Effects of human-animal relationship on animal productivity and welfare

Abstract

This is a literature review of the effects of humans ́ relationships with farm animals on animal productivity and welfare, including the following topics: definition of the concept and description of different tests that have been developed to measure human-animal relationship (HAR). Temperament and tameness, which have been considered as farm animal characteristics that are important in HAR, as are stockperson attitudes. Some international farm animal welfare protocols are also described, together with negative and positive stimuli that affect farm animal welfare and productivity. In addition to some factors affecting the quality of HAR. We conclude that even with improved precision farming and automation: a) a good HAR is still fundamental to improve farm animal welfare with associated health and production benefits and b) with the numerous tests assessing fear of humans, many are not commercially applicable.

Full text

J Anim Behav Biometeorol (2020) 8:196-205
ISSN 2318-1265
doi.org/10.31893/jabb.20026
Effects of human-animal relationship on animal productivity and
welfare
Daniel Mota-Rojas ▪ Donald Maurice Broom ▪ Agustín Orihuela ▪ Antonio Velarde ▪
Fabio Napolitano ▪ María Alonso-Spilsbury
D Mota-Rojas ▪ M Alonso-Spilsbury
Neurophysiology, behaviour and assessment of welfare in
domestic animals. Department of Animal Production and
Agriculture, Universidad Autónoma Metropolitana (UAM),
Mexico City, Mexico.
DM Broom
Department of Veterinary Medicine, University of
Cambridge, Cambridge, United Kingdom.
A Orihuela (Corresponding author)
Facultad de Ciencias Agropecuarias, Universidad Autónoma
del Estado de Morelos, Cuernavaca, Morelos, México.
A Velarde
Institute of Agrifood Research and Technology - IRTA,
Animal Welfare Program, Veinat Sies S-N, Monells 17121,
Spain.
F Napolitano
Scuola di Scienze Agrarie, Forestali, Alimentari ed
Ambientali, Università degli Studi della Basilicata, 85100
Potenza, Italy.
email: agustin.orihuela.trujillo@gmail.com
Abstract This is a literature review of the effects of humans´
relationships with farm animals on animal productivity and
welfare, including the following topics: definition of the
concept and description of different tests that have been
developed to measure human-animal relationship (HAR).
Temperament and tameness, which have been considered as
farm animal characteristics that are important in HAR, as are
stockperson attitudes. Some international farm animal
welfare protocols are also described, together with negative
and positive stimuli that affect farm animal welfare and
productivity. In addition to some factors affecting the quality
of HAR. We conclude that even with improved precision
farming and automation: a) a good HAR is still fundamental
to improve farm animal welfare with associated health and
production benefits and b) with the numerous tests assessing
fear of humans, many are not commercially applicable.
Keywords: fear, sensitive period, tameness, wellbeing
Introduction
According to Waiblinger et al (2006) and Ellingsen et
al (2014), human-animal relationships (HAR) can be defined
as “the degree of relation or distance that exists between an
animal and a human being, perceived, developed and
expressed through their mutual behaviour”. To create a
relation between any two individuals, entails on the one
hand, repeated encounters and, on the other, certain cognitive
abilities; that is, the capacities that allow individuals to
associate the positive or negative emotional content of
interactions with another individual, and then recall it when
predicting future encounters (Sankey et al 2010).
Farm animals, may perceive interaction with humans
as: a) negative, when they fear people, avoiding contact with
them; b) neutral, when the fear level is low but animals still
avoid contact; and c) positive, when fear is absent, and
animals allow physical (Claxton 2011; des Roches et al
2016). Handling that includes abrupt movements, pushing
and the use of prods, shouts and kicks is considered negative,
while handling characterised by slow movements, whispers
and petting have positive effects on animals (Ellingsen et al
2014). Non-aggressive controlling interactions, such as
gentle stick use, gentle handling and instructive talking, are
considered neutral (Waiblinger et al 2002). Classic
conditioning processes can occur when farm animals
associate either negative or positive handling with specific
humans responsible for their care (Rushen et al 1999ab) and
may also lead them to generalise their responses to other
people (Waiblinger et al 2006).
The use of positive reinforcements, like feeding or
tactile contact, often fosters learning in farm animals
(Rochais et al 2014) and may stimulate physiological
reactions that can be interpreted as “anti-stress effects”
(Lürzel et al 2015). This is one of the means of improving
the quality of HAR.
The objective of this literature review is to show the
effects of humans´ relationships with farm animals on animal
productivity and welfare.
REVIEW
Received: May 02, 2020 ▪ Accepted: May 19, 2020 ▪ Published Online: June 04, 2020

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Measures of HAR
Evaluating the quality of HAR is an important means
of improving animal welfare. This process must consider the
behaviour of the animals towards stockpersons as well as the
behaviour of the stockpersons towards the animals. HAR is
considered in international animal welfare protocols for
monitoring welfare in production units. For example, the
Welfare Quality®protocols (WQ® 2009abc; des Roches et al
2016), as well as others included in the Animal Welfare
Indicators project (AWIN) (Caroprese et al 2016).
Assessing the quality of HAR requires the gathering
of evidence that is: a) valid (i.e., reflects what actually
occurs); b) reliable (i.e., the tendency to give consistent
results with repeated measurement); and c) viable (in terms
of time, financial resources and safety) (Napolitano et al
2011; des Roches et al 2016).
Important human factors to be considered during this
assessment are stockpersons’ attitudes, personality,
knowledge, experience and degree of work satisfaction. The
attitude towards any kind of animal will affect the quality of
interaction and the type of handling. Attitudes during animal
handling have been classified as: a) tranquil or friendly; b)
dominant; c) impatient; and d) aggressive (Waiblinger et al
2006).
Figure 1shows the model proposed by Hemsworth
and Coleman (1998) to describe the effect of HAR on animal
productivity and welfare, as well as the reciprocal
relationship between the attitude of a person who handles
farm animals and the animal’s behavioural response towards
him. Within this topic Welp et al (2004) found that dairy
cows show greater vigilance behaviour, an indicator of fear,
in the presence of people who have negative attitudes
towards them, in comparison with unfamiliar individuals and
people with whom they have positive interaction, indicating
that animals are able to discriminate among people with
distinct behaviours.
Figure 1 Model of human-animal relationship proposed by Hemsworth and Coleman (1998), adapted from Hemsworth (2003). Most studies
on this topic highlight the sequential relations among the attitudes and behaviour of operators towards their animals, fear r esponses, and the
effect of fear on the welfare and productivity of farm animals.
To evaluate general beliefs and attitudes towards
animals, and levels of work satisfaction among stockpersons,
several questionnaires have been used. For example, in the
dairy (Breuer et al 2000) and sheep industries (Napolitano et
al 2011). However, some behavioural tests are difficult to
interpret, for example, human approaches to animals can be
perceived as threatening, but the fear the animals feel may
induce flight or a freezing reaction (Bourguet et al 2015).

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Furthermore, activities like feeding reduce the possibility to
flee so may be inhibited. The response of the animals may
also vary as a function of social rank, the gregarious nature
of the animals (Carbajal and Orihuela 2010) and the inter-
individual distances that they keep within the group (Boissy
and Le Neindre 1997). Many responses are species-
dependent and goats (Mattiello et al 2010) are usually
considered more curious than sheep because of the
exploratory behaviour they often manifest towards people.
It is also important to evaluate animals’ reactions
during handling procedures (Napolitano et al 2013) because
tests that consider this factor may be used to select animals
less afraid of humans and, therefore, easier to manage
(Windschnurer et al 2009). Animals raised in semi-natural
conditions tend to show less interest in humans, perhaps
related to the fact that their only contact with them occurs
when they are captured in the field and separated from their
mother or herd (Rochais et al 2014).
Farm animals are more likely to approach stationary
persons than persons actively moving toward them, and
humans in squatting position more than those in standing
position (Hemsworth et al 1986b; Lyons et al 1988). Farm
animal species can also recognize individual humans and are
more likely to approach those who treat them well than those
who act in an aggressive way. Similarly, the location of prior
positive or negative handling experiences can determine how
animals approach or avoid the same person in two different
places if that person treated them differently in each place
(Rushen et al 1999a). Several behavioural tests have been
used to assess fearfulness towards humans, as reviewed by
Waiblinger et al (2006).
The stockpersons´ attitudes towards farm animals can
be measured by the animal responses to humans in
standardized test situations like the reactivity to an
approaching human (Muns et al 2015; Brajon et al 2015) and
the avoidance distance test (Edwards et al 2010).
Studies on cattle, poultry and pigs have suggested that
the test of reactivity to an approaching moving human, based
on the avoidance responses of the animals, reflects the HAR
(Waiblinger et al 2006). The human approach test, assesses
fear of humans, offering also the possibility to measure the
social relationship with humans, the management quality and
the extent of individual differences (Waiblinger et al 2006).
The WQ protocols rely on human approach tests. A human
approach test is also included in the AWIN protocols for
horses and sheep (AWIN 2015ab), whereas the AWIN
protocol for goats relies on a stationary human test (AWIN,
2015c). In cattle, the test of reactivity to a stationary human
seems to be less relevant, because it is based on animal
approach behaviour towards humans and reflects not just
reactivity to humans but a mix of motivations depending on
the context of the test (de Passillé and Rushen 2005).
Conversely, this type of test seems more appropriate for
goats, which are generally more exploratory than other farm
animals.
The response of sows in stalls to approaching hand
contact and the response of free-moving sows in groups to
approach by an observer, had been validated by Scott et al
(2009) for on-farm welfare assessment in different housing
systems. However, according to Powell et al (2016), it
should be noted that the human approaching touch is a valid
measure of fear to humans in experimental settings, but
impractical for on-farm use due to the need for animals to be
individually tested in a purpose-built test arena.
The Stationary Person Test, the Avoidance Distance
Test and the Touch Test had been validated to effectively
measure the human-hen relationship in non-caged systems
(Graml et al 2008a). It is worth noting that a complex test
including stationary and moving elements has also been
validated for birds (Raubek et al 2007). The Avoidance
Distance Test has also been recommended by Windschnurer
et al (2008) for on-farm welfare assessment for dairy cows.
However, some inconsistencies in dairy calves´ responses
had also been observed (Meagher et al 2016).
Other means to assess the HAR are: (i) use an
interview about stockperson practices (Kling-Eveillard et al
2017); (ii) observing stockpersons during common
(Ellingsen et al 2014; Rueda et al 2015) or less common
handling events (Destrez et al 2018); (iii) assess farmers´
attitudes through a questionnaire (Bertenshaw and
Rowlinson 2009; Hemsworth et al 2000; Fukasawa et al
2017); or (iv) use video-recording (Johansson et al 2015).
However, according to Spoolder (2007), it is more relevant
to assess the quality of the HAR directly by looking at
farmers´ attitudes and handling practices than by assessing
fear of humans.
Regardless of the test used, there are some
confounding factors that might be considered when
interpreting the results. The nature of human contact can
significantly modulate how farm animals perceive humans,
affecting their behavioural responses (for a review, see
Boivin et al 2003; Waiblinger et al 2006; Adler et al 2019).
Effects on productivity and welfare
The nature of HAR matters as it will modulate not
only the welfare of the animal, including its health, but also
productivity and product quality (Hemsworth et al 2009;
Tallet et al 2018). Research on HAR and animal production
has been mainly focused on its effect on stress, productivity
and meat quality (Hemsworth 2003; Hemsworth et al 2009;
Zulkifli et al 2013).
Negative effects
Negative handling such as shouting and hitting, leads
to poor animal welfare, including fear, acute and chronic

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stress (Hemsworth et al 2000). Fear responses towards
humans may affect the productivity (Rushen et al 1999ab),
health and stress physiology of farm animals (Hemsworth et
al 2000; Hemsworth 2009; Hemsworth and Coleman 2011);
as in pigs (Hemsworth 2008; Hemsworth and Coleman 2011;
Probst et al 2013), hens (Barnett et al 1994; Graml et al
2008b; Edwards et al 2010), and dairy cows (Lürzel et al
2015; Ivemeyer et al 2018; Adler et al 2019).
In Pigs
Poor handling results in high levels of fearfulness
(Hemsworth and Barnett 1991). Negative behaviours
displayed by the stockperson (e.g. slapping, hitting and
kicking) are strongly associated with a high level of fear in
pigs (Hemsworth et al 1989a).
Stressful, human handling affects pig weight gains
negatively (Gonyou et al 1986; Hemsworth and Barnett
1991). Hemsworth et al (1981) subjected gilts to either
pleasant or unpleasant human contact for three 2-min
periods/week, from 11 to 22 weeks of age. The authors noted
that the juvenile females with the pleasant handling treatment
had higher weigh gain than those with other treatments.
Lensink et al (2009a), observed that the fear response
to humans of nulliparous sows was linked with their
behaviour towards humans and nervousness around first
farrowing, and these negative interactions were mostly
related with prophylactic and therapeutic procedures
(Lensink et al 2009b).
Unpleasant physical contact with humans reduced
testicle size and delayed coordinated mating response in
boars, and reduced pregnancy rate in sows, when compared
with those receiving positive human handling (Hemsworth et
al 1986c).
A study undertaken by Sommavilla et al (2011)
showed that loud tones, making threatening postures and
forcing piglets in the creep area during the suckling period
were perceived as aversive, and increased the withdrawal
response of piglets to human approach on the day of weaning
compared with piglets that received a neutral treatment.
Similarly, Brajon et al (2015) showed that rough handling,
even without physical stress, was enough to activate a fear
response in weaned piglets.
In Poultry
High fear of humans is associated with reduced egg
production, growth, feed efficiency, product quality and
sexual activity whilst increasing aggression, handling
difficulties and immunosuppression (Barnett et al 1993;
1994; Gross and Siegel 1982; Jones 1996).
Visual or physical contact with humans can elicit
behavioural inhibition, withdrawal panic and violent escape
reactions in chickens (Jones 1996), often with associated
injury as well as adrenal responses. Fear reactions, like panic
or violent escape attempts, not only waste energy and thereby
impose a metabolic cost, but they can also result in injury or
even death when the birds run into obstacles or pile on top of
each other (Waiblinger et al 2006).
In Cattle and Buffaloes
Poor HAR is associated with reduced milk production
by cows (Seabrook 1984; Waiblinger et al 2002). Aversion
to shouts has been reported (Waynert et al 1999; Pajor et al
2000). Ellingsen et al (2014) observed that stockpersons with
a nervous handling style or who were dominant and
aggressive, induced a negative mood in more cows. des
Roches et al (2016) confirmed that cows’ fear of people is
linked to negative attitudes displayed by caretakers toward
cows and is reduced in farms where several caretakers are
present. Likewise, cattle show more intense fear responses to
humans in larger farms with higher levels of mechanization,
due to the lower frequency of contact with the stockperson
(Mattiello et al 2009). Rushen et al (1999b) reported that the
presence of an aversive stockperson at milking, who had
previously hit or occasionally used a battery-operated
prodder over a 5-day period, led cows to increase their
residual milk. Similarly, Munksgaard et al (1997) observed
that, following the aversive treatment of striking the cow
forcefully with an open hand, cows urinated and defecated
more frequently. In addition, Arias and Špinka (2005) found
that in farms with more neurotic stockpersons, the cows had
lower milk yields per standardized lactation and higher
veterinary costs. Hemsworth et al (2000) found that the use
of negative interactions with cattle by stockpersons was not
only negatively correlated with milk yield, but also with
percent protein and fat, and positively correlated with milk
cortisol concentration.
There is evidence that excitable temperament in
stockpersons increases the risk of aggressive handling and
tends to decrease labour efficiency, for example, by
increasing the time needed to perform artificial insemination
and reducing cows’ body hygiene (Rueda et al 2015). Heifers
that faced negative handling and were more reactive during
handling had higher dirtiness scores and these were
associated with lower pregnancy rates (Ceballos et al 2018).
Furthermore, cows that required more handling time in the
corral, produced fewer viable embryos (Macedo et al 2011).
Aggressive and mild-escape behaviours during head-lock
restraint had negative effects on reproductive performance of
dairy heifers (Kasimanickam et al 2018). Moreover, fear of
humans may also decrease meat quality, such as tenderness
(Ferguson and Warner 2008; Probst et al 2012).
In dairy buffaloes the number of negative interactions
performed by stock-people was positively correlated with the
number of kicks by buffaloes during milking and with the

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number of exogenous oxytocin injections used to induce
milk let-down (Napolitano et al 2019). These results support
the hypothesis that the behaviour of stock-people and
buffaloes are related and indicate room for improvement
following appropriate stock-people training programmes.
Positive effects
In contrast, a positive relationship is notably
characterized by absence of fear reactions to humans and
animals that are easier to handle (Waiblinger et al 2006).
Positive interactions such as pats, gentle slaps or talking to
the animals showed positive effects reducing fear and human
avoidance. Also, among the interactions with humans that
can be perceived as positive, food provision is an efficient
way of attracting animals (Jago et al 1999; Tallet et al 2005;
Graml et al 2008a). Stockpersons with positive attitudes
towards animals often have animals with increased
productivity (Rushen and de Passillé 2015).
In Pigs
Human-animal interactions as short as
4h/sow/reproductive cycle, may influence both the
performance and welfare of the animals (Prunier and Tallet
2015). Janczak et al (2003) found that sows showing less fear
of humans had higher reproductive success and more
adaptive maternal behaviour.
According to Hemsworth et al (1994), human
recognition can happen in situations of intensive handling.
Intact males, that are commonly raised in stable groups in
some countries, when they were positively handled were
more socially active, both in their groups and with an
unfamiliar human (Tallet et al 2013).
In Poultry
Handling studies on poultry show that regular positive
gentle handling can enhance growth performance, feed
efficiency (Gross and Siegel 1982; Zulkifli and Siti Nor
Azah 2004), egg production (Barnett et al., 1994), disease
resistance to infection, antibody protection (Graml et al
2008a; Edwards et al 2010; Al-Aqil et al 2013) and first-
week survival (Cransberg et al 2000).
In adult laying hens, reduction in fear of humans and
a decrease in plasma corticosterone concentration were
shown following additional handling, consisting of walking,
talking, feeding and touching single birds (Barnett et al 1994;
Graml et al 2008a). Similarly, Edwards et al (2010) showed
for laying hens that 12 min/day of visual contact with
humans during rearing resulted in reduced avoidance
behaviour of humans during adulthood and there was a trend
for hens receiving positive handling to have a lower
corticosterone response to human contact than those
receiving negative handling. Visible human presence
associated with predictable approach, human voice, slow
movements and gentle handling for weighing, were effective
in inducing habituation to humans in laying hens (Bertin et al
2019).
Al-Aqil et al (2013) subjected broiler chicks to a
pleasant physical contact 30 sec/day from 1 to 28 days of age
and found that those chickens had lower
heterophil/lymphocyte ratios (h/l) and plasma corticosterone
levels than their neglected counterparts following road
transportation. Zulkifli et al (2002) suggested that allowing
broiler chickens to see the experimenter for 10 min twice
daily from 0 to 3 weeks of age, with no attempt to initiate
tactile interaction with the birds, was sufficient to alleviate
fear and stress reactions to handling and crating, and improve
their antibody response. In a study conducted by Zulkifli et al
(2004), some chicks were randomly caught, picked up and
stroked gently for 10 min twice daily, and other chicks were
picked up individually and stroked gently for 30 sec once
daily in their home pen. While positive visual contact had no
effect on performance, birds that were handled pleasantly
had improved body weight and feed conversion ratios.
In Cattle and Buffaloes
Hemsworth et al (1989b) reported that the
stockperson’s presence and positive handling during calving
of heifers led to faster approach to an experimenter in a test
situation, lower cortisol concentrations, and less stepping and
kicking responses during milking in the first weeks of
lactation than heifers that calved without human presence.
According to Ellingsen et al (2014), stockpersons who
handle their calves patiently, pet them and calmly talk to
them during handling, induce in their animals’ higher levels
of positive mood. The influence of gentle interactions on
weight gain in group-housed dairy calves has been studied by
Lürzel et al (2015). Gentle stroking in dairy cattle has been
shown to reduce heart rate increased during a veterinary
procedure (Schmied et al 2010). In addition, in beef cattle,
gentle touching at an early age seems to reduce the cortisol
release at slaughter (Probst et al 2012).
The HAR is also relevant for udder health. Ivemeyer
et al (2011; 2018) found that positive behaviour of
stockpersons during milking was associated with lower
somatic cell counts and with lower prevalence of mastitic
quarters.
As also observed in cattle, in dairy buffaloes the
number of positive interactions performed by stock-people
was positively correlated with milk production (Napolitano
et al 2019).
Factors affecting the quality of HAR
At least three aspects are important in affecting the
quality of HAR: 1) a genetic influence indicating the

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relevance of genetic selection, 2) the development of
husbandry practices that improve animal´s perception of
humans, sometimes by habituation (Boissy et al 2002; Faure
et al 2003) and 3) early positive human contact, that could
influence future emotional experiences in animals to
stressors when in the presence of humans.
Genetic influences
Genetic dispositions contribute to personality
differences, partly explaining differences in HAR within a
herd or between breeds (Andersen et al 2006). Stockpersons
deliberately or accidentally select tame animals for breeding
stock because they are easier to handle and manage (Price
and Orihuela 2010), and tameness heritability has been
estimated to be about 22 (Le Neindre et al 1995) to 38%
(Hemsworth et al 1990).
Lankin (1997) studied the behavior of 11 breeds of
sheep and concluded that breeds subjected to intensive
selection for commercial purposes were tamer toward
humans than breeds which had not been subjected to such
selection. Also, Lyons et al (1988) examined the tameness of
dairy goats toward humans, both within and between twin
sets. One sibling of each twin set was reared by the mother
while the other was hand reared. The tameness scores of the
hand-reared goats were better than for their dam-reared twin.
Habituation
In habituation, the animal´s fear of humans is
gradually reduced by repeated exposures in a neutral context,
when a person´s presence has no obvious reinforcement
properties (Price and Orihuela 2010). For example, Jones et
al (1993) found that domestic chicks showed decreased
avoidance of humans following twice daily exposures to
humans.
Similarly, Prado et al (2001) found that bucks raised
under semi-intensive conditions but habituated to the human
presence, became easier to train for semen collection using
an artificial vagina, than bucks raised under extensive
conditions, with little or no human presence.
Early contact
Positive human animal contacts and handling can
efficiently affect the quality of the relationship when the
interactions are conducted at a young age. Indeed, Le
Neindre et al (1996) found that young range-reared cattle
increased their tolerance of human presence if exposed to
human handling just after weaning.
Early tactile stimulation influences the postnatal
development of pigs (Tanida et al 1995; de Oliveira et al
2015). Early gentle contact with humans enhances approach
behaviour to human beings (Hemsworth et al 1986a). Piglets
whose back was stroked by humans for 2 min from 5 to 35
days of age, were less fearful in a novel environment and less
fearful of being handled by people (de Oliveira et al 2015).
Muns et al (2015) found that positive contact reduced the
duration of escape behaviour of piglets to tail-docking on day
15. Furthermore, according to Büttner et al (2018) positive
HAR (e.g. calm speech, petting, food provision), carried out
3 times/week by one person for 15 min in each pen during
the rearing period, can reduce the occurrence of tail-biting in
weaned piglets.
Several authors have showed that previous positive
handling may improve ease of handling later in life in several
species. For example, favoring ease of handling while
loading calves for transport (Lensink et al 2001), and
reducing fear related reactions at the abattoir in beef cattle,
which can be the reason for improved tenderness of meat
(Probst et al., 2012); reducing vocalizations in unfamiliar
environments (Boivin et al 2000; Tallet et al 2008), heart
rate, cortisol concentration (Tosi and Hemsworh 2002) and
flight distance in lambs (Markowitz et al 1998); and reducing
kicking in dairy cows during rectal palpation (Waiblinger et
al 2004) and fear of humans in chickens (Jones and
Waddington 1993).
Domestic horse foals showed less fear of humans if
they had contact with humans during their first 5 days of age,
even if they were just observing their mothers being fed by
hand and brushed (Hausberger et al 2008) or when exposed
to motionless humans (Henry et al 2006).
There is some evidence that mothers may be an
important social model, modulating or buffering the
behavioral and physiological responses associated with the
development of HAR in their young (Waiblinger 2017;
2019).
Final Considerations
We conclude that even with improved precision
farming and automation: a) a good HAR is still fundamental
to improve farm animal welfare with associated health and
production benefits and b) with the numerous tests assessing
fear of humans, many are not commercially applicable.
Conflict of Interest
The authors declare that there are no conflicts of
interest with this work.
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