Received: 18 November 2021 Revised: 26 November 2022 Accepted: 22 December 2022

DOI: 10.1111/asj.13809

RESEARCH ARTICLE

Effect of different odors on the fighting behavior of weaning

piglets after merging into a large pen

Weijie Zhao 1 | Na Yang 1 | Lei Zhu 2 | Yisheng Lin 3 | Qiman Zhang 3 |

Gang Shu 1 | Songbo Wang 1 | Ping Gao 1 | Xiaotong Zhu 1 | Lina Wang 1 |
Qingyan Jiang 1

1
Guangdong Provincial Key Laboratory of
Animal Nutrition Control, College of Animal Abstract
Science, South China Agricultural University,
In intensive pig production, the fighting behavior of weaning piglets after merging
Guangzhou, People’s Republic of China
2
Chuxiong Anyou Livestock Co., Chuxiong,
pens is relatively common. Fighting behavior not only easily causes injury in pigs but
People’s Republic of China also affects the production performance of pigs. To reduce fighting behavior in farms,
3
Guangdong Ruisheng Technology Group Co., this study aimed to explore the possible effect of odorous substances on piglet fight-
Ltd., Guangzhou, People’s Republic of China
ing behavior after merging into a large pen. Six different sprays were tested: original
Correspondence creamy, cheese flavor, orange flavor, truffle, vanilla and pigpen flavor. In each experi-
Xioatong Zhu, Lina Wang and Qingyan Jiang,
College of Animal Science, South China
ment, two groups were set (one odor-sprayed and no sprayed control), and 12 pigs
Agricultural University, Wushan Avenue, were used per group. After mixing, the frequency of occurrence of various piglet
Tianhe District, Guangzhou 510642, People’s
Republic of China.
behaviors in different pens was recorded. During this period, salivary cortisol levels
Email: xtzhu@scau.edu.cn, wanglina@scau.edu. and skin lesion scores were evaluated. As a result, the piglets sprayed with the origi-
cn and qyjiang@scau.edu.cn
nal creamy, cheese flavor and vanilla substances obtained significantly higher average
Funding information daily gain and feed intake and showed a significantly lower incidence of fighting
National Natural Science Foundation of China,
behavior, and the skin lesion score and salivary cortisol of piglets were also reduced
Grant/Award Numbers: 31672464, 31790411,
31828010 significantly. All the other odorous substances had no significant effects on the fight-
ing behavior and production performance of piglets.

KEYWORDS
cortisol, fighting behavior, odor substance, production performance, weaned piglets

1 | I N T RO DU CT I O N
In modern intensified pig raising farms, to save production costs,
weaning piglets from two or three litters are normally merged into
larger pens to improve the usage efficiency of pig pens. However, this
approach has resulted in a series of problems; one of the most promi-
nent problems is the increased fighting behavior of piglets. Fighting
behavior is the response to a conflict between individual animals for a
mating partner, food, space and other resource competition, which
usually consists of attack and escape (Weller et al., 2019). When
weaning piglets from different litters are mixed together, fighting is
significantly increased to establish a new hierarchy (Verdon
et al., 2019), which increases the risks of skin damage and stress (van
Nieuwamerongen et al., 2014).
Piglet fighting behaviors usually include any one or combination
of pushes, head knocks and bites (Samarakone & Gonyou, 2009). The
frequency and severity of aggression associated with the formation of
a dominance hierarchy appears to depend on a balance between
social experience and individual differences, such as size (Hsu
et al., 2006). Piglets that had been exposed to anise prenatally showed
aggression compared with those that had not been exposed prenatally
(Oostindjer et al., 2010). Indeed, numerous studies have shown that
social mixing induces an increase in piglets’ aggressive behavior
(Hötzel et al., 2004).

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https://doi.org/10.1111/asj.13809

2 of 9
It has been reported that fighting behavior can be caused by
genetic factors, individual differences and other external factors, such
as competition for food or a place of rest or play (Peden et al., 2018).
Fighting piglets usually make loud noises, have an elevated heart rate
(Geverink et al., 2003; Marchant-Forde et al., 2003), and show signifi-
cantly reduced average daily gain (D’Eath, 2002). Increased fighting
behavior reduces the feed conversion rate and has harmful effects on
piglets (Colson et al., 2012). On the one hand, weaned piglets that are
more aggressive have reduced performance, such as reduced food
conversion efficiency and decreased weight gain (Stookey &
Gonyou, 1994; Turpin et al., 2017). On the other hand, as fighting
increases, pig mortality and respiratory disease incidence increase,
and backfat thickness decreases (Janczak et al., 2003).
Numerous studies have shown that mixing unfamiliar pigs at
weaning leads to immediate severe fights that are necessary to build a
new hierarchy (Hwang et al., 2016). Pigs recognize each other mostly
by olfactory mechanisms. Research on maternal behavior during nest
leaving in free-ranging domestic pigs found that sows maintain con-
tact with newborn piglets by sniffing and humming (Ocepek &
Andersen, 2018). Nose-to-nose contact initiated by a sow or piglet
may represent the beginning of a mother-offspring relationship, and
shortly after the piglets are born, the mother and individual offspring
in the nest group will establish social relationships (Portele
et al., 2019). Additionally, it has been reported that piglets are most
attracted to the odors associated with maternal feces and skin secre-
tions (Morrow-Tesch & McGlone, 1990a). Piglets with different sow
odors fight when mixed (Kanaan et al., 2012). Piglet sensory systems
and odors from the sow’s udder were associated with piglet nipple
attachment (Morrow-Tesch & McGlone, 1990b). The sense of smell
mainly plays a priming role in eating behavior. It has been demon-
strated that odor exposure induces appetite specifically for food.
However, the influence of odors on food choice and intake is less
clear (Boesveldt & de Graaf, 2017). The recognition of each other by
piglets may influence fighting behaviors. Therefore, can interfering
with olfactory recognition of the pig effectively reduce fighting behav-
ior after weaning piglets?
Some studies have shown that salivary cortisol reflects
hypothalamic–pituitary–adrenal activity in response to different
stressors in pigs, and cortisol is a salivary biomarker associated with
aggression at weaning and stress in piglets (Escribano et al., 2019).
The skin lesion score is an important indicator of fighting after pigs
are mixed (Turner et al., 2006).
In the past, piglets were coated with sow feces or secretions dur-
ing the fostering process (Horrell, 1982). However, due to the smell of
feces and urine, this process was not well accepted by operators. In
addition, after merging, the piglets may come from sows with three lit-
ters or more. Interference with foreign odors is a method worth
exploring. To study the effect of different odor substances on the
fighting behavior and performance of piglets, six synthetic odorous
substances, including original creamy, cheese flavor, orange flavor,
truffle, vanilla and pigpen flavor, were used before mixing groups of
weaning piglets. Pigpen flavor was used to simulate the normal way
that was done in the pig farm. Feces and urine from one of the sows
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ZHAO ET AL.
were smeared on weaning piglets to make them smell the same.
Creamy and cheese are by products of milk and have a smell similar to
milk. They are often used as attractants in the feed of weaned piglets
and improve feed palatability (Seabolt et al., 2010), so original creamy
and cheese flavor were selected for testing. Additionally, pigs are sen-
sitive to the smell of truffles, and their sense of smell has been used
to find them in the forest (Lavelle et al., 2017). Vanilla was reported to
be used as an attractant for wild boar hunting (Campbell &
Long, 2008). Therefore, the flavors of truffles, vanilla and orange were
used because they are all from natural plants or fruits. They were used
as analogs to truffles. After mixing the groups, fighting, resting, feed-
ing, drinking, excreting, exploring, manipulating and climbing behaviors
of piglets in different pens were recorded. During this period, salivary
cortisol levels and skin lesion scores were evaluated.
2 | M A T E R I A L S A N D M ET H O D S
2.1 | Ethics statement
All animal experiments were conducted with the permission number
SYXK (Guangdong) 2014-0136. The experimental design and proce-
dures used in this study were reviewed and approved by Guangdong
Provincial Key Laboratory of Animal Nutrition Control, College of
Animal Science, South China Agricultural University, Guangzhou,
Guangdong, People’s Republic of China. All experiments were
conducted in accordance with “The Instructive Notions with Respect
to Caring for Laboratory Animals” issued by the Ministry of Science
and Technology of the People’s Republic of China.
2.2 | Reagents
Sprays were synthetic and purchased from Guangdong Ruisheng
Technology Co., Ltd. (Guangzhou, China), which are packaged in
hydraulic spray bottles, 550 ml per bottle (Table 1). Cortisol kits were
purchased from Beijing North Institute of Biotechnology (Beijing,
China).
2.3 | Animals and housing
In this study, 144 Seghers piglets, with an initial weight of approxi-
mately 9.23 ± 0.07 kg, half male and half female, were selected. Six
different sprays were tested: original creamy, cheese flavor, orange
flavor, truffle, vanilla and pigpen flavor. Each spray was tested sepa-
rately. For each experiment, four litters of weaning piglets (six
35-day-old piglets from each litter) were selected for the experiment.
Before mixing the groups, the piglets in each litter were first divided
into two groups: three piglets were sprayed with odor on the head
and neck for 3 s (approximately 1 ml per piglet), and the other three
piglets were not sprayed. Then, the piglets sprayed with odor from
four litters were merged into a large pen as the treatment group,
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ZHAO ET AL. 3 of 9

TABLE 1 Composition of sprays TABLE 2 Composition and nutrient levels of basal diets

Sprays Composition (%) Items Percentage (%)

Original Ethyl vanillin ≥1.0, vanillin ≥1.5, δ-Decalactone ≥1.0, Ingredients
creamy Ethyl Maltol ≥7.0, γ-Nonanolactone ≥6.0, Corn 52.84
Cinnamaldehyde ≥2.0, γ-Decalactone ≥2.0, butyric
acid ≥6.0 Soybean meal 14.71

Cheese Ethyl vanillin ≥1.5, γ-Octalactone ≥1.8, γ- Wheat bran 23.53

Nonanolactone ≥3.0, vanillin ≥10.0, δ-Decalactone Soybean 3.92
≥2.0, benzyl alcohol ≥8.0, butyric acid ≥7.0, ethyl Vitamin E 1
butyrate ≥3.0
Premix 4
Orange Sweet orange oil ≥0.5, β-ionone ≥0.5, Citral ≥1.0,
Ethyl butyrate ≥3.0, Octanal ≥3.0, decanal ≥6.0, Nutrient levels
Ethyl vanillin ≥3.0, ethyl Maltol ≥6.0 Digestible energy (DE, MJ) 13.69
Vanilla Fennel oil ≥0.5, cinnamon oil ≥0.1, Litsea cubeba oil Crude protein 20.6
≥0.5 Lysine 0.91
Benzyl alcohol ≥0.4, ethyl butyrate ≥3.0, β-ionone
≥0.5, thymol ≥3.0 Calcium 0.88

Truffle Benzaldehyde ≥2.8, α-Terpineol ≥0.1, ethyl vanillin Phosphorus 0.74

≥1.0, benzyl alcohol ≥10, oil of eucalyptus ≥0.1,
Cinene ≥0.1,
2-Undecanone ≥1.0
TABLE 3 Description of the behaviors of piglets
Pigpen Octanoic acid ≥0.6, Caproic acid ≥0.6, butyric acid
≥1.5, Type Description
Ethyl vanillin ≥5, vanillin ≥10, Fighting Reciprocal pushing, biting, head knocking, and
4-Methyl-5-beta-hydroxyethyl thiazole ≥0.5 chasing
Feeding Head in the feeder

whereas the other piglets without odor sprayed were also mixed in a Drinking Drinking water from waterer

large pen as the control group. The weaned piglets were housed in Excreting Defecating or urinating
4 m  4 m slatted floor pens with one feeder and two drinking nipples Resting Lying down, eyes are open or closed
in each pen. Light/dark cycles are provided by natural light. The tem- Exploring Standing, walking or not, sniffing the ground and/or
perature was controlled at 22–24 C. Ventilation is performed by a walls
ventilator at both ends of the pig house. The relative humidity of the Manipulating Nosing or chewing feeder, drinker, floor etc.
pigpen is 60%–75%. The diameter of the feeder is 60 cm. Climbing Forelegs on the back of another pig
For all treatments, food (Table 2) and water were supplied ad libi- Lying on Body weight not supported by the legs, at least 3
tum. All piglets were weighed when the groups were mixed and side legs extended on the side
10 days after mixing the groups. The weight of the feed was mea- Lying on Body weight is not supported by the legs, at least 3
sured every day. We calculated feed intake by weighing the feeder belly legs “crossed” under the piglet

before and after the piglets were fed. Sitting Body weight supported by buttocks and forelimbs

2.4 | Behavioral observations

Piglets were continuously video-taped during the 3 days after merging
into a large pen. Scan sampling was performed every 10 min between
08:00 and 18:00 to assess piglet posture and activity (60 scans/day/
treatment), as described in Table 3 (Colson et al., 2012). Afterwards,
we calculated the percentage of piglets engaged in one behavioral cat-
egory relative to the total number of observations. Cameras were pur-
chased from Sony China Corporate (HDR-XR160E).
2.5 | Cortisol measurement
Saliva was collected from three piglets in each pen at 10:00 on Days
1–3. Before saliva collection, the feeders were removed from the pen
to reduce the residual food in the mouth of piglets. The piglet chewed
a piece of gauze until it was drenched. The wettest part was cut and
placed into a glass syringe, and the extruded saliva was collected into
2 ml centrifuge tubes. Experimenters use tweezers to hold the gauze
and put it to the pig’s mouth to wait for chewing. In addition, experi-
menters did not touch the piglets. Experimenters wore gloves when
handling the gauze. After centrifugation (10,000 rpm, 10 min), the
saliva was collected and stored at 20 C until analysis. Then, saliva
was used for further analysis of cortisol according to the instructions
of the manufacturer (radioimmunoassay). According to the manufac-
turer’s instructions, the cortisol kit passed ISO 9001 quality manage-
ment system certification. Because the amount of saliva collected by
each pig was similar, the concentration of cortisol was not corrected
for the amount of saliva that was collected.
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4 of 9 ZHAO ET AL.

2.6 | Skin lesion score
The skin lesion score was analyzed as previously described (Nicolaisen
et al., 2019). On the fourth day after mixing the groups, three piglets
were selected from every pen, 36 piglets in total were observed, and
the number of new wounds and new scars on the head, ears, neck,
shoulders, buttocks, tail and other parts of the body was recorded
during the test. Each pig was evaluated by three people. Observers
were blinded to the treatment of the piglets. The severity of the
lesions was scored using a categorical classification ranging from 0 to
4 as the severity increased: a score of 0 corresponded to no lesions,
1 corresponded to ≤5 superficial lesions (scratches), 2 corresponded
to 6–10 superficial lesions or ≤5 deep lesions (evidence of hemor-
rhage), 3 corresponded to 11–15 superficial lesions or 6–10 deep
lesions, and 4 corresponded to ≥16 superficial lesions or >10 deep
lesions.
2.7 | Statistical analysis
GraphPad Prism 8.0 was used for statistical analysis. Each experiment
was independent, which means that only the control group and one of
the treatment groups were compared each time, so comparisons were
performed using t tests and chi-square tests, with p < 0.05 represent-
ing a significant difference.
vanilla substances had significantly difference in the proportion of
behaviors (Figure 1). In these group, the piglets fighting behavior
decreased significantly (Table 4).
3.2 | Feeding behaviors and production
performance
No significant difference in the frequency of occurrence of eating,
drinking and excreting was observed in piglets in different pens
(Figure 2a–c). However, compared with control piglets, the piglets
sprayed with the original creamy, cheese flavor and vanilla substances
had significantly increased average daily gain (control 154.34 ± 4.59 g/
day vs. original creamy 216.00 ± 5.11 g/day, control 152.84 ± 2.17 g/
day vs. cheese 181.33 ± 1.36 g/day, control 152.08 ± 5.93 g/day
vs. vanilla 170.64 ± 4.95 g/day, Figure 2d) and feed intake (control
389.23 ± 5.05 g/day vs. original creamy 412.13 ± 8.57 g/day, control
344.72 ± 5.10 g/day vs. cheese 403.61 ± 7.14 g/day, control 389.15
± 8.89 g/day vs. vanilla 396.68 ± 10.68 g/day, Figure 2e) and signifi-
cantly decreased feed-gain ratio (control 2.52 ± 0.12 vs. original
creamy 1.91 ± 0.14, control 2.26 ± 0.11 vs. cheese 1.95 ± 0.2, control
2.56 ± 0.22 vs. vanilla 2.32 ± 0.08).
3.3 | Resting behaviors and posture

The frequency of occurrence of resting behavior in piglets from differ-

3 | RESULTS ent pens was not significantly different (Figure 3a). There was no
impact of treatment on the proportion of sitting (Figure 3b), lying on
3.1 | Observed behavior in each group the back (Figure 3c) or lying on the belly (Figure 3d).

The videos of piglet behaviors were analyzed, and the data analysis
were conducted with chi square test (Table 4 and Figure 1). The per-
centage of piglets engaged in one behavioral category relative to the
total number of observations were calculated. Compared with control
piglets, the piglets sprayed with the original creamy, cheese flavor and
3.4 | Aggressive and stress
Observations of piglet fighting behavior showed that after the pig-
lets were sprayed with the original creamy, cheese flavor and vanilla

TABLE 4 Contingency table of observed behavior in each group

Fighting Eating Drinking Excreting Resting Exploring Manipulating Climbing

Control 34 100 16 10 481 55 14 10
Original creamy 10 107 20 11 495 52 16 9
Control 30 93 17 10 492 55 14 9
Cheese 9 118 19 11 494 45 18 6
Control 25 105 17 11 471 46 17 10
Orange 25 111 19 11 477 42 19 9
Control 35 115 17 6 479 40 18 10
Vanilla 11 111 15 12 496 46 20 9
Control 24 106 14 10 476 59 19 10
Truffle 24 97 14 11 476 62 20 11
Control 25 106 13 12 481 54 15 11
Pigpen 26 106 13 10 492 47 15 10
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ZHAO ET AL. 5 of 9

F I G U R E 1 Observed behavior in
each group. Asterisk (*) means the two
group had significantly difference in the
proportion of behaviors. p < 0.05, versus
the control group

F I G U R E 2 Effect of spraying piglets with different substances on feeding behaviors and production performance after merging into a large
pen. (a–c) Proportion of eating, drinking and excreting behavior after piglets were sprayed with different substances. (d) Average daily gain of
piglets sprayed with different substances. (e) Average daily food intake of piglets sprayed with different substances. (f) Feed-gain ratio of piglets
sprayed with different substances. The figure shows the results of six independent experiments. In each experiment two treatments were
compared (one odor-sprayed and no sprayed control), and 12 pigs were used per treatment. *p < 0.05, **p < 0.01 versus the control group

substances, their fighting behavior decreased significantly decreased in the original creamy group, cheese group and vanilla
(Figure 4a). The skin lesion score of the piglets in these groups was group compared with the control group (Figure 4c). The other
also reduced significantly compared with that of piglets in the con- behaviors were not significantly different among the groups
trol group (Figure 4b). Additionally, salivary cortisol was significantly (Figure 4d–f).
 17400929, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/asj.13809 by College Of Veterinary & Animal Sciences, Pookode, Kerala, Wiley Online Library on [16/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 of 9 ZHAO ET AL.

F I G U R E 3 Effect of spraying piglets

with different substances on resting
behaviors and posture after merging into
a large pen. (a) Proportion of resting
behavior after piglets were sprayed with
different substances. (b–d) Proportion of
different resting behaviors (siting, lying on
the belly and lying on the side) after
piglets were sprayed with different
substances. The figure shows the results
of six independent experiments. In each
experiment, two treatments were
compared (one odor-sprayed and no
sprayed control), and 12 pigs were used
per treatment.

F I G U R E 4 Effect of spraying piglets with different substances on aggression and stress after merging into a large pen. (a) Proportion of
fighting behavior after piglets were sprayed with different substances. (b) Skin lesion score after piglets were sprayed with different substances.
(c) Salivary cortisol levels after piglets were sprayed with different substances. (d–f) Proportion of exploring, manipulating and climbing behaviors
after piglets were sprayed with different substances. The figure shows the results of six independent experiments. In each experiment, two
treatments were compared (one odor-sprayed and no sprayed control), and 12 pigs were used per treatment. *p < 0.05, **p < 0.01 versus the
control group

ZHAO ET AL.
4 | DISCUSSION
Fighting behavior is common in swine husbandry, especially during
regrouping after weaning, which may be one of the most serious and
common causes. Piglets have to adapt to the new environment and
new feeding regimes and establish new social hierarchies (Fels
et al., 2014). Therefore, the piglets will exhibit some behavioral
changes. For example, after regrouping, piglets may show fighting or
submissive behavior to cope with stress (Sun et al., 2017). Addition-
ally, salivary cortisol is often used to assess animal welfare (Morrison
et al., 2007). In another study, piglets with low salivary cortisol levels
were less aggressive than those with high salivary cortisol levels
(Clouard et al., 2016). In our study, salivary cortisol was significantly
decreased in the original creamy group, cheese group and vanilla
group compared with the control group; at the same time, piglet fight-
ing behavior was decreased significantly in these groups. Fighting
behavior among piglets is an important factor leading to skin damage.
Other studies have shown that scented toys can reduce skin damage
and fighting behavior in weaned piglets (Guy et al., 2009). Our results
showed that the skin lesion score of the piglets in these groups was
also reduced significantly compared with that of piglets in the control
group. In other studies, the rest behavior of the piglets in the control
group was approximately 70%, which was consistent with our study,
and the proportion of other behaviors was relatively small, which was
roughly the same as our results (Colson et al., 2012; D’Eath, 2002).
In our study, as we expected, milk-related original creamy and
cheese flavor showed a significant effect. This suggests that the famil-
iar milk-related smell during sucking can reduce weaning stress and
fighting between piglets. It has been reported that neonatal rats pri-
marily use olfaction for attachment and prefer the smell of milk
(Zimmerberg et al., 2009). In another study, pain was relieved in
human newborns when they were exposed to odors from their
mother’s milk (Nishitani et al., 2009). Other studies have shown that a
few essential oils are currently in use as aromatherapy agents to
relieve anxiety, stress, and depression (Herz, 2009). Popular anxiolytic
oils include lavender, rose, orange, bergamot, lemon, sandalwood,
clary sage, Roman chamomile, and rose-scented geranium
(Setzer, 2009). However, there are no reports on the effects of vanilla
flavor. Its mechanism needs further study.
Olfactory information is essential for a wide range of animal
behaviors, including navigation, foraging, predator aversion, kin recog-
nition, bond formation, mate selection, and sexual and parenting
behaviors (Brennan & Keverne, 2004). In another study, piglets were
released an olfactory cue (perhaps adrenal in origin) toward the end of
a fight to signal submission (McGlone, 1985). In addition, the influence
of smell on fighting behavior is not only manifested in pigs. Other
studies have shown that the main olfactory epithelium signaling path-
way was injured, and mice failed to mate or fight (Mandiyan
et al., 2005). Male hamsters appear to use familiarity with a former
opponent’s odors to adaptively regulate their responses to variations
in social threat (Petrulis et al., 2004). In recent years, evidence has
emerged that chemosignals affect humans’ social interactions, danger
detection and risk-taking behavior, social aspects of eating, and
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7 of 9
performance under stressing conditions (Calvi et al., 2020). In sum-
mary, spraying the piglets with odorous substances probably elimi-
nated the differences in their individual odors and increased the
mutual recognition and familiarity of piglets with the new environ-
ment and other piglets, thereby effectively reducing the occurrence of
fighting behaviors and improving production performance. Therefore,
our research results can be applied to production to reduce weaning
piglet fighting behavior.
In conclusion, the original creamy, cheese flavor and vanilla sub-
stances can significantly reduce the fighting behavior of piglets after
merging into a large pen and improve production performance.
ACKNOWLEDG MENT
This work was supported by the National Natural Science Foundation
of China (31672464, 31790411 and 31828010).
CONFLICTS OF INTEREST
The authors declare no conflicts of interest.
ORCID
Weijie Zhao https://orcid.org/0000-0002-7373-350X
Lina Wang https://orcid.org/0000-0001-8133-3349
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