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Research Article
Originally Published 31 October 2017
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Enjoyment of Spicy Flavor Enhances Central Salty-Taste Perception and Reduces Salt Intake and Blood Pressure

Qiang Li, Yuanting Cui, Rongbing Jin, Hongmei Lang, Hao Yu, Fang Sun, Chengkang He, … Show All … , Tianyi Ma, Yingsha Li, Xunmei Zhou, Daoyan Liu, Hongbo Jia, Xiaowei Chen, and Zhiming ZhuAuthor Info & Affiliations
Hypertension
Volume 70, Number 6
https://doi.org/10.1161/HYPERTENSIONAHA.117.09950
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Abstract

High salt intake is a major risk factor for hypertension and is associated with cardiovascular events. Most countries exhibit a traditionally high salt intake; thus, identification of an optimal strategy for salt reduction at the population level may have a major impact on public health. In this multicenter, random-order, double-blind observational and interventional study, subjects with a high spice preference had a lower salt intake and blood pressure than subjects who disliked spicy food. The enjoyment of spicy flavor enhanced salt sensitivity and reduced salt preference. Salt intake and salt preference were related to the regional metabolic activity in the insula and orbitofrontal cortex (OFC) of participants. Administration of capsaicin—the major spicy component of chili pepper—enhanced the insula and OFC metabolic activity in response to high-salt stimuli, which reversed the salt intensity–dependent differences in the metabolism of the insula and OFC. In animal study, OFC activity was closely associated with salt preference, and salty-taste information processed in the OFC was affected in the presence of capsaicin. Thus, interventions related to this region may alter the salt preference in mice through fiber fluorometry and optogenetic techniques. In conclusion, enjoyment of spicy foods may significantly reduce individual salt preference, daily salt intake, and blood pressure by modifying the neural processing of salty taste in the brain. Application of spicy flavor may be a promising behavioral intervention for reducing high salt intake and blood pressure.

Introduction

See Editorial Commentary, pp 1087–1088
High salt intake is a major risk factor for hypertension and is associated cardiovascular events.1–3 The World Health Organization has proposed salt reduction as the key dietary target for 2025 to reduce mortality from the main noncommunicable diseases.4 Most countries in the world have a traditionally high salt intake and consume dietary salt far beyond the 5 g/d recommended by the World Health Organization.5–7 The worldwide prevalence of hypertension has tremendously increased during the previous several decades.8 Thus, effectively restricting salt consumption is crucial for preventing hypertension induced by high salt intake in the population.
Current measures for reducing salt intake include education on healthy lifestyles, a campaign for the use of salt spoons, and the promotion of low-sodium salt with the addition of magnesium and potassium.9 However, traditional cooking habits and changes in the taste of food have dampened the effectiveness of salt reduction at the population level.6,7 High salt intake is associated with altered salt sensitivity and the development of a demand for salted food.9,10 Thus, an alternative strategy for reducing salt intake may be to modify the perception of saltiness.
It is well established that the central gustatory system and the mesolimbic structures are critical for taste signal processing and hedonic responses to foods. Palatability is the consequence of the stimulation of brain reward pathways, which indicates that an individual’s salt preference may be associated with the neural hedonic properties of salted foods.11 The orbitofrontal cortex (OFC), as the secondary taste cortex, has been shown to be specifically associated with hedonic aspects and thus the subjective pleasantness of taste.12
Capsaicin—the major pungent component of chili pepper—has been shown to influence salt sensitivity in humans.13 Epidemiological and experimental studies have indicated an extensive protective role of spicy food or capsaicin against cardiometabolic diseases.14–18 It is worth examining whether spicy food consumption may reduce dietary salt intake and whether spicy flavor may affect salty-taste perception. Therefore, we hypothesized that capsaicin administration could reduce salt intake by modifying the neural processing of salty-taste signals. To test this hypothesis, we initially examined the participants’ preferences for salty and spicy flavors, salt intake, and blood pressure in a community-based cross-sectional study. We subsequently validated the effect of capsaicin on the neural perception of saltiness through a randomized, double-blind interventional study. Finally, we validated our hypothesis in rodents using optogenetic approaches.

Methods

Detailed Methods are provided in the online-only Data Supplement. The human study was conducted according to the principles of the Declaration of Helsinki. All protocols and experimental procedures were approved by the institutional ethics committee of the hospital, Institutional Animal Care and Research Advisory Committee, Daping Hospital, Third Military Medical University.

Statistical Analyses

In human study, the baseline characteristics of the participants were compared between the groups using the χ2 test for categorical variables and the 2 sample t test for continuous variables. The 2 sample t test was used to evaluate differences in the positron emission tomography images between the groups. Linear regression analysis was performed to assess the relationships among salt intake, salt preference, and changes in regional glucose metabolism. Multivariable adjustment for variables, including age, sex, educational level, work status, fasting blood glucose, body mass index, and waist circumstance, as well as the corresponding 95% confidence intervals (95% CIs), were estimated by covariance analysis with a univariate general linear model. Numeric results are presented as the mean±SD or the mean and 95% CI. The positron emission tomography/computed tomography images were processed using statistical parametric mapping (SPM 8.0), and a critical P≤0.005 (uncorrected) with a cluster filter of 5 voxels (1 voxel=8 mm3) was used to identify significant differences. SPM{t} maps were superimposed on a standard magnetic resonance imaging brain template. In the animal study, the results are represented as the mean±SEM. Comparisons between the groups were made using a 2-tailed unpaired Student t test or 1-way ANOVA with Tukey multiple comparisons test. The Mann–Whitney nonparametric U test was used to analyze data with an abnormal distribution. Numeric statistical analyses were conducted using SPSS software, version 13.0 (SPSS, Inc), or GraphPad Prism software, version 5.0 (GraphPad Software); a 2-sided P value of <0.05 indicated statistical significance.

Results

Baseline Characteristics of the Study Participants

The baseline characteristics of the participants are presented in Table 1. A preference for higher salt was associated with an older age, heavier physical labor, higher prevalence of hypertension, and lower levels of education. Sensitivity to salt was also changed in the high-salt preference group, along with a less sensitive perception of saltiness (P=0.02) and a higher threshold for declaring a solution to be intolerably salty (P<0.01). Notably, the qualitative analysis indicated a graded effect of salt preference on daily salt intake (P<0.01), with mean values of 11.7±4.8, 13.1±5.3, and 14.3±4.7 g/d in the low-, medium-, and high-salt preference groups, respectively. The participants with a high salt preference had higher systolic blood pressure (131±15 versus 122±18 mm Hg, respectively; P<0.001) and diastolic blood pressure (82±11 versus 75±11 mm Hg, respectively; P<0.001) than the participants who had a low salt preference. Our findings indicated only minor changes after adjustment for several participant characteristics (Table S2 in the online-only Data Supplement). The participants with a high salt preference had higher salt intake (≈1.8 g/d; 95% CI, 0.7–2.9 g/d; P<0.01), systolic blood pressure (≈5.0 mm Hg; 95% CI, 1.7–8.4 mm Hg; P<0.01), and diastolic blood pressure (≈4.4 mm Hg; 95% CI, 2.0–6.7 mm Hg; P<0.001) than the participants who had a low salt preference.
Table 1. Characteristics of the Participants in the Cross-Sectional Study*
VariablesLow-Salt Preference Group (n=416)Medium-Salt Preference Group (n=94)High-Salt Preference Group (n=96)P Value
Age, y39.0±10.539.7±9.844.0±8.4<0.001
Male sex, n (%)202 (48.6)50 (53.2)36 (37.5)0.07
≥College graduate, n (%)196 (47.1)29 (30.9)11 (11.5)<0.001
Heavy physical labor, n (%)†141 (33.9)39 (41.5)50 (52.1)<0.01
BMI, kg/m2‡23.7±3.623.8±3.324.4±3.30.19
Type 2 diabetes mellitus, n (%)11 (2.6)2 (2.1)4 (4.2)0.65
Hypertension, n (%)76 (18.3)14 (14.9)32 (33.3)<0.01
Fasting plasma glucose, mmol/L5.4±1.35.3±1.35.4±0.90.94
Salt perception, mmol/L   0.02
 1092 (22.1)20 (21.3)15 (15.6) 
 30200 (48.1)38 (40.4)36 (37.5) 
 >50124 (29.8)36 (38.3)45 (46.9) 
Salty superthreshold, mmol/L   <0.01
 500208 (50.0)38 (40.4)28 (29.2) 
 75095 (22.8)28 (29.8)33 (34.4) 
 >1000113 (27.2)28 (29.8)35 (36.5) 
Spice preference, μmol/L   <0.01
 <3227 (54.6)61 (64.9)74 (77.1) 
 5148 (35.6)25 (26.6)18 (18.8) 
 741 (9.8)8 (8.5)4 (4.1) 
24-h urinary sodium excretion, mmol/24 h191.4±82.11221.9±90.47243.2±80.16<0.001
Salt intake, g/d§11.7±4.813.1±5.314.3±4.7<0.001
Blood pressure, mm Hg
 Systolic122±18124±16131±15<0.001
 Diastolic75±1177±1282±11<0.001
BMI indicates body mass index.
*
Plus-minus values are means±SD.
†
Work status includes light and heavy physical labor. Works like officer, teacher, casher, cooker, driver, doctor, and student are considered light physical labor, whereas works such as farmer, factory worker, wood worker, and construction worker are considered heavy physical labor.
‡
The BMI is the weight in kilograms divided by the square of the height in meters.
§
Daily salt intake was derived from 24-hour urinary sodium excretion, which has adjusted according to the reference.37,38

Spicy Flavor Reduced Salt Intake and Blood Pressure by Modifying Salt Preference and Sensitivity

We subsequently examined whether spicy flavor affected salt intake and blood pressure. A higher salt preference was associated with a lower spice preference, which was represented by the proportion of participants who rated a given capsaicin solution as tolerable (Table 1; P<0.01). Furthermore, a high spice preference was associated with a more sensitive perception of saltiness (Table S1; P=0.001) and a lower threshold for declaring a solution to be intolerably salty (Table S1; P=0.001). These findings indicated that a spice preference may affect salt preference and sensitivity.
Next, we investigated whether spice preference affected salt intake and thus blood pressure. A qualitative analysis indicated that the degree of spice preference affected salt intake and blood pressure (Figure 1A through 1C). The mean salt intake was 13.4±5.1, 10.9±4.5, and 10.3±3.9 g/d in the low, medium, and high-spice preference groups, respectively. Moreover, the participants with a high spice preference had a lower systolic blood pressure (118±15 versus 126±17 mm Hg, respectively; P<0.01) and lower diastolic blood pressure (73±9 versus 78±12 mm Hg, respectively; P<0.01) than the participants who had a low spice preference. These values showed few changes after adjustment for several participant characteristics (Table 2). After adjustment, the participants with a high spice preference maintained a lower salt intake (2.5 g/d; 95% CI, 1.1–3.8 g/d; P<0.001), lower systolic blood pressure (6.6 mm Hg; 95% CI, 2.4–10.9 mm Hg; P<0.01), and lower diastolic blood pressure (4.0 mm Hg; 95% CI, 1.0–7.0 mm Hg; P<0.05) than the participants who had a low spice preference.
Table 2. Effects of Spice Preference on Salt Intake and Blood Pressure
 Spice Preference GroupOriginal MeasurementDifference in Outcome Compared With the Reference Group (95% CI)
UnadjustedModel 1Model 2Model 3
Salt intake, g/d (95% CI)Low13.40 (reference)0 (reference)0 (reference) 
 Medium10.9−2.5 (−3.4 to −1.5)*−1.8 (−2.7 to −1.0)*−1.8 (−2.7 to −1.0)* 
 High10.3−3.1 (−4.5 to −1.7)*−2.5 (−3.9 to −1.1)*−2.5 (−3.8 to −1.1)* 
Systolic blood pressure, mm Hg (95% CI)Low1260 (reference)0 (reference)0 (reference)0 (reference)
 Medium121−4.9 (−8.8 to −1.1)†−1.4 (−4.1 to 1.4)−1.5 (−4.1 to 1.2)−1.1 (−3.8 to 1.6)
 High118−8.0 (−13.4 to −2.7)†−6.6 (−11.0 to −2.3)†‡−7.2 (−11.4 to −2.9)†‡−6.6 (−10.9 to −2.4)†‡
Diastolic blood pressure, mm Hg (95% CI)Low780 (reference)0 (reference)0 (reference)0 (reference)
 Medium75−3.4 (−5.8 to −1.0)†−1.3 (−3.2 to 0.6)−1.3 (−3.2 to 0.5)−1.1 (−3.0 to 0.8)
 High73−5.1 (−8.4 to −1.8)†−4.1 (−7.2 to −1.1)†−4.3 (−7.3 to −1.3)†−4.0 (−7.0 to −1.0)§
Model 1 includes adjustment for age, sex, educational level, and work status. Model 2 adjusts for model 1 parameters, as well as BMI and diabetes mellitus. Model 3 adjusts for model 2 parameters and daily salt intake. BMI indicates body mass index; and CI, confidence interval.
*
P<0.001, §P<0.05, †P<0.01, medium or high-spice preference groups vs low-spice preference group.
‡
P<0.05, high-spice preference groups vs medium-spice preference group.
Figure 1. Salty taste, salt intake, and blood pressure (BP) in participants according to spice preference. Participants were allocated to low, medium, and high-spice preference groups according to their favorite spicy concentrations in the spice-preference test. The individual salt preference scores were calculated according to the self-reported average frequency of salt food intake (for a detailed description, refer to the Methods in the online-only Data Supplement). Salt intake (A) and systolic (B) and diastolic (C) BP in the low, medium, and high-spice preference groups. **P<0.01, ***P<0.001, medium- or high-spice preference groups vs low-spice preference group.

Capsaicin Administration Increased Insular and OFC Responses to Salty Taste

High levels of cognitive processing influenced the responses to environmental stimuli, such as salty foods. We subsequently examined how brain metabolism changes in response to a salt stimulus in individuals with high salt consumption. The salt intake and salt preference scores were positively correlated with the regional metabolic activity as determined by positron emission tomography/computed tomography in the insula and OFC under stimulation with 150 or 200 mmol/L NaCl (Figure S1). In humans, responses recorded from the insula have been correlated with the subjective intensity of taste.19 Intensity-dependent changes in metabolic activity were identified in the insula and thalamus using different concentrations of NaCl stimulation (150 and 200 mmol/L; Figure S2). This finding indicated that increased brain metabolic activity is associated with high salt intake and high-salt preference scores in humans.
We subsequently addressed whether changes in salt-induced brain metabolic activity may be modified by capsaicin administration. A human behavioral study showed that capsaicin administration at 0.5 μmol/L did not produce a burning sensation on the tongue but did increase the perception of saltiness.13 We showed that 0.5-μmol/L capsaicin administration significantly increased activity in the insula and OFC in response to high salt stimulation (Figure 2A and 2B). Notably, the intensity-dependent metabolic activity changes reversed when 0.5 μmol/L capsaicin was added to the solution of 150 mmol/L NaCl (Figure 2C and 2D). Most importantly, the brain regions activated by capsaicin overlapped with the brain regions stimulated by salty taste (Figure 2E). These results indicate that capsaicin can modify the sensation of salt intensity via the activation of brain regions involved in the hedonic experience of salt.
Figure 2. Influence of capsaicin on salt taste cognitive processing and reward circuits. A and B, Increased glucose metabolism in the insula and orbitofrontal cortex (OFC) in response to capsaicin. The normalized glucose metabolism increased bilaterally in both the insula and the OFC with the oral administration of 150 mmol/L NaCl combined with capsaicin compared with those without capsaicin administration. The images represent 2 sample t tests for the 150 mmol/L plus capsaicin group (n=8) vs the 150-mmol/L NaCl group (n=8). ***P<0.001, 150 mmol/L plus capsaicin group vs 150-mmol/L NaCl group. C and D, The dose-dependent increase in glucose metabolism in the insula and OFC was compensated for by the addition of capsaicin in a lower concentration salt solution. The images show 2 sample t tests for the 150 mmol/L plus capsaicin group (n=8) vs the 200-mmol/L NaCl group (n=8). ***P<0.001, the 200-mmol/L NaCl group vs the 150 mmol/L plus capsaicin group. A volume of interest (VOI; 2 mm radius) centered at the peak voxel of clusters within the image space was established to calculate the relative metabolism in the 2 groups. The peak coordinates of each VOI are provided in parentheses. The significance threshold was set at P<0.005, and SPM t-v maps were superimposed on a standard magnetic resonance imaging (MRI) brain template. E, Brain regions with significant metabolic differences in the comparisons between the 150-mmol/L NaCl group and the 150 mmol/L plus capsaicin group (red) and between the 150 mmol/L plus capsaicin group and the 200-mmol/L NaCl group (blue). The normalized glucose metabolism in the insula and OFC was higher in the 150 mmol/L plus capsaicin group than the 150-mmol/L NaCl group or the 200-mmol/L NaCl group. The significance threshold was set at P<0.005, and SPM t maps of the 2 sample t tests for each comparison were superimposed on 1 standard MRI brain template.

Peripheral Salty-Taste Signals and Spicy Flavor Evoked Neuronal Population Activities of OFC

We further examined the findings in rodent models. We used a fiber fluorometry method to record the neuronal population activity in terms of calcium wave signals20 and investigated the potential role of capsaicin in central salty-taste processing in both anesthetized and freely moving mice (Figure 3A and 3B). The calcium waves evoked by different concentrations of NaCl solutions with or without capsaicin exhibited distinct waveforms (Figure 3A and 3B), which indicate that salty tastes were encoded by neurons in the OFC. Notably, the time courses of calcium waves are in the range of 2 to 5 seconds, which are highly comparable with the typical activation timing of functional magnetic resonance imaging signals.21 Furthermore, the amplitude of the 200-mmol/L NaCl–evoked waves was significantly higher than the 150-mmol/L NaCl–evoked waves in the anesthetized mice, whereas the amplitude of the 150-mmol/L NaCl–capsaicin-evoked waves was significantly higher than the 150-mmol/L NaCl–evoked waves in both the anesthetized (Figure 3C and 3D) and freely moving (Figure 3E and 3F) mice. Thus, these results suggested that a peripheral salt stimulus could evoke higher OFC activity levels and in a dose-dependent manner, which could be affected by a capsaicin stimulus. Nevertheless, the frequency of the 150-mmol/L NaCl–capsaicin-evoked waves was significantly larger than the 150-mmol/L NaCl–evoked waves in the freely moving mice but not the anesthetized mice (Figure S4A and S4B), which indicates that the OFC neural excitability could be changed by a capsaicin stimulus at normal physiological conditions.
Figure 3. Neuronal activity in the orbitofrontal cortex of wild-type mice evoked by different salt solution stimuli with capsaicin. A, The waveforms of anesthetized mice evoked by deionized water, 150 mmol/L NaCl, 200 mmol/L NaCl, and 150 mmol/L NaCl with 0.5-μmol/L capsaicin solutions, respectively. B, The waveforms of freely moving mice after drinking deionized water, 150 mmol/L NaCl, 200 mmol/L NaCl, and 150 mmol/L NaCl with 0.5-μmol/L capsaicin solutions, respectively. C, The amplitude of calcium signals in anesthetized mice evoked by a concentration gradient of salt solutions with or without capsaicin. **P<0.01 vs without capsaicin. D, The amplitude of calcium signals evoked by each type of solution in anesthetized mice. *P<0.05, ***P<0.001 vs deionized water. #P<0.05 vs 150 mmol/L NaCl. E, The amplitude of calcium signals emerged in 300 s after drinking concentration gradient of salt solutions with or without capsaicin in freely moving mice. **P<0.01 vs without capsaicin. F, The amplitude of calcium signals emerged in 300 s after drinking each type of solution in freely moving mice. ***P<0.001 vs deionized water. #P<0.05 vs 150 mmol/L NaCl. Data are presented as the mean±SEM.

Interventions Related to OFC Altered Salt Preference

Finally, we investigated whether intervening in OFC activity could result in changes in the salty-capsaicin preference through activating or inhibiting neuronal activity by means of optogenetics in mice. The salt preference of mice was determined by calculating the relative ratio of licking actions for different solutions (Methods in the online-only Data Supplement). In 1 example of a naive mouse, the ratio of licks for the 150-mmol/L NaCl solution was significantly higher than the 200-mmol/L NaCl solution (Figure S5A), which indicates that the mouse prefers the former salt level. However, the mice exhibited a significantly lowered preference for the 150-mmol/L NaCl with capsaicin solution than only the 150-mmol/L NaCl solution (Figure S5A), which suggests that the existence of capsaicin may enhance the sensitivity of salt. To confirm the neuronal projection from the primary taste cortex to OFC, AAV-EGFP (adeno-associated virus–vector expressing enhanced green fluorescent protein; retro) was injected into the OFC of mice, and the retrogradely labeled neurons in the area of insula cortex was identified (Figure 4A). The mice were then injected with AAV-ChR2 (AAV vector expressing channelrhodopsin-2) or AAV-ArchT (archaerhodopsin) for the activation or inhibition of neuronal activities in the OFC. We subsequently analyzed mouse licking behavior in the gustometer with a 30-minute test session during which they underwent optogenetic stimulation or inhibition through an optical fiber (Figure 4B and 4C; Figure S5B). By stimulating the OFC activity, the preference for the 200-mmol/L NaCl solution was further decreased, whereas the preference for the 150-mmol/L NaCl solution significantly increased in the mice (Figure 4D and 4E). In contrast, the mice exhibited a significantly increased preference for the 200-mmol/L NaCl solution and a decreased preference for the 150-mmol/L NaCl solution after OFC activity inhibition (Figure 4D and 4E). These results suggested that the stronger activation of the OFC strengthened the aversion for high-salt solutions and hedonic for low-salt solutions, vice versa. Furthermore, the mice exhibited a decreased preference for the 150-mmol/L NaCl solution with capsaicin during OFC activity stimulation (Figure 4F), which indicates that capsaicin may influence the perception of salty taste in the OFC. To validate the effect of optogenetic stimulation on the OFC, we also recorded the spontaneous and optogenetically evoked calcium waves in the OFC of Thy1-ChR2 transgenic mice. Spontaneous and optogenetically evoked calcium waves recorded at a given location had similar waveforms (Figure S5C), which indicates that the optogenetically activated neuronal population is largely the same as the neuronal population involved in the salt preference control pathways.
Figure 4. Optogenetic intervention on orbitofrontal cortex (OFC) alters the salt preference of wild-type (WT) mice. A, A brain slice of a WT mouse with retrogradely labeled neurons (shown as green spots) in the insula cortex. The scale bar indicates 80 μm. B, Schematic diagram representing the optical fiber stimulation setup, AAV expression, and optical fiber administration on OFC. C, A brain slice of a WT mouse with photosensitive protein (shown as red spots) expressed in the OFC. The black trace represents the optic fiber trace to conduct optogenetic stimulation or inhibition. The scale bar indicates 200 μm. D–F, Ratio of licks for 200 mmol/L NaCl (D), 150 mmol/L NaCl (E), and 150 mmol/L NaCl with 0.5 μmol/L capsaicin (F) solution of ChR2-injected and ArchT-injected mice with or without optogenetic intervention. Data are presented as the mean±SEM. *P<0.05, **P<0.01.

Discussion

The major findings in this study demonstrate that the enjoyment of spicy taste enhanced the sensitivity to salty taste and lowered the daily salt intake and blood pressure in participants. Furthermore, high salt intake and salt preference were closely correlated with increased brain activity in the insula and OFC of the participants. Capsaicin administration increased activation of the insula and OFC in response to high-salt stimuli, which reversed the salt intensity–dependent differences in activity in the insula and OFC. Similar to humans, salty-taste information processed in the OFC was affected in the presence of capsaicin in mice. Optogenetic stimulation on the OFC strengthened the aversion for high-salt solutions and hedonic for low-salt solutions, which could be reversed by the addition of capsaicin in salt solutions.
The estimation of dietary salt intake using various methodologies has indicated that the mean salt consumption is ≈11.0 to 14.0 g/d (2.5 g salt contains 1 g sodium) in the population,6,22 which far exceeds the dietary salt intake level recommended by the World Health Organization. Substantial effort has been made to reduce salt intake; however, the high consumption of dietary salt in China has hardly changed during the previous several decades.9,23 Similarly, despite numerous initiatives, sodium consumption in the United States has been relatively constant and well above recommended amounts for more than a decade.10 Thus, the identification of an alternative strategy for reducing salt intake is critical for the prevention of salt-induced hypertension.
Chili pepper is perhaps the world’s most widely consumed spice,24–26 and both spicy and hot are reported to be among the most appealing flavors in both China and the United States.27 A human study showed that the administration of capsaicin at a low concentration that does not cause a burning sensation on the tongue may enhance saltiness.13 In this study, we showed that the participants who liked spicy food had a reduction of ≈2.5 g in their daily salt intake, which is noteworthy because the reduction of daily salt intake by 3 g has been shown to produce a protective effect against hypertension and related cardiovascular diseases.28 Furthermore, Lv et al14 also showed that consumption of spicy foods was inversely associated with total and certain cause-specific mortality in a Chinese population. Because chili pepper is the most popular flavor substitute worldwide, the consumption of spicy foods may beneficially reduce dietary salt intake in the general population.
The human preference for salted food is the hedonic response to saltiness and is strongly influenced by its sensory properties.29 The central gustatory system and the mesolimbic structures play critical roles in discerning salt-taste signals as aversive or pleasant. The insula has appeared to be more sensitive to the intensity of taste and is involved in establishing emotionally relevant sensory experiences30; the OFC is suggested as a secondary taste cortex that receives inputs from the insula cortex,31 which has been shown to be particularly associated with hedonic aspects and thus the subjective pleasantness of taste in humans.32 Moreover, the OFC has been suggested in the control of appetite and food intake.33 In our human neuroimaging study, we determined that the metabolic activity changes of the OFC in response to salt stimulus were positively correlated with individual daily salt intake and salt preference. Similar findings were obtained in the animal study, with increased OFC activity in response to ascending concentrations of NaCl solutions applied peripherally. Seemly discrepancy results of salt preference were obtained in the intervening of OFC activity from our optogenetic experimental studies. Nevertheless, it has also been reported that both pleasant and aversive tastes were presented in the OFC.34 Furthermore, the OFC has been reported to play a key role in guiding behavior adaptively on the basis of reward value, including receiving rewards and punishments and processing of the values.35 Thus, it is rationale to assume that the OFC activity represented pleasantness for lower concentrations of salt solution, with an aversion reaction for higher concentrations of salt solution. This finding also explains the dose-dependent increment of neural calcium wave amplitudes recorded at the OFC in response to various concentrations of salt solutions.
In this study, we determined that capsaicin administration increased the metabolic activity in both the insula and the OFC in response to salty-taste stimuli. Notably, capsaicin mediated an increase in brain activity that could reverse the differences in the intensity-dependent activity induced by salty-taste stimuli identified in these brain regions. As reported, a remarkable difference of the OFC from other related brain nuclei was the greater convergence of neurons to taste features, which provided a basis for different behavioral responses to particular combinations of oral sensory stimuli.31 Taken together with the findings of our optogenetic experimental study on the OFC, it seems that capsaicin may turn the aversion reaction for a salt solution into a lower concentration. Our previous studies have also indicated a protective role of capsaicin in cardiometabolic diseases.15,18,36 Through direct intervention on OFC neuronal activities while monitoring salty-taste preference, we provided additional evidence of the influence of capsaicin on central salty-taste perception (Figure S6).

Study Limitations

Our study has several limitations. First, our clinical study was limited by its cross-sectional nature. It is unknown whether the current findings may be generalized to other populations outside of China. Moreover, the correlation between the enjoyment of spicy flavor and reduced salt intake must be validated through a prospective intervention study. Second, an accuracy measurement of individual daily salt intake is helpful to evaluate this relevance; however, it is difficult to use in a population survey. Third, the animal studies suggested a potential salt-reduction effect of capsaicin; however, the underlying mechanisms remain elusive.

Perspectives

High salt intake contributes to the pathogenesis of hypertension and its associated cardiovascular events. Healthy lifestyles have been used to reduce salt intake for many years; however, traditional cooking habits and changes in the taste of food have dampened the effectiveness of salt reduction at the population level. This clinical trial combined with an experimental study for the first time shows that salt intake and salt preference were related to the regional metabolic activity in the insula and OFC of individuals. Furthermore, capsaicin administration enhanced insula and OFC metabolism in response to high-salt stimuli; thus, the enjoyment of spicy foods significantly reduced individual salt preference, daily salt intake, and blood pressure by modifying the neural processing of salty taste in the brain (Figure S6). Capsaicin rich in Chili pepper is perhaps the world’s most widely consumed food with spicy flavor. Considering the unsatisfactory effect of the existing salt-reduction strategy, this study provided insights for the enjoyment of spicy flavor as a promising and precise behavioral intervention for reducing high salt intake and blood pressure.

Acknowledgments

We gratefully acknowledge the participation of all study subjects and the technical assistance of Wenjun Jin, Jian Lu (Brain Research Center, Third Military Medical University, Chongqing, China), Tingbing Cao, and Lijuan Wang (Chongqing Institute of Hypertension, Chongqing, China) with our experiments. We thank Professor Bernd Nilius (Department of Cell Molecular Medicine, Laboratory Ion Channel Research, Campus Gasthuisberg, Leuven, Belgium) and Professor Martin Tepel (Department of Nephrology, Odense University Hospital, University of Southern Denmark, Odense, Denmark) for their suggestions in study design and implementation.

Novelty and Significance

What Is New?

•
This study is the first investigation to demonstrate the enjoyment of spicy flavor enhances central salty-taste perception.
•
Capsaicin administration enhances insula and orbitofrontal cortex metabolism in response to high-salt stimuli and reverses the salt intensity–dependent differences in activity in these brain areas.
•
Optogenetic intervention on the orbitofrontal cortex alters salt preference in rodents.

What Is Relevant?

•
Enjoyment of spicy foods may significantly reduce individual salt preference, daily salt intake, and blood pressure by modifying the neural processing of salty taste in the brain.
•
The consumption of foods with spicy flavor promotes a novel lifestyle intervention for reducing high salt intake and blood pressure.

Summary

Spicy food supplementation is a promising strategy for salt reduction at the population level, either as a functional dietary factor or in conjunction with conventional lifestyle changes.

Supplemental Material

File (hyp_hype201709950_supp1.pdf)

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Published In

Go to Hypertension
Go to Hypertension
Hypertension
Volume 70 • Number 6 • December 2017
Pages: 1291 - 1299
PubMed: 29089370

Copyright

© 2017 American Heart Association, Inc.

History

Received: 2 July 2017
Revision received: 11 July 2017
Accepted: 28 August 2017
Published online: 31 October 2017
Published in print: December 2017

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Keywords

  1. blood pressure
  2. brain
  3. hypertension
  4. orbitofrontal cortex
  5. risk factors

Subjects

  1. Diet and Nutrition
  2. Hypertension
  3. Imaging

Authors

Affiliations

Qiang Li*
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Yuanting Cui*
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Rongbing Jin
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Hongmei Lang
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Hao Yu
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Fang Sun
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Chengkang He
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Tianyi Ma
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Yingsha Li
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Xunmei Zhou
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Daoyan Liu
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Hongbo Jia
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Xiaowei Chen
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author
Zhiming Zhu
From the Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Collaborative Innovation Center for Brain Science, Chongqing Institute of Hypertension (Q.L., Y.C., H.L., H.Y., F.S., C.H., T.M., Y.L., X.Z., D.L., Z.Z.), Department of Medical Image, Daping Hospital (R.J.), and Brain Research Center (X.C.), Third Military Medical University, China; and Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences (H.J.).
View all articles by this author

Notes

*
These authors contributed equally to this work.
The online-only Data Supplement is available with this article at http://hyper.ahajournals.org/lookup/suppl/doi:10.1161/HYPERTENSIONAHA.117.09950/-/DC1.
Correspondence to Zhiming Zhu, Department of Hypertension and Endocrinology, Center for Hypertension and Metabolic Diseases, Daping Hospital, Chongqing Institute of Hypertension, Third Military Medical University, Chongqing 400042, China, E-mail [email protected] or Rongbing Jin, Department of Medical Image, Daping Hospital, Third Military Medical University, Chongqing 400042, China, E-mail [email protected]

Disclosures

None.

Sources of Funding

This study was supported by grants from the National Basic Research Program of China (2013CB531205) and the National Natural Science Foundation of China (81721001, 81630015, 31430042, 91339000, and IRT1216).

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Enjoyment of Spicy Flavor Enhances Central Salty-Taste Perception and Reduces Salt Intake and Blood Pressure
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