DV: Daily Value; FCID: Food Commodity Intake Database; HEI-2005: Healthy Eating Index-2005; IU: International Units; mg: microgram; NHANES: National Health and Nutrition Examination Survey; RDA: Recommended Dietary Allowance; UV: Ultra Violet; USDA: United States Department of Agriculture

Mushrooms have been consumed as part of the human diet since prehistoric times [1]. Many are edible [1], and, although they are classed botanically as fungi, from a practical, and more importantly, a culinary standpoint, they are considered as vegetables [2]. Recently, they have been informally categorized among the “white vegetables”, which have recently been recognized as a “forgotten source of nutrients” [3].

Mushroom intake data are sparse. Over the past 40 years, retail per capita availability of mushrooms has more than tripled from only 0.9 pounds/person in 1970 to 3.1 pounds/person in 2010 [4]. These data are limited; however, because they do not assess actual consumption. There are no recent data looking at individual mushroom consumption; however, data from the 1996-1996, 1998 Continuing Survey of Food Intake by Individuals (CSFII) showed that nearly10% of individuals consumed mushrooms on a given day [5].

Button mushrooms (Agaricus bisporus), the most widely consumed mushrooms in the United States, provide a variety of nutrients, including protein, dietary fiber, riboflavin, niacin, potassium, phosphorus, zinc, selenium, and copper to the diet; they also provide provitamin D, which can be converted to vitamin D upon exposure to ultraviolet (UV) light. Mushrooms are also low in energy, total and saturated fatty acids, and sodium. Different types of mushrooms also vary slightly in nutrient content [6]. Using a serving size of 84 g (3 ounces) [7], the common white button mushroom is a “good” source (≥ 10% of the Daily Value [DV]) of niacin, pantothenic acid, copper, and selenium, and an “excellent” source (≥ 20% of the DV) of riboflavin [6].

The single study (unpublished report by Block Dietary Data Systems for the Mushroom Council) suggested that more mushroom consumers compared with non-mushroom consumers participating in the National Health and Nutrition Examination Survey (NHANES) III met the Recommended Dietary Allowance (RDA)/Dietary Reference Intake for: energy; protein; carbohydrate; dietary fiber; vitamins A, E, C, B6, and B12; thiamin; riboflavin; niacin; folate; calcium; copper; iron; magnesium; phosphorus; zinc; and selenium. This suggested that mushroom consumers had a more nutrient-rich diet than nonmushroom consumers. That study also showed that mushroom consumers consumed 5.4 servings of vegetables/day compared with only 3.4 servings/day for non-mushroom consumers. Coupled with their pleasing aroma and taste, their nutritional profile makes mushrooms a desirable food source.

There are no published studies that have looked at mushroom consumption and a potential association with better nutrient intake or diet quality. The purpose of this study was to determine whether there was an association between mushroom consumption and nutrient intake or diet quality.

Study overview, population, and analytic sample

The NHANES is a cross-sectional surveillance program conducted on a continual basis by the National Center for Health Statistics of the Centers for Disease Control and Prevention. A major objective of the NHANES is to examine relationships between diet, nutrition, and health [8]. Detailed descriptions of the survey design, content, operations, and procedures, including study manuals and quality assurance/control methods, can be found elsewhere [9]. For consumption trends, data from NHANES III to 2007-2010 were used. For nutrient intake and diet quality analyses, data from adult (19+ years) participants in the NHANES 2001-2010 were combined to increase sample size [10,11]. Analyses included only individuals with complete and reliable dietary records as determined by the National Center for Health Statistics staff. Females who were pregnant or lactating were excluded from the study. Since this study was a secondary analysis without individual identifiers, institutional review was not required [12].

Dietary intake and nutrient analysis

Dietary data were collected via a single interviewer administered 24-hour dietary recall using an automated multiple-pass method [13,14]. Detailed descriptions of the dietary interview methods are provided in the NHANES Dietary Interviewers Procedure Manual, which includes pictures of the Computer-Assisted Dietary Interview system screens, measurement guides, and charts that were used to collect dietary information [15].

The United States Environmental Protection Agency-USDA Food Commodity Intake Database (FCID) commodity codes [16] were used to determine mushroom consumption. Mushroom intake was determined using two methods. Consumer Definition 1 was: grams of intake by food code times the weight of mushrooms per 100 g of the food code (n=281). This definition included foods that were mostly mushrooms or mushrooms alone, for example steak with mushrooms served on the side, and mushrooms as a recipe component, for example mushrooms in beef burgundy. Consumer Definition 2 was: grams of mushroom intake from commodity database for food codes (n=32) designated as “mushrooms” or a dish that was mainly mushrooms, for example stuffed mushrooms or sautéed mushrooms. Consumers were defined as those individuals consuming any amount of mushrooms. All consumers in Definition 2 were also designated as consumers in Definition 1. To assess nutrient intake the USDA Food and Nutrient Database for Dietary Studies [17] was used. The Vitamin D Addendum to USDA Food and Nutrient Database for Dietary Studies 3.0 [18] was used to determine vitamin D intake.

Food group equivalents and diet quality

Food group equivalent intakes (formerly called MyPyramid equivalents) were determined using MyPyramid Equivalents Database 1.0 (NHANES 2001-2002) [19] or 2.0 (NHANES 2003-2004) [20]; when necessary, food group equivalent intakes from NHANES 2005- 2006 and 2007-2008 were hand matched to similar foods. The Health Eating Index-2005 (HEI-2005) score was used to determine diet quality [21]. The SAS code used to calculate HEI-2005 scores was downloaded from the Center for Nutrition Policy and Promotion website [22].

Statistical analyses

For the initial analyses, SUDAAN v10.0 (Research Triangle Institute; Raleigh, NC) was used to adjust analyses for sampling weights and the sampling units and strata information as provided by NHANES [10,11]. Least-square means (± standard errors) were calculated using PROC REGRESS of SUDAAN. Linear regression was used to determine differences in mushroom consumers and non-consumers for nutrients and food groups for each consumer definition of mushrooms. For all linear regressions, covariates were age, gender, ethnicity, poverty index ratio, and physical activity level, smoking status, and alcohol consumption. Demographic information used as covariates was determined from the NHANES interview [23]; alcohol consumption was obtained from the 24-hour recall data. Nutrient and food group intakes were also adjusted for total energy intake; HEI-2005/HEI-2005 sub-components were not adjusted for energy since scoring based on 1000 calorie basis [21]. Dietary day 1 weights were used for all analyses. Statistical differences for variables of interest were determined via t-test comparing to the no mushroom groups. A probability of p<0.01 was considered significant.

Demographics and mushroom consumption

Subjects were adults 19+ years (N=24,807) participating in the NHANES 2001-2010. Using Consumer Definition 1, 9.7% of the population were mushroom consumers; whereas, using Consumer Definition 2, 1.9% of the population were mushroom consumers. Table 1 shows that, using either definition, overall, mushroom consumers were mostly non-Hispanic White, generally younger, had higher incomes, had a lower prevalence of smokers, participated more in vigorous exercise, had a higher level of education, and had a higher prevalence of alcohol consumers, although the amount of alcohol consumed was not different from non-mushroom consumers. In Consumer Definition 2, more females than males consumed mushrooms.

Table 1: Demographic and Lifestyle Characteristics of the Adults Aged 19+ years Participating in the National Health and Nutrition Examination Survey 2001-2010 Characterized by Mushroom Consumption Definition.

Consumption levels of mushrooms depended on the definition used to identify mushroom consumers. From 2001-2010 consumption of mushrooms was 20.6 ± 0.8 g and 39.5 ± 2.6 g for Consumer Definition 1 and 2, respectively. There was no change in reported mushroom consumption from 1988 to 2010 (Table 2).

Table 2: Mushroom Consumption by Adults Aged 19+ years Participating in the National Health and Nutrition Examination Survey 2001-2010 Characterized by Mushroom Consumption Definition.

Energy, macronutrient, and micronutrient intakes

Using Consumer Definition 1, mushroom consumers had higher (p<0.01) mean intakes of energy (2307 ± 26 v 2162 ± 10 kcal), protein (85.3 ± 0.8 v 82.9 ± 0.3 g), thiamin (1.8 ± 0.0 v 1.6 ± 0.0 mg), niacin (26.0 ± 0.3 v 24.7 ± 0.1 mg), folate (572.8 ± 10.3 v 540 ± 4.2 mg), copper (1.4 ± 0.02 v 1.3 ± 0.0 mg), selenium (118.6 ± 1.4 v 109.7 ± 0.5 mg), and sodium (3773.6 ± 33.1 v 3478.8 ± 11.2 mg) than non-consumers (Table 3). Using Consumer Definition 2, mushroom consumers had higher (p<0.01) intakes of protein (88.5 ± 1.3 g v 83.0 ± 0.3), dietary fiber (17.8 ± 0.5 v 16.0 ± 0.1 g), vitamin E (8.5 ± 0.3 mg v 7.4 ± 0.1), riboflavin (2.4 ± 0.1 v 2.2 ± 0.0 mg), niacin (27.2 ± 0.7 v 24.8 ± 0.0 mg), vitamin C (106.0 ± 6.0 v 87.8 ± 1.3 mg), total choline (364.4 ± 8.8 v 333.6 ± 1.8 mg), copper (1.6 ± 0.0 v 1.3 ± 0.0 mg), potassium (3033.2 ± 57.4 v 2720.7 ± 11.8 mg), selenium (121.8 ± 3.1 v 110.4 ± 0.5 mg), and sodium (3718.3 ± 74.2 v 3507.4 ± 10.1 mg) than non-consumers.

Table 3: Energy and Nutrient Intake by Adults Aged 19+ years Participating in the National Health and Nutrition Examination Survey 2001-2010 Characterized by Mushroom Consumption Definition.

Using Consumer Definition 1, mushroom consumers had lower (p<0.01) intakes of total sugars (115 ± 1.7 v 124.1 ± 0.8 g), added sugars (17.2 ± 0.4 v 19.4 ± 0.2 tsp eq), and zinc (11.6 ± 0.1 v 12.2 ± 0.1 mg) than non-mushroom consumers (Table 3). Using Consumer Definition 2, mushroom consumers had lower (p<0.01) intakes of added sugars (16.3 ± 0.9 v 19.2 ± 0.2 tsp eq) than non-mushroom consumers.

Diet quality

Using Consumer Definition 1, mushroom consumers had a higher (p<0.01) total HEI-2005 score (52.4 ± 0.4 v 51.3 ± 0.2) than nonconsumers (Table 4). Mushroom consumers also had higher HEI-2005 component scores for total vegetables (3.5 ± 0.0 v 3.0 ± 0.0), dark green and orange vegetables (1.4 ± 0.0 v 1.2 ± 0.0), total grains (4.4 ± 0.0 v 4.2 ± 0.0), and milk (5.2 ± 0.1 v 4.9 ± 0.1) than non-mushroom consumers. Mushroom consumers had a lower (p<0.01) sodium component score (3.2 ± 0.1 v 4.0 ± 0.0) than non-mushroom consumers. Using Consumer Definition 2, mushroom consumers also had a higher (p<0.01) total HEI-2005 score (54.6 ± 0.9 v 51.4 ± 0.2 than non-consumers. Mushroom consumers also had higher HEI-2005 component scores for total fruit (2.6 ± 0.1 v 2.2 ± 0.0), total vegetables (4.1 ± 0.1 v 3.0 ± 0.0), dark green and orange vegetables (1.8 ± 0.1 v 1.2 ± 0.0), and oils (6.4 ± 0.2 v 5.8 ± 0.0) than non-consumers.

Table 4: Healthy Eating Index-2005 Total Score and Component Scores of Adults Aged 19+ years Participating in the National Health and Nutrition Examination Survey 2001-2010 Characterized by Mushroom Consumption Definition.

This is the first published study showing the association between nutrient intake and diet quality in mushroom consumers. Mushroom consumption was associated with better nutrient intake and diet quality than seen in non-mushroom consumers.

Two separate definitions of mushroom consumers were used in this study. There is concern when examining a food that is frequently used in mixed dishes, such as mushrooms, on how consumers, and consequently consumption levels, of that food should be defined. Should all dishes in which mushrooms were included be considered, even though it is was a minor recipe ingredient and the individual may not have made a conscious effort to consume mushrooms, or should only those who had made a decision to consume mushrooms be considered as consumers? Since there was nothing in the literature that established a precedent, two definitions were used for this study. Consumer Definition 1 contained all foods with mushrooms; whereas, Consumer Definition 2 represented a more deliberate effort on the part of the consumer to consume mushrooms. All individuals in Consumer Definition 2 were also in Consumer Definition 1; however, the antithesis was not the case.

In each Consumer Definition, there were striking differences in the demographics of mushroom consumers and non-mushroom consumers. However, most demographic factors suggested that mushroom consumers had a higher income, more education, and a healthier lifestyle than non-mushroom consumers. This finding was reinforced in that mushroom consumers had better nutrient intakes for many of the nutrients examined and better overall diet quality than non-mushroom consumers.

Unsurprisingly, the level of mushroom consumption was considerably different between the two definitions, with those in Consumer Definition 2 having the higher intake among consumers. There were also differences in the nutrient intakes between mushroom consumers, as defined by the two definitions, when compared with their corresponding non-consumer group. Both consumer definitions showed that many micronutrients were higher in mushroom consumers than in non-mushroom consumers. Especially important was that mushroom consumers in both definitions had lower intakes of added sugars. Micronutrient intake varied by consumer definition, but overall in each mushroom consumption group, intake of most micronutrients was higher than seen in non-mushroom consumers. These were generally positive; including vitamin E, many B vitamins, copper, total choline, and selenium. Those in the Consumer Definition 2 group also had higher potassium intake.

However, sodium intake was higher in both definitions of mushroom consumers than in the corresponding non-mushroom consumer groups; sodium intake was higher in consumers by nearly 300 mg/d when Consumer Definition 1 was used and sodium intake was slightly more than 200 mg/d higher when Consumer Definition 2 was used. Mushrooms are a very low sodium food; thus, it was likely that foods consumed with the mushrooms or salt added during the preparation of mushroom dishes resulted in the higher sodium intakes. This was not surprising since mushrooms are often recipe items in high sodium foods [6], especially pizza, mixed Asian-style dishes, soups, and other prepared foods. This high sodium intake was reflected in the HEI-2005 component score for sodium, where mushroom consumers in Consumer Definition 1 had a lower score than non-mushroom consumers. Although the difference in sodium intake seen among those in Consumer Definition 2 was significant, it is probable that the difference was not enough to be reflected in the HEI-2005 component scores.

It should also be noted that the HEI-2005 component scores for nutrients to limit, SFA, sodium, and solid fat, alcohol, and added sugars, are reversed when compared with the food groups to encourage, with a higher score reflecting a better nutrient intake. For example, with sodium, a perfect HEI-2005 component score of 10.0 would reflect a sodium intake of only 1,500 mg/day [21]. Thus, it is appropriate that although sodium intake was higher in mushroom consumers, the HEI- 2005 component score was lower.

Especially noteworthy among the micronutrients was that vitamin D intake was not different between mushroom consumers and nonmushroom consumers. Vitamin D has been classified as a nutrient of public health concern by the 2010 Dietary Guidelines for Americans [24]. The RDA for vitamin D in adults, which assumes minimal sun exposure, is 600 IU (15 mcg)/day for most adults and 800 IU (20 mcg) for adults older than 70 years [24]. Intakes seen in this study were less than one half of the recommendations in males and less than one third in females. Some common edible varieties of mushrooms are rich natural sources of vitamin D, with concentrations of up to 59 mcg/100 g fresh weight [25]. However, when exposed to sunlight or UV light, ergosterol, the most abundant phytochemical in mushrooms [26,27] undergoes photolysis and yields previtamin D2, tachysterol, and lumisterol. Previtamin D2 then undergoes spontaneous thermal rearrangement to vitamin D2 [28]. The amount of vitamin D in mushrooms treated with UV light can increase dramatically; for example 85 gm of a raw portabella mushroom provides only 0.3 mcg of vitamin D; whereas, the same serving size that has been exposed to UV light provides 9.5 mcg vitamin D or nearly half of the RDA for adults [6].

Why then was the intake of vitamin D among mushroom consumers not higher than non-mushroom consumers in this study? Vitamin D and sterol levels were recently collected on 10 types of mushrooms commonly retailed in the US, with the goal of updating the USDA Nutrient Database [29], suggesting the most current information on vitamin D content is available. However, mushroom species commonly consumed in the US, including white button mushrooms, criminis, and non-UV light treated portabellas were relatively poor sources of vitamin D [29]. Moreover, not all mushrooms are UV light treated; and consumers may not know or recall if their mushrooms were UV light treated. This may be especially true of mushrooms consumed in a restaurant setting, where they would have no way to know if the mushrooms had been UV light treated. More widespread UV light treatment of mushrooms would provide an excellent source of this nutrient of public health concern.

Regardless of how mushroom consumers were defined, diet quality was higher among consumers than non-consumers. Both definitions of consumers had higher intakes of total vegetables, dark green and orange vegetables, and total grains. Consumer Definition 1 consumers also had higher HEI-2005 component score for milk, perhaps reflecting that pizza with cheese was the third most common food consumed with mushrooms (data not shown). The oil sub-component was also higher in those in Consumer Definition 2. Since mushrooms have virtually no fat, these findings may reflect foods consumed with mushrooms, oils added during preparation, or at the table, for example in a salad with mushrooms. Mushroom consumers defined by Consumer Definition 2, also had higher intakes of total fruit; along with higher intakes of vegetables, which may have contributed to the higher potassium intake seen in this group. Intake of fruit and vegetables is low in all groups in the US [30]; therefore, consumption of mushrooms should be encouraged.

A principal limitation of this study is that cross-sectional studies cannot be used to determine cause and effect. Thus, any positive or negative findings may be the result of foods consumed with mushrooms or may reflect how the mushrooms were prepared. Twenty-four hour dietary recalls have several inherent limitations. Participants rely on memory to self-report dietary intakes; therefore, data are subject to non-sampling errors, including underreporting of energy and examiner effects. The one-day intake used in this study may not represent usual intake of individuals over time. However, a single 24-hour dietary recall is appropriate when reporting mean group intakes [31]. The choice was made to use a single 24-hour dietary recall when the 2001-2002 data sets were included in the analyses to assure adequate sample size; at that time, only NHANES collected only one day of dietary data. Due to multi-collinearity of diet, foods other than mushrooms may have contributed to differences in nutrient intake of the participants. This may be especially true for foods that did not contribute substantial amounts of mushrooms, like some mushroom soups.

Mushroom consumption, regardless of the way it was defined, was associated with a better nutrient profile and diet quality than that seen in non-consumers. Mushroom consumption should be encouraged by health professionals, including registered dietitians; nutrition education programs that increase awareness and consumption of mushrooms should be designed and delivered. Ways to prepare mushrooms without sodium should be emphasized in consumer messages. Consumers should also be encouraged to seek out UV light treated mushrooms to help increase vitamin D intake in the diet. Further studies are needed to confirm these results and to determine the association of mushroom consumption with health risk markers, including obesity, cardiovascular risk factors, and metabolic syndrome.

This work is a publication of the United States Department of Agriculture (USDA/ARS) Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas. The contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations imply endorsement from the U.S. government. Support was obtained the Mushroom Council and the USDA-Agricultural Research Service through specific cooperative agreement 58-6250- 6-003. Partial support was received from the USDA Hatch Project LAB 93951. The funding sources had no input into the study design or the interpretation of the results.

Aside from the above funding disclosure, the authors declare no conflicts of interest. All authors participated equally in this study and in the preparation of this manuscript.