The Hunger for Salt: A Tribute to Derek Denton and Jay Schulkin with an Updated Collection of Papers on Salt Appetite.

This collection of outstanding papers is a trove for all concerned with salt intake [...].

Sex Differences in Salt Appetite: Perspectives from Animal Models and Human Studies.

Salt ingestion by animals and humans has been noted from prehistory. The search for salt is largely driven by a physiological need for sodium. There is a large body of literature on sodium intake in laboratory rats, but the vast majority of this work has used male rats. The limited work conducted in both male and female rats, however, reveals sex differences in sodium intake. Importantly, while humans ingest salt every day, with every meal and with many foods, we do not know how many of these findings from rodent studies can be generalized to men and women. This review provides a synthesis of the literature that examines sex differences in sodium intake and highlights open questions. Sodium serves many important physiological functions and is inextricably linked to the maintenance of body fluid homeostasis. Indeed, from a motivated behavior perspective, the drive to consume sodium has largely been studied in conjunction with the study of thirst. This review will describe the neuroendocrine controls of fluid balance, mechanisms underlying sex differences, sex differences in sodium intake, changes in sodium intake during pregnancy, and the possible neuronal mechanisms underlying these differences in behavior. Having reviewed the mechanisms that can only be studied in animal experiments, we address sex differences in human dietary sodium intake in reproduction, and with age.

Vegans, vegetarians and omnivores differ in nutrient hedonics, salt and sweet preference and flavouring.

BACKGROUND: Dietary content can influence taste responses. Therefore, we compared nutrient hedonics (liking foods by nutrient content), and seasoning, including taste responses to the prime flavours salt and sweet in 30 vegan, 37 vegetarian and 56 omnivore men and women. METHODOLOGY: Questionnaires and taste tests examined macronutrient and electrolyte intake and hedonics, seasoning, salt and sweet preferences and psychophysical taste responses. RESULTS: Compared to omnivores, vegans had lower protein, Ca++, Na+ intake, and increased carbohydrate (CHO) intake. Independently of intake, hedonics for protein Ca++and Na+ were reduced and increased for CHO. Psychophysical responses to NaCl and sucrose also differed slightly, vegans and vegetarians scoring high concentrations of sucrose as more intense, Vegans reported more sweetening and less salting of food, added more sucrose to a test tea, less salt to a test soup, but did not differ in seasoning with oil or hot spice. PRINCIPAL CONCLUSIONS: Habitual vegan, vegetarian and omnivore diets may alter taste responses to nutrient content and salt and sweet, the latter more pronounced in vegan and vegetarian women. Recognizing diet-dependent changes in taste hedonics can inform diets and products.

Exposure to War Prior to Conception: Maternal Emotional Distress Forecasts Sex-Specific Child Behavior Problems.

OBJECTIVES: Exposure to maternal stress during the prenatal period adversely affects child outcomes. Recent investigations have shifted to an even earlier period, the preconception period, to better understand the role of this formative period in human health and disease. We investigated the links between maternal emotional distress following preconception exposure to war, and child outcomes at age 10. MATERIAL AND METHODS: Before becoming pregnant, mothers were exposed to missile bombardment on the north of Israel in the 2006 war. Mothers who conceived within 12 months after the war were recruited and compared to mothers who conceived during the same period but lived in Israel but outside missile range. During the initial assessment, mothers completed a questionnaire on emotional distress. At 10 years of age, mothers and children (N = 68) reported on child socio-emotional outcomes. RESULTS: Multiple regression analyses revealed that, in girls, higher maternal emotional distress following preconception war exposure predicted more internalizing and externalizing behavior problems, and more behavior regulation problems. In boys, maternal emotional distress was not significantly related to outcomes. CONCLUSION: Maternal emotional distress following preconception exposure to war forecasts sex-specific child behavioral problems as reported by the mother and the child. Though the results warrant cautious interpretation because of the relatively small sample size and differential attrition, our findings add to the small but growing body of research on the consequences of maternal stress exposure prior to conception for the next generation.

Exertional sodium loss does not increase immediate salt appetite or dietary sodium intake in athletes.

We tested whether salt preference increases immediately after exertion-induced Na+ loss in sweat, and whether this may generalise to an increase in habitual dietary Na+ intake. For the first aim, trained athletes (n = 20) exercised in 2 ambient temperatures and sweat Na+ loss related to immediate salt preference assessed by taste, intake and psychophysical tests. For the second aim, we compared dietary and urinary Na+, and salt preference, seasoning and hedonics in the athletes and sedentary men (n = 20). No relationship was found between sodium loss during exercise and immediate preference for salt or psychophysical responses, and no differences in comparison to sedentary men. However, athlete diet had fewer foods (29.4 ± 1.5 vs 37.8 ± 1.9, p < 0.001), less seasoning (19 vs 32. p = 0.011) and more athletes reported dietary limitations (31 vs 11, p < 0.05), although nutrient content did not differ. Together these might suggest athlete adherence to a healthy diet at the expense of variety and flavour and a dissociation between dietary reports and intake. Athletes, more than controls, liked foods rich in energy and K+ suggesting compensatory-driven hedonics, although overall their intake did not differ. The findings are consistent with the absence of a salt appetite responding to Na+ loss in humans, and specifically that trained athletes do not increase their preference for salt in immediate response to exertion-induced Na+ loss and are not at risk for increased dietary Na+ compared to sedentary men.

Salt need needs investigation.

Expensive and extensive studies on the epidemiology of excessive Na intake and its pathology have been conducted over four decades. The resultant consensus that dietary Na is toxic, as well as the contention that it is less so, ignores the root cause of the attractiveness of salted food. The extant hypotheses are that most Na is infiltrated into our bodies via heavily salted industrialised food without our knowledge and that mere exposure early in life determines lifelong intake. However, these hypotheses are poorly evidenced and are meagre explanations for the comparable salt intake of people worldwide despite their markedly different diets. The love of salt begins at birth for some, vacillates in infancy, climaxes during adolescent growth, settles into separate patterns for men and women in adulthood and, with age, fades for some and persists for others. Salt adds flavour to food. It sustains and protects humans in exertion, may modulate their mood and contributes to their ailments. It may have as yet unknown benefits that may promote its delectability, and it generates controversy. An understanding of the predilection for salt should allow a more evidence-based and effective reduction of the health risks associated with Na surfeit and deficiency. The purpose of this brief review is to show the need for research into the determinants of salt intake by summarising the little we know.

Acculturation of immigrant diet, basic taste responses and sodium appetite.

In young new Ethiopian immigrants (EI, about 0·5 years since immigration; n 20), veteran Ethiopian immigrant students (ES, about 13 years since immigration; n 30) and native Israeli students (NS; n 82), dietary macronutrients and electrolytes, and responses to basic tastes were compared in a cross-sectional design. From EI, to ES, to NS, dietary energy, protein, fat, and Na+ increase, whereas carbohydrates, K+ and Ca2+ do not differ. Corrected for energy intake, only Na+ increases. EI consume less dietary Na+, like foods with less Na+ content, salt their food less, yet show a greater hedonic response to salt taste. In contrast, preference for sweet does not differ. Taste psychophysics, 6-n-propylthiouracil (PROP) responses and lingual fungiform papillae density differ by group (and sex), but do not relate to dietary intake. Together, these changes could reflect dietary acculturation, increasing overall intake, Na+ in particular, accompanied by decreasing taste sensitivity, and changes in sensory perception and preference in these Ethiopian immigrants. The fact that immigrants find salt more hedonic, yet eat less of it, could suggest increased sensitivity to its taste, and might suggest restoring sensitivity to reduce Na+ intake for all. Similar alterations in taste sensory responses might be obtained in other forms of dietary flux. Understanding dietary acculturation can focus efforts (e.g. on Na+), to anticipate the disease burden of diets of affluence among immigrants. Yet, these immigrants' nutrition is healthier in its low fat and Na+, suggesting that nutritional advice should focus on preservation, as well as prevention. Our study adds Ethiopian nutritional acculturation to that of the varied immigrant groups around the world.

Body image drawings dissociate ethnic differences and anorexia in adolescent girls.

OBJECTIVES: To distinguish between ethnic differences among segregated schoolgirls and restrictive anorexia nervosa using a simple culture-fair test of body image (BI) figure drawings. METHODS: Several responses to BI figure drawings by 178 adolescent schoolgirls from three ethnically distinct and segregated schools and communities in Israel, Jewish secular (JS), Jewish Haredi (H), and Christian Arab (C), and a group of 14 severely restricting anorexic girls (AN). BI evaluations were analyzed by MANCOVA, followed by paired or Student-t tests for comparisons between responses and groups respectively. Pearson r served for correlations and the Fisher Z for differences between slopes. RESULTS: Despite the total ethnic segregation among the schoolgirls, there are commonalities; all prefer a thinner ideal BI, and are similarly dissatisfied with their BI. However, ethnic differences also emerge: C underestimate their BI and how others view them, and H true and Ideal BI evaluations correlate, unlike the other groups. Despite this variability, and in stark contrast, the anorexic girls show a gross misperception of their BI, even in comparison to girls equated for BMI. DISCUSSION: The findings show that figure drawings evaluation of BI is a simple and robust instrument dissociating clinical and ethnic responses. Clinicians may consider body figure drawings as a simple, supportive, diagnostic for first-line recognition for risk of AN in adolescent girls.

Salt appetite is not increased in summer heat.

We tested the hypothesis that salt appetite increases in summer heat due to increased sodium loss due to increased drinking and perspiration. A test battery in the same sample of healthy young people tested in summer and winter revealed no seasonal differences in salt appetite (or fluid intake) despite a 10 °C rise in mean environmental temperature. Unexpectedly, sweet preference is reduced in summer.

Pre-Conception War Exposure and Mother and Child Adjustment 4 Years Later.

Evidence is accumulating for the transgenerational effects of maternal stress on offspring. A particular increasing concern is the possible transgenerational effects of community exposure to war and terror. Here, 107 mothers that had been exposed to war, were assessed with their 3 year old children (52 % girls) who had been conceived after the end of the war, and thus never directly exposed to war. The circumscribed nature (missile bombardment) and temporal limits (34 days) of the tragic 2006 Lebanon war in the north of Israel, affords a unique methodological opportunity to isolate an epoch of stress from preceding and subsequent normal life. We find that war experience engenders higher levels of mothers' separation anxiety, lower emotional availability in mother-child interaction, and lower levels of children's adaptive behavior. The novelty of these findings lies in documenting the nature and strength of transgenerational effects of war-related stress on offspring that were never exposed. In addition, because these effects were obtained after 4 years of a continuing period of normality, in which the children were born and raised, it suggests that an extended period of normality does not obliterate the effects of the war on mother and child behavior as assessed herein. Despite the study limitations, the results are indicative of persisting transgenerational effects of stress.

Transgenerational sex-specific impact of preconception stress on the development of dendritic spines and dendritic length in the medial prefrontal cortex.

Perinatal adverse experience programs social and emotional behavioral traits and is a major risk factor for the development of behavioral and psychiatric disorders. Little information is available on how adversity to the mother prior to her first pregnancy (preconception stress, PCS) may affect brain structural development, which may underlie behavioral dysfunction in the offspring. Moreover, little is known about possible sex-dependent consequences of PCS in the offspring. This study examined spine number/density and dendritic length/complexity of layer II/III pyramidal neurons in the anterior cingulate (ACd), prelimbic/infralimbic (PL/IL) and orbitofrontal cortex (OFC) of male and female rats born to mothers exposed to unpredictable variable stress at different time points prior to reproduction. Our main findings are that in line with our hypothesis adversity to the mother before her pregnancy results in highly complex changes in neuronal morphology in the medial prefrontal, but not in the orbitofrontal cortical regions of her future offspring that persist into adulthood. Moreover, our study revealed that (1) in the PCS2 group (offspring of dams mated two weeks after stress) spine numbers and dendritic length and complexity were increased in response to PCS in the ACd and PL/IL, (2) these regional effects depended on the temporal proximity of adversity and conception, (3) in the ACd of the PCS2 group only males and the left hemispheres were affected. We speculate that these transgenerational brain structural changes are mediated by stress-induced epigenetic (re)programming of future gene activity in the oocyte.

Does salt increase thirst?

Our diet is believed to be overly rich in sodium, and it is commonly believed that sodium intake increases drinking. Hence the concern of a possible contribution of dietary sodium to beverage intake which in turn may contribute to obesity and ill health. Here we examine whether voluntary, acute intake of a sodium load, as occurs in routine eating and snacking, increases thirst and drinking. We find that after ingesting 3.5 or 4.4 g NaCl (men) and 1.9 or 3.7 g (women) on nuts during 15 minutes, there is no increase in thirst or drinking of freely available water in the following 2 h compared with eating similar amounts of sugared or unflavored nuts. This suggests that routine ingestion of boluses of salt (~30-40% of daily intake for men, ~ 20-40% for women) does not increase drinking. Methodological concerns such as about nuts as vehicle for sodium suggest further research to establish the generalizability of this unexpected result.

Salt appetite in the elderly.

The present study investigated whether salt appetite in the elderly is impaired similar to thirst because of the commonality of their physiological substrates and whether alterations in salt appetite are related to mood. Elderly (65-85 years, n 30) and middle-aged (45-58 years, n 30) men and women were compared in two test sessions. Thirst, psychophysical ratings of taste solutions, dietary Na and energy intakes, seasoning with salt and sugar, number of salty and sweet snacks consumed, preferred amounts of salt in soup and sugar in tea, and an overall measure of salt appetite and its relationship with mood, nocturia and sleep were measured. Elderly participants were found to be less thirsty and respond less to thirst. In contrast, no impairment of salt appetite was found in them, and although they had a reduced dietary Na intake, it dissipated when corrected for their reduced dietary energy intake. Diet composition and Na intake were found to be similar in middle-aged and elderly participants, despite the lesser intake in elderly participants. There were no age-related differences in the intensity of taste or hedonic profile of Na, in salting habits, in tests of salting soup, or number of salty snacks consumed. No relationship of any measure of salt appetite with mood measured by the Positive and Negative Affect Schedule, frequency of nocturia, or sleep duration was observed. The age-related impairment of the physiology of mineralofluid regulation, while compromising thirst and fluid intake, spares salt appetite, suggesting that salt appetite in humans is not regulated physiologically. Intact salt appetite in the elderly might be utilised judiciously to prevent hyponatraemia, increase thirst and improve appetite.

Dietary sodium, added salt, and serum sodium associations with growth and depression in the U.S. general population.

It is not known why salt is so attractive to humans. Here, guided by hypotheses suggesting that the attraction of salt is conditioned by postingestive benefits, we sought to establish whether there are such benefits in a population by analyzing the National Health and Nutrition Examination Survey (NHANES) 2007-2008 database (n = ~ 10,000). We focus on two potential benefits supported by the literature, growth and moderation of depression, and examine their relationship to sodium, dietary, added at table, and serum. We find that during growth (<18 years), there is a specific increase in adjusted dietary sodium intake, independent of caloric or other electrolyte intakes. We find that adding salt and depression are related. In contrast, and in women only, dietary sodium and depression are inversely related. The relationships are correlational, but we speculate that this constellation may reflect self-medication for depression by adding salt, and that men may be protected by their higher dietary sodium intake. Additional findings are that women add more salt than men below age ~30, after which men add more, and below 40 years of age, serum sodium is lower in women than in men. It remains possible that small but beneficial effects of sodium could condition salt preference and thus contribute to population-wide sodium intake.

Prereproductive stress to female rats alters corticotropin releasing factor type 1 expression in ova and behavior and brain corticotropin releasing factor type 1 expression in offspring.

BACKGROUND: Human and animal studies indicate that vulnerability to stress may be heritable and that changes in germline may mediate some transgenerational effects. Corticotropin releasing factor type 1 (CRF1) is a key component in the stress response. We investigated changes in CRF1 expression in brain and ova of stressed female rats and in the brain of their neonate and adult offspring. Behavioral changes in adulthood were also assessed. METHODS: Adult female rats underwent chronic unpredictable stress. We extracted mature oocytes and brain regions from a subset of rats and mated the rest 2 weeks following the stress procedure. CRF1 expression was assessed using quantitative reverse-transcription polymerase chain reaction. Tests of anxiety and aversive learning were used to examine behavior of offspring in adulthood. RESULTS: We show that chronic unpredictable stress leads to an increase in CRF1 messenger RNA expression in frontal cortex and mature oocytes. Neonatal offspring of stressed female rats show an increase in brain CRF1 expression. In adulthood, offspring of stressed female rats show sex differences in both CRF1 messenger RNA expression and behavior. Moreover, CRF1 expression patterns in frontal cortex of female offspring depend upon both maternal and individual adverse experience. CONCLUSIONS: Our findings demonstrate that stress affects CRF1 expression in brain but also in ova, pointing to a possible mechanism of transgenerational transmission. In offspring, stress-induced changes are evident at birth and are thus unlikely to result from altered maternal nurturance. Finally, brain CRF1 expression in offspring depends upon gender and upon maternal and individual exposure to adverse environment.

Transgenerational effects of infantile adversity and enrichment in male and female rats.

To discover whether the accumulation of life's experiences, adverse and enriching, inform, and serve the following generation by inheritance we examine whether stress to a weanling female will influence her future offspring, whether prereproductive enrichment to the dam, or postweaning enrichment to the offspring, can reverse the transgenerational effects of stress, and whether, like adversity, enrichment might have transgenerational effects. Female rats were exposed to stressors when they were 27-29 days old. Half of these females and their controls were then raised in an enriched environment from weaning until mating at 60 days to examine whether preproduction enrichment reverses the effects of preproduction stress on offspring. Half of the offspring of each group were raised in an enriched environment after weaning, to see whether it reverses the effects of preproduction stress and buttresses prereproductive enrichment. Behavior was examined in 625 adult offspring in 16 groups covering all permutations of the experimental variables (preproduction weanling stress (PS), preproduction enrichment (PE), offspring enrichment (OE), sex). Exploration, avoidance learning, startle, and social interaction were tested. Results reveal that very early prereproductive experience in females, adverse or enriching, will transgenerationally influence their future offspring, depending on the behavior tested and sex. Our finding that enrichment, whether to the parent or offspring generation, can ameliorate the transgenerational impact of adversity, has novel implications for the malleability of transgenerational inheritance, and its individual, social, and therapeutic impact.

Intact sensory function in anorexia nervosa.

BACKGROUND: In anorexia nervosa (AN), taste and smell are believed to be anhedonic, hunger and pain are muted, and body-image distortion obscures wasting, which together facilitate self-starvation. However, the emphasis on these deficits may be biased because other sensory systems have been sparsely investigated. OBJECTIVES: Objectives of the study were to clarify whether these dysfunctions are specific or part of a pattern of sensory-perceptual deficits in AN patients and to test the gustatory senses dissociated from ingestion to clarify whether any deficit is sensory or affective. DESIGN: In 15 adolescent, first-episode, hospitalized, restrictive AN patients and 15 matched healthy controls who responded to gustatory stimuli (intensity and hedonics of 5 basic tastes and tastes and odors of foods and nonfoods), size estimation (manual and oral judgment of size and shape, kinesthesia, and body size and esthetics), cold pain, and auditory and visual processing were compared. RESULTS: AN patients did not differ on most tests, were better at odor recognition, were less successful in central auditory processing and oral assessment of size and shape, and may have been more sensitive to cold. Body-image dissatisfaction in AN patients was not related to dysfunctional size estimation. CONCLUSIONS: There is no systematic sensory-perceptual deficit in AN patients, and specifically, not in gustatory function. The few differences shown might be due to fear of food-related stimuli or comorbidity.

Salt preference of nursing mothers is associated with earlier cessation of exclusive breastfeeding.

Successful breastfeeding is predicated on its initial success. Salt appetite during lactation may be relevant to breastfeeding success because sodium is essential for development of foetus and neonate. Here we examined whether maternal salt preference might facilitate breastfeeding. Nursing mothers (n=327) were categorized as high, medium or low salt preferring, and the relationship to persistence of exclusive breastfeeding during the first 25 days postnatal was evaluated. Contrary to expectation, we find that mothers with low salt preference persisted in breastfeeding beyond day 7 postnatal in comparison to mothers with high salt preference, and mothers with high salt preference had the shortest exclusive breastfeeding duration up to postnatal day 25. Awareness of this among health workers and nursing mothers could contribute to successful breastfeeding.

The excess salt appetite of humans is not due to sodium loss in adulthood.

In seeking the determinants of high salt intake, studies in rat have shown that sodium depletion in utero, neonatally, or in maturity, permanently enhances salt appetite. In humans too, salt appetite is permanently enhanced after perinatal sodium loss, but it is not known if sodium loss in adults also enhances salt intake. If it does, it might contribute to high sodium intake and its associated pathologies. Therefore, using methods that revealed the perinatal determinants of sodium appetite, here we evaluated whether salt appetite is enhanced in adults with a varied history of sodium loss. We find that putative sodium loss due to hyperhidrosis, hemorrhage, dehydration, or breastfeeding, does not increase salt appetite significantly. The findings contrast with the many studies showing enduring enhancement of salt appetite by perinatal sodium loss in humans, and suggest that lifelong salt appetite is established very early in development. In turn this counsels very early intervention to prevent lifelong excess sodium intake.

Adversity before conception will affect adult progeny in rats.

The authors investigated whether adversity in a female, before she conceives, will influence the affective and social behavior of her progeny. Virgin female rats were either undisturbed (controls) or exposed to varied, unpredictable, stressors for 7 days (preconceptual stress [PCS]) and then either mated immediately after the end of the stress (PCS0) or 2 weeks after the stress ended (PCS2). Their offspring were raised undisturbed until tested in adulthood. PCS offspring showed reduced social interaction; in the acoustic startle test, PCS males were less fearful, whereas PCS females were more fearful; in the shuttle task, PCS0 males avoided shock better; and in the elevated maze, PCS0 females were more active and anxious. The 2-week interval between stress and mating assuaged the effects on offspring activity and shock avoidance but not the changes in social behavior and fear in male and female offspring. Hence, PCS to the dam, even well before pregnancy, influences affective and social behavior in her adult offspring, depending on how long before conception it occurred, the behavior tested, and sex. (PsycINFO Database Record (c) 2009 APA, all rights reserved).