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  <front>
    <journal-meta>
      <journal-title-group>
        <journal-title>PLOS
Medicine. 2016. p. e1002036. Available from: http://dx.doi.org/10.1371/journal.pmed.1002036
[36] Yang C</journal-title>
      </journal-title-group>
    </journal-meta>
    <article-meta>
      <article-id pub-id-type="doi">10.1093/nar/gky1032</article-id>
      <title-group>
        <article-title>OBO Foundry Food Ontology Interconnectivity</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <string-name>Damion Dooley</string-name>
          <xref ref-type="aff" rid="aff2">2</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Liliana Andrés-Hernández</string-name>
          <xref ref-type="aff" rid="aff9">9</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Georgeta Bordea</string-name>
          <xref ref-type="aff" rid="aff1">1</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Leigh Carmody</string-name>
          <xref ref-type="aff" rid="aff10">10</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Duccio Cavalieri</string-name>
          <xref ref-type="aff" rid="aff4">4</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Lauren Chan</string-name>
          <xref ref-type="aff" rid="aff3">3</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Pol Castellano-Escuder</string-name>
          <xref ref-type="aff" rid="aff0">0</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Carl Lachat</string-name>
          <xref ref-type="aff" rid="aff5">5</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Fleur Mougin</string-name>
          <xref ref-type="aff" rid="aff1">1</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Francesco Vitali</string-name>
          <xref ref-type="aff" rid="aff7">7</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Chen Yang</string-name>
          <xref ref-type="aff" rid="aff5">5</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Magalie Weber</string-name>
          <xref ref-type="aff" rid="aff6">6</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Matthew Lange</string-name>
          <xref ref-type="aff" rid="aff8">8</xref>
        </contrib>
        <aff id="aff0">
          <label>0</label>
          <institution>Biomarkers and Nutritional &amp; Food Metabolomics Research Group,University of Barcelona</institution>
          ,
          <addr-line>Barcelona</addr-line>
          ,
          <country country="ES">Spain</country>
        </aff>
        <aff id="aff1">
          <label>1</label>
          <institution>Bordeaux Population Health, University of Bordeaux</institution>
          ,
          <addr-line>Bordeaux</addr-line>
          ,
          <country country="FR">France</country>
        </aff>
        <aff id="aff2">
          <label>2</label>
          <institution>Centre for Infectious Disease Genomics and One Health, Simon Fraser University</institution>
          ,
          <addr-line>Burnaby, BC</addr-line>
          ,
          <country country="CA">Canada</country>
        </aff>
        <aff id="aff3">
          <label>3</label>
          <institution>College of Public Health and Human Sciences, Oregon State University</institution>
          ,
          <addr-line>Corvallis, OR</addr-line>
          ,
          <country country="US">USA</country>
        </aff>
        <aff id="aff4">
          <label>4</label>
          <institution>Department of Biology, University of Florence</institution>
          ,
          <addr-line>Florence</addr-line>
          ,
          <country country="IT">Italy</country>
        </aff>
        <aff id="aff5">
          <label>5</label>
          <institution>Department of Food Technology, Safety and Health, Ghent University</institution>
          ,
          <addr-line>Ghent</addr-line>
          ,
          <country country="BE">Belgium</country>
        </aff>
        <aff id="aff6">
          <label>6</label>
          <institution>INRAE, UR BIA, Biopolymères Interactions Assemblages</institution>
          ,
          <addr-line>Nantes</addr-line>
          ,
          <country country="FR">France</country>
        </aff>
        <aff id="aff7">
          <label>7</label>
          <institution>Institute of Agricultural Biology and Biotechnology - National Research Council</institution>
          ,
          <addr-line>Milano</addr-line>
          ,
          <country country="IT">Italy</country>
        </aff>
        <aff id="aff8">
          <label>8</label>
          <institution>International Center for Food Ontology Operability Data and Semantics</institution>
          ,
          <addr-line>Davis, California</addr-line>
          ,
          <country country="US">USA</country>
        </aff>
        <aff id="aff9">
          <label>9</label>
          <institution>Southern Cross Plant Science, Southern Cross University</institution>
          ,
          <addr-line>Lismore, NSW</addr-line>
          ,
          <country country="AU">Australia</country>
        </aff>
        <aff id="aff10">
          <label>10</label>
          <institution>The Jackson Laboratory for Genomic Medicine</institution>
          ,
          <addr-line>Farmington, CT</addr-line>
          ,
          <country country="US">USA</country>
        </aff>
      </contrib-group>
      <pub-date>
        <year>2021</year>
      </pub-date>
      <volume>13</volume>
      <fpage>11</fpage>
      <lpage>18</lpage>
      <abstract>
        <p>Since its creation in 2016, the FoodOn ontology has become an interconnected partner in various academic and government inter-agency ontology work spanning agricultural and public health domains. This paper examines existing and potential data interoperability capabilities arising from FoodOn and partner food-related ontologies belonging to the encyclopedic Open Biological and Biomedical Ontology Foundry (OBO) vocabulary platform, and how research organizations and industry might utilize them for their own operations or for data exchange. Projects are seeking standardized vocabulary across all direct food supply activities ranging from agricultural production, harvesting, preparation, food processing, marketing, distribution and consumption, as well as indirectly, within health, economic, food security and sustainability analysis and reporting tools. To satisfy this demand and provide data requires establishing domain specific ontologies whose curators coordinate closely to produce recommended patterns for food system vocabulary.</p>
      </abstract>
      <kwd-group>
        <kwd>eol&gt;Ontology</kwd>
        <kwd>data harmonization</kwd>
        <kwd>OBO Foundry</kwd>
        <kwd>food systems</kwd>
        <kwd>public health</kwd>
        <kwd>epidemiology</kwd>
        <kwd>multiontology framework</kwd>
        <kwd>One Health</kwd>
      </kwd-group>
    </article-meta>
  </front>
  <body>
    <sec id="sec-1">
      <title>1. Introduction</title>
      <p>
        Ontologists and semantic web advocates envision a future in which stakeholders in all sectors will
be able to take advantage of a harmonious federated data landscape built on the interoperability
prowess of ontologies. This data interconnectivity vision has been supported by academic and
government research sectors, exemplified in curation consortia such as the open source inter-agency
Open Biological and Biomedical Ontology Foundry (OBO) [
        <xref ref-type="bibr" rid="ref1">1</xref>
        ], which contains a collection of domain
specific ontologies that facilitate interoperability by adhering to a set of curation and logic patterns.
OBO promotes best practices to their member ontologies for ensuring such vocabulary is clear and
accessible while allowing shared principles governing ontology development to evolve. OBO
provides a web service for permanent links to term resolution (called purls), as well as guidelines for
establishing term hierarchies, term deprecation, and logically tested, versioned quality control within
an encyclopedic (domain specific) curation environment of experts. OBO’s standard OWL ontology
format is suited to expressing international standards in minute detail as data structures with
context-sensitive terminology, synonymy, and categorical, numeric and textual variables. Tools such
as the OBO Dashboard [
        <xref ref-type="bibr" rid="ref2">2</xref>
        ] are helping with the continuous improvement of ontology quality.
      </p>
      <p>
        The OBO approach was presaged by a paper advocating for the separation of curated biomedical
vocabulary from the content of clinical and research databases [
        <xref ref-type="bibr" rid="ref3">3</xref>
        ]. Relative to food, Lange et. al.
explored requirements and a prototype for a multi-ontology framework for describing and guiding
agriculture, food, diet and health [
        <xref ref-type="bibr" rid="ref4">4</xref>
        ]; a current review of farm-to-fork data harmonization approaches
[
        <xref ref-type="bibr" rid="ref5">5</xref>
        ] reinforces how important ontologies are in this effort.
      </p>
      <p>
        OBO houses many evolving ontologies that support a One Health [
        <xref ref-type="bibr" rid="ref6">6</xref>
        ] paradigm, including FoodOn
[7], which provides a food-centric perspective which networks with many of the aforementioned
ontologies and which can also be used in conjunction with food production and processing ontologies
outside the OBO landscape. One key OBO Foundry curation principle, called The Minimum
Information to Reference an External Ontology Term (MIREOT) [8], is the reuse of terms from other
OBO ontologies to avoid the costly and confusing situation where term entities having similar or
identical semantics but different identifiers exist in multiple ontologies. Reusability patterns include
the wholesale import of large branches of ontologies, for example, the ENVO import of FoodOn food
products; as well as selective term reuse; both approaches are described on the FoodOn technical
reuse page. This principle has been particularly important in the growth, expansion, and development
of FoodOn and related ontologies listed below:
●
●
●
●
●
●
●
●
      </p>
      <p>The Agronomy Ontology (AGRO) covers agricultural management practices applied to
matrices of crop plots [9].</p>
      <p>The Chemical Entities of Biological Interest (ChEBI) ontology organizes molecular entities
- mainly 'small' chemical compounds (natural or synthetic) - pertinent to the processes of
living organisms [10].</p>
      <p>The Farm to Fork Food Ontology (FoodOn) provides terms for generic (non-branded) food
products available at any point in the global food supply chain, as well as facets of terms for
food production processes and food characteristics. FoodOn can be reused in OBO wherever
food product references occur [7].</p>
      <p>The Compositional Dietary Nutrition Ontology (CDNO) covers nutritional composition
terms (vitamins, carbohydrates etc.) of organism anatomical parts like seeds, or fruit (which
form the fundamental layer of food products in FoodOn) in a diet-and-nutrition community
friendly ontology [11].</p>
      <p>The Human Disease Ontology (DOID) names food related allergies and their food product
triggers [12].</p>
      <p>The Medical Action Ontology (MAxO) project is exploring the relation between nutrition
deficiency and rare diseases [13]
The Health Surveillance Ontology (HSO) describes animal health, public health and food
safety surveillance systems, including proactive surveillance and reactive investigation
methods and objectives [14].</p>
      <p>Environmental Conditions, Treatments, and Exposures Ontology (ECTO) provides
language to describe experimental and environmental factors for public health and
environmental monitoring objectives [15].</p>
      <p>The Food-Biomarker Ontology (FOBI) documents chemical biomarkers of consumed food
products left in stool or urine [16].</p>
      <p>The Food Interactions with Drugs Evidence Ontology (FIDEO) focuses on vocabulary
useful to identify research on the influence of food consumption on oral drug ingestion [17].
The Ontology for Nutritional Studies (ONS) focuses on vocabulary for modeling nutritional
studies, including diet and dietary pattern variations [18].</p>
      <p>The Ontology for Nutritional Epidemiology (ONE) focuses on detailing nutritional study
document structure (e.g. research manuscripts, dietary surveys, food-based dietary guidelines,
etc.) and dataset characteristics [19].</p>
      <p>The Process and Observation Ontology (PO2) details characteristics and sampling regimes
of foods during their manufacturing process, as well as the processing steps they are subjected
to [20].</p>
    </sec>
    <sec id="sec-2">
      <title>2. Methods</title>
      <p>The process of developing an ontology within the context of OBO can resemble a stand-alone
ontology effort to start - both stand-alone and OBO infused efforts may involve reuse of parts from
other ontologies, and with just a few curators representing one or more stakeholder groups. However,
as the OBO community is engaged, the development methodology requires familiarization with many
aspects of OBO interdependence:
●
●
●
●
●
●</p>
      <p>Adoption of OBO standardized term URL’s that usually point to an ontology search engine
term result like ontobee.org [21]. Along with the MIREOT principle, this fulfills the
encyclopedic FAIR data vision of OBO.</p>
      <p>A service model whereby new term requests (NTR) are handled usually via Github requests
or larger bulk review and import projects. This is critical for satisfaction of peer networked
ontologies, otherwise bottlenecks occur.</p>
      <p>An ontology is expected to attract more than one user, thus encouraging other stakeholders to
be identified and even encouraged to join the curation team. Eventually monthly, bi-weekly or
weekly curation calls are needed depending on its growth curve and volunteer or funded
development capacity. This greatly improves an ontology’s standing as a de facto or more
official standard.</p>
      <p>Specialized workgroups can focus on particular problems, for example the Food Process
Ontology Workgroup (progress will be reported at IFOW 2021).</p>
      <p>Ontology scope evolution to allow branches of terms to be added or calved off into a new
ontology if core skilled curation teams can support them.</p>
      <p>Other structural and logical constraints aimed at supporting data harmonization within OBO
[22] including Basic Formal Ontology (BFO) [23] compatibility.</p>
      <p>A workgroup called the Joint Food Ontology Workgroup [24] was launched in the spring of 2020
as an informal methodology for term development within the food systems domain. FoodOn had
previously received batches of requests for diet and nutrition terms from a few other ontologies, but
was aware that ONS was under development as a new entry into OBO, and could be a potential niche
home for the requested terms. The workgroup convened once a month with representation from the
NTR-requesting ontologies as well as USDA, FDA, and other academic and research agencies keen to
help and to assess the appropriate reuse of ontologies within their operations. During that time a
corpus of over 60 diet and dietary pattern terms was discussed, reviewed, approved and then handed
to ONS for implementation. A similar discussion group called the Food Process Ontology Workgroup
is under way, tasked with reviewing process related ontologies and creating a generic food processing
model, and closely related recipe and ingredient model.</p>
      <p>Through this methodology, each additional project strengthens the capacity of OBO in general, and
FoodOn in particular, to become the lingua franca for the unambiguous mapping / exchanging /
synthesizing of agriculture, food, diet, and health -related data. The key value-add is that knowledge
produced by this federated activity exists precisely because the unique combination of vocabularies
that comprise FoodOn, and indeed the entire OBO Foundry, is not constrained by the narrower
mandates of any particular organization.</p>
      <sec id="sec-2-1">
        <title>2.1. FoodOn: A farm to fork food ontology</title>
        <p>FoodOn entered the OBO Foundry in 2016, calving-off food terms from ENVO [25], and
subsequently integrated with other OBO food chemistry and nutrition ontologies in a piecemeal
fashion as research projects required it. FoodOn also inherited, and has since evolved, the basic
structure of LanguaL [26], a popular food composition database (FCD) vocabulary originating in US
FDA CFSAN in 1975. FoodOn’s mandate is to describe and provide precomposed terms for generic
(non-branded) food products that a food producer, food manufacturer/processor, or consumer can find
in the food supply chain, ranging from wild or farmed food, to processed, wholesale, retail, prepared,
vendor, restaurant or home-cooked food. This includes extensive food description facets, such as
applied cooking treatments, preservation methods, packaging, and food source organism taxonomy.
FoodOn is being used or introduced collaboratively into a number of databases and standards, for
example:
●
●</p>
        <p>The USDA FoodData Central website (https://fdc.nal.usda.gov) now provides FoodOn
identifiers and categories for its Foundation Foods database entries, with plans to expand
ontology capability in the future.</p>
        <p>The FDA CFSAN GenomeTrakr database (Whole Genome Sequencing (WGS) Program |
FDA, Poster) which contains over 45,000 foodborne pathogen genomic sequences and their
metadata, which are matched to FoodOn, NCBITaxon and ENVO ontology terms using a
textual sample description to ontology term software called LexMapr. GenomeTrakr records
●
●
●
●
●
are then submitted to the NCBI Biosample sequence repository to assist in foodborne
outbreak and antimicrobial resistance research.</p>
        <p>WikiFCD (https://wikifcd.wiki.opencura.com), a wikibase database of food composition and
nutrient information that explores crowdsourcing curation.</p>
        <p>The Genomic Standards Consortium (GSC) of minimum information standards
(checklists) (MiXS)(https://gensc.org/mixs/) is adding a food package [27] for agriculture and
industry-situated sampling metadata for pathogen and metagenomic analysis.</p>
        <p>The draft ISO/TC 34/SC 9 standard "Microbiology of the Food Chain — Whole Genome
Sequencing, Typing and Genomic Characterization of Foodborne Bacteria"
The FDA Seafood Product List is being worked on collaboratively by FoodOn and FDA
staff to expand the mapping of common language fish names to precise scientific taxonomy
names in order to improve food traceability and authentication.</p>
        <p>FoodKG (https://foodkg.github.io/), a knowledge graph launched in 2019 representing over 1
million recipes which is constructed with an ontology combining FoodOn, CHEBI and other
resources like the USDA Nutrient Database, and the http://im2recipe.csail.mit.edu/
photograph-recipe matching project, enables querying of recipes by ingredient, cook time,
course type, and meal type.</p>
        <p>FoodOn reuses CHEBI, ENVO, CDNO and ONS terms, among others. Not all OBO ontologies
are integrated with FoodOn, for example, the Drug Ontology (DRON) has ‘cucumber allergenic
extract’ but no FoodOn, UBERON or NCBITaxon term references related to it, so partner ontology
integration is an ongoing refinement. As well, new terms are being introduced into OBO via
partnerships, such as an Institute for Food Safety at Cornell University list of over 350 food related
equipment and tool terms.</p>
        <p>Additionally FoodOn imports agency hierarchies to varying depths from European, North
American and some international standards as they were represented in LanguaL - including the
EFSA FoodEx2 Exposure hierarchy, the US Code of Federal Regulations (CFR) hierarchy, and GS1
food categories. An upcoming objective is to map to these branches more extensively by way of ‘has
member’ relation to FoodOn’s own food product hierarchy, to enable data exchange and
harmonization to the deepest level of food product classes.</p>
      </sec>
      <sec id="sec-2-2">
        <title>2.2. AGRO: The Agronomy Ontology</title>
        <p>The Agronomy Ontology (AgrO) describes agronomic management practices, implements,
and variables used during agronomic experiments. AgrO was started in 2017 in the context of the
CGIAR Platform for Big Data in Agriculture, from traits and parameters identified by agronomists
and crop modelers and from the Environment Ontology (ENVO). As an OBO Foundry ontology,
AgrO reuses terms coming from several ontologies including ENVO, CheBI, UO, PATO, TO/CO and
FoodOn. A main use case for AgrO is the Agronomy Field Information Management System
(AgroFIMS). AgroFIMS enables the design of agronomic trials and the digital collection of
agronomic data that is annotated from the start with agronomic terms coming from AgrO.</p>
        <p>AgrO relies on FoodOn as the source of terms for crop residues [AGRO:00000154] that derive
from food products. In the near future, AgrO will have dependencies on FoodOn for food and
nutrition terms important at the post harvest stage.</p>
      </sec>
      <sec id="sec-2-3">
        <title>2.3. CDNO: Compositional Dietary Nutrition Ontology</title>
        <p>CDNO, launched in 2020 and now a key part of FoodOn, provides terminology for nutritional
attributes from crops, livestock, and fisheries that contribute to human diet and which are referenced
in precision food commodity laboratory analytics.</p>
        <p>CDNO defines a comprehensive nutrition-oriented hierarchy to organize ChEBI chemicals and
associated concentrations by following a design pattern that involves the reuse of the term
‘concentration of ’ from PATO and the term ‘material entity’ from the BFO (Figure 3). (This view was
created because of ChEBI’s inherent hierarchy of molecular entities and their roles is not easy for
nutritionists to navigate [11]). The CDNO hierarchy is complemented by proposed classes for
physical and functional attributes and dietary functional roles. One goal of this work is to allow
harmonisation of the nutrient measures used for international standards such as the FAO sponsored
International Network of Food Data Systems (INFOODS)[28] system for tagging nutrient measures in
food composition databases as well as the USDA Nutrient DB codes. However, the nomenclature
required to describe variation in analytic measures is a future mission.</p>
        <p>CDNO was developed with the primary aim of adding value to datasets and their comparison,
where terms from the ‘nutritional component concentration’ class are associated in the data curation
process with specific food raw materials and associated metadata at any point in the supply chain,
from cultivation/production in agriculture through to processing and consumption. CDNO, FoodOn
and Plant Ontology (PO) curators worked together in a collaborative effort to establish an initial set of
over 58 food raw materials entities, defining the source of plant samples and crop production
processes or stages from which the food raw material was taken. This process required analysis and
attribution of existing terms from the PO and NCBI Taxon ID, in order to represent specific plant food
products. For example “an apple fruit” is represented with the label ‘apple (whole)’ in FoodOn as a
subclass of PO ‘pome fruit’ [PO:0030110] which ‘derives from’ [RO:0001000] the organism ‘Malus
domestica’ [NCBITaxon:3750]. Species-specific datasets in tabular form can simply have columns for
organism, anatomical part, and FoodOn term if desired, while graph database treatments can have
structures created directly from CDNO and FoodOn OWL axioms that reflect specific material dietary
nutritional component concentrations.
2.4.</p>
      </sec>
      <sec id="sec-2-4">
        <title>DO: The Human Disease Ontology</title>
        <p>The Human Disease Ontology (DO) uses Relation Ontology (RO) term “has allergic trigger” to
attach an allergic disease to the food(s) that trigger it. This relation is used for other connections in
addition to food, for example, to connect penicillin to penicillin allergy. Food allergies (a subclass of
gastrointestinal allergy, defined as “An allergic disease that is located_in the gastrointestinal tract”)
have fish and shellfish, fruit, milk, wheat and vegetable subclasses, and corresponding relations to
FoodOn food products that cause them. This branch DOID also supports the Immune Epitope
Database (IEDB) [29] by way of an IEDB “slim” export file of almost the entire food allergy branch.
It appears that the vegetable allergy branch is accidentally omitted from this slim file (shown in Figure
4), and a Github issue has been raised to remedy the omission. There may be further opportunity for
modelling disease here by linking to allergy symptoms.</p>
      </sec>
      <sec id="sec-2-5">
        <title>2.5. HSO: The Health Surveillance Ontology</title>
        <p>HSO is a knowledge model for data collection, collation and reporting of One Health surveillance
activity. It recognizes that although detailed surveillance data may not be easily harmonizable and/or
shareable due to specific national agency reporting requirements, top-down semantic harmonization of
reporting elements is required to pool summary data for international / multi-agency contexts.
Engaging multilaterally about what essential components of public health, animal health, and food
safety surveillance data are, lead the HSO curation team to develop vocabulary and a model centred
around a ‘surveillance activity’, a subclass of Ontology for Biomedical Investigations (OBI) [30]
planned process’. HSO is an outcome of the One Health suRveillance Initiative on harmOnization
of data collection and interpretatioN (ORION) project and is currently interoperable with various
catalogues in EFSA's Standard Sample Description.
2.6.</p>
      </sec>
      <sec id="sec-2-6">
        <title>MAxO: The Medical Action Ontology</title>
        <p>MAxO, launched in 2020, is a broad
ontology that provides a structured vocabulary
to medical procedures, interventions,
therapies, treatments, or clinical
recommendations, including nutritional
recommendations. MAxO was designed to
provide a thorough resource for annotating
diseases, in particular, rare diseases, where
nutritional needs are often critical. In order to
capture the relationship between treatments
and diseases, the Phenotypic Observation
Explication Tool (POET) was developed to
establish a relationship between MAxO,
Human Phenotype Ontology (HPO), and
Mondo Disease Ontology (Mondo) terms. This
tool will allow researchers to actively
participate in annotating diseases in their
expertise. MAxO annotations and the POET
tool will be available on the HPO website
(hpo.jax.org) by 2022.</p>
        <p>MAxO provides a lexicon of 76 dietary intake avoidance behaviour terms, and an “avoided food”
object property to detail which FoodOn products are being avoided. Moreover, MAxO utilizes 5
FoodOn terms for nutritional supplementation recommendation. These terms will be used to annotate
diseases that require nutrition therapy or management.</p>
      </sec>
      <sec id="sec-2-7">
        <title>ECTO: The Environmental Conditions, Treatments, and Exposures</title>
      </sec>
      <sec id="sec-2-8">
        <title>Ontology</title>
        <p>ECTO has been gradually evolving since 2016 with a focus on documenting precomposed
experimental treatments, non-experimental exposures, and environmental conditions that may impact
humans and other organisms. ECTO ranges widely and encompasses terms such as ‘exposure to
arsenic’ or ‘exposure to increased temperature’ which can be meaningful for modeling experimental
designs. Additionally, this broadly scoped ontology includes exposure terms related to food and
nutrient exposures such as “ingestion of skim milk”. ECTO currently has 160+ food ingestion terms,
17 vitamin and mineral ingestion terms, and a developing Dead Simple OWL Design Pattern
(DOSDP) [31] which will integrate exposures to specific diets that refer to terms found within the
Ontology for Nutritional Studies. In turn, terms within ECTO can be utilized to describe and
document research designs in toxicology and exposures, epidemiology, and nutrition in support of
standardized language and data harmonization across the literature. ECTO terms can also be leveraged
for modeling components of human disease, environmental toxin exposure, and alteration of
biological function.
2.8.</p>
      </sec>
      <sec id="sec-2-9">
        <title>FOBI: The Food-Biomarker Ontology</title>
        <p>FOBI, launched in 2020, is aimed at describing the relationships between foods and food
metabolome, that is, the collection of all metabolites in the body directly derived from the digestion
and biotransformation of foods and their constituents. FOBI is composed of two interconnected
branches: a “Foods” branch consisting of raw foods and multi-component foods; and a “Biomarkers”
branch containing food intake biomarkers classified by their chemical classes. The food branch is
composed mainly of FoodOn terms, while the biomarker branch is composed of both ChEBI terms
and FOBI specific terms. At the moment, FOBI has a total of 1197 terms, containing 590 food
biomarkers connected by a “BiomarkerOf” object property to 29 foods adopted from FoodOn, such as
“cacao food product”.</p>
      </sec>
      <sec id="sec-2-10">
        <title>2.9. FIDEO: Food Interactions with Drugs Evidence Ontology</title>
        <p>The first version of FIDEO [32], released in
2020, represents interactions between foods and
food supplements and drugs. Supporting
evidence is equally represented to allow medical
professionals to assess clinical significance of
interactions. FoodOn terms and food categories
are reused whenever possible, but other
domain-specific food categories are locally
defined. While initial efforts were focused on the
design of the ontology based on the Basic
Formal Ontology (BFO) and the OBO Foundry
principles, more recent efforts are focused on a
user-friendly visual interface that allows search
and exploration of interactions [33] and on
integrating food-drug interactions from various
sources including compendia and existing
databases to FIDEO using ROBOT [34].</p>
      </sec>
      <sec id="sec-2-11">
        <title>2.10. ONS: Ontology for Nutritional Studies</title>
        <p>Since its first publication in 2018, the ONS has committed to describe nutritional studies in their
multifaceted nature. A central concept in ONS is ‘diet’ [ONS:1000001], an ‘information content
entity’ [IAO:0000030] defined as “the sum of food consumed by a person or other organism”. The
diet concept is closely related to ‘dietary pattern’ [ONS:0000094], defined as “the quantity,
proportion, variety and combination of different foods and drinks consumed in meals, and the
frequency with which they are habitually consumed”. In ONS conceptualization, ‘dietary pattern’
denotes ‘diet’. Dietary pattern is intended to represent a ‘data item’ [IAO:0000027] typically resulting
from assays in the context of nutritional epidemiology (i.e. ‘Food Frequency Questionnaire’
[ONE:0000007]), containing a specification of foods consumed and, as a result, denoting the type of
diet to which a subject has adhered.</p>
        <p>Curation and development revolving
around the initial diet concept in ONS has
greatly benefited from the collaboration with
the Joint Food Ontology Workgroup. Thanks
to this interaction, multiple different
subclasses of the diet (and related dietary
pattern) were defined. The annotation on food
classes inclusion or exclusion for the various
flavours of diet (and related dietary pattern)
rely completely on the import and use of
classes from FoodOn, at different granularity
levels. As an example, the ‘vegan diet’
[ONS:1000021] and the ‘vegan dietary
pattern’ [ONS:2000021] would be both
annotated as characterized by eating
vegetables [‘eats’ some ‘plant food product’;
RO:0002470 some FOODON:00001015] and
by excluding the consumption of animal
products [not(‘eats’ some ‘vertebrate animal
food product’; not(RO:0002470 some
FOODON:00001092)] (Figure 11).</p>
      </sec>
      <sec id="sec-2-12">
        <title>2.11. ONE: Ontology for Nutritional Epidemiology</title>
        <p>The ONE [19] details nutritional epidemiology manuscript and dataset characteristics. The ONE is
structured according to a set of minimal requirements for the reporting of nutritional epidemiology
research ([35]). The first version of ONE extends IAO document parts so they can cover research
paper structure, and as well description of food surveys which form the underlying datasets for many
studies. Abstract, discussion, ethics, methods, results and supplementary methods specific to dietary
studies are defined. Classes of quality assessments of study designs and dietary recall methods are
also defined (Figure 12).</p>
        <p>The ONE was used previously to
assess reporting completeness of
manuscripts that present findings of
nutritional epidemiology [36].</p>
        <p>Ontology classes regarding
food-based dietary guidelines (FBDGs)
were added into ONE in 2021 to
illustrate its potential applications for
population dietary recommendations.</p>
        <p>Food-based dietary guidelines
represent a wealth of accumulated diet
knowledge summarized from nutrition
studies [37,38].
FBDGs are important documents for policy makers, healthcare workers and educators, etc. to guide
the general public, in order to help them build healthier eating habits. Applications of ontology will
unlock information contained in the guidelines for automated modelling of trends to assess dietary
habits.</p>
        <p>The ONE curators are currently developing a Natural Language Processing (NLP)-SPARQL
linkage to enable a natural language query of ONE, as well as dashboard development to visualize
nutritional knowledge contained in research manuscripts and population based recommendations.</p>
      </sec>
      <sec id="sec-2-13">
        <title>2.12. PO2: Process and Observation Ontology</title>
        <p>Based partly on the Sensor, Observation, Sample, and Actuator (SOSA) ontology [39], but also
situated within the BFO hierarchy, and drawing upon OWL-Time, QUDT and IAO, the PO2 ontology
is designed to monitor industrial food processing, and describe food formulation. PO2 can represent a
food transformation process described by a set of experimental observations available at different
scales and evolving in time through the different unit operations of a production process. The
ontology contains a core layer dedicated to the generic modeling of both transformation and
characterization processes, while domain specific sub-ontologies specialize the PO2 core model for
different projects. It has been implemented in databases covering dairy, meat, and biorefinery
production, to represent the unique characteristics of foods during their manufacturing process. PO2
has been tested in fit-for-purpose software for maintaining these databases. PO2 curators participate in
the Food Process Ontology Workgroup which is helping to build FoodOn’s food transformation
process branch. The ontology is available at http://agroportal.lirmm.fr/ontologies/PO2.</p>
      </sec>
    </sec>
    <sec id="sec-3">
      <title>Discussion</title>
      <p>The development of the OBO food related ontologies is occurring in a semi-autonomous parallel
fashion, with interconnectivity issues arising on a weekly basis, and with the need to train new talent
to help curate the growing volume of what is at the basic level a catch-up exercise to standardize and
digitize vocabulary being used in research, policy and industry across the food spectrum. Knowledge
is beginning to accrue within these OBO ontologies as they express at a class level the subject
predicate object facts or assertions provided by the collective language that OBO can provide. These
are much like “nanopublications” [40] that should be combinable to build larger and larger knowledge
graphs about food. The FoodKG project demonstrates that factoid (“How much fat is in butter?”),
comparison (“Which has more fat, butter or olive oil?”) and constraint (“Which dish has chicken,
onion, and garlic?”) competency questions [41] can be applied to a knowledge graph composed of an
import of triples from different sources. An overlap between ontology and knowledge base often
occurs - axioms at the class level are expressing knowledge about class behaviour that instances
conform to and inherit properties from. For example, FoodOn and DOID ontologies together hold the
fact that Apium graveolens is the key organism of “celery food product” which “is allergic trigger of”
“celery allergy”. Future additions of codified food allergies will enable hypothesis development and
class-level associations that do not currently exist. For instance, potential cross allergenicities may be
found to other foods originating from other organisms in the same taxonomic group, or
grown/processed with similar methods. For example Figure 14 shows how parsley, dill and celery
allergies each arise from different food products, yet each are also derived from organisms contained
within the same sub-family, Tribe-level taxonomic hierarchy. Based on this information, one could
hypothesize potential allergies for consumers who are allergic to any one of these products. Using the
same logic, one can imagine similar hypotheses being generated about foods that have been produced
or processed with similar classes of exogenous chemicals.</p>
      <p>The relative recency of the OWL standard has contributed to methodological growing pains
stemming from its roots in formal logic and philosophy which are not easy to comprehend in terms of
capability, computability, and ontology and database infrastructure especially for implementing term
reuse and deprecation functionality. A new Core Ontology for Biology and Biomedicine (COB) is
being lauded as a simpler development starting point that avoids a number of abstract BFO terms and
contains many commonly reused OBO terms [42]. Tools like robot templates are enabling term
curation of some kinds to be separated from the more intricate steps required for curation in a
multiuser environment (see https://foodon.org/design/robot-managed-vocabularies/). As well, OBO is
developing guidelines for multilingual labelling, and providing domain specific labels for terms
shared between ontologies - via exact synonyms that are marked as belonging to a particular subset of
ontology, which for example CDNO can use to provide nutritionist-friendly labels on ChEBI
chemicals. Longstanding issues about the presentation of Vitamins as chemicals or as roles have
recently been resolved between members of the Joint Food Ontology Workgroup and ChEBI; as well
JFOW member dialogue has clarified the domain coverage and scope between ONE and ONS.</p>
      <p>A larger challenge is to see how OBO might evolve to support domains that are outside of the life
sciences. OBO would seem to have a natural counterpart in the Industrial Ontology Foundation (IOF),
launched in 2016 (and now part of OAGi), but as IOF is yet to launch its core ontology (scheduled for
late summer 2021) there is not yet an ability to assess IOF ontology domains to trade terms with.
Consequently ENVO remains the home for “manufactured product”, and a large influx of food
industry and other equipment useful for laboratory and food process modelling, and biosample site
description, will be listed under that class.</p>
      <p>OBO-allied ontologies and SKOS or basic RDF based vocabularies in business operations or
strategy and sustainability policy sectors can potentially add value together in a knowledge graph.
Some, like OWL-Time fit well under BFO zero- and one-dimensional temporal regions. Others like
the GS1 Global Product Classification for Food/Beverage/Tobacco [43] require much more work to
link to OBO food related ontologies for describing nutrients, allergens, ingredients and serving sizes
for example. This is critical for supporting traceability requirements of many blockchain projects
under development since GS1 standardized vocabulary is pervasive in business. The W3C PROV-O
[44] provenance ontology is often resorted to for process modelling, but fails to satisfy various
functional needs, and so the Food Process Ontology</p>
      <sec id="sec-3-1">
        <title>Workgroup is determining what extra</title>
        <p>functionality OBO needs - for equipment description, operating conditions, and extensions to PATO or
FoodOn food characteristics - to cover this space.</p>
        <p>On the horizon, the European Food and Safety Administration (EFSA) will be creating a
pan-european food composition database presumably supported by the EFSA FoodEx2 vocabulary
thesaurus, and this will need a gateway to OBO and other ontology based knowledge by way of
terminology mapping. At first glance agency in-house food-related vocabularies would seem to
benefit from conversion into globally accessible vocabularies that OBO contains, but technical,
resource development, trust, versioning and regulatory issues suggest a more complex incremental
alignment will occur. Some organizations may prefer a cautious medium-term use of open-source
ontologies as a lingua franca hub of data exchange vocabulary with external partners.</p>
      </sec>
    </sec>
    <sec id="sec-4">
      <title>4. Conclusion</title>
      <p>Taken together, the above work represents an explosion of knowledge and data harmonization
about food systems within OBO Foundry, and is emerging as the language for a federated database
model. The successful reuse of terms is demonstrated, and the methodology of inter-agency curation
points the way to faster de-facto standardization of vocabulary. The semantic web way of thinking
about vocabulary through OWL ontologies that easily generalize and specialize about food related data in
the world is proving to be a success in managing the complexity of life science knowledge, and a
promising model for describing activity in health and sustainability policy and business domains as well.</p>
    </sec>
    <sec id="sec-5">
      <title>5. Acknowledgements</title>
      <sec id="sec-5-1">
        <title>This work is primarily supported by the USDA</title>
      </sec>
      <sec id="sec-5-2">
        <title>Non-Assistance Cooperative Agreement 58-8040-8-014-F and Genome Canada Grant 286GET to W. Hsiao.</title>
      </sec>
    </sec>
    <sec id="sec-6">
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