct answers was higher for the group of non-smokers in both perception evaluations. Regarding the influence of gender and age, we did not find any differences in olfactory and gustatory alterations in both study groups.

Table 2
Comparison of the variables of the gustatory perception and olfactory perception tests between the groups (n=24)

Variable	Group	Mean	Standard deviation	p-value
GPT	Non-smoker	14.38	1.10	0.000*
	Smoker	11.79	1.56
OPT	Non-smoker	6.25	0.79	0.000*
	Smoker	4.46	0.88

• ^*
  Significant difference p≤0.01
• ^Caption
  : GPT = gustatory perception test; OPT = olfactory perception test; SD = standard deviation

Table 3 displays a comparison between the groups with regard to the degrees of alteration of orbicularis and mentalis muscle compensation during the deglutition of liquid and solid foods. Through the results of the ^χ2 test and Fisher's exact test, we observed statistically significant results, as the contraction of the mentalis muscle presented a lesser degree of alteration among the non-smokers during the deglutition of both consistencies evaluated. A larger number of non-smokers did not contract this muscle on the course of swallowing. Furthermore, we found significant results that point to the fact that the group of smokers had more individuals with medium alteration of this muscle. Although we did not observe statistically significant results concerning the orbicularis muscle, we verified that the group of smokers had more participants who presented higher degrees of compensatory deglutition in this muscle. There were no differences in compensatory swallowing pertaining to age and gender in both study groups. Moreover, we did not observe significant differences between the groups regarding the time taken to prepare the bolus which could justify the muscle behavior performed during swallowing due to the variability of bolus cohesion and consistency.

Table 3
Comparison of the variables of muscle compensation during swallowing between the groups

Variable	Category	Group				Total		p-value
		Non-smoker		Smoker
		n	%	n	%	n	%
COS	Absent	2	8.3	–	–	2	4.2	0.130 ns
	Mild	11	45.8	6	25.0	17	35.4
	Medium	7	29.2	9	37.5	16	33.3
	Accentuated	4	16.7	9	37.5	13	27.1
CMS	Absent	10	41.7	1	4.2	11	22.9	0.003*
	Mild	11	45.8	13	54.2	24	50.0
	Medium	–	–	5	20.8	5	10.4
	Accentuated	3	12.5	5	20.8	8	16.7
COL	Absent	4	16.7	1	4.2	5	10.4	0.180 ns
	Mild	12	50.0	8	33.3	20	41.7
	Medium	5	20.8	8	33.3	13	27.1
	Accentuated	3	12.5	7	29.2	10	20.8
CML	Absent	13	54.2	4	16.7	17	35.4	0.004**
	Mild	10	41.7	13	54.2	23	47.9
	Medium	–	–	6	25.0	6	12.5
	Accentuated	1	4.2	1	4.2	2	4.2

• ^*
  Significant correlation p≤0.01
• ^**
  Significant correlation p≤0.05
• ^Caption
  : ns = not significant; COS = contraction of the orbicularis muscle when swallowing solids; CMS = contraction of the mentalis muscle when swallowing solids; COL = contraction of the orbicularis muscle when swallowing liquids; CML = contraction of the mentalis muscle when swallowing liquids

With regard to the influence of olfactory and gustatory alterations in the compensatory swallowing of smokers, Table 4 displays the relation between these variables. Through the results of Spearman's correlation coefficient, we verified that all correlations presented significant results. This relation occurs inversely, that is, the lower the scores on the olfactory and gustatory tests, the higher the degree of compensation alteration during the deglutition of liquid and solid foods.

Table 4
Influence of olfactory and gustatory alterations in the compensatory swallowing of smokers

	Smokers (n=24)
	GPT		OPT
	r	p-value	r	p-value
COS	-0.523	0.009*	-0.422	0.040**
CMS	-0.428	0.037**	-0.808	0.000*
COL	-0.529	0.008*	-0.508	0.011**
CML	-0.598	0.002*	-0.627	0.001**

• ^*
  Significant correlation p≤0.01
• ^**
  Significant correlation p≤0.05
• ^Caption
  : GPT = gustatory perception test; OPT = olfactory perception test; COS = contraction of the orbicularis muscle when swallowing solids; CMS = contraction of the mentalis muscle when swallowing solids; COL = contraction of the orbicularis muscle when swallowing liquids; CML = contraction of the mentalis muscle when swallowing liquids

In relation to how long the participants have smoked and how many cigarettes are usually consumed, Table 5 summarizes the influence of these factors in the alteration of muscle compensation and in the scores of olfactory and gustatory evaluations. Through the results of Spearman's correlation coefficient, we verified that the larger the quantity of cigarettes smoked in a day, the higher the degree of compensation of the orbicularis muscle during the deglutition of solid and liquid foods. Regarding the time of consumption, we observed that this variable only influences the contraction of the orbicularis muscle when an individual swallows liquids, in inverse correlation. Besides this, we did not observe any differences concerning the influence of these variables in the participants' gustatory and olfactory perception.

Table 5
Correlation of the variables with the quantity of cigarettes smoked per day and time of tobacco consumption

Variable	Correlation
	Quantity of cigarettes smoked per day		Time of tobacco consumption
	r	p-value	r	p-value
COS	0.560	0.004*	-0.296	0.160 ns
CMS	0.163	0.447 ns	-0.262	0.217 ns
COL	0.430	0.036**	-0.417	0.043**
CML	0.366	0.079 ns	-0.156	0.468 ns
GPT	-0.266	0.209 ns	-0.330	0.115 ns
OPT	-0.379	0.068 ns	0.135	0.529 ns

• ^*
  Significant correlation p≤0.01
• ^**
  Significant correlation p≤0.05
• ^Caption
  : ns = not significant; COS = contraction of the orbicularis muscle when swallowing solids; CMS = contraction of the mentalis muscle when swallowing solids; COL = contraction of the orbicularis muscle when swallowing liquids; CML = contraction of the mentalis muscle when swallowing liquids; GPT = gustatory perception test; OPT = olfactory perception test

DISCUSSION

Studies in the literature show differences in the olfactory and gustatory recognition capability of individuals who smoke as opposed to those who do not smoke. Smoking is a risk factor for the appearance of sensory disorders⁽¹⁴⁾, and this fact corroborates the evidence presented in this study. Previous studies show that the gustatory recognition capability of smokers is inferior to that of non-smokers; for this reason, the concentration of the stimulus tested needs to be increased for the substance to be recognized correctly. In other words, smokers have higher thresholds of sensory recognition in comparison to non-smokers^(15-17). This difficulty occurs due to modifications in the shape, number and vascularization of an individual's taste buds, which interferes with taste detection and perception⁽¹⁵⁾. Concerning the sense of smell, alterations in recognition occur due to structural and, consequently, functional modifications in the neuroepithelium⁽¹⁸⁾, resulting in a recognition capability inferior to that of non-smokers^(14-19). It is known that the olfactory neuroepithelium is the only type of cell in the nervous system capable of regenerating itself by producing new cells. Nevertheless, the constant exposure of the olfactory tissue to smoke diminishes its natural capability of producing new sensory cells and induces an increase in the number of apoptosis in this tissue, resulting in the loss of odor recognition^(20,21).

In addition to significant differences in sensory alterations found upon comparing smokers to non-smokers, we also verified a disparity between the groups in relation to the degree of compensations during swallowing. Regarding the compensations performed by the mentalis muscle during deglutition, the non-smokers obtained statistically higher results for the absence of compensations in this muscle for both food consistencies tested. This result is justified by the fact that compensatory swallowing is not expected in individuals who have no risk factors associated with the appearance of this inadequacy⁽²¹⁾. The habit of smoking can be considered a risk factor for this situation, as observed in the differences of muscle behavior between the groups. Considering that smoking interferes indirectly with swallowing by means of desensitizing the sensory receptors directly involved in the feeding process⁽¹⁴⁾, such compensations are more commonly observed in smokers, in accordance with the aforementioned data.

Another significant result pertains to the larger number of individuals with a medium degree of compensation alteration in the group of smokers. Due to the positioning and the movements performed by the oral muscles during the act of smoking, the modification of this muscle activity occurs in this region⁽²²⁾. According to the data in the literature, the mentalis muscle tends to present increased contractions due to the inadequate muscle functioning of other facial structures, which explains this difference in the results between the groups for this variable⁽²³⁾. Another aspect to be considered is facial ageing. It is known that smoking causes the early functional ageing of facial structures, even though this association has not been observed as significant⁽²⁴⁾; it is also associated with increased facial tonicity⁽²⁵⁾. This modification in tonicity can prompt the performance of unexpected movements during the process of swallowing.

Another aspect that can influence the performance of these compensations is the individual's anatomic features, such as bone formation, dental occlusion, and facial type⁽²¹⁾. However, the individuals in this study were not paired based on these elements, and we excluded those who presented abnormal aspects that could directly and significantly influence their swallowing patterns from both groups. Participants in the groups of smokers and non-smokers presented variations in relation to these characteristics, manifested randomly, and the group as a whole showed significance with regard to the muscle behavior performed during deglutition.

Studies in the literature show that the influence of olfactory and gustatory stimulation in swallowing is related to the stimulation of the glossopharyngeal nerve, which generates a motor response according to the stimulus presented⁽¹⁾. Moreover, the type of stimulus can modify the amplitude and the latency of a muscle contraction and increase the intraoral pressure exercised during the swallowing process⁽⁴⁾, activating the central pathways that elicit this reflex⁽⁵⁾. In addition to the fact that different stimuli prompt diverse motor responses, sensory recognition capability also affects swallowing performance positively, even if only for a short period after the stimulus is presented⁽⁴⁾. Given that sensory recognition capability is altered in smokers, changes occur in the normal functioning of the oral phase of swallowing, caused by modifications in the motor responses elicited by environmental stimuli. Once this stimulus pathway is less active, alterations in the muscle patterns of swallowing can be observed, such as perioral muscle compensation. Based on these data, it is possible to verify an inverse relation between sensory perception capability and deglutition functioning, as evidenced on Table 4.

According to the data we have described so far, olfactory and gustatory perception directly influences muscle behavior during swallowing in smokers. Added to this fact, we must also consider that the muscle movements performed during inhaling cigarette smoke is a factor that certainly influences this behavior, altering muscle formation due to the repetition of this action. However, although we considered the influence of this motor habit in the compensations observed, it does not seem sufficient to explain this situation, as we also observed an association between sensory perceptions of smell/taste and muscle compensation during swallowing in non-smokers.

Other aspects that must be considered when measuring the influence of smoking in sensory recognition capability and compensatory swallowing are the quantity of cigarettes and how long this substance has been consumed. In this study, we found that the quantity of cigarettes consumed influenced only the compensatory swallowing of the orbicularis muscle, which is attributed to an increase of muscle activity in this region, prompted by the movements of consuming tobacco, also increasing local tonicity^(22,25). Furthermore, it is known that the amount of nicotine consumed is directly related to tonicity and, consequently, to sensations of tension and relaxation; in other words, the higher the dose, the harder the muscle tonus and the sensation of rigidness⁽²⁵⁾.

Regarding the influence of the length of time of cigarette consumption, we found statistically significant results only for the compensation of the orbicularis muscle during the swallowing of liquid foods; this represents an inverse correlation, that is, the longer the time of tobacco consumption, the less compensatory swallowing performed by this muscle. In spite of this, we believe that the use of a larger number of individuals could have demonstrated significant results also for the deglutition of solid foods, given that the same type of movement is performed when swallowing this consistency. A plausible explanation for this occurrence was reported in a study on the sensation of relaxation brought by smoking. It is known that the liberation of nicotine in the central nervous system is stimulant; however, many individuals report a sensation of relaxation after smoking. This sensation was attributed to the fact that many smokers associated this habit with moments of relaxation, which, on a long-term basis, relates the habit to this condition⁽²⁵⁾. The same occurs in the case of oral muscles, as compensatory swallowing is a characteristic associated with excessive muscle tonicity, and, for this reason, the phenomenon cited above can occur after a long period of exposure to smoking. It is believed that this relation does not happen in the same way in the mentalis muscle because the latter is not directly exposed to alterations caused by tobacco; instead, it is indirectly affected by sensory modifications and by the functioning of other facial muscles, as described previously.

Concerning the influence of the quantity of cigarettes consumed and the time of consumption of this substance in characteristics of sensory perception, the statistical data found in this study do not corroborate previous research studies in which the authors state that olfactory and gustatory perceptions are directly related to these variables; in other words, the longer the time and the larger the quantity of cigarette consumption, the worse the performance on these tests⁽¹⁴⁾. Notwithstanding, the statistical data displayed on Table 5 point to a relational tendency between the time and quantity of tobacco consumption with alterations in sensory perceptions. We believe that studies with a larger number of participants might corroborate the data found in the literature. We observed divergences regarding the influence of time and quantity of cigarettes consumed, since time is inversely related, and quantity is directly related, to muscle compensations during swallowing. Nevertheless, the quantity of cigarettes consumed is a factor that has more relevance in the appearance of muscle compensations during deglutition, considering that smokers present more compensations in comparison to non-smokers. Furthermore, it is known that pulmonary debility is a risk factor for alterations in the normal functioning of swallowing, leading to dysphagia due to a lack of coordination between breathing and the transportation of the bolus to the stomach. Thus, both sensory perception alterations and pulmonary deficit become crucial aspects in diagnosing swallowing alterations^(9,10).

The influence of age in modifications of olfactory recognition capability remains controversial even in individuals not exposed to agents that change this perception. As observed in the present study, a previous research study showed that an individual's ability to recognize smells does not change with age, even in individuals who smoke⁽²⁶⁾. However, there are other works that show that this capability does change negatively even in non-smokers⁽²⁷⁾. We believe that this variety of results is due to the type of evaluation conducted. Authors who affirm that such decrease does not occur do not take into consideration the quantity of solute in the essence evaluated, but only the recognition or non-recognition of a substance. Thus, when it comes to olfactory aspects, this capability will remain preserved as long as the essences are tested with a quantity of solute that enables this recognition by individuals in different age ranges.

Concerning the sense of taste, age directly influences the recognition of some tastes in lower solute concentrations, but age does not influence an individual's capability of recognizing other tastes⁽²⁸⁾. Considering that we counted both types of response for the formulation of the total gustatory recognition score, there was no relation between the gustatory recognition score and the age of the individuals evaluated in this study.

With regard to gender, we did not find statistically significant results pertaining to the influence of this variable in olfactory and gustatory aspects. Upon comparing these findings to other data in the literature, we observed once again that the studies do not have results in common⁽²⁹⁾. This variability is attributed to the diversity of individuals evaluated, as the other studies were carried out with various populations exposed to different eating habits.

As for the influence of gender and age in compensatory swallowing, we did not find statistical correlations between these variables. Moreover, we did not find studies on the relation between compensatory swallowing and age in the literature. Nevertheless, considering that high compensation degrees are not expected in individuals who do not have associated comorbidities, that is, who present no alterations in the oral phase of swallowing, we believe that changes in an individual's normal pattern over time, even in smokers, could suggest a pathological process associated with ageing conditions, and that it should be analyzed more judiciously⁽³⁰⁾.

Considering the data discussed, it is important to highlight that speech-language pathologists are the professionals with expertise on deglutition alterations. Therefore, it is necessary to consider smoking as a factor that may influence swallowing alterations by affecting sensory perception. Detecting this risk factor is fundamental in thorough analyses of the etiology of deglutition modifications with the purpose of achieving an all-encompassing comprehension of alterations of phono-articulatory organs related to smoking and not limiting the investigations only to the modifications classically described in the literature.

In this study, we observed that smokers have inferior sensory recognition capability in comparison to non-smokers, and that this decrease implicates, significantly, in the appearance of muscle compensations during the process of swallowing. The data show that sensory modifications influence an individual's deglutition pattern, and that these alterations are aspects that must be considered in differential diagnoses of changes in deglutition.

Despite the important findings that have, for the first time, pointed to the influence of olfactory and gustatory changes in deglutition in smokers, evaluations conducted with a larger number of participants and maintaining the adequate methodological criteria are necessary for the purposes of confirming the results describe here and possibly bringing significance to aspects that were not recognized in this article. A suggestion for future studies is to include the participation of more evaluators to apply the study protocol, so as to minimize possible subjective influences that come from observations of a single evaluator during data collection.

CONCLUSION

Smokers have inferior sensory recognition capability in comparison to non-smokers, which implicates in the emergence of muscle compensation during swallowing.

ACKNOWLEDGMENTS

The conduction of this study was only possible thanks to the individuals who volunteered to be assessed, dedicating their time and patience to the process of testing; and to the incessant work of the authors and the fellows who read this article innumerable times, until it was satisfactorily written.

• Erratum

  In the article “Influence of gustatory and olfactory perception in the oral phase of swallowing in smokers”, published in journal CoDAS, 2014, volume 26, issue 1, the DOI number was published incorrectly.
  Where it reads:
  http://dx.doi.org/10.1590/S2317-17822014000100010
  It should be read:
  http://dx.doi.org/10.1590/2317-1782/20142013068

REFERENCES

• ¹
  Yamamura K, Kitagawa J, Kurose M, Sugino S, Takatsuji H, Mostafeezur RM, et al. Neural mechanisms of swallowing and effects of taste and other stimuli on swallow initiation. Biol Pharm Bull. 2010;33(11):1786-90.
• ²
  Estrela F, Schneider FL, Aquini MG, Marrore ACH, Steffani MA, Jotz GP. Controle neurológico da deglutição. In: Jotz GP, De Angelis EC, Barros APB. Tratado da deglutição e disfagia: no adulto e na criança. Rio de Janeiro: Revinter; 2009. p. 30-4.
• ³
  Costa MMB, Santana E, Almeida J. Oral taste recognition in health volunteers. Arq Gastroenterol. 2010;47(2):152-8.
• ⁴
  Wahab NA, Jones RD, Huckabee ML. Effects of olfactory and gustatory stimuli on neural excitability for swallowing. Physiology & Behavior. 2010;101:568-75.
• ⁵
  Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25:323-33.
• ⁶
  Neto FXP, Targino MN, Peixoto VS, Alcâ;ntara FB, Jesus CC, Araújo DC, et al. Anormalidades sensoriais: olfato e paladar. Arq Int Otorrinolaringol. 2010;15(3):350-8.
• ⁷
  Brasil. Ministério da Saúde. Convenção-Quadro para o Controle do Tabaco. Rio de Janeiro: Instituto Nacional de Câ;ncer; 2010.
• ⁸
  Pinto M, Ugá MAD. Os custos de doenças tabaco-relacionadas para o Sistema Único de Saúde. Cad Saúde Pública. 2010;26(6):1234-45.
• ⁹
  Chaves RD, Carvalho CRF, Cukier A, Stelmach R, Andrade CRF. Sintomas indicativos de disfagia em portadores de DPOC. J Bras Pneumol. 2011;37(2): 176-83.
• ¹⁰
  Mokhlesi B. Clinical implications of gastroesophageal reflux disease and swallowing dysfunction in COPD. Am J Respir Med. 2003;2(2):117-21.
• ¹¹
  Henriques AA, Furtado AD, Vargas AF, Prado CBMDA, Barreto SSM. Implicações do fumo na gustação e na olfação - revisando o tema. Rev Bras Otorrinolaringol. 2010;66(5):521-6.
• ¹²
  Furlaneto CJ, Passaretti T, Junior CM. Políticas de controle ao uso do tabaco em ambiente de trabalho por empresas da Grande São Paulo. Rev Inst Ciênc Saúde. 2010;26(3):281-8.
• ¹³
  Briner HR, Simmen D. Smell Diskettes as a screening test of olfaction. Rhinology.1999;37:145-8.
• ¹⁴
  Vennemann MM, Hummel T, Berger K. The association between smoking and smell and taste impairment in the general population. J Neurol. 2008;255:1121-6.
• ¹⁵
  Pavlidis P, Nikolaidis V, Anogeianaki A, Koutsonikolas D, Kekes G, Anogianakis G. Evaluation of young smokers and non-smokers with Electrogustometry and Contact Endoscopy. BMC Ear Nose Throat Disord. 2009;9:9.
• ¹⁶
  Borges CRMB, Ferreira TAPC, Silveira EA. Limite de detecção de gostos básicos: fatores associados ao tabagismo. In: Compeex - Congresso de Pesquisa, Ensino e Extensão; 2011. Out 22-26. Goiás.
• ¹⁷
  Sato K, Endo S, Tomita H. Sensitivity of three loci on the tongue and soft palate to four basic tastes in smokers and non-smokers. Acta Otolaryngol Suppl. 2002;122(4):74-82.
• ¹⁸
  Deems DA, Doty RL, Settle RG, Moore-Gillon V, Shaman P, Mester AF, et al. Smell and taste disorders, a study of 750 patients from the University of Pennsylvania. Arch Otolaryngol Head Neck Surg. 1991;117(5):519-28.
• ¹⁹
  Katotomichelakis M, Balatsouras D, Tripsianis G, Davris S, Maroudias N, Danielides V, et al. The effect of smoking on the olfactory function. Rhinology. 2007;45(4):273-80.
• ²⁰
  Vent J, Robinson AM, Gentry-Nielsen MJ, Conley DB, Hallworth R, Leopold DA, et al. Pathology of the olfactory epithelium: smoking and ethanol exposure. Laryngoscope. 2004;114(8):1383-8.
• ²¹
  Altman EBC. Deglutição atípica. In: Kudo AM (coord.). Fisioterapia, Fonoaudiologia e Terapia Ocupacional em Pediatria. São Paulo: Sarvier; 1990. p. 116-31.
• ²²
  Mueller V, Mucha RF, Pauli P. Electromyographic activity of the lip muscle as a measure of puffing on a cigarette. Physiol Behav. 2003;78(4-5):741-9.
• ²³
  Lima RMF, Amaral AKFJ, Aroucha EBL, Vasconcelos TMJ, Silva HJ, Cunha DA. Adaptações na mastigação, deglutição e fonoarticulação em idosos de instituição de longa permanência. Revista CEFAC. 2009;11(3):405-22.
• ²⁴
  Oliveira AC, Anjos CAL, Silva ÉHAA, Menezes PL. Aspectos indicativos de envelhecimento facial precoce em respiradores orais adultos. Pró-Fono. 2009;19(3):305-12.
• ²⁵
  Fagerström KO, Götestam KG. Increase of muscle tonus after tobacco smoking. Addict Behav. 1977;2(4):203-6.
• ²⁶
  Wysocki CJ, Gilbert AN. National geographic smell survey: effects of age are heterogenous. Ann N Y Acad Sci. 1989;561:12-28.
• ²⁷
  Heft MW, Robinson ME. Age differences in orofacial sensory thresholds. J Dent Res. 2010;89(10):1102-5.
• ²⁸
  Mojet J, Christ-Hazelhof E, Heidema J. Taste perception with age: generic or specific losses in threshold sensitivity to the five basic tastes? Chem Senses. 2011;26(7):845-60.
• ²⁹
  Stinton N, Atif MA, Barkat N, Doty RL. Influence of smell loss on taste function. Behav Neurosci. 2010;124(2):256-64.
• ³⁰
  Cook IJ. Oropharyngeal dysphagia. Gastroenterol Clin North Am. 2010;38(3):411-31.

• Study carried out at the Universidade Federal de Ciências da Saúde de Porto Alegre - UFCSPA - Porto Alegre (RS), Brazil.
• *KWS and DCGMV were responsible for data collection, database tabulation, and manuscript writing; SSE contributed with data tabulation and analysis, and preparation of the tables and statistical data of the manuscript.

Publication Dates

• Publication in this collection
  Feb 2014

History

• Received
  18 Apr 2013
• Accepted
  13 Dec 2013