A novel challenge in agriculture is the production of tailored foods, i.e., foods specifically suitable for target groups of people with particular nutritional needs. In fact, in recent years, a number of studies have highlighted the possibility of producing vegetables for specific physiological conditions, such as biofortified vegetables, with the aim of counteracting different nutritional deficits [1
]. In general, these authors reported evidence on the use of specific growing protocols aimed to increase the content of specific nutrients in plant tissues, such as iodine (I), silicon (Si), calcium (Ca), selenium (Se), zinc (Zn), and iron (Fe). However, although most research on tailored foods has been focused on biofortification in order to increase the content of nutrients in plant tissues, it should be noted that in populations with specific physiological conditions, it is recommended to reduce the uptake of specific nutrients in order to improve their health condition. An example of this is reducing potassium (K) and sodium (Na) intake for chronic kidney disease (CKD) patients in order to improve their physiological condition. Chronic kidney disease is defined as a condition of impaired renal function [9
]. Epidemiological data show that CKD is a widespread disease with an increasing trend in the world population. It is estimated that about 10% of the worldwide population is affected by CKD, and millions die each year because they do not have access to affordable treatments [10
]. Nutritional approaches play an important role in improving the physiological condition of these patients. In order to prevent the occurrence of hyperkalemia (i.e., K level in the blood higher than normal), it is recommended to avoid eating foods with high levels of K, including fruits and vegetables. Vegetables, in fact, are generally rich in K; higher levels are present in leafy vegetables such as spinach (5580 mg/kg of fresh weight) and Swiss chard (3790 mg/kg of fresh weight) [11
] This element constitutes up to 10% of plant dry weight and is considered a macronutrient essential for plants, with fundamental effects on their health, growth, and development [13
]. As a result, it is difficult to reduce the physiological K concentration in plants without having detrimental effects on yield and marketable quality, because of the fundamental physiological functions of K, including enzyme activation, osmotic regulation, photosynthesis, and translocation of the products of photosynthesis [14
]. Recently, Renna et al. (2018) [16
] reported reduction of K tissue concentration in microgreens of two cultivars of chicory (Cichorium intybus
L.) and one cultivar of lettuce (Lactuca sativa
L. group crispa). However, microgreens are unconventional vegetables, considered niche products generally accessible only to restricted groups of people. Unlike microgreen cultivation, characterized by a short growing cycle (generally 20 days from germination), reduction of K in conventional vegetables such as baby leaf vegetables, with plants cultivated over a complete growing cycle to be ready for selling, is more difficult. Both (i) the extent of the reduced level of K available to plants as supplied in the fertilization program and (ii) the time of exposure to K deprivation have been reported to negatively affect market quality and yield [13
] and/or nutritional quality (i.e., ion content), generally with an increase of Na content in vegetables [17
Among different cultivation techniques, a floating hydroponic system, which involves growing plants on trays floating in tanks filled with a nutrient solution (NS), has proven to be an interesting tool to obtain baby leaf vegetables with modified tissue concentrations of specific minerals (Ca and Si) [2
] in edible parts of the plants. By acting on the mineral composition of the NS, it is possible to modify to a certain extent the tissue concentration of target ions. The objectives of this study were as follows: (i) To define a cultivation protocol suitable to produce baby leaf vegetables (spinach and Swiss chard) with low K tissue content, without negatively affecting plant growth and marketable quality, with a main focus on the application of the technique; (ii) to verify possible interactions of reduced K tissue concentration with the content of Ca and Mg, important factors for the nutritional needs of CKD patients, and oxalate, an important antinutritional compound, in the edible parts of plants; and (iii) to assess the ion bioaccessibility of these products by using an in vitro gastrointestinal digestion process.
We hypothesized that a floating hydroponic system with reduced concentration of K in the NS compared to the typical level for hydroponic production of baby leaf vegetables (200 mg/L) [3
] could be adopted to obtain tailored baby leaf vegetables for CKD patients with low K tissue content, satisfactory levels and bioaccessibility of other important nutrients (Ca and Mg), and no increase of oxalate.
The present study reports the successful soil-less production of two baby leaf species (spinach and Swiss chard) with low K contents for CKD, also providing, for the first time, to the best of our knowledge, an evaluation of ion bioaccessibility after an in vitro gastrointestinal digestion process. We used an NS with overall ion composition similar to what was reported by Hoagland and Arnon [23
], but we reduced the K concentration from 200 mg/L (usually used for growing baby leaf vegetables in a soilless system) to 50 mg/L. We found that in these growing conditions, K content in baby leaf vegetables was successfully reduced by about 39% and 27% in Swiss chard and spinach, respectively (Table 4
). The K requirement for optimal plant growth is in the range of 2–5% of the dry weight of the plant’s vegetative parts [24
]. For spinach, although plants subjected to K deprivation showed a significant decrease in K tissue level, the K tissue concentrations were always in the sufficiency range (3.6% and 4.6%, respectively, in K50
, considering average dry matter of 7.3%; Table 2
). In fact, plants did not show any typical symptoms of K deficiency. On the other hand, Swiss chard plants subjected to K deprivation in the experimental conditions showed a K concentration lower than or close to the limit of sufficiency range (1.8 and 2.5%, respectively, in K50
, considering average dry matter of 6.4% (Table 2
)), as confirmed by the negative effects observed in growth parameters for this species (Table 2
Our findings demonstrate that in the conditions of the study, reduced K concentration in the NS is effective for producing baby leaf vegetables with reduced K content for CKD patients. At the same time, the overall crop performance of spinach was not influenced by the K deprivation conditions tested in the study, in either quality or yield terms, while for Swiss chard a slight reduction of yield and a little modification of color parameters were observed (Table 2
). The yield decrease in Swiss chard could be the result of the potentially detrimental effects of K deficiency in plant tissues on important physiological mechanisms in the plant, such as impairment of stomatal opening, thereby affecting CO2
]. Considering that the proposed cultivation technique is aimed at producing a niche product, i.e., food tailored for a restricted population (CKD patients), we consider a 15–23% yield reduction satisfactory if the product is compliant with the normal quality standard, as in our case. Anyway, considering that for CKD patients the K intake from food must be restricted to 1500 mg per day [26
], it is important to note that 100 g of baby Swiss chard grown using NS with a low K level (50 mg/L) would provide about 19% of the recommended K daily intake, while 100 g of the same baby leaf vegetable grown with usual K concentration (200 mg/L) would provide about 31% of the recommended intake. Similarly, 100 g of baby spinach would provide about 33% and 45% of the K daily intake recommended for CKD patients in the case of low and usual K concentration in the NS, respectively.
Dietetic-nutritional therapy is an important component of the conservative treatment of patients suffering from CKD that must anticipate and be integrated with pharmacological therapy [27
]. The current nutritional approach is to limit the consumption of food sources rich in K, including vegetables, with the aim of reducing the intake of this nutrient. However, a diet low in vegetables and fruits also results in a reduction of vitamins, minerals, and bioactive compounds, generally with antioxidant and anti-inflammatory activity, as well as alteration of the intestinal microbiota [28
]. In advanced stages of CKD, a state of dysbiosis of the intestinal microbiota occurs, with alteration of intestinal permeability and bacterial composition, imbalance of microbial metabolism in the proteolytic sense, and increased production of uremic toxins, such as p-cresol and indoxyl sulfate [29
]. The results of the present study suggest that the availability of baby leaf vegetables with reduced K content could allow reducing K intake for the same serving of vegetables and/or increasing the amount of servings without excessively increasing K intake. Our findings, in agreement with other studies focused on the reduction of K tissue content in leafy vegetables [16
], suggest that the effect is species-dependent. This underlines the opportunity to select appropriately targeted genotypes suitable for cultivation processes in order to produce food products tailored for specific nutritional needs, such as those of CKD patients.
When the K content in the NS was reduced to 50 mg/L, the average Na content increased in both baby leaf species (Table 4
). We would like to point out that rainwater was used in the experiment and no Na was intentionally added in the NS preparation. The concentration of Na in the final NS was negligible (≈8 mg/L), as an effect of impurities normally present in fertilizers and stored rainwater. For Swiss chard, increased Ca and Mg was observed (Table 4
). According to Marchner [24
], it is likely that plants compensate for K reduction by increasing the tissue concentration of cations with similar roles in physiological processes, such as enzyme activity, pH control, and osmotic regulation. In particular, the role of Na in replacing the K in both biochemical and physiological nonspecific functions should be considered [31
]. From a nutritional point of view, it is important to highlight that high intake of Na may increase the risk of some diseases, thus the World Health Organization [32
] recommends not exceeding a daily intake of 2000 mg. The results of the present study show that 100 g of baby leaf vegetables with reduced K content supplied 47 and 61 mg of Na from spinach and Swiss chard, respectively (Table 4
). These amounts represent only 2–3% of the recommended daily intake and can be considered absolutely negligible with respect to the recommended limits. Furthermore, according to the USDA National Nutrient Database for Standard Reference, values of Na concentration for spinach and Swiss chard are, respectively, 790 [11
] and 2130 [12
] mg/kg fresh weight, much higher than the values found in the present study. Furthermore, increased Mg and Ca content in Swiss chard represents an interesting result, considering that generally CKD is a complex disease and its progression is associated with a number of serious complications, including metabolic bone diseases [33
]. In fact, preservation of bone is the primary focus of Ca control in kidney disease. Kidney failure reduces the production and conversion of vitamin D to active calcitriol 1.2(OH2
that in normal kidney function controls the absorption of Ca in the intestinal tract during digestion. The therapeutic approach for CKD includes, in most cases, pharmacological treatment based on Ca supplementation [34
]. The increased Ca and Mg, both cations associated with beneficial effects on bone mineral density, observed in the K50
Swiss chard may help to reduce the consumption of mineral supplements. Moreover, the potential availability of vegetables tailored for CKD patients could remedy the limitations these patients are generally subjected to in terms of consuming this food group, with the possibility of taking in healthy compounds typical of vegetables.
Regarding other nutritional traits, the K level in the NS did not affect the carotenoid, chlorophyll, or phenol content (Table 3
), suggesting that by using NS with low K concentration, it is possible to obtain reduced K in baby leaves without negatively affecting important aspects of the vegetables’ nutritional quality. Furthermore, we found that the oxalate content in spinach was successfully reduced by about 17% in samples grown with 50 mg/L of K with respect to spinach grown with 200 mg/L of K. The use of Chenopodiaceae with a high oxalate content as food may be associated with a negative impact on human health [35
], due to the negative effects of this antinutritional compound on reduced bioavailability of Ca, Mg, and Fe in the intestinal tract during digestion [35
]. Therefore, we can underline the positive impact of reduced K concentration in NS for baby leaf vegetable production with regard to reduced antinutritional compounds such as oxalate.
In addition to what was reported in other studies aimed at producing vegetables with low K content [16
], we assessed the quality of K-reduced vegetables by evaluating ion bioaccessibility after in vitro gastrointestinal digestion. We found that the processes tested in this study for reducing K content in the edible parts of baby leaves did not modify the ion bioaccessibility in either species. Therefore, considering average K bioaccessibility of about 56.4% for Swiss chard (Table 5
), hypothetical consumption of 100 g of baby leaf implies K bioaccessibility of 158 and 259 mg for K50
samples, respectively. At the same time, considering average K bioaccessibility of about 59.5% for spinach (Table 5
), hypothetical consumption of 100 g of spinach would imply K bioaccessibility of 291 and 399 mg for K50
samples, respectively. Besides K, it would be interesting to evaluate the bioaccessibility of other ions. Thus, while Mg bioaccessibility appears to be similar in both species, Swiss chard showed Ca bioaccessibility about threefold lower than spinach. Also, compared to Ca bioaccessibility values observed in a previous study carried out by this research group on four leafy vegetable species (mizuna, tatsoi, basil, and endive), Swiss chard showed, on average, lower values [3
]. At the same time, Swiss chard showed slightly lower bioaccessibility of oxalate. According to previous studies [2
] the bioaccessibility of mineral nutrients can be considerably affected by several factors, including mineral type and food matrix composition. At any rate, all the results of the present study suggest that bioaccessibility, defined as the ability of a nutrient to be released into the gastrointestinal tract, can be considered as a useful tool to better estimate real nutrient intake from vegetable products, especially when innovative cultivation protocols are applied.