Nutritional composition and consumer acceptance of tomato paste fortified with palm weevil larvae (Rhynchophorus phoenicis Fabricius) in the Ashanti region, Ghana

Abstract Edible insects, such as palm weevil larvae, have been promoted as an alternative source of nutrients in developing countries for their nutritional benefits, cost‐effective rearing, and yearly availability. Unfortunately, consumer acceptance remains a barrier to their utilization. A supplemental palm weevil larvae and tomato paste were developed as part of efforts to understand whether incorporating edible insects into staple foods could help overcome this barrier. Palm weevil larvae flour and tomato paste were mixed in three formulations that had 8, 15, and 30% of palm weevil larvae flour. Samples were subjected to proximate and mineral content analyses and sensory evaluation. Among the blends, tomato paste containing 30% palm weevil larvae had the highest protein, fat, and total solids content as compared to unfortified tomato paste. Iron and zinc levels also increased with increasing levels of palm weevil larvae flour. Carbohydrate and crude fiber concentrations of the samples, however, decreased with increasing fortification levels. The overall acceptance and willingness to purchase fortified tomato paste as determined by sensory evaluation was high for all samples and increased with increasing knowledge about palm weevil larvae's nutritional benefits. Overall acceptance and willingness to purchase fortified tomato paste were significantly dependent on the samples' color and consumers' overall liking of the products. Tomato paste fortified with palm weevil larvae can provide a complementary source of iron for Ghanaians.

Various strategies have been promoted as effective ways of reducing iron deficiency anemia at population level including food fortification and iron supplementation. In Ghana, however, their implementation has not proven successful due to inadequate and inconsistent fortification across the country, inequitable distribution of supplements, and/or low adherence to supplementation (Appiah et al., 2020;Nasir et al., 2020;Osendarp et al., 2018). To overcome such challenges, food-to-food fortification is suggested as a complementary strategy that utilizes locally found underutilized animal-or plant-based micronutrient-rich sources to fortify nutritious, affordable, locally available, accessible, and acceptable food vehicles, commonly consumed by the population (Chadare et al., 2019). Evidence on the effectiveness of food-to-food fortification has been reported in the literature, particularly for increasing iron content and bioavailability (Kruger et al., 2020). A recent review assessed the impact of fortifying starchy staple foods with vegetables, fruits, and animal products at levels varying between 10% and 50% on the iron content and in vitro iron bioavailability (Kruger et al., 2020). Results from this review indicated an average increase of 50% in the fortified foods' iron content, as well as a significant increase in the iron's in vitro bioavailability (Kruger et al., 2020). Of all the studies assessed, one was of particular interest to this research as it evaluated the impact of adding mopane worms to fermented cereals for their iron content and bioavailability (Gabaza et al., 2018). Results from this study indicated a significant increase in most of the selected cereals' iron content but no significant change in their iron bioavailability.
Edible insects are considered important food sources to improve the iron status of resource-limited populations owing to their nutritional value and cost-effective farming. Edible insects are rich sources of complete animal protein and contain essential vitamins and minerals (such as iron and zinc) in quantities comparable to those of beef. Edible insects' nutritional value varies with insect's diet, sex, species, growth environment, and developmental stage (van Huis, 2021). Edible insects' protein content ranges from 35% to 60% (dry weight), their iron content ranges from 4 to 62 mg per 100 g of dry matter, and their zinc content ranges from 9 to 27 mg per 100 g of dry matter (Gorbunova & Zakharov, 2021;Latunde-Dada et al., 2016;Mwangi et al., 2018). Insect consumption, or entomophagy, is practiced by over 2 billion people in 113 countries in Africa, Asia, and Latin America (van Huis, 2021). In Ghana, the most commonly consumed insects are termites, shea tree caterpillars, grasshoppers, locusts, field crickets, and palm weevil larvae (Rhynchophorus phoenicis Fabricius) (Anankware et al., 2016). Palm weevil larvae, locally called akokono, are available all year long in palm-growing communities, and are particularly abundant during the rainy season from May to October (Anankware et al., 2016).
Despite the numerous benefits of edible insects, consumer acceptance remains a barrier to their utilization due to the disgust factor associated with their consumption (Imathiu, 2020). As such, to overcome this obstacle, incorporating edible insects into staple foods could promote their utilization as a food source and help reduce micronutrient deficiencies and malnutrition. For a successful fortification, the selection of the appropriate food vehicle, fortificant, and level of fortification is crucial. According to the Food and Agriculture Organization and the World Health Organization (Allen, De Benoist, Dary, Hurrell, & Organization, 2006;Chadare et al., 2019), the food vehicle should be consumed frequently and in adequate quantities by the majority of the population, accessible financially and physically, and centrally processed. As for the fortificants, underutilized plant or animal species that are nutrient-rich and require little agricultural inputs are preferred. Finally, the fortification level should vary between 1% and 50% in such a way that the fortificant enhances the nutritional quality of the food vehicle without compromising its organoleptic properties or its acceptability by consumers.
Tomato paste was considered a potential food vehicle to be fortified with palm weevil larvae. Fresh and canned tomatoes (such as tomato paste) are a staple food in Ghanaians' diets and are widely consumed in Ghana (Ministry of Food and Agriculture (MoFA), 2020).
According to a study conducted by Aggey et al. (2007), tomato paste is used by at least 7 in 10 Ghanaian households in preparing their meals during lean tomato season. Tomato paste constitutes the base of several Ghanaian stews and dishes. Tomatoes and its derivatives are generally good sources of essential nutrients, although low in iron (Sainju et al., 2003), and appear to have low levels of antinutrients including phytates, glycosides, saponins, and tannins (Oyetayo & Ibitoye, 2012).
To evaluate the feasibility, effectiveness, and sustainability of this strategy, it is necessary to assess consumers' acceptability of the developed product and evaluate the nutritional changes imparted by the addition of akokono flour. To the best of our knowledge, no study has looked at consumer acceptance of palm weevil larvaebased tomato paste. Thus, the objective of this study was to explore Ghanaian consumers' acceptance of varying fortification levels of palm weevil larvae-tomato paste and to investigate the main determinants for their willingness to pay (WTP) for the products.

| MATERIAL S AND ME THODS
Using the Association of Official Analytical Chemists (AOAC) methods (Association of Official Analytical Chemists, 1995), we examined the nutritional composition of akokono-based tomato paste.
A sample of 88 untrained panelists consisting of community men and women conducted a sensory evaluation of three tomato paste samples with varying concentrations of akokono flour. Finally, these participants evaluated their acceptance and willingness to purchase the tested samples.

| Raw materials
Samples of tomato paste with varying palm weevil larvae compositions were prepared. Full-fat palm weevil larvae flour was provided by Legendary Foods' farm site in Kumasi, Ghana. All the other ingredients including the tomato paste were purchased from a local market in Kumasi, Ghana. The sensory evaluation was carried out in selected communities in Kumasi Ghana, while the analyses were performed in laboratories of the Department of Food Science at McGill University, Canada. All reagents used for the proximate and mineral analyses were obtained from Sigma Aldrich Co. (USA).

| Preparation of palm weevil larvae-fortified tomato paste
The palm weevil larvae-fortified tomato paste was prepared by mixing 100 g of tomato paste with varying weights of akokono flour (8, 15, and 30 g) and heating it for 5 to 10 minutes at 70 °C until the appropriate texture was reached.

| Proximate analysis
The proximate analysis was carried out according to AOAC (Association of Official Analytical Chemists, 1995) and done in triplicate.

| Determination of moisture content
Moisture content of the tomato paste was determined according to the official methods of analysis (AOAC 927.05) (Association of Official Analytical Chemists, 1995). Samples were weighed and placed into dried and weighed moisture dishes before being dried in a vacuum oven at 70 °C overnight, after which the dishes were placed in a desiccator to cool to room temperature and until a constant weight was obtained. The moisture content was expressed as a percentage of the average weight loss after drying the samples based on the following formula: W2 − W3 W2 − W1 * 100 where W1 is the weight of the dish, W2 is the weight of the dish and the initial wet sample, and W3 is the weight of the dish with the dried sample.

| Determination of ash content
Ash is defined as the inorganic residue left after the food's organic residue has been burnt. Ash content was determined the according to the official methods of analysis (AOAC 942.05) (Association of Official Analytical Chemists, 1995). Akokono-based tomato paste samples were weighed (1 g each) and transferred into dry and weighed crucibles. Samples were incinerated for 2 h at 550°C in a muffle furnace. Samples were then allowed to cool to room temperature before being placed in a desiccator and weighed afterward.

| Mineral analysis
Mineral analysis was carried out in order to determine the content of iron and zinc using inductively coupled plasma mass spectrometry (ICP-MS) (Jajda et al., 2015). Samples of 0.5 g each were weighed into 50-mL pre-cleaned Falcon tubes to which were added 6 mL of trace-metal-grade nitric acid. The samples were heated in a water bath at 90°C for 2 hours and then allowed to cool at room temperature. Hydrogen peroxide (3 mL) was added to these samples which were then heated in a water bath at 90°C for an additional hour until particulates were not visible. Solutions were diluted to 2% nitric acid and analyzed using ICP-MS. All mineral analyses were performed in duplicate.

| Sensory evaluation of tomato paste (hedonic tasting)
A consumer acceptability study was conducted among 88 participants (panelists) from five selected communities in Kumasi for all three tomato paste formulations. Each panelist evaluated a sample set of three random samples which were each assigned a three-digit blinding code. Kilcast's recommendations for sample presentation were respected (Kilcast, 2010). Saltine crackers were used as palate cleansers. Panelists were asked to rate the samples on the following parameters: color, taste, texture and consistency, mouthfeel, and overall liking using a 5-point Likert scale. Panelists were also questioned about their overall acceptance of the products and their willingness to purchase them. They were then briefed on the nutritional benefits of palm weevil larvae after which they were asked to answer the previous questions again. All participants were informed about the allergenic potential of insects and the ones with a known shellfish allergy were denied participation. Participants were informed that their participation was voluntary and were asked to sign a consent form.

| Statistical analyses
Sensory evaluation data were analyzed using frequencies and pro-

| Determination of nutrient composition
The nutrient composition of the tomato paste enriched with akokono is presented in Table 2 (dry basis), Table 3 (wet basis), and mg per 100 g of tomato paste (wet basis) with increasing concentrations of akokono flour. As for akokono flour, it had a low moisture content (5.92%), high protein (23.9 g per 100 g wet basis) and fat (54.1 g per 100 g wet basis) contents, moderate carbohydrate (11.8 g per 100 g wet basis) and fiber (5.36 g per 100 g wet basis) contents, and good iron (3.74 mg per 100 g wet basis) and zinc contents (12.1 mg per 100 g wet basis).
The estimated amount of nutrients that would be consumed on a daily basis assuming a consumption of 200 g of tomato paste per day was presented in ing this sensory evaluation, while 31.6% indicated being occasional consumers (less than once a month). Consuming akokono, however, was more popular than purchasing it as 31% of participants engaged in the former while 5% engaged in the latter, as seen in Figure 1.
This implies that akokono is either being offered as a delicacy or is self-harvested.

| Likert scale scores for overall liking and sensory attributes
The median Likert scale rating for all samples was 2, or "Like," indicating that participants generally liked all samples. As seen in  Table 7).

| Statistical interpretation of tomato paste fortified with akokono formulations
For the multivariate analysis of variance (MANOVA), Wilks lambda's F-value greater than 1 and p-value less than 0.05 indicate that all formulations were perceived by the panelists as different (as seen in Table 6). In addition, the total-sample standardized canonical coefficient indicates the attribute that is more responsible for the differences. Our results from canonical 1 (

| DISCUSS ION
This study presents the nutritional composition of tomato paste samples fortified with palm weevil larvae (akokono), an edible insect consumed in Ghana, and evaluates Ghanaian community members' acceptance and willingness to purchase the prepared product formulations.

| Nutrient composition of akokono-based tomato paste
The samples' macronutrient composition will be analyzed based on the dry-basis values obtained (
The addition of akokono increased tomato paste's protein content and complemented efficiently its amino acid composition. Our proximate analyses showed that akokono and tomato paste's protein contents (25.5% and 16.8% dry weight basis, respectively) corroborated the values reported in the literature stating that akokono's protein content varied between 19.50% and 69.78% (dry weight basis) (Rumpold & Schlüter, 2013), and tomato paste's protein content ranged between 10.50% and 25.03% (Ali et al., 2021). According to several studies, palm weevil larva contains almost all of the essential amino acids in adequate quantities except for tryptophan (Chinarak et al., 2020;Ekpo & Onigbinde, 2005;Elemo et al., 2011;Womeni et al., 2012). Of particular interest are its high levels of leucine, lysine, and threonine, which are limiting amino acids in grains and cereals. Tomato paste contains on average 2.80 mg of leucine, 2.45 mg of lysine, and 1.37 mg of threonine per 100 g of protein (Ali et al., 2021), which is almost 15 times less than what is found in akokono. Akokono are comprised of 47 to 59 mg of leucine, 42 to 64 mg of lysine, and 29 to 31 mg of threonine per 100 g of protein (Rumpold & Schlüter, 2013).
The dry weight basis fiber content remained relatively stable with the addition of palm weevil larvae. This was expected as both tomato paste and palm weevil larvae have similar fiber contents. Canned tomato paste's fiber content has been reported in the literature as varying between 4.97% and 6.61% (dry weight basis) (Abdullahi et al., 2016) which aligns with the value we found (4.17% ± 0.20), while akokono's fiber content has been reported as varying between 2.58% and 22.9% (dry weight basis) (Rumpold & Schlüter, 2013), which compares to our akokono's fiber results of 5.70% ± 0.007 (dry weight).
As for the iron and zinc contents, their wet-basis values were analyzed as they were more indicative of the amount that would

| Sensory evaluation of samples fortified with akokono flour and factors influencing consumer acceptability and willingness to purchase
Our results showed no typical consumer profile for akokono as participants from different genders, age groups, income levels, and educational attainments were all interested in akokono and expressed willingness to purchase akokono-based products.
The logistic regression analyses showed that the overall acceptance of the tomato paste samples and consumers' willingness to purchase them were significantly dependent on the samples' color and consumers' overall liking of the products (p < 0.05). Our findings corroborate with Smarzyński et al. (2019) and their colleagues who also identified color as a determining factor in consumers' acceptance of a pork pâté fortified with cricket powder (Smarzyński et al., 2019). Visual cues like color are essential determinants of a  -Lopera et al., 2015;Grunert, 1997). As a result, if a product's color is unacceptable, flavor and texture are unlikely to be properly judged. When Keneko and colleagues (2002) evaluated consumer acceptability of color in tomato-processed products, they determined that a peak color acceptance existed for all tomato products, stating that those were undesirable if they were too red or too brown (Claybon & Barringer, 2002). For tomato paste specifically, they found that consumers preferred it to be closer to the "red" end of the spectrum, indicating that consumers wanted a fresher product, rather than a more processed one, which would have been associated with a browner product (Claybon & Barringer, 2002). Taste and texture also motivated women's overall acceptance and willingness to purchase the akokono-based tomato paste, if sold on the market. The sensory evaluation was performed on women, majorly (over 80%), as they are responsible for food purchasing and preparation in the household. When asked to justify their liking and willingness to purchase, women mentioned they were motivated by the fact that the tomato paste's taste and color remained appealing despite adding akokono. Some specified they would only buy akokono if it were added to tomato paste, as they would know how to cook it and could seamlessly incorporate it into theirs and their children's diets. The use of palm weevil larvae in a known and commonly consumed food product such as tomato paste seemed to have increased familiarity with akokono and reduced the taboo associated with entomophagy. Familiarity, which is achieved by integrating insects into already well-known products and combining favorite dishes with insects, has been reported as essential in increasing acceptance of edible insects and decreasing neophobia among consumers (Wendin & Nyberg, 2021).
Most women preferred the tomato paste sample with the second highest concentration of akokono and indicated that they would use it in stews to diversify their diets and make them more nutri-  (Worsley, 2002), including in Ghana (Rose Omari, 2017) and Ethiopia (Melesse & van den Berg, 2021).
A study conducted in Ethiopia highlighted that nutrition knowledge was positively related to healthy attitudes, practices, and diet quality (Melesse & van den Berg, 2021). In Ghana, people were generally aware of iron deficiency anemia and its association with poor eating habits (Awuah et al., 2021;Rose Omari, 2017

| CON CLUS ION
This study found that the addition of palm weevil larvae improved the nutritional composition of tomato paste, specifically in terms of its protein, fat, zinc, and iron contents. In addition, participants preferred the 15% palm weevil larvae-fortified tomato paste sample owing mainly to its color and taste. For food-to-food fortification to be successful, it is important to recognize the importance of a food's sensory aspects and develop food products with familiar tastes and textures. Health and nutrition were additional common motives for participants' acceptance and willingness to purchase palm weevil larvae and its derived products. We found among participants, however, a lack of knowledge and awareness about palm weevil larva's nutritional benefits, cooking and preparation, income generation potential, and access points. This highlights the need for nutrition education to support the consumption of palm weevil larvae-tomato paste as a potential feasible strategy to curtail micronutrient deficiencies, such as iron deficiency anemia.
Based on the results of our study, we consider that further research should: 1) assess the effect of heat on the nutritional composition of palm weevil larvae-fortified tomato paste, 2) examine the microbial quality of palm weevil larvae-fortified tomato paste, and 3) evaluate the impact of daily consumption of palm weevil larvaefortified tomato paste on women's iron status.

CO N FLI C T O F I NTE R E S T S TATE M E NT
The authors declare that they do not have any conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

E TH I C A L S TATEM ENTS
This study was approved by the Institutional Review Board of

McGill University and Kwame Nkrumah University of Science and
Technology.

I N FO R M E D CO N S E NT
Written informed consent was obtained from all study participants.