*Systematic Review* **Edible Insect Consumption for Human and Planetary Health: A Systematic Review**

**Marta Ros-Baró <sup>1</sup> , Patricia Casas-Agustench 1,2,\* , Diana Alícia Díaz-Rizzolo 1,3 , Laura Batlle-Bayer 4, Ferran Adrià-Acosta 5, Alícia Aguilar-Martínez 6,7 , Francesc-Xavier Medina 6,7 , Montserrat Pujolà <sup>8</sup> and Anna Bach-Faig 6,9,\***


**Abstract:** This systematic review aimed to examine the health outcomes and environmental impact of edible insect consumption. Following PRISMA-P guidelines, PubMed, Medline ProQuest, and Cochrane Library databases were searched until February 2021. Twenty-five articles met inclusion criteria: twelve animal and six human studies (randomized, non-randomized, and crossover control trials), and seven studies on sustainability outcomes. In animal studies, a supplement (in powdered form) of 0.5 g/kg of glycosaminoglycans significantly reduced abdominal and epididymal fat weight (5–40% and 5–24%, respectively), blood glucose (10–22%), and total cholesterol levels (9–10%), and a supplement of 5 mg/kg chitin/chitosan reduced body weight (1–4%) and abdominal fat accumulation (4%) *versus* control diets. In other animal studies, doses up to 7–15% of edible insect inclusion level significantly improved the live weight (9–33%), reduced levels of triglycerides (44%), cholesterol (14%), and blood glucose (8%), and increased microbiota diversity (2%) *versus* control diet. In human studies, doses up to 7% of edible insect inclusion level produced a significant improvement in gut health (6%) and reduction in systemic inflammation (2%) *versus* control diets and a significant increase in blood concentrations of essential and branched-chain amino acids and slowing of digestion (40%) *versus* whey treatment. Environmental indicators (land use, water footprint, and greenhouse gas emissions) were 40–60% lower for the feed and food of edible insects than for traditional animal livestock. More research is warranted on the edible insect dose responsible for health effects and on environmental indicators of edible insects for human nutrition. This research demonstrates how edible insects can be an alternative protein source not only to improve human and animal nutrition but also to exert positive effects on planetary health.

**Keywords:** edible insects; health; sustainability; alternative proteins; planetary health; systematic review

#### **1. Introduction**

There is an urgent need to redesign food systems to improve human and planetary health [1]. It is likely that food systems are already operating beyond some planetary boundaries [2–4]. Therefore, more environmentally friendly but also affordable, healthy,

**Citation:** Ros-Baró, M.;

Casas-Agustench, P.; Díaz-Rizzolo, D.A.; Batlle-Bayer, L.; Adrià-Acosta, F.; Aguilar-Martínez, A.; Medina, F.-X.; Pujolà, M.; Bach-Faig, A. Edible Insect Consumption for Human and Planetary Health: A Systematic Review. *Int. J. Environ. Res. Public Health* **2022**, *19*, 11653. https:// doi.org/10.3390/ijerph191811653

Academic Editor: Paul B. Tchounwou

Received: 27 July 2022 Accepted: 14 September 2022 Published: 15 September 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

and safe approaches need to be adopted to feed the expanding human population [5], which is projected to reach 9.7 billion by 2050 [6]. One of the major challenges is to re-align future protein supply and demand, especially animal protein [7], which is expected to rise by 70–80% between 2012 and 2050 [8]. Underutilized plants, insects, and single-cell organisms (e.g., algae, fungi, and bacteria) as well as cultured meat are being considered as novel protein sources to sustainably meet future global requirements [9,10].

Although insects have been consumed since early in human evolution, a new trend in food science began in 2013, when the Food and Agriculture Organization of the United Nations (FAO) pointed out the need to examine modern food science practices to increase the trade, consumption, and acceptance of insects [11]. In regulation 2015/2283 [12] of the European Parliament and the Council of the European Union, whole insects and their parts were included in the category of novel foods. Furthermore, in 2015, the European Food Safety Authority (EFSA) provided a scientific opinion on insect consumption and suggested a list of insect species with high potential use as food for animal feed and human food [13,14]. In 2021, the EFSA issued a positive opinion on the safety of dried yellow mealworm—*Tenebrio mellitus larvae* (*TM larvae*) [13], *Locusta migratoria (LM)* [15], and *Acheta domesticus (AD)* [16]—as a novel food according to European Union regulation 2015/2283 [17]. From a nutritional point of view, edible insects are being proposed as an alternative source of protein for humans and animals [18] due to their high levels of essential amino acids (EAA), unsaturated fatty acids, micronutrients (e.g., vitamin B12, iron (Fe), zinc, and calcium), and fiber [19]. Furthermore, edible insects have various bioactive compounds in their composition with potential health effects [20].

Previous systematic reviews on edible insects have focused on studying their nutritional composition [19,21,22], the presence of viruses [23], their effect on human and animal health [24–26], and allergic risks [27]. However, the global impact of edible insects on health and the environment remains to be elucidated. Previous reviews on health outcomes centered on either humans or animals and did not adopt a comprehensive approach. In the present review, data were retrieved from human studies on all relevant health outcomes (changes in growth, blood parameters, gut microbiome, changes in muscle mass composition, etc.), on the grams of edible insect, on the insect or part of insect used, and on the insect inclusion level. The aim of this systematic review was to provide an overview of human trials and animal studies to evaluate the effect of edible insect supplementation on health outcomes as well as studies on the environmental impact of edible insects as an alternative and more sustainable source of protein for humans and animals.

#### **2. Material and Methods**

#### *2.1. Search Strategy*

We conducted a systematic review in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines [28] and registered it in PROS-PERO (https://www.crd.york.ac.uk/prospero/ (accessed on 3 June 2021)) for humans (CRD42021243673) and animals (CRD42021243772). Following the PRISMA-P checklist, studies were identified by the electronic search of three databases (PubMed, Pro-Quest Medline, and Cochrane Library) for studies published between October 2010 and 28 February 2021. Combinations of the following search terms were used: "GHG", "greenhouse gas emission", "environmental impact", "environmental", "sustainability", "sustainable", "water use", "phosphor emission", "land use", "nitrogen emission", "eco-friendly", "climate-friendly", "life cycle assessment", "sustainable", "alternative animal-source", "entomophaga", "insect", "insecta", "insects", "edible", "consumption", "nutrition", "supplementation", "protein", "health", and "complementary". Boolean connectors (AND, OR) were used to search for associations between these terms.

#### *2.2. Eligibility Criteria*

Studies were eligible for inclusion if they were human investigations (experimental studies, randomized and controlled trials, and observational studies such as cohort, cross-

sectional, and case-control studies) or investigated animal consumption of edible insects (placebo or reference treatment) reporting data on health and sustainability. The review also included ecological studies that evaluated greenhouse gas emission (GHG), water footprint (WFP), land use (LU), and/or energy use (EU) as environmental indicators and those that assessed the feed conversion ratio. We excluded edible insect studies on nutrition composition, acceptance, food technology, gastronomy, allergy, and toxicology. Systematic reviews, meta-analyses, and cell culture, in vitro, and ex vivo studies were all excluded.

#### *2.3. Study Selection and Data Extraction*

Search results were downloaded to EndNote (Clarivate Analytics, Philadelphia, PA) and duplicates were removed. Titles and abstracts were screened in duplicate by two of three authors (M.R.-B., P.C.-A., and A.B.-F.) for eligibility. The third author resolved disagreements. Full texts were obtained for any article that appeared to meet eligibility criteria.

Information was extracted from the animal studies on: author(s), year and country of publication, type of animal, sample size, sex, and age, length of intervention(s) (days), edible insect use, number of intervention groups with sample sizes, insect inclusion rate of complementary food product (CFP) (g/100 g expressed in %), variables/outcome, and evaluated health parameters.

Information was extracted from the human studies on: author(s), year and country of publication, sample size, sex, and age, length of intervention(s) (days), edible insect use, intervention groups with sample sizes, daily food portion of intervention with insects (g), insect inclusion rate of CFP (g/100 g expressed in %), insect inclusion level of CFP (expressed in g) per each age group, protein inclusion level of CFP per day (expressed in g), variables/outcomes, and evaluated health parameters.

Information was extracted from the sustainability articles on: GHG (Kg CO2), which falls under the indicator global warming potential equivalent (GWP), EU (MJ) as a measure of fossil fuel depletion, LU (m2), for the amount of arable land used in the production chain, and finally the WFP (m3). The environmental impact was subsequently coupled with a functional unit (FU), a quantitative measure indicating the function of a product. For insects, FUs were expressed in kilograms of protein [29]. The environmental impacts of different steps within the system border were added together to express the total impact on certain environmental indicators. Finally, the total impact was divided by the number of FUs to yield the environmental impact per FU, which was used to compare environmental indicators between similar food products.

#### *2.4. Quality Assessment*

Quality and risk of bias were assessed using the Syrcle's risk of bias tool [30] for preclinical animal studies and the Cochrane risk of bias tool [31] for human studies. Both tools covered the following bias domains: selection bias (random sequence generation and allocation concealment), performance bias (blinding of participants and personnel), detection bias (blinding the outcome assessment), attrition bias (incomplete outcome data), reporting bias (selective reporting), and others. According to the score obtained, studies were classified as having a low, high, or unclear risk of bias (Table 1).


**Table 1.** Risk of bias in animal and human studies on the health effects of edible insects.

Summary of risk of bias: review of the opinions of the different authors on each element of bias risk for each study. The minus sign (-) indicates low risk of bias, plus sign (+) high risk of bias, and question mark (?) unclear risk.

Limitations of this review include gaps in the data available on the nutritional composition and quantity of edible insects administered in human studies and on the form of their administration, and some of this information could only be obtained after contacting the authors. Few studies specify the metamorphic phase of the edible insect, hampering comparisons of the % protein and composition of the complementary food product. It was also sometimes difficult to determine the stage at which values were assigned (e.g., farm gate or mill gate) and to gather information on the diet fed to the edible insects.

#### **3. Results**

#### *3.1. Literature Search Results*

The database search retrieved 4487 articles. After removing duplicates, the titles and abstracts of 3960 articles were assessed independently and in duplicate by two investigators. Eligibility criteria were finally met by 25 studies, which were included in the present systematic review (Figure 1). Tables 2–4 summarize the findings of these studies, categorized as animal [32–42,49], human [43–48], or sustainability [7,50–55] studies.

**Figure 1.** Flow chart of the selection of reviewed articles.


decreased

 compared

(S).

 to (a)

**2.**Effectofedibleinsectsonanimalhealth.




compared

 to (a) (NS).





domesticus;

GbG: *Grillodes bimaculatus* protein; BUN: Blood urea nitrogen; SOD: Superoxide

 RF:

Rhynchophorus

 phoenicis fabricius; MD:

glycosaminoglycan;

 LDL: low density

 dismutase;

 GPX:

malnourished;

 Fe: Iron; SD: standard diet; BP: blood pressure; DB: diabetes; CaG: *Dung beetle* (*C. molossus*)

lipoprotein;

 ALP: alanine

Glutathione

 peroxidase.

transaminase;

 SHR:

spontaneously

hypertension

 rats; WKY: Wistar Kyoto Rats;

glycosaminoglycan;

CRP:C-reactive


to (a) (S).
