OBES SURG DOI 10.1007/s11695-015-1683-x
ORIGINAL CONTRIBUTIONS
Olfactory and Gustatory Function After Bariatric Surgery Franca Holinski 1 & Charalambos Menenakos 2 & Georg Haber 2 & Heidi Olze 1 & Juergen Ordemann 2
# Springer Science+Business Media New York 2015
Abstract Background Neither hormone levels nor malabsorption alone fully explains the distinct weight loss after bariatric surgery in morbidly obese patients. Postoperatively, patients regularly report a change in the sense of taste and the development of food aversions. Hedonic and sensory components like olfactory and gustatory stimuli significantly affect appetite and flavour. Methods We prospectively analysed the orthonasal olfactory and gustatory function with psychophysical testing in 44 patients undergoing laparoscopic Roux-en-Y gastric bypass (RYGB), sleeve gastrectomy (SG) or adjustable gastric banding (AGB) and in 23 healthy controls. Results About 22.7 % of morbidly obese patients were hyposmic, showing significantly lower thresholddiscrimination-identification (TDI) scores (p=0.009) with decreased discrimination and identification ability. In addition, 22.7 % of patients were tested to be limited in gustatory function, with significantly lower taste strip test (TST) scores (p= 0.003). Six months after surgery, olfactory and gustatory function was not different when compared to healthy controls. Conclusions Due to obesity, patients frequently show impaired olfactory and gustatory function. Six months after laparoscopic bariatric surgery, both chemosensory functions * Franca Holinski [email protected] 1
Department of Otorhinolaryngology, Head, and Neck Surgery, Charité, University Medicine Berlin, Charité Campus Mitte, Charitéplatz 1, 10117 Berlin, Germany
2
Centre for Bariatric and Metabolic Surgery, Department of General, Visceral, Vascular, and Thoracic Surgery, Charité, University Medicine Berlin, Charité Campus Mitte, Charitéplatz 1, 10117 Berlin, Germany
improve. The TDI test is an appropriate tool to measure olfactory function in obese patients. Keywords Olfactory function . Gustatory function . Obesity surgery . Bariatric surgery . Gastric banding . Sleeve gastrectomy . Threshold-discrimination-identification test . Taste strip test . Bypass surgery
Introduction Worldwide, the proportion of obese people doubled between 1980 and 2008 [1]. In the treatment of morbid obesity, bariatric surgery is considered the gold standard [2], i.e. it results in a grand and lasting loss of weight as well as a reduction of considerable co-morbidities. Obese patients, who undergo laparoscopic Roux-en-Y gastric bypass (RYGB) and laparoscopic adjustable gastric banding (AGB), regularly report a change of taste and the development of food aversions [3]. The reasons for the onset of these symptoms remain unclear, although there are several hypotheses. One of them is that they might result from neurobiological changes in the hypothalamus satiety and hunger regulation areas [4]. Secondary to the restrictive component, surgery may lower ingestion by diminished feelings of hunger, i.e. the enhanced release of satiating hormones like glucagon-like peptide (GLP)-1 and peptide YY (PYY) as well as a reduced plasma level of the hunger-promoting ghrelin [5]. Without doubt, research indicates that changes in plasma ghrelin and malabsorption cannot fully explain the magnitude of weight loss after bariatric surgery. Several studies indicate that olfactory stimuli significantly affect two main factors: namely the experience of flavours in the majority of food as well as appetite [6]. Sensory and hedonic components of food-related flavours depend on
OBES SURG
olfactory perception. Research also indicates that olfactory perception-related food preferences are not innate, but they are rather learnt during life. Food-related odours reliably stimulate salivation, insulin release and gastric acid secretion [6]. De Wijk et al. found that the orthonasal odour perception, rather than flavour, might be a better predictor of short-term intake and over-eating [7]. Jurowich et al. observed a significant increase in olfactory function as measured with the threshold-discrimination-identification (TDI) test (i.e. the threshold score) in highly obese patients within 24 weeks after sleeve gastrectomy (SG), but not after RYGB. They suggest that substantial weight loss per se does not affect the olfactory function [8]. With cross-cultural smell identification test (CCSIT), Richardson et al. found that olfactory dysfunction did not significantly change after RYGB in 55 patients. Further, they suggest that absolute olfactory dysfunction is not a result of obesity but maybe a contributing factor influencing the development of obesity [9]. With a survey, Tichansky et al. found a change (in 82 % RYGB, 46 % AGB) and partial loss in taste (in 92 % AGB, 59 % RYGB) in highly obese patients [3]. So far, only a few studies exist investigating the gustatory function in obese subjects. These studies are lacking controls as well as a great number of patients. Data suggest that taste thresholds, i.e. sweet thresholds, alter to lower concentrations after RYGB. Finally, the different methods used have led to incongruent published results [10]. To consolidate this data, we have, for the first time, in this study, prospectively analysed the orthonasal olfactory function and the gustatory function with psychophysical testing in highly obese adult patients undergoing laparoscopic bariatric surgery. We compared the data with that of a healthy control group.
Methods Patient Inclusion Between January 2011 and April 2012, highly obese patients (BMI >40 or >35 kg/m2 with relevant co-morbidities) who submitted to bariatric surgery were recruited from the ambulatory service of the centre for bariatric and metabolic surgery of our institution in compliance with the international guidelines concerning indications for bariatric surgery [11]. At the same time, we included a control group consisting of healthy, non-obese subjects derived from the staff of our hospital and students. Numerous exclusion criteria were included and determined upfront using a questionnaire such as age below 18 or above 65 years, pregnancy, illnesses that are known to affect olfaction (such as Parkinson’s syndrome, Alzheimer, posttraumatic olfactory dysfunction, post-upper respiratory tract infection, allergy, sinonasal disease, endonasal surgery with
olfactory disorder, existence or therapy of a malignant tumour via radiotherapy and chemotherapy) and previous bariatric surgery. An otorhinolaryngologist examined each participant and, through nasal endoscopy, evaluated the anatomy of the nasal cavities and olfactory cleft. Those whose sense of smell could possibly be affected by anatomical abnormalities were excluded. Further otorhinolaryngeal testing comprised of the TDI test (psychophysical orthonasal olfactory function) and the taste strip test (psychophysical gustatory function). The tests were conducted directly before surgery (V0) as well as 2 weeks (V1), 3 weeks (V2) and 6 months (V3) after surgery. The trial was registered with and approved by the local medical ethics committee (EA4/087/11). All the participants gave their written informed consent. The patients underwent one of the following laparoscopic bariatric procedures: AGB, SG or RYGB. The decision as to which procedure to use was made based on international guidelines. The procedures had been performed by two surgeons specialised in bariatric surgery using standard minimal invasive surgical techniques. Orthonasal Olfactory Function with TDI Test The TDI test (Sniffin’ sticks test battery; Burghart, Wedel, Germany) is standardised and recommended by the working group on olfaction and gustation of the German Society for Otorhinolaryngology, Head and Neck Surgery [12]. It is a tripartite instrument measuring threshold (T), discrimination (D) and identification (I) ability with each of 16 odoriferous pens. Participants are partly blindfolded and have to make a choice (forced choice) in this procedure to identify their olfactory function in, preferably, an objective manner. The TDI test is a reliable (r=0.72) and validated tool [13]. For odour presentation, the pen cap is removed for approximately 3 s and the tip of the pen is placed approximately 1–2 cm in front of the nostrils. Thresholds are determined using a single-staircase technique. Two successive correct identifications of the pen containing the odour or one incorrect identification trigger a reversal of the staircase to the next higher or the next lower dilution step. Seven reversals have to be obtained. The threshold is determined as the mean of the last four staircase reversals. For odour discrimination (D), 16 triplets of pens are presented, with two containing the same odorant and one containing the target odorant. The subjects’ task is to identify the sample with a different smell. The test result is the sum score of correctly identified pens. Odour identification is assessed for 16 common odours (orange, leather, cinnamon, menthol, banana, lemon, liquorice, garlic, coffee, apple, pineapple, rose, fish, anise, clove and turpentine), and the subjects identify odours by selecting the best label from a list of four descriptors. Results of the three subtests are presented as a composite TDI score (range 1–48), which is the sum of the results
OBES SURG
obtained for threshold (range 1–16), discrimination (range 0– 16) and identification (range 0–16) measures. A composite score of 15 or less indicates functional anosmia, up to 30 indicates hyposmia, while above 30 is indicative of normosmia.
Olfactory Function
Filter paper strips [14] (taste strips; Burghart, Wedel, Germany) with the tip area impregnated with one of the four basic qualities (sweet, sour, bitter and salty) were presented in four concentrations each (sweet 0.4, 0.2, 0.1 and 0.05 g/ml sucrose; sour 0.3, 0.165, 0.09 and 0.05 g/ml citric acid; salty 0.25, 0.1, 0.04 and 0.016 g/ml sodium chloride; bitter 0.006, 0.0024, 0.0009 and 0.0004 g/ml quinine hydrochloride). Distilled water was used as solvent. Sixteen strips were applied in a randomised fashion to the middle of the anterior third of the extended tongue, and the participants had to identify them using force choice paradigm. Before each administration, the mouth was rinsed with water. A score between 16 and 9 indicates a normal gustatory function, and a score below 9 indicates a limited gustatory function. Repeated measures indicated good reproducibility of the results for the taste strips (r69=0.68) [14].
Ten of 44 (22.7 %) patients and two of 23 (8.7 %) controls were defined hyposmic in the preoperative testing (V0), demonstrating significantly lower TDI scores in obese patients (32.7±3.5 vs. 35.2±4.0, p=0.009, Table 2). None of the participants were categorised as anosmic at all time points. Seven of the 10 (70 %) hyposmic patients and zero out of 2 (0 %) hyposmic controls changed to normal olfactory function 6 months postoperatively (V3). Three of 34 (8.8 %) patients and one of 21 (4.8 %) controls with normal olfactory function changed to hyposmic categorization 6 months postoperatively (V3). Compared to almost stable TDI scores in the control group, the TDI score in obese patients significantly increased 6 months after surgery (p=0.011), mainly based on a significant increase of the discrimination score (p=0.01). After 6 months, six of the 44 (13.6 %) patients and three of the 23 (13.0 %) controls were defined as hyposmic, showing no significant difference in their TDI score (34.3±3.5 vs. 35.6±3.4, p=0.15, Table 2). Compared to the controls, at all time points, the identification scores of the patients were significantly lower (V0: p=0.05, V3: p=0.012, Table 2). In the course of the study, patients showed a tendency towards lowered TDI scores (i.e. T and I subscores) post surgery (V1) rising again at 3 (V2) and 6 (V3) months (Fig. 1).
Statistical Analyses
Gustatory Function
The collected data were analysed using SPSS 21.0 for Windows (IBM Deutschland GmbH). Data are reported as mean and standard deviation (SD). A normal distribution of continuous data was examined and confirmed with the Shapiro-Wilk test. Differences in body weight, BMI and TDI and taste strip scores (aggregated and in domains; preoperatively (V0) and postoperatively (V1–3)) were assessed with paired Student’s t test within groups and Student’s t test and one-way analysis of variance (ANOVA) for comparisons between groups. Pearson’s correlation coefficient (r) was evaluated for correlations. A difference was considered significant at a p value of
ORIGINAL CONTRIBUTIONS
Olfactory and Gustatory Function After Bariatric Surgery Franca Holinski 1 & Charalambos Menenakos 2 & Georg Haber 2 & Heidi Olze 1 & Juergen Ordemann 2
# Springer Science+Business Media New York 2015
Abstract Background Neither hormone levels nor malabsorption alone fully explains the distinct weight loss after bariatric surgery in morbidly obese patients. Postoperatively, patients regularly report a change in the sense of taste and the development of food aversions. Hedonic and sensory components like olfactory and gustatory stimuli significantly affect appetite and flavour. Methods We prospectively analysed the orthonasal olfactory and gustatory function with psychophysical testing in 44 patients undergoing laparoscopic Roux-en-Y gastric bypass (RYGB), sleeve gastrectomy (SG) or adjustable gastric banding (AGB) and in 23 healthy controls. Results About 22.7 % of morbidly obese patients were hyposmic, showing significantly lower thresholddiscrimination-identification (TDI) scores (p=0.009) with decreased discrimination and identification ability. In addition, 22.7 % of patients were tested to be limited in gustatory function, with significantly lower taste strip test (TST) scores (p= 0.003). Six months after surgery, olfactory and gustatory function was not different when compared to healthy controls. Conclusions Due to obesity, patients frequently show impaired olfactory and gustatory function. Six months after laparoscopic bariatric surgery, both chemosensory functions * Franca Holinski [email protected] 1
Department of Otorhinolaryngology, Head, and Neck Surgery, Charité, University Medicine Berlin, Charité Campus Mitte, Charitéplatz 1, 10117 Berlin, Germany
2
Centre for Bariatric and Metabolic Surgery, Department of General, Visceral, Vascular, and Thoracic Surgery, Charité, University Medicine Berlin, Charité Campus Mitte, Charitéplatz 1, 10117 Berlin, Germany
improve. The TDI test is an appropriate tool to measure olfactory function in obese patients. Keywords Olfactory function . Gustatory function . Obesity surgery . Bariatric surgery . Gastric banding . Sleeve gastrectomy . Threshold-discrimination-identification test . Taste strip test . Bypass surgery
Introduction Worldwide, the proportion of obese people doubled between 1980 and 2008 [1]. In the treatment of morbid obesity, bariatric surgery is considered the gold standard [2], i.e. it results in a grand and lasting loss of weight as well as a reduction of considerable co-morbidities. Obese patients, who undergo laparoscopic Roux-en-Y gastric bypass (RYGB) and laparoscopic adjustable gastric banding (AGB), regularly report a change of taste and the development of food aversions [3]. The reasons for the onset of these symptoms remain unclear, although there are several hypotheses. One of them is that they might result from neurobiological changes in the hypothalamus satiety and hunger regulation areas [4]. Secondary to the restrictive component, surgery may lower ingestion by diminished feelings of hunger, i.e. the enhanced release of satiating hormones like glucagon-like peptide (GLP)-1 and peptide YY (PYY) as well as a reduced plasma level of the hunger-promoting ghrelin [5]. Without doubt, research indicates that changes in plasma ghrelin and malabsorption cannot fully explain the magnitude of weight loss after bariatric surgery. Several studies indicate that olfactory stimuli significantly affect two main factors: namely the experience of flavours in the majority of food as well as appetite [6]. Sensory and hedonic components of food-related flavours depend on
OBES SURG
olfactory perception. Research also indicates that olfactory perception-related food preferences are not innate, but they are rather learnt during life. Food-related odours reliably stimulate salivation, insulin release and gastric acid secretion [6]. De Wijk et al. found that the orthonasal odour perception, rather than flavour, might be a better predictor of short-term intake and over-eating [7]. Jurowich et al. observed a significant increase in olfactory function as measured with the threshold-discrimination-identification (TDI) test (i.e. the threshold score) in highly obese patients within 24 weeks after sleeve gastrectomy (SG), but not after RYGB. They suggest that substantial weight loss per se does not affect the olfactory function [8]. With cross-cultural smell identification test (CCSIT), Richardson et al. found that olfactory dysfunction did not significantly change after RYGB in 55 patients. Further, they suggest that absolute olfactory dysfunction is not a result of obesity but maybe a contributing factor influencing the development of obesity [9]. With a survey, Tichansky et al. found a change (in 82 % RYGB, 46 % AGB) and partial loss in taste (in 92 % AGB, 59 % RYGB) in highly obese patients [3]. So far, only a few studies exist investigating the gustatory function in obese subjects. These studies are lacking controls as well as a great number of patients. Data suggest that taste thresholds, i.e. sweet thresholds, alter to lower concentrations after RYGB. Finally, the different methods used have led to incongruent published results [10]. To consolidate this data, we have, for the first time, in this study, prospectively analysed the orthonasal olfactory function and the gustatory function with psychophysical testing in highly obese adult patients undergoing laparoscopic bariatric surgery. We compared the data with that of a healthy control group.
Methods Patient Inclusion Between January 2011 and April 2012, highly obese patients (BMI >40 or >35 kg/m2 with relevant co-morbidities) who submitted to bariatric surgery were recruited from the ambulatory service of the centre for bariatric and metabolic surgery of our institution in compliance with the international guidelines concerning indications for bariatric surgery [11]. At the same time, we included a control group consisting of healthy, non-obese subjects derived from the staff of our hospital and students. Numerous exclusion criteria were included and determined upfront using a questionnaire such as age below 18 or above 65 years, pregnancy, illnesses that are known to affect olfaction (such as Parkinson’s syndrome, Alzheimer, posttraumatic olfactory dysfunction, post-upper respiratory tract infection, allergy, sinonasal disease, endonasal surgery with
olfactory disorder, existence or therapy of a malignant tumour via radiotherapy and chemotherapy) and previous bariatric surgery. An otorhinolaryngologist examined each participant and, through nasal endoscopy, evaluated the anatomy of the nasal cavities and olfactory cleft. Those whose sense of smell could possibly be affected by anatomical abnormalities were excluded. Further otorhinolaryngeal testing comprised of the TDI test (psychophysical orthonasal olfactory function) and the taste strip test (psychophysical gustatory function). The tests were conducted directly before surgery (V0) as well as 2 weeks (V1), 3 weeks (V2) and 6 months (V3) after surgery. The trial was registered with and approved by the local medical ethics committee (EA4/087/11). All the participants gave their written informed consent. The patients underwent one of the following laparoscopic bariatric procedures: AGB, SG or RYGB. The decision as to which procedure to use was made based on international guidelines. The procedures had been performed by two surgeons specialised in bariatric surgery using standard minimal invasive surgical techniques. Orthonasal Olfactory Function with TDI Test The TDI test (Sniffin’ sticks test battery; Burghart, Wedel, Germany) is standardised and recommended by the working group on olfaction and gustation of the German Society for Otorhinolaryngology, Head and Neck Surgery [12]. It is a tripartite instrument measuring threshold (T), discrimination (D) and identification (I) ability with each of 16 odoriferous pens. Participants are partly blindfolded and have to make a choice (forced choice) in this procedure to identify their olfactory function in, preferably, an objective manner. The TDI test is a reliable (r=0.72) and validated tool [13]. For odour presentation, the pen cap is removed for approximately 3 s and the tip of the pen is placed approximately 1–2 cm in front of the nostrils. Thresholds are determined using a single-staircase technique. Two successive correct identifications of the pen containing the odour or one incorrect identification trigger a reversal of the staircase to the next higher or the next lower dilution step. Seven reversals have to be obtained. The threshold is determined as the mean of the last four staircase reversals. For odour discrimination (D), 16 triplets of pens are presented, with two containing the same odorant and one containing the target odorant. The subjects’ task is to identify the sample with a different smell. The test result is the sum score of correctly identified pens. Odour identification is assessed for 16 common odours (orange, leather, cinnamon, menthol, banana, lemon, liquorice, garlic, coffee, apple, pineapple, rose, fish, anise, clove and turpentine), and the subjects identify odours by selecting the best label from a list of four descriptors. Results of the three subtests are presented as a composite TDI score (range 1–48), which is the sum of the results
OBES SURG
obtained for threshold (range 1–16), discrimination (range 0– 16) and identification (range 0–16) measures. A composite score of 15 or less indicates functional anosmia, up to 30 indicates hyposmia, while above 30 is indicative of normosmia.
Olfactory Function
Filter paper strips [14] (taste strips; Burghart, Wedel, Germany) with the tip area impregnated with one of the four basic qualities (sweet, sour, bitter and salty) were presented in four concentrations each (sweet 0.4, 0.2, 0.1 and 0.05 g/ml sucrose; sour 0.3, 0.165, 0.09 and 0.05 g/ml citric acid; salty 0.25, 0.1, 0.04 and 0.016 g/ml sodium chloride; bitter 0.006, 0.0024, 0.0009 and 0.0004 g/ml quinine hydrochloride). Distilled water was used as solvent. Sixteen strips were applied in a randomised fashion to the middle of the anterior third of the extended tongue, and the participants had to identify them using force choice paradigm. Before each administration, the mouth was rinsed with water. A score between 16 and 9 indicates a normal gustatory function, and a score below 9 indicates a limited gustatory function. Repeated measures indicated good reproducibility of the results for the taste strips (r69=0.68) [14].
Ten of 44 (22.7 %) patients and two of 23 (8.7 %) controls were defined hyposmic in the preoperative testing (V0), demonstrating significantly lower TDI scores in obese patients (32.7±3.5 vs. 35.2±4.0, p=0.009, Table 2). None of the participants were categorised as anosmic at all time points. Seven of the 10 (70 %) hyposmic patients and zero out of 2 (0 %) hyposmic controls changed to normal olfactory function 6 months postoperatively (V3). Three of 34 (8.8 %) patients and one of 21 (4.8 %) controls with normal olfactory function changed to hyposmic categorization 6 months postoperatively (V3). Compared to almost stable TDI scores in the control group, the TDI score in obese patients significantly increased 6 months after surgery (p=0.011), mainly based on a significant increase of the discrimination score (p=0.01). After 6 months, six of the 44 (13.6 %) patients and three of the 23 (13.0 %) controls were defined as hyposmic, showing no significant difference in their TDI score (34.3±3.5 vs. 35.6±3.4, p=0.15, Table 2). Compared to the controls, at all time points, the identification scores of the patients were significantly lower (V0: p=0.05, V3: p=0.012, Table 2). In the course of the study, patients showed a tendency towards lowered TDI scores (i.e. T and I subscores) post surgery (V1) rising again at 3 (V2) and 6 (V3) months (Fig. 1).
Statistical Analyses
Gustatory Function
The collected data were analysed using SPSS 21.0 for Windows (IBM Deutschland GmbH). Data are reported as mean and standard deviation (SD). A normal distribution of continuous data was examined and confirmed with the Shapiro-Wilk test. Differences in body weight, BMI and TDI and taste strip scores (aggregated and in domains; preoperatively (V0) and postoperatively (V1–3)) were assessed with paired Student’s t test within groups and Student’s t test and one-way analysis of variance (ANOVA) for comparisons between groups. Pearson’s correlation coefficient (r) was evaluated for correlations. A difference was considered significant at a p value of
