Impact of Thermal Processing on the Nutrients, Phytochemicals, and Metal Contaminants in Edible Algae

Abstract

Edible algae products have increasingly become a larger component of diets worldwide. Algae can be a source of essential micronutrients and bioactive phytochemicals, although select varieties also often contain elevated concentrations of heavy metal contaminants. Due to the effects thermal processing of foodstuffs can have on levels of nutrients, phytochemicals, and contaminants, it is important to consider the role processing has on the levels of these components in algae food products. Here, we evaluate the literature covering how different types of processing, including commercial thermal application and in-home preparation, affect constituents such as vitamins, minerals, carotenoids, pigment compounds, and metal contaminants. Overall, the literature suggests that there are optimum processing conditions and specific cooking techniques that can be used to increase retention of important nutritional components while also reducing concentrations of metal contaminants. Although further research is needed on how thermal processing affects individual compounds in algae and their ultimate bioavailability, these data should be taken into consideration in order to inform design of product processing to both increase retention of nutritional components and limit metal contaminants.

Introduction

Archeological artifacts have indicated that humans have long been consuming algae as part of their diets. Indeed, written records documenting algae consumption in China have existed for more than two millennia, but perhaps its earliest reported use dates back to over 12,000 years ago in what is now modern-day Chile (Dillehay et al. 2008, Bangmei and Abbott 1987). More recently, the global algae industry has been growing at a rapid pace, with one projection estimating that the market will reach at least $50 billion USD by 2027, approximately 80-90% of which is related to products for human consumption (McHugh 2003, Grosshagauer, Kraemer, and Somoza 2020). Of the algae-based food products, 40% are consumed in a relatively unprocessed form recognizable to consumers—such as dried sheets—with the remaining 60% as algae-derived food ingredients such as alginates, agar, and carrageenan (Wells et al. 2017). Whereas historically the consumption of algae has largely been consolidated to certain localized markets, particularly to the Asia Pacific region, areas such as the continental United States (US) and Western Europe have experienced an increasingly expanding market for algae and related products that incorporate algae as a major ingredient (Bouga and Combet 2015). As an indicator of this increase, there have been calls for changes in labeling regulations to highlight specific compounds found within algae (Bouga and Combet 2015).

Products that include edible algae have expanded globally as part of the evolving food industry’s desire to satisfy the consumer’s appetite for novel and functional products. For instance, studies conducted on Australian consumers suggest that algae-based foods have a potential growth opportunity in Western societies especially via populations in market segments who prioritize health, the environment, snacks, and new trends (Birch, Skallerud, and Paul 2019a, 2019b). Increased interest in algae-containing foods may be related to increased research documenting its content of micronutrients and potentially bioactive phytochemicals. This increased attention has led to changes in foods and dietary supplement formulations to incorporate algae to address market demand (Tanna and Mishra 2018, Haskell-Ramsay et al. 2018). For example, the seaweed kelp is widely used as a source of iodine (I) in various dietary supplements, and different types of algae (e.g., Spirulina and Dunaliella salina) are also incorporated into supplements due to high concentrations of pro-vitamin A carotenoids and other phytochemical constituents (Grosshagauer, Kraemer, and Somoza 2020, Hu et al. 2008). Aside from compounds with potentially beneficial effects on health endpoints, it is important to consider that algal organisms can also accumulate metal contaminants (Banach, Hoek-van den Hil, and van der Fels-Klerx 2020). The most prominent of these potential contaminants are the toxic heavy metals, including arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg) (Brandon, Janssen, and de Wit-Bos 2014, Hwang et al. 2010). Therefore, such products need to be viewed in its totality to fully characterize both the target nutrients of interest, in addition to any possible contaminants.

Regardless of the known phytochemicals or contaminants present in fresh, unprocessed algae, these products generally undergo several stages of processing before being consumed, as with many other types of foods (Li et al. 2019, Hamid et al. 2020). Consequently, it is critical to characterize how post-harvest processing, inclusive of storage, thermal processing, and in-home cooking, affects these nutrients, phytochemicals, and contaminants. Here, we first review the major types of whole algae food products consumed within diets, we describe the major nutrients, phytochemicals, and metal contaminants in these foods, and then finally evaluate the literature that describes how processing affects the concentrations of these constituents. As the focus of this review is on whole or algae-based products, this review will not include studies involving seaweed extracts or algae-derived ingredients. Still, it is important to recognize that ingredients derived from algae—hydrocolloids likely being the most well-known—are widespread in the food supply and provide critical functional attributes in multiple foods (Porse and Rudolph 2017).

Algae varieties found in the diet

Algae is a general term that can be used to describe aquatic organisms that are unicellular eukaryotes, multicellular eukaryotes, and prokaryotes, with specific examples including microalgae, seaweeds, and blue-green algae, respectively (Figure 1) (Hoek et al. 1995). To complicate matters, algae taxonomy is a field that is still developing, so it is not uncommon for organisms to have several different names and taxonomic classifications (Lim et al. 2017). The multiplicity of names may also be due partly to challenges in translating indigenous or traditional names into appropriate taxonomic terms (Abbott 1978). There are at least tens of thousands of varieties of algae, but only a small fraction of this number is consumed in the human diet. Over 70 species of algae have been reported in the Chinese diet and more than 50 in the Japanese diet, with roughly 20 of the species overlapping in both countries (Bangmei and Abbott 1987, Arasaki and Arasaki 1983). In addition, taxonomic names of multiple varieties of edible Hawaiian algae, including endemic species, have also been well documented (Abbott 1984). Information on per capita consumption of algae products is limited, as evidenced by data published by the Food and Agriculture Organization (FAO) which contains values for only three out of 163 countries in their database (FAO 2020). For the most recent year available (2013), per capita consumption of algae (or “aquatic plants”) specify that Korea, China, and Japan consumed 61, 26, and 2.5 g per day, respectively.

Figure 1.

Overview of the types of organisms often referred to as algae. Prokaryotic cyanobacteria have previously been considered a type of algae, but more recently the term algae has been used to exclusively refer to eukaryotic species. *Multicellular, eukaryotic types of algae are commonly referred to as macroalgae or seaweed.

Eukaryotic algae can be broadly described by its color or appearance as brown, green, or red (Figure 2). Most algae species with relevance to food are marine, but some types of green algae are found in freshwater or even on land. Brown algae are from class Phaeophyceae, which includes a group of kelps that are often referred to in the US by their Japanese common names such as kombu (Laminaria japonica) and wakame (Undaria pinnatifida). Different species of kelp may be used in dietary supplements as a source of micronutrients, used as a seasoning or prepared as a tea (e.g., kombu), or simply served with a meal as a vegetable (e.g., wakame) (Nisizawa et al. 1987). Green algae are classified within the phylum Chlorophyta and include organisms from genus Chlorella, which has been promoted as an environmentally-sustainable source of protein and can be found in dietary supplements (Safi et al. 2014). Red algae within the phylum Rhodophyta, include seaweed nori (Porphyra spp.) and dulse (Palmaria palmata). Although disputed within the taxonomy field, algae terminology has often been inclusive of prokaryotes, such as cyanobacteria, which are known to exist across marine, freshwater, and terrestrial environments. More recently, an increasing number of biologists and taxonomists have considered algae to be inclusive of only eukaryotic organisms, but to avoid confusion, we will use the term algae to broadly include both eukaryotic species and prokaryotic cyanobacteria. Cyanobacteria from the genus Spirulina are currently commonly marketed as dietary supplements due to their high concentration of micronutrients and phytochemicals. However, Spirulina has a history of being a traditional source of food in various societies, including those in the region of West-central Africa surrounding Lake Chad (Hoek et al. 1995). Aside from Spirulina, cyanobacteria from marine (Brachytrichia quoyi) and terrestrial (Nostoc flagelliforme) environments have been commonly consumed in China (Bangmei and Abbott 1987).

Figure 2.

Examples of algae from Ocean Era’s (formerly Kampachi Farms) research facility at the Natural Energy Laboratory of Hawaii Authority (NELHA) on the Big Island of Hawaii, US. (A) cultivated red algae (Halymenia hawaiiana), (B) cultivated red algae (Gracilaria parvispora), (C) cultivated green algae (Caulerpa lentillifera), (D) wild-collected brown algae (Sargassum spp.) and (E) Ocean Era’s land-based tank array system for tropical macroalgae culture. Photos taken by Keelee Martin © Ocean Era, LLC. Used with permission.

Overview of the post-harvest processing of algae

Algae historically have been largely wild-harvested from bodies of water, but the increased demand of these products has driven producers to cultivate algae in more controlled environments (see Figure 1E). If strategically implemented, commercial production can also be leveraged to remediate depleted waters, combat invasive algal species, and reduce the burden on natural algae in locations with decreasing wild populations of algae (Hart et al. 2014, Li et al. 2020). Freshly harvested algae can be stored prior to consumption, although the high moisture content of the seaweed necessitates immediate processing or addition of a preservative such as mineral salts (e.g., sodium chloride) to prevent growth of spoilage organisms (Wang, Zhang, and Fang 2019). Some types of algae are commonly consumed fresh or unprocessed, such as ogo (Gracilaria spp.) and limu lipoa (Dictyopteris plagiogramma), which are commonly consumed in Hawaii, sea grapes (Caulerpa lentillifera) in Japan, and dulse (Palmaria palmata) in Ireland. However, the majority of commercial algae-based foods are processed prior to consumption.

There are several methods for post-harvest processing of algae, with different types of drying typically being most common (Santiago and Moreira 2020). Depending on climate, algae can be dried in the sun after harvest (“solar drying”), which has the advantage of being economical and is usually done within close proximity to the location of harvest. Algae products are also frequently subjected to toasting or hot air drying due to high water activity of the material. More recently, certain algae drying methods have used microwave heating due to purported cost and energy savings, in addition to other methods such as novel infrared drying techniques (Wang, Zhang, and Fang 2019, Uy et al. 2005). Freeze drying can be also used to dehydrate seaweed, but this process can be energy intensive and is likely to be targeted for use on high-value products. Spray drying is generally well-suited to process unicellular algae such as Spirulina because this process can drive off the high water content that is inherent in its bulk cultivation. Although drying represents a major processing strategy for commercially produced algae-based foods, not all commercial algae-based foods are dried products. Nori tsukudani is a centuries-old jam or paste-like food made from boiling seaweed (Monostroma spp.) with seasoning, typically soy sauce and sweet rice wine (Mouritsen, Rhatigan, and Pérez-Lloréns 2018). Modern commercialized versions are made shelf-stable via thermal processing and are packaged in glass jars, but use of high pressure processing and cold plasma processing have been more recently applied on algae, which may be related to ongoing research of these methods to process a variety of other food products (Beyrer et al. 2020, del Olmo, Picon, and Nuñez 2020, Bansal et al. 2019, Chakraborty et al. 2017). Although less popular in Western markets, thermally processed algae purees have emerged as niche products. Other food applications include the use of algae to partially substitute ingredients in products such as minced fish and noodles (Debbarma et al. 2017, Dewi 2011).

Overview of nutritional and phytochemicals in algae

Algae contain an array of macronutrients, micronutrients, and a variety of phytochemicals (Table 1). The potential impacts of algae consumption on human health outcomes have been previously reviewed elsewhere (Brown et al. 2014), so here we focus on the effect of thermal processing on major components—macronutrients, micronutrients, and phytochemicals—in algae.

Table 1.

Nutrient composition of select algae varieties found in the diet and in food supplements.^a,b

Nutrient	Unitc	Himanthalia	Undaria (wakame)	Porphyra (nori)	Ulva (sea lettuce)	Palmaria (dulse)	Laminaria (kelp)	Spirulina	Chlorella
Vitamin A (β-carotene)	mg/100g FW	4.3	N/A	3.9	N/A	2.0	5.0–11*	100–120	36
Vitamin B12	μg/100g FW	N/A	0.35	0.77	6.3	1.8	0.50	60–240**	0–240**
Vitamin C	mg/100g FW	47	170	33–150	110	0.61–62	32	ND	N/A
Vitamin E (α-tocopherol)	mg/100g FW	2.2	16	0.34–1.3	ND	0.17–15	3.1	2.8–75	N/A
Calcium	mg/100g DW	57–910	930	390–690	620	280	690–1,000	220–1,300	590
Copper	mg/100g DW	0.19	0.38–0.56	0.19–2.9	0.40–0.57	0.76	0.2–1.7	0.12–0.49	0.06
Iodine	mg/100g DW	20	7.4	2.5	3.0	19	130–900	N/A	N/A
Iron	mg/100g DW	1.8–9.5	4.7–13	10–78	21–240	24	3.3–87	49–880	260
Magnesium	mg/100g DW	170–830	830–1,200	280–570	880	190	660–770	370–400	340
Manganese	mg/100g DW	4.1	0.85–0.87	2.2–2.7	N/A	N/A	0.4–3.8	2.6–11	2.1
Potassium	mg/100g DW	2,600–6,700	8,700–11,000	1,400–3,500	470	2200	3,800–12,00	1,600–3,100	50
Zinc	mg/100g DW	3.2–3.8	1.7–6.1	3.7–4.2	1.1–1.7	0.57	0.1–5.4	0.5–79	1.2

^aData compiled from Careri et al. (2001); Cha et al. (2012); Cofrades et al. (2010); Dey and Rathod (2013); Edelmann et al. (2019); Ferraces-Casais et al. (2012); García-Casal et al. (2007); García-Sartal et al. (2013); Grosshagauer et al. (2020); Kakita and Obika (2017); MacArtain et al. (2007); Ruperez (2002); Schiener et al. (2015); Tokusoglu and Unal (2003).

^bAbbreviations used: DW, dry weight; FW, fresh weight; N/A, not available; ND, not detected.

^cData not presented as per dry weight in literature source was corrected for moisture content.

^*Data presented as mg/100g DW.

^**Data presented as μg/100g DW.

Algae are typically composed of greater than 70% carbohydrates and fibers, which includes components such as cellulose, alginate, carrageenan, sugar alcohols, and glucans. (Schiener et al. 2015, Stiger-Pouvreau, Bourgougnon, and Deslandes 2016). Many of these carbohydrates are used by the food industry to impart certain desired physical properties to foods. Additionally, some of these components have putative bioactive properties, such as sulfated polysaccharides, which reportedly has in vitro anti-viral activity against dengue virus and SARS-CoV-2 (Kwon et al. 2020, Talarico et al. 2005).

The lipid content of algae can range from less than 1% for kelp, ~10% for chlorella, and as high as 70% in certain types of microalgae (Callegari et al. 2020, Schiener et al. 2015, Chi et al. 2019). The fatty acid composition of green algae is composed of both saturated and unsaturated fatty acids, with palmitic acid (C16:0), oleic acid (C18:1), and linolenic acid (C18:3) being the predominant constituents, although the n-3 fatty acid concentrations in select microalgae can position them as a potential alternative to fish oils (Ryckebosch et al. 2014).

Algae can be a significant source of protein, containing both essential and non-essential amino acids. Several red algae varieties contain high amounts of glutamate and aspartate relative to the other amino acids present in the plant, which may be why these foods are often used as flavor enhancers in food preparation (Cofrades et al. 2010). Multiple assays have also been conducted to estimate its protein quality. For instance, studies to determine the protein efficiency ratio (PER) of Chlorella and Spirulina have found that that it is ~2.0 for these algae, as compared to 2.7 for casein (Kose et al. 2017, Dawczynski, Schubert, and Jahreis 2007, Becker 2007). The protein digestibility-corrected amino acid score (PDCAAS) of red seaweed (Porphyra sp.) has been reported as ~0.43 compared to 1.0 for casein (Cian et al. 2014). The digestible indispensable amino acid score (DIAAS) is currently the recommended protein quality measurement for human nutrition (Leser 2013), but has not been well reported for algae because of a lack of standardized data on ileal digestibility of algal amino acids (Angell et al. 2016). The PER and PDCAAS values of previously reported algae species exclude it from being deemed an excellent quality source of protein. However, algae have been posited as a sustainable source of dietary protein due to its low land usage, relatively high yield, and low energy input, which may make it appropriate for partial protein supplementation in animal feed or formulated human foods (Klamczynska and Mooney 2017, Schwenzfeier, Wierenga, and Gruppen 2011). Because thermal processing has been reported to affect liberation of amino acids from an algae food matrix, it is important to continue to characterize the degree to which processing ultimately affects protein quality in this matrix (Maehre et al. 2016).

Significant amounts of essential minerals and trace metals can be present in algae. Kelp in particular is known to contain high amounts of the trace element I. In the Japanese diet, it is estimated that up to 1-3 mg I per day is obtained from algae such as kelp, and amounts as high as 4.8 mg I per day are consumed by Taiwanese populations from algae sources (Zava and Zava 2011, Domínguez-González et al. 2017). Sea spaghetti (H. elongata), wakame (U. pinnatifida) and nori (P. umbilicalis) all contain 1-10% dry weight (DW) of the minerals potassium (K), sodium (Na), and calcium (Ca), and 0.3-0.8% magnesium (Mg). Other notable nutritional elements in algae include iron (Fe), manganese (Mn), zinc (Zn) (Cofrades et al. 2010, Tokuşoglu and Üunal 2003). These levels of minerals in algae are consistent with another report indicating that Fucus, Laminaria, wakame, Chondrus, and nori contain ~3-11% DW Na and K and 0.4-1% DW Ca and Mg (Rupérez 2002). Additionally, clinical studies assessing the Fe bioavailability from several types of cooked algae have determined it to range from 12-22%, which is higher than the Fe bioavailability of 5-12% typically observed in those consuming vegetarian diets (Masuda, Yamamoto, and Toyohara 2015, García-Casal et al. 2007).

Multiple studies have characterized the amount of both water- and fat-soluble vitamins in algae, such as B vitamin complex, ascorbic acid (vitamin C), pro-vitamin A carotenoids, and tocopherols (vitamin E) (Seshadri, Umesh, and Manoharan 1991, Edelmann et al. 2019, MacArtain et al. 2007). Spirulina and nori in particular have been described as being a potential vegetarian source of vitamin B₁₂ because this vitamin can be found in relatively high concentrations in these algae varieties (Croft et al. 2005). Although initial pre-clinical animal studies assessing the bioavailability of B₁₂ from algae appeared to be promising, human studies have produced mixed results and do not appear to support it being bioavailable (Dagnelie, van Staveren, and van den Berg 1991, van den Berg, Brandsen, and Sinkeldam 1991). Nori and Himanthalia contain ascorbic acid at levels ranging from 30-50 mg/100 g fresh weight (FW), but other species (i.e., kombu and dulse) contain only very low amounts (<1 mg/100 g FW) (Ferraces-Casais et al. 2012). All four types of these algae contain limited amounts of α-tocopherol (0.2-2.2 mg/100 g FW) and pro-vitamin A β-carotene (2-4 mg/100 g FW). As a comparison, Spirulina can contain β-carotene at levels approximately 100-fold higher (Seshadri, Umesh, and Manoharan 1991). These results indicate that variability of nutritional components in algae can be significant and that ongoing analytical work is needed to more fully characterize the occurrence of these compounds in algae.

Pigments, particularly carotenoids, have been extracted from various algal species. Some research has focused on carotenoids in the context of pro-vitamin A (Seshadri, Umesh, and Manoharan 1991, Kakita and Obika 2017); however algae are also a source of carotenoids without pro-vitamin A activity (Careri et al. 2001). Unlike other dietary carotenoid sources, such as fruits and vegetables, algae are a source of unique carotenoids that are not found in terrestrial plants, including astaxanthin, fucoxanthin, diatoxanthin, and diadinoxanthin (Boussiba and Vonshak 1991, Maeda et al. 2018, Ambarsari et al. 1997). Carotenoid composition varies depending on the type of algae, the type and intensity of light exposure, and environmental stress/nutrient starvation (Ota et al. 2018, Kondzior, Tyniecki, and Butarewicz 2019, He, Duncan, and Barber 2007, Boussiba et al. 1999, Kobayashi et al. 1992). Haematococcus pluvialis, a freshwater green alga, has also been well studied and is used commercially, particularly for its ability to biosynthesize and accumulate high amounts of astaxanthin. The actual amount of astaxanthin in Haematococcus pluvialis depends on growth conditions; thus, much research efforts have gone toward manipulating environmental and nutritional conditions, such as optimizing application of light wavelengths and targeting mineral concentrations necessary for its growth, such as Fe, P, and sulfur (S) (He, Duncan, and Barber 2007). Much of this research indicates that astaxanthin yields are roughly 2-4% DW of Haematococcus pluvialis (Martínez et al. 2019, Olaizola 2000, Boussiba et al. 1999, Irshad et al. 2019).

Chlorophylls and other non-carotenoid pigments such as phycobiliproteins are found in algae. Chlorophyll exists abundantly in various plants and algae as light harvesting pigments for the photosynthesis process and is used in the food industry as natural food color (Humphrey 2004). Unlike flowering plants, algae do not require exposure to light in order to initiate chlorophyll synthesis (Suzuki and Bauer 1995). When cultured under optimal conditions, Chlorella has been reported to contain ~4% DW chlorophyll (Kong et al. 2014). Phycobiliproteins, found mainly in red algae and cyanobacteria, are high-value pigment proteins that have applications for food, cosmetic, and biomedical industries (Pereira et al. 2020). Phycobiliproteins can be divided into the two main classes, phycoerythrins and phycocyanins, and these compounds have been reported in Gracillaria spp. at 0.46-1.3 mg/g and 0.11-0.28 mg/g for phycoerythrin and phycocyanin, respectively (Tello-Ireland et al. 2011, Gómez et al. 2005, Beer and Eshel 1985). As extracted and purified compounds, phycobiliproteins are of interest for their potential bioactive effects, but have also shown functional potential as emulsifiers in food systems (Chen et al. 2017).

Generally speaking, varying pigment yields across studies may be partly due to differences in biosynthesis from algae, but yields are greatly influenced by extraction conditions and quantification methodology. Solvent choice can influence yields by selectively extracting certain polar or nonpolar carotenoids or pigments more efficiently, and certain extraction techniques have been shown to be more effective at physically liberating pigments from algae cells, as also with other food matrices (Simon and Helliwell 1998, Varapasad et al. 2019, Shinwari and Rao 2018b). Indeed, carotenoid profiles from identical algae sample have been shown to be qualitatively different when extracted using pressurized liquid extraction (PLE) compared to a combination of PLE and supercritical antisolvent fractionation (SAF), an isolation and concentration technique, potentially due to differences in carotenoid relative solubility or potential transformation during processing (Gallego et al. 2020). Quantification methodology that relies on spectrophotometry should be interpreted with caution because it can overestimate carotenoid and other pigment concentrations and does not distinguish between different compounds or isomers. For example, presence of chlorophyll degradation products, including chlorophyllide a and phaeophytin a, resulted in at least a ~10% overestimation of chlorophyll when quantified from algae using spectrophotometry compared to high pressure liquid chromatography (HPLC) (Schagerl and Künzl 2007).

Effect of thermal processing on vitamin retention in algae

Ongoing research has characterized how post-harvest processing affects concentrations of select micronutrients in algae-based foods (Table 2). Because several vitamins are in vitro antioxidants, they may be particularly sensitive to oxidative and thermal degradation. Figure 3 displays a simplified schematic of how processing affects the nutritional and phytochemical constituents in algae. Jensen (1969) performed one of the earliest studies on this topic and determined the effect of processing and storage on water- and fat-soluble vitamins in algae. In this study, fresh Norwegian kelp (Ascophyllum nodosum) was harvested, processed by drying at 40°C, and then subsequently held in a storage silo for up to 16 days. The results showed that although there was 50% loss of ascorbic acid during storage of the fresh material, the fat-soluble vitamins β-carotene and α-tocopherol were highly retained over this period. Further monitoring of target vitamins during storage indicated that humidity and temperature (4-25°C) were significant factors that corresponded to decreased levels of these compounds over time. Similarly, retention of ascorbic acid in brown algae (S. hemiphyllum) was found to be affected by the type of drying method, with the data indicating that freeze-dried algae contained up to 3-fold greater amounts of this vitamin compared to samples that were hot air or solar dried (Chan, Cheung, and Ang 1997).

Table 2.

Summary of literature on the effect of processing on vitamin concentrations in algae.^a

Vitamin	Algae	Processing	Approximate retention after processingb	Analytical Method	Reference
Vitamin A (β-carotene)	Ascophyllum (rockweed)	Storage at 4–25°C	30–60%	Paper chromatography	Jensen 1969
Vitamin A (β-carotene)	Spirulina	Spray dried	90%	Column chromatography	Seshadri, Umesh, and Manoharan 1991
Vitamin A (β-carotene)	Laminaria (kombu)	Dried at 45°C, then boiled	200%	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Vitamin A (β-carotene)	Undaria (wakame)	Dried at 45°C, then boiled	290%	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Vitamin A (β-carotene)	Fucus	Hot air dried at 25–60°C	No change	HPLC-UV/VIS-MS	Silva et al. 2019
Vitamin C (ascorbic acid)	Ascophyllum (rockweed)	Storage at 4–25°C	50%	Titration with 2,6-dichlorophenol-indophenol	Jensen 1969
Vitamin C (ascorbic acid)	Sargassum (brown seaweed)	Sun dried, oven dried, or freeze dried	Freeze dried (no change); oven dried (70%); sun dried (30%)	2,4-dinitrophenylhydrazine method	Chan, Cheung, and Ang 1997
Vitamin C (ascorbic acid)	Undaria (wakame)	Dried at 45°C, then boiled	0%	HPLC-UV/VIS	Amorim, Lage-Yusty, and López-Hernández 2012
Vitamin E (α-tocopherol)	Ascophyllum (rockweed)	Storage at 4–25°C	0–50%	Paper chromatography	Jensen 1969
Vitamin E (α-tocopherol)	Undaria (wakame)	Dried at 45°C, then boiled	No change	HPLC-FL	Amorim, Lage-Yusty, and López-Hernández 2012
Vitamin E (α-tocopherol)	Laminaria (kombu)	Dried at 45°C, then boiled	No change	HPLC-FL	Amorim, Lage-Yusty, and López-Hernández 2012

^aAbbreviations used: HPLC, high-performance liquid chromatography; MS, mass spectrometer; VWD, variable wavelength detector; UV/VIS, ultra violet/visible detector; FL, fluorescence detector.

^bRetention was estimated by calculating [compound concentration after processing]/[compound concentration before processing]*100%. Values greater than 100% may indicate enhanced extractability from a modified food matrix due to processing.

Figure 3.

Simplified flowchart of the overall post-harvest processing scheme of algae and the effect on vitamin and phytochemical constituents. After algae is harvested, it can be consumed fresh or subjected to drying processes to prevent spoilage. After the consumer receives the product, it can be consumed as is, or otherwise be further thermally processed before consumption. Processing methods are presented in ascending order of increasing effect on loss of vitamin and phytochemical components.

Limited data suggest that in-home processing can affect the levels of ascorbic acid in kombu (Laminaria sp.) and wakame (Undaria pinnatifida) (Amorim, Lage-Yusty, and López-Hernández 2012). Boiling these algae for 20-60 min resulted in significant reductions of ascorbic acid, which is consistent with literature demonstrating that boiling vegetables reduces levels of water-soluble vitamins, such as ascorbic acid (Delchier, Reich, and Renard 2012).

Effect of thermal processing on phytochemical retention in algae: Carotenoids, chlorophyll and other pigments, and phenolic compounds

Carotenoids

Besides the vitamins present in algae, there are multiple phytochemical compounds with putative bioactive effects on human health. Some of these compounds include carotenoids, including pro-vitamin A β-carotene, lutein, zeaxanthin, and astaxanthin, which are often present in high concentrations (up to 4% DW) in certain types of algae (Ambati et al. 2018, Terasaki et al. 2012). Carotenoids from algae can be extracted from the plant matrix to produce highly concentrated extracts of β-carotene that can then be used as a food/dietary supplement ingredient (Dey and Rathod 2013, Poojary et al. 2016). Notably, algae have also been optimized for carotenoid accumulation and are grown commercially as a carotenoid source. In particular, Spirulina and Haemotococcus pluvialis are often used commercially to produce well-characterized carotenoid extracts (Park et al. 2018, Hu et al. 2008, Boussiba et al. 1999). However, research on these algae has primarily focused on increasing carotenoid biosynthesis or optimizing extraction yields as opposed to understanding the effect of post-harvest food processing on carotenoid concentrations.

Still, there is ongoing research on how different types of processing methods affect levels of carotenoids and other pigment compounds in algae (Table 3). Seshadri et al. (1991) found that spray drying Spirulina at an inlet temperature of 95-120°C reduced β-carotene concentrations by ~10%, and storage of the dried material in dark-tinted containers over 45 d resulted in an additional 60% loss. Similarly, microalgae (Phaeodactylum tricornutum) spray dried at an inlet temperature of 180° C contained 25% lower total carotenoids compared to either fresh or freeze-dried algae (Ryckebosch et al. 2011). However, the spray-dried algae stored over 35 d at temperatures ranging from −20°C to 20°C did not have any additional reduction in total carotenoids. The authors in this study did not perform analysis for individual carotenoids, so it is not possible to determine directly if specific compounds were more susceptible to degradation from the storage conditions. In contrast, a report by Stévant et al. found that fucoxanthin (a xanthophyll) may not be sensitive to certain thermal processing conditions because the authors reported that brown algae (Saccharina latissima) dried at temperatures ranging from 25-70°C did not have significantly different levels of fucoxanthin compared to freeze-dried algae (Stévant et al. 2018). Similar results were reported in Fucus, where no difference in fucoxanthin levels were found between sample dried at 60°C and control (Silva et al. 2019). Not surprisingly, one study found that subjecting sea lettuce to solar drying resulted in lowest retention of total carotenoids when compared to freeze, vacuum, or hot air drying (Uribe et al. 2019). Together, these results indicate that stability of certain carotenoids in an algae matrix can be affected by thermal processing and subsequent storage, but that these conditions can be optimized in order to achieve greater retention of targeted carotenoid compounds.

Table 3.

Summary of literature on the effect of processing on carotenoids and other pigment compounds in algae.^a

Compound	Algae	Processing	Approximate retention after processingb	Analytical Method	Reference
Carotenoids, total	Phaeodactylum tricornutum	Spray dried or freeze dried	Spray dried (75%); freeze dried (no change)	Spectrophotometry	Ryckebosch et al. 2011
Carotenoids, total	Pyropia orbicularis	Vacuum dried at 40–80°C	4–60%	Spectrophotometry	Uribe et al. 2018
Carotenoids, total	Spirulina	Cold atmospheric pressure plasma, 7–15mW/cm2	65–85%	Spectrophotometry	Beyrer et al. 2020
Carotenoids, total	Ulva (sea lettuce)	Freeze dried (control), hot air dried at 70°C, solar dried, or vacuum dried at 70°C	Hot air dried (70%), vacuum dried (60%); solar dried (50%)	Spectrophotometry	Uribe et al. 2019
Chlorophyll pigments (a/b)	Ulva (sea lettuce)	Freeze dried (control), hot air dried at 70°C, solar dried, or vacuum dried at 70°C	Hot air dried (25–65%); solar dried (30–60%), vacuum dried (20–70%)	Spectrophotometry	Uribe et al. 2019
Chlorophyll pigments (chlorophyll + pheophytins + pheophoribides)	Ulva (sea lettuce)	Boiled or microwaved at 800W	70–85%	HPLC-UV/VIS	Chen and Roca 2018
Chlorophyll pigments (chlorophyll + pheophytins + pheophoribides)	Laminaria (kombu)	Boiled or microwaved at 800W	65–75%	HPLC-UV/VIS	Chen and Roca 2018
Chlorophyll pigments (chlorophyll + pheophytins + pheophoribides)	Porphyra (nori)	Boiled or microwaved at 800W	80–90%	HPLC-UV/VIS	Chen and Roca 2018)
Chlorophyll a	Laminaria (kombu)	Air dried at 45°C, then boiled	0%	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Chlorophyll a	Undaria (wakame)	Air dried at 45°C, then boiled	0%	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Chlorophyll a	Spirulina	Cold atmospheric pressure plasma, 7–15mW/cm2	40–100%	Spectrophotometry	Beyrer et al. 2020
Fucoxanthin	Laminaria (kombu)	Air dried at 45°C, then boiled	120%	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Fucoxanthin	Undaria (wakame)	Air dried at 45°C, then boiled	150%	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Fucoxanthin	Saccharina (kelp)	Air dried at 25–70°C	No change	HPLC-UV/VIS	Stévant et al. 2018
Fucoxanthin	Fucus	Air dried at 25–60°C	200% at 40°C; no change for other treatments	HPLC-UV/VIS-MS	Silva et al. 2019
Lutein	Undaria (wakame)	Air dried at 45°C, then boiled	13-fold increase	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Lutein	Fucus	Air dried at 25–60°C	No change	HPLC-UV/VIS-MS	Silva et al. 2019
Lutein	Ulva (sea lettuce)	Air dried at 25–60°C	3-fold increase at 25°C; no change for other treatments	HPLC-UV/VIS-MS	Silva et al. 2019
Pheophytin a	Laminaria (kombu)	Air dried at 45°C, then boiled	24-fold increase	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Pheophytin a	Undaria (wakame)	Air dried at 45°C, then boiled	30-fold increase	HPLC-VWD	Amorim, Lage-Yusty, and López-Hernández 2012
Phycocyanin	Gracilaria chilensis	Air dried at 40–70°C	2–3-fold increase at 40–50°C; no change for other treatments	Spectrophotometry	Tello-Ireland et al. 2011
Phycocyanin	Pyropia orbicularis	Vacuum dried at 40–80°C	110–170%	Spectrophotometry	Uribe et al. 2018
Phycocyanin	Spirulina	Cross flow dried (60°C), spray dried (150°C), or oven dried (60°C)	50%	Spectrophotometry	Sarada, Pillai, and Ravishankar 1999
Phycocyanin	Spirulina	Cold atmospheric pressure plasma, 7–15mW/cm2	40–100%	Spectrophotometry	Beyrer et al. 2020

^aAbbreviations used: HPLC, high-performance liquid chromatography; VWD, variable wavelength detector; UV/VIS, ultra violet-visible detector.

^bRetention was estimated by calculating [compound concentration after processing]/[compound concentration before processing]*100%. Values greater than 100% may indicate enhanced extractability from a modified food matrix due to processing.

Although preliminary, some limited data suggest that in-home processing can increase levels of certain carotenoids in algae. For instance, levels of β-carotene, fucoxanthin, and lutein have reportedly increased after boiling kombu (Laminaria sp.) and wakame (Undaria pinnatifida) (Amorim, Lage-Yusty, and López-Hernández 2012). It is possible that these increases may be the result of conversion/degradation of other compounds to carotenoids, but the authors note that this increase may be related to increased extractability of the compounds and not true increases, because compound recovery could not be adequately tested. Thus, it is difficult to ascertain in this context whether increases in carotenoids were in fact directly due to the cooking process.

Aside from the effects of processing on carotenoid content, processing may potentially be leveraged to increase the bioaccessibility or bioavailability of carotenoids in algae for human consumption. One study that used microfluidization to dramatically decrease particle size of Chlorella sp. from ~2,463 nm to 361 nm in diameter found significant increases in in vitro bioaccessibility of zeaxanthin and β-carotene compared to fresh samples (Cha et al. 2012). Additionally, chemical structure of carotenoids is known to potentially influence bioaccessibility and bioavailability, but specific isomer structure is not always investigated in bioavailability studies. Although not studied specifically for algae, other carotenoid-rich foods have been shown to have differences in bioavailability depending on carotenoid isomer form. Indeed, cis-lycopene is more bioavailable compared to all-trans-lycopene in tomato products (Unlu et al. 2007), and the 3S,3’S-astaxanthin isomer appears to exhibit greater bioavailability compared its other isomers (Rüfer et al. 2008). Because thermal processing can drive isomerization of these compounds (Unlu et al. 2007), further research on how processing affects the carotenoids in algae should be pursued.

Chlorophyll and other pigment compounds

Research on pigments such as chlorophyll has been the topic of ongoing work not only due to the bioactive nature of these compounds, but also because degradation of these pigments can result in color changes that may be viewed as less appealing to the consumer. In one study, nori (Porphyra umbilicales), kombu (Laminaria ochroleuca) and sea lettuce (Ulva sp.) were thermally processed by microwave cooking for 15 min (800 W) or boiling in water for 20 min (Chen and Roca 2018). These samples were then analyzed for chlorophylls, chlorophyll degradation products, and pheophytins, which are compounds that can form via heat-catalyzed transformation. Both cooking methods resulted in up to ~35% loss of total chlorophyll pigments, with the microwaved algae generally having greater retention compared to boiling. Although a large percentage (~70-80%) of chlorophyll loss from boiling could be attributed to increases in degradation and conversion products, amounts that could not be accounted for may be due to these compounds portioning into the cooking water. However, due to the authors not reporting analysis of the cooking water, it is difficult to definitely conclude if release of these pigments into the water was the underlying reason for the inability to achieve mass balance.

In another study, processing Spirulina using oven drying/cross-flow drying at 60°C or spray drying at 150°C resulted in a ~50% decrease of phycocyanin under both conditions (Sarada, Pillai, and Ravishankar 1999). Follow-up experiments on isolated phycocyanin found that the pigment began to degrade at temperatures above 30°C, which is consistent with the author’s data on pigment stability in the algae matrix. Another study investigated the effects of convective hot air drying on the pigments phycoerythrin and phycocyanin from red algae (Gracillaria chilensis) (Tello-Ireland et al. 2011). The results suggest that there may be an optimal drying temperature resulting in maximum pigment retention because pigment retention exhibited a non-linear relationship with temperature, with the peak value at 50°C containing ~30-50% higher phycobiliproteins compared to fresh samples. However, it is unclear whether this increase was due to pigment conversion or other factors such as improved extraction.

Because potential for the use of novel technologies to process algae products has been increasing, some studies have considered its impact on important pigment compounds. In one instance, Spirulina powder subjected to processing by cold atmospheric pressure plasma to inactivate pathogens had up to 60% reduction in chlorophyll a (Beyrer et al. 2020). Results such as these indicate the importance of novel technologies to process algae, but more direct comparisons of novel and legacy methods should be more directly compared in order to help inform the value of these technologies on retention of pigment compounds while reducing pathogenic organisms.

Although there are few studies on the topic, the type of processing may differentially impact the bioavailability of chlorophyll compounds from algae. In one study, authors Chen and Roca (2019) used an in vitro model to show that total chlorophylls from nori, kombu, and sea lettuce exhibited increased bioaccessibility in microwaved compared to boiled algae. Because thermal processing has been demonstrated to alter bioaccessibility of chlorophylls (Ferruzzi, Failla, and Schwartz 2001), it is critical to fully assess the impact of processing on these compounds in algae and to determine the mechanisms driving these observed phenomena.

Phenolic Compounds

Phenolic compounds are a class of phytochemicals with one or more phenolic functional groups, and numerous studies have associated consumption of these compounds with various markers of health status in humans (Redan et al. 2016). Because characterization of individual phenolic compounds in algae is ongoing, studies on how processing affects phenolic compounds in algae have generally used non-specific assays that determine total rather than individual concentrations of these compounds (Charles, Sridhar, and Alamsjah 2020, Badmus, Taggart, and Boyd 2019, Ling et al. 2015). The Folin-Ciocalteu method and other nonspecific assays are commonly used to estimate total phenolic compounds in foods and extracts, but they do not provide the selectivity and specificity needed to differentiate phenolic compounds of different classes (Ho et al. 2018). Total phenolic compounds in fresh algae determined using Folin-Ciocalteu’s reagent has ranged from a low of less than 1 mg gallic acid equivalents (GAE) per 100 g dulse up to 230 mg/100 g GAE for algae in genus Himanthalia (Ferraces-Casais et al. 2012, Jacobsen et al. 2019). Some studies have identified phenolic compounds that appear to be unique to algae, such as eckol and phlorotannins, which are both found in brown algae (Tanna and Mishra 2018), and others have tentatively identified phenolic compounds in algae that are also found in terrestrial plants, such as the flavonoids catechin, epicatechin, epigallocatechin, and quercetin glycosides (Santoso, Yoshie, and Suzuki 2004). Many of these phenolic compounds are in vitro antioxidants so they, similar to antioxidant vitamins, are often sensitive to factors such as temperature and oxygen (Oliveira et al. 2011, Malec et al. 2014, Jiménez-Escrig et al. 2001). As such, the influence of drying methods on phenolic compounds and other phytochemicals in algae has been studied by multiple authors (Table 4).

Table 4.

Summary of literature on the effect of processing on total phenolic compounds in algae.^a

Algae	Processing	Approximate retention after processingb	Reference
Fucus	Air dried at 50°C	2%	Jimenez-Escrig et al. 2001
Fucus	Air dried at 25–60°C	60–70%	Silva et al. 2019
Fucus spp.	Freeze dried (control), oven dried at 40–60°C, or microwaved dried at 385–700W	5–50%	Badmus, Taggart and Kenneth G. Boyd 2019
Gracilaria	Air dried at 25–60°C	No change	Silva et al. 2019
Halidrys	Freeze dried (control), oven dried at 40–60°C, or microwaved dried at 385–700W	Oven dried (40–50%); microwave cooking (no change)	Badmus, Taggart and Kenneth G. Boyd 2019
Himanthalia elongate	Autoclaved at 85–121°C	130–160% at 85–95°C; 40–100% at 100–121°C	Rajauria et al. 2010
Himanthalia elongata	Boiled, steamed, or microwaved at 450–900W	Boiling (15%); steaming (70%) microwave cooking (115–130%)	Cox, Abu-Ghannam, and Gupta 2012
Himanthalia elongata	Oven dried at 25–40°C	50–70%	Gupta, Cox, Abu-Ghannam 2011
Kappaphycus alvarezii (elkhorn sea moss)	Freeze dried (control), solar dried, oven dried at 60°C, or vacuum dried at 60°C	solar dried (90%); oven dried (120%); vacuum dried (130%)	Neoh, Matanjun, and Lee 2016
Laminaria spp.	Autoclaved at 85–121°C	25–100% at 100–121°C; 140–190% at 85–95°C	Rajauria et al. 2010
Laminaria (kombu)	Dried at 45°C, then boiled	120%	Amorim, Lage-Yusty, and López-Hernández 2012
Laminaria (kombu)	Freeze dried (control), oven dried 40-60°C, or microwaved dried at 385–700W	No change	Badmus, Taggart and Kenneth G. Boyd 2019
Pelvetia (brown algae)	Freeze dried (control), oven dried 40-60°C, or microwaved dried at 385–700W	5–10%; no change for oven dried at 40°C	Badmus, Taggart and Kenneth G. Boyd 2019
Pyropia	Oven dried at 50°C	70%	Jimenez-Escrig et al. 2001
Pyropia orbicularis	Vacuum dried at 40–80°C	90–110%	Uribe et al. 2018
Spirulina	Oven dried at 40°C	25%	Agustini et al. 2015
Spirulina	Cold atmospheric pressure plasma, 9–14mW/cm2	90–200%	Beyrer et al. 2020
Ulva (sea lettuce)	Air dried at 25–60° C	No change	Silva et al. 2019
Ulva (sea lettuce)	Freeze dried (control), hot air dried at 70°C, solar dried, or vacuum dried at 70°C	Hot air dried (70%); solar dried (110%), vacuum dried (no change)	Uribe et al. 2019
Undaria (wakame)	Air dried at 45°C, then boiled	65%	Amorim, Lage-Yusty, and López-Hernández 2012

^aTotal phenolic compounds were determined using Folin-Ciocalteu’s reagent.

^bRetention was estimated by calculating [compound concentration after processing]/[compound concentration before processing]*100%. Values greater than 100% may indicate enhanced extractability from a modified food matrix due to processing.

In a study by Rajauria et al. (2010), the brown seaweeds Laminaria spp. and Himanthalia elongate were subjected to thermal processing and then analyzed for retention of phenolic compounds. After seaweed samples were autoclaved in a water bath at temperatures ranging from 85-121°C, the authors found that—similar to pigment retention in algae—levels of total phenolic compounds exhibited a parabolic relationship with temperature, with an optimum at 95°C. In a study on brown algae (Himanthalia elongata), Gupta et al. found that total phenolic compounds decreased by approximately 30-50% when algae samples were dried at temperatures ranging from 25-40°C for 24 h (Gupta, Cox, and Abu-Ghannam 2011). In contrast, another author reported no significant differences in total phenolic compounds when green or red algae were hot air dried at temperatures ranging from 25-60°C (Silva et al. 2019). Novel technologies such as cold atmospheric pressure plasma have been explored as a processing method to reduce pathogens while increasing retention of phenolic compounds. In one study, the authors found no reduction in phenolic compounds in processed Spirulina powder and actually found increases relative to control in the algae treated at 10-14mW/cm² (Beyrer et al. 2020). The reasons for the increase in total phenolic compounds are unclear, but the authors hypothesize that the processing may have resulted in increased extraction efficacy of these compounds.

López-Hortas et al. (2018, 2019) in two different studies evaluated how microwave drying affects levels of phenolic compounds in brown algae (Laminaria ochroleuca and Undaria pinnatifida). Again, the authors found that there was an optimum level of energy application that resulted in greatest retention of phenolic compounds, with the optimum energy application at 300-500W under the experimental range of 50-800W. In a study that tested the effect of thermal processing on phenolic compounds in brown algae (Himanthalia elongata), phenolic compounds were determined in samples after boiling, steaming, or microwave cooking (Cox, Abu-Ghannam, and Gupta 2012). Microwave cooking resulted in a slight increase in total phenolic compounds, in contrast to steaming and boiling, which resulted in a decrease of ~30% and >70%, respectively. It is unknown whether the boiling treatment degraded the phenolic compounds because the cooking water was not analyzed to determine mass balance of these compounds.

Red algae from Malaysia were subjected to different drying treatments where samples were either freeze dried, oven dried, sun dried, or vacuum dried and then analyzed for total phenolic compounds (Neoh, Matanjun, and Lee 2016). Retention of total phenolic compounds were highest in vacuum-dried samples and lowest in samples that were sun dried. In another study on red algae (Pyropia orbicularis), changes in phenolic compounds with vacuum drying red seaweed were documented (Uribe et al. 2018). Similar to other studies, the results of this study indicated that total phenolic compounds increased slightly (~10% compared to control) at the experimental temperatures of 40-80°C. In a study involving Spirulina, the authors determined that total phenolic compounds decreased by ~75% after drying sample at 40°C for 10 h (Agustini et al. 2015).

Limited data suggest that in-home processing can affect the levels of phenolic compounds in algae. In one study, phenolic compounds decreased in wakame (Undaria pinnatifida) but not in kombu (Laminaria sp.) after being cooked in boiling water (Amorim, Lage-Yusty, and López-Hernández 2012). These results are generally in agreement with other studies finding that boiling and blanching can drive loss of phenolic compounds and nutrients in plant materials (Redan, Vinson, and Coco 2013). Although not specifically tested in these studies on algae, research on other plant materials has demonstrated that loss of phenolic compounds during boiling can largely be attributed to these components partitioning to the water fraction (Wachtel-Galor, Wong, and Benzie 2008).

Processing temperatures (and times) should be optimized to ensure retention of phenolic compounds from algae. Generally, thermal processing may allow for enhanced release (i.e., enhanced extractability) of phenolic compounds up to a point, but excessive thermal processing can lead to degradation. However, there is some difficulty in determining the factors that are driving the observed parabolic relationship between certain thermal treatments and levels of phenolic compounds in algae. One explanation is that thermal treatment is able to denature endogenous enzymes that oxidize phenolic compounds, such as polyphenol oxidase and peroxidases, resulting in higher retention of these compounds at temperatures where these enzymes are denatured (Ludikhuyze et al. 2003). Use of blanching and other heat treatments to deactivate such enzymes has been well-characterized in many other foods, and such treatments for use on algae are likely to have similar outcomes (Rawson et al. 2011, Shinwari and Rao 2018a). Another possibility is that drying the freshly harvested material induces an adaptive stress response by the plant, which in turn increases levels of phenolic compounds. Alternatively, it is also likely that the observed increases may be due to release of free reducing sugars during the thermal treatment, which can then act as analytical interferences to inflate the values of such nonspecific assays. Follow-up analysis of individual compounds and additional mechanistic experiments are needed in further determining the effect of thermal processing on such compounds in the algae matrix.

It is important to note that many of the aforementioned studies only performed analysis of the compounds in the material and did not consider the in vivo bioavailability of these components. The bioavailability and downstream potential biological effects of these phytochemicals are important because some compounds derived from algae have been reported to have low oral bioavailability, which could ultimately affect potential bioactivity (Asai, Yonekura, and Nagao 2008). Additionally, the process of digestion is critical to fully understanding bioavailability of these compounds because the pH environment may affect compound stability of these phytochemicals (Guo et al. 2019). Further, some research has indicated that high-molecular weight molecules in algae such as phlorotannins can be catabolized by gut microbiota to yield compounds with increased bioavailability (Corona et al. 2017).

Effect of thermal processing on concentrations of elemental and trace metal components in algae

Minerals and trace metals

Algae can be a significant source of nutritionally relevant elements, including macro- and trace minerals. Due to the high amounts of the trace mineral I in several types of algae, there are multiple studies that have determined how processing affects concentrations of I and other elements in algae (Table 5). In one study, the authors found that levels of I in kelp decreased by ~90% after being boiled for 20 min (Chung et al. 2013). Subsequent analysis of the cooking water showed that virtually all I lost from the kelp had been released into the water. Furthermore, a systematic study determined how different steps of postharvest processing affects I concentrations from the three main classes of algae (red, green, and brown) (Nitschke and Stengel 2016). The authors performed analysis for I after freshly harvesting the material, washing, drying over 72 h, rehydrating over 24 h, and then finally boiling for 20 min. The results revealed that I concentrations were minimally affected after washing and drying, but that rehydration and cooking reduced I concentration by up to 75%. In a study focusing on the trace minerals Cu, Fe, Se, and Zn, the authors determined how boiling affected the concentrations of nutritional elements in different types of algae (García-Sartal et al. 2013). In this study, the authors found that cooking kombu, wakame, nori, and sea lettuce in boiling water for up to 60 min decreased Cu, Fe, Zn, and Se levels by amounts ranging from 50-90%, 20-80%, 0-35%, and 20-60%, respectively. Combined, these results show a clear trend across studies that indicate processing algae by soaking and boiling results in loss of nutritionally relevant minerals.

Table 5.

Summary of literature on the effect of processing on minerals and trace elements in algae.^a

Element	Algae	Processing	Approximate retention after processingb	Analytical Method	Reference
Arsenic, inorganic	Hizikia fusiforme (hijiki)	Soaked in water, then boiled	10%	LC-ICP-MS	Ichikawa et al. 2006
Arsenic, total	Porphyra (nori)	Boiled	No change	ICP-MS	Cheyns, Waegeneers, Wiele, and Ruttens 2017
Arsenic, inorganic	Hizikia fusiforme (hijiki)	Soaked in water, then boiled	60%	LC-ICP-MS	Cheyns, Waegeneers, Wiele, and Ruttens 2017
Arsenic, inorganic	Hizikia fusiforme (hijiki)	Soaked water or NaCl solution (0–2%), then boiled	20%	LC-ICP-MS	Park et al. 2019
Copper	Laminaria (kombu)	Boiled	80%	ICP-MS	García-Sartal et al. 2013
Copper	Undaria (wakame)	Boiled	20%	ICP-MS	García-Sartal et al. 2013
Copper	Porphyra (nori)	Boiled	40%	ICP-MS	García-Sartal et al. 2013
Copper	Ulva (sea lettuce)	Boiled	50%	ICP-MS	García-Sartal et al. 2013
Iodine	Laminaria (kelp)	Boiled	10%	ICP-MS	Chung et al. 2013
Iodine	A. esculenta	Dehydrated, rehydrated, then boiled	75%	LC-DAD	Nitschke and Stengel 2016
Iodine	P. palmata	Dehydrated, rehydrated, then boiled	30%	LC-DAD	Nitschke and Stengel 2016
Iodine	U. intestinalis	Dehydrated, rehydrated, then boiled	10%	LC-DAD	Nitschke and Stengel 2016
Iron	Porphyra (nori)	Dried, then toasted	120%	GF-AAS	Masuda, Yamamoto, and Toyohara 2015
Iron	Laminaria (kombu)	Boiled	70%	ICP-MS	García-Sartal et al. 2013
Iron	Undaria (wakame)	Boiled	90%	ICP-MS	García-Sartal et al. 2013
Iron	Porphyra (nori)	Boiled	70%	ICP-MS	García-Sartal et al. 2013
Iron	Ulva (sea lettuce)	Boiled	50%	ICP-MS	García-Sartal et al. 2013
Selenium	Laminaria (kombu)	Boiled	50%	ICP-MS	García-Sartal et al. 2013
Selenium	Undaria (wakame)	Boiled	80%	ICP-MS	García-Sartal et al. 2013
Selenium	Porphyra (nori)	Boiled	50%	ICP-MS	García-Sartal et al. 2013
Selenium	Ulva (sea lettuce)	Boiled	30%	ICP-MS	García-Sartal et al. 2013
Zinc	Laminaria (kombu)	Boiled	110%	ICP-MS	García-Sartal et al. 2013
Zinc	Undaria (wakame)	Boiled	70%	ICP-MS	García-Sartal et al. 2013
Zinc	Porphyra (nori)	Boiled	No change	ICP-MS	García-Sartal et al. 2013
Zinc	Ulva (sea lettuce)	Boiled	60%	ICP-MS	García-Sartal et al. 2013

^aaAbbreviations used: DAD, diode array detector; GF-AAS, graphite furnace-atomic absorption spectroscopy; iAs, inorganic arsenic; ICP-MS, inductively coupled plasma-mass spectrometry; LC, liquid chromatography

^bRetention was estimated by calculating [element concentration after processing]/[element concentration before processing]*100%. Values greater than 100% may indicate enhanced extractability from a modified food matrix due to processing.

Heavy metals

Several metal contaminants have been reported to occur in algae at varying levels, including the toxic heavy metals As, Cd, Pb, and Hg, with As receiving much of the research attention (Luvonga et al. 2020, Almela et al. 2002). The element As naturally occurs as both organic and inorganic species (iAs), with exposure to the inorganic forms (As^III and As^V) having the strongest association with toxic endpoints and chronic disease, including different types of cancer (CONTAM 2009). The As species in various types of algae have been characterized and has shown that As generally occurs in these foods as the organic forms of arsenosugars and methylated species (Taylor and Jackson 2016, Li et al. 2017). Organic forms of As have been researched in several animal and human clinical studies, and they have been found to be rapidly excreted, with low potential for toxicity (Taylor and Jackson 2016, Taylor, Goodale, et al. 2017, Taylor, Li, et al. 2017). Due to the different levels of toxicity associated with inorganic versus organic forms, it is critical that analytical methods used in surveys of As in algae products differentiate between chemical As species. Accordingly, governmental agencies such as the US Food and Drug Administration (FDA) have ongoing work on the development and evaluation of methods used for speciation of As in seaweed and seafood products (Wolle and Conklin 2018, Redan and Jackson 2020).

An analysis of wakame, nori, and kombu found that they all contained non-detectable levels of iAs, but concentrations of arsenosugars ranged from 18-46 mg/kg. In contrast, hijiki can be a concern from the viewpoint of food safety because it has been reported to contain levels as high as 120 mg/kg iAs (~120 ppm) (Food Standards Australia New Zealand 2016). In addition, in vitro bioaccessibility of iAs from hijiki has been found to be relatively high, reaching approximately 80% (Brandon, Janssen, and de Wit-Bos 2014). To place these values in perspective, Food Standards Australia New Zealand (FSANZ) set a maximum limit of 1 mg/kg iAs for seaweed, which aligns with the Food Chemicals Codex (FCC) recommended limit of 1 mg/kg total As for kelp used as a food ingredient (FCC 2016, FSANZ 2016). The FCC indicates that the purpose for this limit is related to use of kelp as an I source in dietary supplements, but this limit may not have been intended for algae consumed in larger amounts. Although there are currently no other regulatory limits specifically related to algae products intended for human consumption, it is interesting to note Health Canada’s limit of 0.1 mg/kg total As for ready-to-drink beverages and the FDA proposed limit of 0.1 mg/kg and 0.01 mg/kg iAs for rice and apple juice, respectively (Health Canada 2017, FDA 2018). Because levels of iAs in hijiki have at times exceeded the FCC’s recommended limit, multiple health communication warnings by governmental bodies have advised caution when consuming this algae (FSANZ 2016, Canadian Food Inspection Agency 2019).

In addition to the direct analysis of heavy metals in algae, it is important to consider how food processing can affect levels of these elements in algae. Several studies have demonstrated that iAs can be decreased in foods after processing, including use of typical in-home methods. For instance, a study performed in Japan that tested the effect of soaking and cooking hijiki on levels of As species found that levels of total arsenic were reduced by ~90% after soaking and subsequent boiling for 20 min (Ichikawa et al. 2006). Another study tested how cooking nori and hijiki by soaking and boiling affected As levels (Cheyns et al. 2017). The authors found that cooking nori reduced levels of iAs by only 6-24%—although iAs in nori was already low (<0.15 mg/kg)—but cooking hijiki reduced iAs by 70%. In another study on hijiki, a 50% reduction in iAs was observed after boiling, but ~80% was reduced after the seaweed had first been soaked in a 2% NaCl solution and then afterwards boiled (Park et al. 2019). The addition of NaCl to the soaking water may promote solubilization of iAs, which is consistent with other research demonstrating that chloride ions can solubilize heavy metals (Abt and Robin 2020). Due to several other studies indicating that reduction of iAs in other foodstuffs can be obtained through rinsing/washing and boiling, this effect appears to be a robust phenomenon (Gray et al. 2016, Redan et al. 2019, Redan 2020). Together, these results may help in producing a product with As concentrations more likely to be within compendial standards or potential regulatory limits.

Although research has suggested that levels of As can be reduced after cooking, these processes may also be able to drive conversion of organic forms of As to iAs species, according to preliminary studies. Conversion of organic arsenic to iAs has thus far been reported to occur in shellfish under certain conditions, including boiling (Liao et al. 2018). These experiments suggest that it is important to more thoroughly characterize any conversion of As species in algae and other seafood to provide strategies for prevention of species conversion.

Aside from As, there are some studies that have investigated the effect of processing on in vitro bioaccessibility of metals from algae. In a study that examined in vitro bioaccessibility, a 3-phase model of digestion found that kelp cooked in a microwave at 900W exhibited no difference in Cd bioaccessibility compared to an unprocessed control (Wang, Duan, and Teng 2014). In contrast, a study that tested the effect of cooking kombu by boiling found that in vitro bioaccessibility of rare earth elements significantly increased from approximately 30% before cooking to 80% after cooking (Liu et al. 2017). Thus, as with other types of foods, processing may promote release of metals from the food matrix during digestion, but these results will need to be followed up with in vivo studies to confirm whether these results translate to animals and humans.

Summary & Conclusion

Edible algae contain a considerable amount of various phytochemicals and nutritional compounds, such as important minerals and water- and fat-soluble vitamins. Although limited amounts of algae are consumed in its fresh, unprocessed state, the vast majority is typically subjected to multiple stages of processing, such as drying and other forms of thermal treatments before being made available to the consumer. There have also more recently been efforts to pursue use of technologies such as HPP and cold plasma to process algae. The research presented in this review indicate that each of these processing stages can significantly impact levels of key nutritional constituents, phytochemicals, and metal contaminants, and have particular aspects that can provide certain advantages or limitations depending on the desired outcome of processing (summarized in Figure 4). As such, ongoing algae research should further explore how processing affects not only important phytochemicals and nutrients in these products, but also potential contaminants. Additionally, efforts to further characterize and identify phenolic compounds in algae will be crucial to better assess how processing affects concentrations of these phytochemicals. Because the demand for algae-based foods is projected to increase rapidly in the future, it is critical that research efforts continue to focus on the major chemical constituents in algae by characterizing how post-harvest processing affects both the retention of important nutritional compounds and reduction of potential contaminants.

Figure 4.

Major potential effects of dry and wet thermal processing on nutrient, phytochemical, and metal contaminant concentrations in algae. (A) Dry heat can induce degradation of ascorbic acid (vitamin C), carotenoids, and chlorophyll pigments. Heat can increase phenolic compound retention via denaturation of polyphenol oxidase. (B) Cooking in boiling water reduces water-soluble compounds including ascorbic acid, phenolic compounds, certain chlorophyll/pigment compounds, and trace metals (both nutrients and contaminants). These decreases may be due to migration into the water phase. Addition of sodium chloride (NaCl) to cooking water may increase inorganic arsenic (iAs) release. Heat may convert arsenosugars (As-Sugars) to iAs, although this has not yet been definitively shown. Abbreviations used: As-Sugars, arsenosugars; iAs, inorganic arsenic; PPO, polyphenol oxidase; ox-phenolics, oxidized phenolic compounds.

There are still many gaps in this area of literature that leave room open for further research. One area in particular is related to characterization of individual phenolic compounds and pigments in algae and how processing affects these components. Much of the research in this review has focused on studies that utilized nonspecific assays or methodologies that may be affected by analytical interferences. Studies designed to use analytical instrumentation that can quantitate and characterize individual compounds (e.g.,, HPLC or mass spectrometry-based detection) is needed to move this field forward. We also have noted that a limitation of the literature is that it has only largely considered the effect of thermal processing on the concentrations of phytochemical components in algae, but not how processing ultimately affects the bioavailability of these compounds. Because thermal processing has repeatedly been shown to affect bioavailability of nutritional and phytochemical constituents in other food matrixes, it is expected that future research may find that bioavailability of these compounds may also be altered in a processed algae matrix. Although further research is needed on thermally processed algae products, the existing data should be considered to inform consumers and to optimize processing to increase retention of nutritional components while also limiting contaminants. Taken together, these developments should make algae products well-positioned to constitute an ever-larger part of dietary consumption.