T ansla ional Animal Science, 2024, 8, xad134
h ps://doi.o g/10.1093/ as/ xad134
Ad ance access publica ion 8 Decembe 2023
Mea Science
Recei ed Ap il 26, 2023 Accep ed Decembe 7, 2023.
Does anspo s ess ha e any e ec on ca cass quali y o
Nello e ca le (Bos au us indicus) in B azil? — A case s udy
Na halia da Sil a Rod igues Mendes†,‡, Rena o Rod igues Sil a||, Ta ianne Fe ei a de Oli ei a†,
Ma ie-Pie e Ellies-Ou y‡,$, Jean-F ançois Hocque e‡, Sghaie Ch iki‡,¶,1,
†Depa men o Food Science and Technology, School o Ag onomy, Fede al Uni e si y o Goiás-UFG, Campus Samambaia, CEP 74690-900,
Goiânia, B azil
‡Ins i u Na ional de Reche che pou l’Ag icul u e, l’Alimen a ion e l’En i onnemen (INRAE), Uni e si é Cle mon Au e gne, Ve Ag o Sup,
UMR He bi o es, UMR1213, Reche ches su les He bi o es, Theix, 63122 Sain -Genès Champanelle, F ance
||Depa men o Ins i u e o Ma hema ics and S a is ics, Fede al Uni e si y o Goiás, Goiânia, B azil
$Depa men o Feed and Food, Bo deaux Sciences Ag o, CS 40201, 33175 G adignan, F ance
¶ISARA, CEDEX 07, 69364 Lyon, F ance
1Co esponding au ho : [email p o ec ed]
Abs ac
Wi h he inc easing concomi an demands o B azilian bee and in pa icula high-quali y bee , he e is a need o obse a ional s udies o he
e ec s o p e- and pos -slaugh e p ac ices on bee ca cass ai s. We hypo hesized in ou case s udy ha p e-slaugh e anspo o bo ines o e
signi ican dis ances would induce s ess in animals, and ha his would educe ca cass quali y because o highe pH esul ing om long-dis ance
anspo a ion. To es his hypo hesis, 30,230 Nello e ca casses om a p i a e slaugh e house we e e alua ed 24 h pos mo em. Analysis
showed co ela ions be ween animal ma u i y, ul ima e pH, dis ance, and ca cass weigh . Mo e p ecisely, he e was a sligh posi i e co ela ion
be ween ul ima e pH and weigh (bu no wi h anspo a ion dis ance) and a sligh posi i e co ela ion be ween ma u i y and weigh . A linea
eg ession model (R2 = 0.016) ailed o show dis ance ha ing a signi ican e ec on ul ima e pH (P = 0.63), while ca cass weigh signi ican ly a -
ec ed ul ima e pH (P < 0.001) wi h a low coe icien o 0.0003. Ma u i y nega i ely a ec ed ul ima e pH also (P < 0.001) bu wi h also a small
e ec (−0.0008). Resul s ( om 95% con idence in e als o a iance o he andom e ec s and o he andom e o s) showed ha he a iabili y
wi hin a ms was highe han be ween a ms. The linea mixed model showed ha ma u i y had a signi ican e ec on ca cass weigh alue
(P < 0.001) wi h a la ge coe icien o 2.90. The R2 o he linea mixed model was 46.03%. In conclusion, while weigh and ma u i y bo h a ec
ul ima e pH, long dis ances did no signi ican ly impac ul ima e pH and he e o e he bee quali y om Nello e ca le. This could be because o
low s ess du ing anspo , as well as he physical cha ac e is ics o he Nello e b eed ha a o g ea e esis ance o opical clima ic condi ions.
Lay Summa y
Wi h he inc easing concomi an demands o B azilian bee and o high-quali y bee , he e is a need o obse a ional s udies o he e ec s o
p e- and pos -slaugh e p ac ices on bee ca casses. In ou case s udy, we hypo hesized ha p e-slaugh e anspo o bo ines o e signi ican
dis ances would induce s ess in animals and ha his s ess would educe ca cass quali y because o he highe pH which would esul om
long-dis ance anspo a ion. To es his hypo hesis, 30,230 Nello e ca casses om a p i a e slaugh e house we e e alua ed 24 h pos mo em.
Analysis showed co ela ions be ween animal ma u i y, ul ima e pH, dis ance, and ca cass weigh . Mo e p ecisely, he e was a sligh posi i e
co ela ion be ween ul ima e pH and weigh (bu no wi h anspo a ion dis ance) and a sligh posi i e co ela ion be ween ma u i y and weigh .
S a is ical analysis showed ha he a iabili y wi hin a ms was highe han be ween a ms. In conclusion, while ca cass weigh and ma u i y
bo h a ec ul ima e pH, long dis ances did no signi ican ly a ec ul ima e pH, and he e o e had no signi ican e ec on he quali y o bee om
Nello e ca le. This could be because o low s ess du ing anspo , as well as he physical cha ac e is ics o he Nello e b eed ha a o g ea e
esis ance o opical clima ic condi ions.
Key wo ds: animal s ess, bee , ca cass ai s, ea ing quali y
In oduc ion
Bee ea ing quali y is an in insic quali y ai , which depends
on bo h p e- and pos -slaugh e ac o s (Liu e al., 2022;
Pogo zelski e al., 2022). The main a ibu es used o cha ac-
e ize bee ea ing quali y a e la o , juiciness, ende ness, and
o e all liking. These desc ip o s appea o be highly a iable
and dependen on many in e ac ing ac o s ha a e di icul
o manage, such as he an emo em p ope ies (b eed, age,
ma u i y, ca cass a le el, a y acid composi ion o cu s, e c.)
and he pos mo em elemen s (slaugh e p ocesses, such as
ca cass handling, aging, and s o age (De lin e al., 2017)).
P io o slaugh e , animals a e exposed o si ua ions ha can
igge s ess esponses, which can educe he senso y quali y
o he mea (G ube e al., 2010).
An obse a ional case s udy would be able o de e mine
whe he anspo ime migh be a signi ican sou ce o s ess.
Fo he pu poses o his pape , anspo ime means he o al
ime ha an animal is con ined in a ehicle wi hou ood,
© The Au ho (s) 2023. Published by Ox o d Uni e si y P ess on behal o he Ame ican Socie y o Animal Science.
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2Mendes e al.
wa e , o es o anspo i om he a m o he slaugh e -
house. This includes ime spen wai ing o depa a e loading,
ime in ansi , and s a iona y pe iods, as well as wai ing o
o -load (Schwa zkop -Genswein e al., 2012). T anspo
ime can be signi ican in la ge coun ies such as B azil, whe e
li es ock a e o en anspo ed long dis ances om a m o
slaugh e house, which may be loca ed in ano he pa o he
coun y. B azilian legisla ion, No ma i e Ins uc ion 09/2021,
allows a maximum o 12 h con inuous anspo a ion be-
o e equi ing a es s op o ood and wa e (B azil, 2021).
Imp ope handling du ing anspo and a he slaugh e -
house can lead o muscle glycogen deple ion, inadequa e acid-
i ica ion, and high ul ima e pH. This esul s in da ke mea ,
wi h lowe senso ial p ope ies, especially ende ness (G ube
e al., 2010), juiciness, and la o (Hemswo h e al., 2011).
Fo example, i is well known ha an ul ima e pH highe han
6 be ween 12 and 48 h pos mo em esul s in da k mea cu s
(a de ec known as da k, i m, and d y [DFD]) wi h a sho e
shel li e because o inc eased suscep ibili y o mic obial con-
amina ion (Pé ez e al., 2013). Howe e , mos s udies o he
e ec s o anspo ime on bee quali y ha e been conduc ed
using Bos au us au us ca le ea ed and anspo ed in sys-
ems di e en om hose used in B azil (Ma ia e al 2003;
Gonzalez e al., 2012 a,b; Chulayo e al., 2016; Polkingho ne
e al., 2018), whe e zebu ca le, which a e cha ac e ized by
a mo e eac i e empe amen , p edomina e (Cooke e al.,
2020). Zebu bee is ypically less ende wi h less ma bling
han ha o au ine ca le (Bos au us au us), pa icula ly
when compa ed o he Angus b eed (Seideman e al., 1982;
De And ade e al., 2020).
In o ma ion on he e ec s o anspo imes on he quali y
o mea om zebu ca le is s ill sca ce, as he e ha e only been
a limi ed numbe o s udies o hese animals, and mo eo e ,
only in he no he n and sou he n egions o B azil (Fe ei a
e al., 2006; Mendonça e al., 2018; Lace da e al., 2022).
E en hough he cen al-wes e n egion is unques ionably im-
po an o he B azilian bee indus y (ABIEC, 2022) s udies
o he e ec s o anspo ime in his i ally impo an egion
on bee quali y a e lacking.
We hypo hesized ha p e-slaugh e anspo o bo ines
causes s ess o he animals, and esul s in ca casses o
lowe quali y wi h a highe inal pH because o ha s ess.
Consequen ly, he aim o his obse a ional case s udy was o
in es iga e he e ec s o s ess du ing anspo be ween a m
and slaugh e house, speci ically on ul ima e pH o Nello e
ca le, while con olling o ho ca cass weigh and ma u i y.
Ma e ial and Me hods
Ins i u ional Animal Ca e and Use Commi ee
(IACUC)
This slaugh e house is egula ed by he B azilian Fede al
Inspec ion Se ice (S.I.F 2872).
A icle 110 o he Regulamen o Indus ial e Sani á io de
P odu os de O igem Animal - RIISPOA (B azilian Indus ial
and Sani a y Regula ion o Animal P oduc s), equi es
ha ca le be gi en a es pe iod and wa e . Fas ing in he
slaugh e house pens o 24 h p io o slaugh e . P e-ha es
handling con o med o good animal wel a e p ac ices wi h
slaugh e p ocedu es ollowing he Sani a y and Indus ial
Inspec ion Regula ion o Animal O igin P oduc s (B asil,
2004, 2021). These documen s a e he Animal Mo emen
Pe mi and he a me ’s decla a ion o ha ing ollowed he
s anda d and expec ed p o ocols (B asil, 2021). Slaugh e
condi ions con o med o adi ional o Halal p ocedu es
(CIBALLAHAL, 2022).
Da ase
We used a da a se p o ided by a p i a e company loca ed in
Inhumas (Goiás, B azil) (49°28ʹ14.84ʹʹW and 16°20ʹ31.42ʹʹS).
This slaugh e house can p ocess up o 700 ca le pe day (80
o 90 animals/h) and is egula ed by he Fede al Inspec ion
Se ice (S.I.F. 2872). The clima e in his egion is opical wi h
an a e age annual empe a u e o 23.1 °C wi h an a e age
ain all o 1,516 mm wi h a Hea Index in Inhumas o 22%
(B asil, 2022).
The ainy season is equen ly cloudy and o e cas ; he
d y season is almos always cloudless. Th oughou he yea ,
empe a u es gene ally ange om 16 o 32 °C and a ely all
below 13 °C o abo e 36 °C (B asil, 2022).
The company pu chases animals om di e en a eas
o he s a e o Goiás, and main ains hem wi hin a p o-
duc ion sys em ypical o his egion, i.e., a pas u e-based
opical condi ions sys em. These animals a e ep esen a-
i e o he bee ca le ea ed in cen al-wes e n B azil. P e-
ha es handling con o med o good animal wel a e p ac ices
and slaugh e p ocedu es and ollowed he Sani a y and
Indus ial Inspec ion Regula ion o Animal O igin P oduc s
(B asil, 2004) and Technical Regula ions o P e-slaugh e
Managemen and Humane Slaugh e and he s un me hods
au ho ized by he Minis y o Ag icul u e, Li es ock and
Supply (BRASIL, 2021).
The da a se o he pe iod om Janua y o Augus 2021
has 35,126 eco ds o bee ca cass ai s such as b eed
(Nello e o C ossb eed), ca ego y (Bull, Cow, Du ch bull,
Du ch cow, Hei e , Ma uco ox, Tau us), con o mi y, ma-
u i y (age), ca cass weigh , and ul ima e pH. Ca ego ies
a e based on age and sex and can be u he classi ied in o
cal es o hei e s, hei e s, o bullocks, which in u n may be
cas a ed o whole, as well as cows o bulls o slaugh e .
Con o mi y e e s o he s anda ds o which his mea should
be p ocessed o he ma ke o which i is in ended. Du ing
he pe iod in which his s udy was conduc ed, he mea
ollowed he s anda ds es ablished o he ollowing coun-
ies: B azil, China, and Halal consume s’ coun ies (I an and
Saudi A abia) Cen al Islâmica B asilei a De Alimen os Halal
(CIBALLAHAL, 2022).
Ma u i y (age) was de e mined by den i ion: milk ee h (up
o 20 mo), wo ee h (21 o 24 mo), ou ee h (25 o 30 mo),
six ee h (31 o 41 mo), and eigh ee h (42 mo o abo e).
Following he pos -ha es and head inspec ion, he numbe
o pe manen inciso s was eco ded o each Nello e bull. A
pai o ee h was conside ed o be p esen when ei he oo h
o a pai had pene a ed he gum. Ca cass weigh e e s o he
edible po ion a e slaugh e , which is composed o mea , a ,
and bones, and is measu ed in kilog ams (kg). The ul ima e
pH was measu ed wi h a pH-me e (AK103 - Akso P odu os
Ele onicos L da) in he Longissimus ho acis muscle a 13 h
ib o he le hal o he ca cass a pa allel poin s in he same
sec ion, and 24 h pos -slaugh e . Wi h ega d o ca cass em-
pe a u e and amb,ien empe a u e, he slaugh e house ma u-
a ion sys em a ies acco ding o ma ke : Chile equi es 2 o
4 °C o 24 h om 10 °C ambien , while U uguay and o he
coun ies equi e 4 °C o 24 h om 10 °C ambien . B azil’s
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T anspo s ess on Nello e ca le ca cass quali y 3
s anda ds o ca cass empe a u e consis o a minimum o 2
°C and a maximum o 5 °C 24 h a e slaugh e om 10 °C
ambien .
In addi ion, animals we e e alua ed acco ding o a in-
ishing, which was pe o med isually using a 9-poin scale
wi h sco es om 1 o 9 (1 - absen a ; 2,3,4 - sca ce; 5,6,7 -
medium; 8 - uni o m, and 9 - excessi e a ). The dis ance om
a m o slaugh e house is gi en in kilome e s, wi h each 100
km co esponding o 1 h 30 min d i ing ime.
The numbe s o he di e en modali ies o he a iables
a e shown in Table 1. We s a ed wi h 35,126 eco ds o bee
ca casses. O hese, 99.28% we e Nello e b eed, 97.18%
bulls non-cas a ed, 98.99% Halal, and 89.14% a in-
ishing. Res ic ing ou a ge popula ion o Nello e bulls
wi h Halal con o mi y and a e a inishing, meaning 30,230
ca casses, educed he numbe o po en ial con ounding
a iables (Table1). Because o he la ge sample size, each o
he a iables s udied can ha e signi ican e ec s, bu his was
minimized by ocusing on ul ima e pH and he a iables o
in e es , i.e., a dis ance be ween a m and slaugh e house,
ca cass weigh , and ma u i y. Fo his eason, ou sample is
limi ed o ul ima e pH, dis ance om a m o slaugh e house,
ca cass weigh and ma u i y as shown in Table 2.
Slaugh e P ocess and Condi ions
The company ollows egula ly inspec ed p ocedu es o
slaugh e ing animals (B asil, 2004). Animals a e p ocessed
o slaugh e only a e documen s accompanying he lo a e
inspec ed. These a e he Animal Mo emen Pe mi and he
a me ’s decla a ion o ha ing ollowed he s anda d and
expec ed p o ocols. Bo h d i e s and s ockya d s a ha e
been ained in animal wel a e. Animal lo s a e sepa a ed
by o igin. A e unloading, he li es ock ucks a e washed
and disin ec ed. The animals es and a e gi en wa e o a
leas 6 h be o e slaugh e ing. Animals app o ed o slaugh e
pass h ough a sp ay ba h o p essu ized hype -chlo ina ed
wa e . Slaugh e condi ions a e con o med o adi ional o
Halal p ocedu es. A e his, an assis an om he Inspec ion
Se ice de e mines he age o he animals using den i ion and
hen s amps he ca cass wi h i s age g oup. The hal -ca casses
a e g aded o a inishing, absence o p esence o b uising,
sex, and weigh . A e he hal -ca casses a e s amped by he
Fede al Inspec ion Se ice, hey a e weighed and aceabili y
labels a e applied o he hindqua e , o equa e , and lank.
The hal -ca casses a e washed wi h je s o p essu ized wa e
o emo e bone agmen s and blood clo s, hen, hey a e
placed in chille s suspended by he Achilles endon a +4 ± 1
°C o unde go ma u a ion a e a pH d op. A e chilling,
he hal -ca casses a e classi ied by ul ima e pH (see sec ion
“Ins i u ional Animal Ca e and Use Commi ee (IACUC)”).
S a is ical Analysis
The da a we e analyzed using R so wa e ( e sion 4.1.2 - R
Co e Team, 2022). A e desc ip i e analysis, a box plo ac-
co ding o DuToi e al. (2012). Median alues a e indica ed
by he line wi hin he box plo . The box ex ends om he
25 h o 75 h pe cen iles and whiske s indica e he minimum
and maximum alues. Analysis o Va iance (ANOVA) was
pe o med using he ao () unc ion o de e mine he signi i-
can di e ences be ween ca cass cha ac e is ics.
Pea son co ela ion was calcula ed wi h he ggplo 2
package using he “pai s.panels’‘ unc ion.
P incipal Componen Analysis (PCA) was pe o med using
he package “Fac oMineR” o ep esen and model mul idi-
mensional poin cloud da ase s, showing whe he ela ionships
exis be ween he s udied a iables. PCA allows o he calcu-
la ion o new a iables, called p incipal componen s, which
cap u e he a iabili y in he da a. This enables in o ma ion o
be desc ibed wi h ewe a iables han o iginally p esen . The
p incipal componen s a e linea combina ions o he o iginal
a iables. The i s p incipal componen is he combina ion o
a iables ha explains he g ea es amoun o a iabili y in
he da a. The second and subsequen p incipal componen s
desc ibe he maximum amoun o emaining a iabili y and
Table 1. P o iles o ca casses based on b eed, ca ego y, a inishing and
con o mi y
Pa ame e Value n1%
B eed C ossb eed 253 0.72
Nello e 34,873 99.28
Ca ego y Bull 34,135 97.18
Cow 610 1.74
Du ch bull 79 0.23
Du ch cow 8 0.02
Hei e 173 0.49
Ma uco ox 48 0.14
Tau us 73 0.21
Fa inishing Excessi e 6 0.08
Medium 3,748 10.67
Ra e 31,311 89.14
Uni o m 61 0.17
Con o mi y2B azil 1 0.003
China 350 1.00
Halal 34,775 99
1Numbe o ca casses.
2The s anda ds acco ding o which his mea should be p ocessed o i s
in ended ma ke .
Table 2. Raw alues o mean, s anda d de ia ion (SD), coe icien o a ia ion (CV), minimum, and maximum o he measu ed ai s o ou s udied
popula ion o 30,230 ca casses
Mean SD CV (%) Minimum Maximum
Ul ima e pH 5.75 0.07 1.22 5.0 6.04
Dis ance, km 203 115.59 57.44 10 547
Time, h 3 1.73 57.44 0.15 8
Ca cass weigh , kg 298.9 34.14 11.41 150.5 553
Ma u i y, mon hs 203 1.97 48.47 0 8
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4Mendes e al.
mus be independen (o hogonal) be ween hem and o he
i s p incipal componen (Husson e al., 2016).
Mul i a ia e Reg ession Models we e de eloped by using
he “lm” (linea model) unc ion and “lm.be a” R Package
(Beh end , 2014). The linea eg ession models we e ca ied
ou o s udy he ela ionship be ween pH and explana o y
a iables such as ca cass weigh , ma u i y (age), and dis ances
as ollows:
yi=β0+β1xi1+β2xi2+β3xi3+i,
whe e
yi
ep esen s he i h measu ed pH on he bee ca cass,
β0
is he in e cep ,
β1,β2,β3
a e he eg ession coe icien s,
xi1
ep esen s he i h ca cass weigh ,
xi2
ep esen s he phys-
iology animal ma u i y e alua ed on ca cass ( his pa ame e
being highly co ela ed o ch onological age),
xi3
ep esen s
he i h a m and
i
he andom e o .
We i ed a mixed model o analyze i he ca cass pH a -
iance wi hin he a ms was highe han be ween he a ms.
Mixed-e ec models a e used o desc ibe ela ionships be-
ween a esponse a iable and some o he co a ia es in da a
when g ouped acco ding o one o mo e classi ica ion ac o s.
Examples o such g ouped da a include longi udinal da a,
epea ed measu es da a, mul ile el da a, and block designs.
By associa ing common andom e ec s wi h obse a ions
sha ing he same le el o a classi ica ion ac o , mixed e ec s
by g ouping he da a by g ouping he da a models lexibly
ep esen he co a iance s uc u e induced by he g ouping o
he da a (Pinhei o and Ba es, 2000).
The s a is ical model can be exp essed as ollows:
yij =µ+bi+ij,
Whe e
yij
ep esen s he ij h pH measu ed on i h a m and j h
ca cass,
µ
is he in e cep ,
bi
is he andom e ec o i h a m
and
ij
he andom e o .
Addi ionally, we i ed a mixed o model he ca cass weigh
in unc ion o ma u i y using he a m as a andom e ec . The
model was he ollowing:
yij =β0+β1xi+bi+ij,
whe e
yij
ep esen s he ij h weigh measu ed on i h a m and j h
ca cass,
β0
is he in e cep ,
β1
is he s aigh slope,
xi
ep esen s
he ma u i y (age) e alua ed on i h a m,
bi
is he andom e -
ec o i h a m and
ij
he andom e o . Con idence in e als
o he andom e ec a iance ep esen he ul ima e pH a -
iabili y be ween a ms, and con idence in e als o andom
e o ep esen he ul ima e pH a iabili y wi hin a ms. Fo
his model, he likelihood a io es was pe o med o assess
he signi icance o he andom e ec in he model. The alue
o R2 was calcula ed using he sq lib a y. All compu a ions
ela ed o i ing mixed models we e done using he nlme R
package (Pinhei o and Ba es, 2022).
Resul s and Discussion
Desc ip i e Analysis
The pH dis ibu ion is le -skewed and has low a iabili y
(Figu e 1a), wi h a coe icien o a ia ion o 1.22% (Table
2) and an in e qua ile ange less han 0.1. I can be seen ha
he median alue is 5.75 and he e o e 50% o he samples
ha e pH alues less han 5.75. The i s qua ile 25% is o
has an ul ima e pH alue o less han 5.71, and he hi d
qua ile 75% has is o ul ima e pH alues highe han 5.79.
The box plo shows many ou lie s which a e easily de ec able
which con as s wi h he low sample a iabili y o ul ima e
pH (Figu e 1b). This may be because o echnical p oblems
(pH-me e calib a ion, o ins ance), ope a o e o , biological
p oblems in speci ic ca casses, and so on. I is wo h no ing
ha he emo al o ou lie s does no signi ican ly a ec hese
esul s, gi en he la ge sample size.
The ul ima e pH ange in his s udy ag ees wi h he a ail-
able li e a u e (Pé ez e al., 2013) and as equi ed by he
wo ma ke s (I an and Saudi A abia) o which he company
expo s bee wi h Halal con o mi y. I an allows a maximum
ul ima e pH o 6.2 as speci ied by i s egula o y agency,
and Saudi A abia allows a maximum ul ima e pH o 6.0 as
speci ied by i s egula o y agency. The ul ima e pH a e aged
5.74 ± 0.07 which is consis en wi h he indings o Sil a e al.
(2019), whose alues we e 5.78 ± 0.01, whe e hese au ho s
e alua ed he e ec o cas a ion on he ca cass and mea
quali y ai s o Nello e ca le. Ou esul s also i wi h hose
o Lace da e al. (2022), whe e he ul ima e pH mean was
5.82 ± 0.11.
In ou da a, 22.30% o he o al numbe o ca casses had
an ul ima e pH highe han 5.8 and lowe han 6.04 ( he
maximum pH alue in his s udy). We also emphasize ha
an ul ima e pH highe han 5.8 is conside ed DFD mea by
some au ho s, since hese changes in inal pH cause conside -
able losses o he bee sec o , as he mos equen p oblems
caused by s ess in ca le a e weigh loss, ca cass lesions and
al e ed mea quali y, mainly due o inc eased pH (>5.8), a -
ec ing ende ness and mea colo (da k mea ) (Lomiwes e
al., 2014; Hughes e al., 2017).
Pé ez e al. (2013) conside mea o be DFD wi h an ul-
ima e pH highe han 6 be ween 12 and 48 h pos mo em
o esul in da k mea cu s wi h a sho e shel li e because
o inc eased suscep ibili y o mic obial con amina ion. In ou
da a, only 0.023% o he o al numbe o ca casses had an
ul ima e pH highe han 6.0.
We chose o compa e ou pH esul s wi h he li e a u e,
conside ing we did no analyze mea colo , shea o ce, e c.
The ul ima e pH ange in his s udy was accep able o he
wo ma ke s (I an and Saudi A abia) o which he company
expo s bee wi h Halal con o mi y. I an allows a maximum
ul ima e pH o 6.2 as speci ied by i s egula o y agency;
and Saudi A abia allows a maximum ul ima e pH o 6.0 as
speci ied by i s egula o y agency, while B azil allows a max-
imum ul ima e pH o 6.0 as speci ied by i s egula o y agency.
These ul ima e pH alues can be explained by 1) he ac
ha animals we e aised using a pas u e sys em, which leads
o highe ul ima e pH alues han g ain- ed ca le (Apaoblaza
e al., 2020) and 2) he use o non-cas a ed males, which can
lead o inc eased s ess, because cas a ed animals a e easie
o handle han non-cas a ed animals, since cas a ion esul s
in changes in beha io , namely in becoming calme , gen le ,
mo e obedien , and mo e amenable o managemen (Dua e
e al., 2011). These wo easons would jus i y he abno mal
ul ima e pH in some e alua ed ca casses bu a e insigni ican
when compa ed o he e ec s o oad anspo ime on ul i-
ma e pH as conside ed in his s udy (Figu e 1a and b).
The dis ibu ion o dis ances be ween a m and slaugh e -
house is le -skewed wi h a high a iabili y (Figu es 2a and
b), wi h a coe icien o a ia ion o 57.44% (Table 2). The
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T anspo s ess on Nello e ca le ca cass quali y 5
median alue is 181 km and he i s qua ile 25% wi h a
dis ance alue o less han 105 km and he hi d qua ile
75% has a dis ance alue o mo e han 292 km. I should be
no ed ha he slaugh e house in his s udy was loca ed nea
he geog aphic cen e o he Goiás s a e, and ha he a e age
dis ance was no as g ea as hose epo ed in Chile (We ne
e al., 2013) o Canada (Gonzalez e al., 2012 a,b; Wa en e
al., 2010), which had an a e age dis ance g ea e han 400
km. Howe e , he dis ances epo ed o he p esen s udy
a e simila o hose in s udies conduc ed in he no he n and
Figu e 1. F equency dis ibu ion o ul ima e pH alues in bee ca casses, ep esen ed as a his og am (a) and box plo (b).
Figu e 2. F equency dis ibu ion o dis ance be ween a m and slaugh e house (km) in bee ca casses, ep esen ed as a his og am (a) and box plo (b).
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6Mendes e al.
sou he n egions o B azil (Mendonça e al., 2018; Lace da
e al., 2022), and a e in acco dance wi h B azilian legisla ion,
No ma i e Ins uc ion 09/2021, which allows a maximum o
12 h o con inuous anspo be o e equi ing a es s op o
ood and wa e (B asil, 2021).
Al hough animal anspo o long du a ion is mo e likely
o comp omise animal wel a e han ha o sho e du a-
ion, i is impo an o ecognize ha i is no he du a ion
o he jou ney pe se, bu he associa ed nega i e aspec s, i.e.,
lack o ood, lack o wa e and high empe a u e, which a e
he sou ce o any de imen al e ec s. S ess om ex eme
empe a u es and lack o ood, wa e , and es , o example,
a e all exace ba ed by leng h o exposu e, i.e., jou ney du a-
ion (Nielsen e al., 2011). Fu he mo e, once animals ha e
adap ed o hei new si ua ion, dis ance is a ela i ely mino
p oblem when compa ed o loading densi ies, ehicle design,
oad condi ions, o d i e skill (S appini e al., 2009). In his
s udy, hese ac o s we e con olled o , and he dis ance had
no signi ican in luence on bee quali y, as shown by he ul i-
ma e pH alues.
The weigh dis ibu ion is le -skewed and has high a ia-
bili y (Figu e 3a), wi h a coe icien o a ia ion o 11.41%.
The median alue is 296.50 kg wi h he i s qua ile 25%
ha ing a weigh alue o less han 275.50 kg and he hi d
qua ile 75% wi h a weigh alue o mo e han 319.50 kg.
The many ou lie s shown in he box plo (Figu e 3b) can
be explained by di e en ages. This ag ees wi h he esul s
o Bu eš and Ba oň (2012) who e alua ed he e ec s o
gende and age a slaugh e on g ow h, eed in ake, ca -
cass composi ion, and mea quali y o musculus longissimus
lumbo um a ibu es in Cha olais × Simmen al. They ound
ha bulls slaugh e ed a 14 mo o age we e ligh e han hose
slaugh e ed a 18 mo o age a he end o he a ening pe iod.
This same esul in Nello e bulls was also obse ed by Sil a
e al. (2019). The a e age ho ca cass weigh in he p esen
s udy was 298.90 ± 34.14 kg and which ag ees wi h he alue
o 248 ± 34.20 kg obse ed o Nello e bulls by Mello e al.
(2018) and wi h 236.60 kg ound by Sil a e al. (2019).
The ma u i y dis ibu ion is le -skewed and has high a i-
abili y (Figu e 4a), wi h a coe icien o a ia ion o 48.47%.
The median is 4 ee h and he i s qua ile 25% wi h a ma-
u i y alue o less han 2 ee h and he hi d qua ile 75%
has a alue o mo e han 4 ee h. The box plo indica es
many ou lie s (Figu e 4b). This is due o he sample size and
in he p esen s udy, he expe imen al design did no s ipu-
la e he age ange o he animals s udied since he objec i e
was o make an explo a o y analysis o he company’s da a.
This ag ees wi h esul s om Dua e e al. (2011) wi h mos
o he animals wi h 4 pe manen inciso s ee h and when
e alua ing he physical and chemical cha ac e is ics o mea
om Nello e bulls wi h 4 pe manen inciso s ee h he ound
accep able esul s o ende ness.
Co ela ions Be ween Bee Ca cass T ai s
The ma ix co ela ion be ween bee ca casses shows weak
co ela ions be ween ai s and no ela ionship be ween he
wo a iables o in e es namely ul ima e pH and dis ance
(Table 3).
The e was no signi ican co ela ion be ween ul ima e pH
and dis ance ( = 0.01) on he one hand and be ween ul i-
ma e pH and ma u i y ( = 0.01) on he o he hand. In he
condi ions s udied, he hypo hesis ha long dis ances would
signi ican ly in e e e wi h bee quali y was no con i med o
he Nello e b eed. In his s udy, he anspo a ion dis ance
and ime may ha e been insu icien o cause enough s ess
o he animals o deple e glycogen s o es. A longe anspo
ime (14 h) may esul in changes o he umen en i onmen ,
leading o an inc eased ace a e/ p opiona e a io. This would
Figu e 3. F equency dis ibu ion o ho ca cass weigh (kg) in bee ca casses, ep esen ed as a his og am (a) and box plo (b).
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T anspo s ess on Nello e ca le ca cass quali y 7
educe he quan i y o ci cula ing glucose and a ec ul ima e
pH (Deng e al., 2017). This p obably did no occu in he
animals s udied because e en he longes ime (8 h) did no
impede he decline in ul ima e pH.
Ano he ac o may be due o he physical cha ac e is ics
o he Nello e b eed, which is e y esis an o hea due o
i s la ge body su ace a ea and g ea e numbe o swea
glands. The cha ac e is ics o i s hai also acili a e hea ex-
change wi h he en i onmen . In addi ion, he diges i e ac
is 10% smalle han ha o Eu opean ca le b eeds (ACNB,
2022). The e o e, hei me abolism is lowe and gene a es
less hea . Acco ding o Dewell (2010), la ge ca le canno
handle hea s ess as well as smalle ca le because inc eased
a deposi ion p e en s ca le om egula ing hei hea e -
ec i ely. Sola adia ion is a c i ical componen ha can lead
o losses om hea s ess. In ou s udy, he a e age weigh
was 300 kg which con ibu ed o hese animals being able
o handle he hea . This esul ag ees wi h alues o ul i-
ma e pH ob ained by Lace da e al. (2022) who in es iga ed
he e ec s o di e en p e-slaugh e oad anspo imes on
senso y e alua ion and ins umen al measu emen s o mea
quali y o Nello e ca le. They obse ed ha , wi h he longes
anspo being 6 h, no no iceable e ec on ul ima e pH o
mea quali y.
Weak bu signi ican co ela ions we e ob ained be ween
ul ima e pH and ca cass weigh ( = 0.12, P < 0.01) on he
one hand and, be ween dis ance and ca cass weigh on he
o he ( = 0.05, P < 0.01). This is in ag eemen wi h González
e al. (2012a), which aimed o iden i y and quan i y se e al
ac o s a ec ing sh inkage in ca le du ing long-haul com-
me cial anspo (≥400 km; n = 6,152 ips). They concluded
ha anspo du a ion was he a iable wi h he mos in lu-
ence on sh inkage, especially a high ambien empe a u es
because bo h ac o s ha e a mul iplica i e e ec on each o he .
Thus, e e y a emp should be made o educe anspo du-
a ion and sh inkage, such as by a oiding unnecessa y delays
h ough ca e ul ip planning and e icien bo de c ossing in-
spec ion p o ocols o eede ca le. T anspo should be mo e
ca e ully managed du ing ho wea he o minimize a oidable
sh inkage. Again, ho ca cass weigh was ound no o be a -
ec ed by p e-slaugh e oad anspo dis ance. This may be
because e en he longes anspo ime added o he wai ing
ime in he holding pen was insu icien o educe ca cass
weigh . In addi ion, o he ac o s ela ed o anspo a ion
Figu e 4. F equency dis ibu ion o ma u i y (age) in bee ca casses, ep esen ed as a his og am (a) and box plo (b).
Table 3. Co ela ion coe icien s be ween bee ca cass ai s
pH Dis ance Weigh Ma u i y
Ul ima e pH 1 0.0110.1220.0071
Dis ance, km — 1 0.052−0.032
Ca cass Weigh , kg — — 1 0.232
Ma u i y, mon hs — — — 1
1Co ela ion is no signi ican ly di e en (P > 0.05)
2Co ela ion is signi ican ly di e en a 0.01 (P < 0.01).
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8Mendes e al.
can con ibu e o changes in ca cass weigh , such as animal
densi y, and lo mixing in uck compa men s (Mendonça e
al., 2019). Howe e , in he cu en s udy, hese ac o s we e
con olled o , so ha he e ec s o anspo dis ance could
be isola ed and eliably de e mined (Table 3).
T anspo a ion dis ance and ma u i y had a nega i e weak
ela ionship ( = −0.03, P < 0.01), wi h a low co ela ion be-
ween ca cass weigh and ma u i y ( = 0.23, P < 0.01). This
signi ican co ela ion is due o he ac ha he age a which
an animal is slaugh e ed de e mines i s weigh and composi-
ion o he ca cass because o i s s age o ma u i y (Pe hick e
al., 2007).
In he PCA, he dis ance be ween a m and slaugh e house,
ca cass weigh , ma u i y, and ul ima e pH we e conside ed si-
mul aneously in he igh uppe hi d o he plo . This shows
why he i s wo PCAs explain only 57.2% o he o al a -
iabili y o he da ase , wi h 31.6% co esponding o he i s
p incipal componen and 25.6% o he second p incipal com-
ponen . Resul s om P incipal Componen Analysis (PCA)
con i med a low co ela ion be ween ul ima e pH and dis-
ance and a signi ican co ela ion be ween ma u i y and ca -
cass weigh (Figu e 5). The con ibu ion o he ul ima e pH
in he i s dimension is 16.82% and in he second dimension
is 11.91%; dis ance om a m o slaugh e house con ibu es
2.16% and 63.25%, in he i s and second dimensions, e-
spec i ely; ca cass weigh con ibu es 49.47% in he i s
dimension and 0.09% in he second dimension; and animal
ma u i y con ibu es 31.55% and 24.76% in he i s and
second dimensions, espec i ely.
Howe e , hese esul s should be in e p e ed wi h cau ion
due o he la ge amoun o noise in he da a. Because o his,
i is impo an o emphasize ha in he cu en s udy, ou
p o ocol was insu icien o adequa ely es ou hypo hesis,
because he p ima y objec i e o he p esen case s udy was o
make an explo a o y analysis o he company’s da a, aking
in o conside a ion all he da a ob ained du ing he 6-mo
pe iod e alua ed, o ha e a obus da ase wi h p e- and pos -
slaugh e da a.
pH as a Func ion o Ca cass Weigh , Ma u i y,
Dis ance
Resul s om he eg ession analysis showed ha dis ance
does no ha e a signi ican e ec on pH (P = 0.634). Ca cass
weigh signi ican ly a ec s pH (P < 0.001) wi h a low coe i-
cien o 0.000266, and, as such, has a e y small e ec .
Animal ma u i y (age) nega i ely a ec s pH as well
(P < 0.001) bu also wi h a e y small e ec ( he coe icien
being −0.000806).
yi=5.67 +0.000266xi1−0.000806xi2+0.00000165xi3
Whe e yi ep esen s he measu ed ul ima e pH, xi1
ep esen s he ca cass weigh , xi2 ep esen s he animal ma u-
i y e alua ed o he ca cass, xi3 ep esen s he dis ance be-
ween he a m and he slaugh e house.
The alue o R2 was 0.016, which indica es ha only 1.6%
o o al a iabili y can be explained by his eg ession model.
The e o e, 98.4% o he a iabili y is a ibu able o o he
Figu e 5. P incipal componen analysis. This analysis was pe o med using he ollowing a iables: dis ance, ul ima e pH, weigh , ma u i y. P ojec ion o
a iables in a “XY” plane de ined by he axes o he i s wo p incipal componen s (PC1 and PC2), showing he pe cen age o explained a iabili y in
he wo PCs o he plo .
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T anspo s ess on Nello e ca le ca cass quali y 9
ac o s no conside ed he e. Thus, esul s om he mul iple
eg essions model con i m he p e ious esul s om he PCA.
Howe e , he e ec s e en hough small we e de ec able due
o he la ge sample size.
pH Va iabili y Be ween and Wi hin Fa ms
Resul s om 95% con idence in e als o a iance o he
andom e ec s and o he andom e o showed ha he
a iabili y wi hin a ms is highe han be ween a ms
(Table4).
These esul s may be explained by he ac each a m is
a a di e en dis ance om he slaugh e house, and by each
a m ha ing p o ided se e al ca casses wi h di e en cha -
ac e is ics. Because o his, he a iabili y o he pH o he
ca casses p o ided by each a m is g ea e han he a i-
abili y o ca cass pH be ween a ms. The es ima e o he
andom e ec a iance is smalle han he es ima e o he
andom e o a iance o he model. This may be due o
he high a iabili y in he cha ac e is ics o ca casses and
in mea quali y o ca le is mul i ac o ial. Indeed, he high
a iabili y as epo ed by Clinqua e al. (2022) is o en
linked o he p io i ies o he a ming sys em. The conclu-
sion eached was ha he di e si y o a ming sys ems is a
consequence o he di e si y in se e al ac o s: b eed (dai y
o bee ), age, and sex (bulls, s ee s, hei e s, cull cows) used
o p oduce bee . Fu he , he e a e o he ac o s linked o
a ming p ac ices (e.g., die , especially g azing) ha ha e a
s ong in luence on he senso y, nu i ional, echnological,
and ex insic a ibu es o mea quali y (Clinqua e al.,
2022).
Liu e al. (2022) also epo ed he syne gies and an agonisms
be ween bee quali y dimensions. To gi e wo examples: he
e ec o gene ics alone (highly muscled b eeds, local b eeds,
e c.), and di e en die s (pas u e s inland, o ganic s con en-
ional on g ass) ha e di e en e ec s on he a ibu es o mea
quali y. These wo ac o s a y o a g ea e o lesse deg ee
wi hin a gi en a m’s he d as well as be ween he he ds o di -
e en a ms. Al hough he s udy o gene ic imp o emen o
he Nello e b eed is widesp ead in B azil, he animals used in
he p esen s udy we e no gene ically iden i ied as Nello e ei-
he indi idually o in agg ega e bu we e classi ied as Nello e
by he a ms. This esul s in a iabili y o ca cass cha ac e is-
ics, e en when hey come om he same a m as epo ed in
he li e a u e, e en when he animals a e o he same gende .
This jus i ies he esul ob ained h ough he mixed model
(Table 4).
I is wo h no ing ha imp o emen s a he a m le el can
be impeded o e en elimina ed by poo anspo , subs anda d
slaugh e and p ocessing p ac ices. All hese conside a ions
explain why in e -animal a iabili y in quali y can be high,
e en when a popula ion o animals a e p oduc s o he same
a ming sys em (Dua e e al., 2011). In he p esen s udy,
p e- and pos -slaugh e p o ocols we e hose ecommended
by B azilian legisla ion.
Modeling he Rela ionship Be ween Ca cass Weigh
and Ma u i y and Fa ms
Resul s om a linea mixed model show ha ma u i y has
a signi ican e ec on he ca cass weigh (P < 0.001) wi h a
la ge coe icien o 2.90. A a io likelihood es ou pe o med
he mixed model mul iple eg ession. The alue o R2 in he
linea mixed model is 46.03%, which indica es ha his o al
a iabili y can be explained by he mixed eg ession model.
The e o e, 53.97% o he a iabili y is a ibu able o o he
ac o s no conside ed he e. The Linea Mixed Model o
he ela ionship be ween ca cass weigh and ma u i y and
he a ms con i ms he esul s o Pea son’s co ela ion be-
ween ca cass weigh and ma u i y (Table 3), as well as by
PCA (Figu e 5). As p e iously no ed, hese esul s we e also
ound by o he esea che s (Bu eš and Ba oň, 2012; Sil a e
al., 2019). Consis en wi h Pe hick e al. (2007), Sil a e al.
(2019), and Bu eš and Ba oň (2012), we conclude ha he
age a which an animal is slaugh e ed de e mines he weigh
and composi ion o he ca cass based on he s age o ma u i y
eached.
Se e al ac o s should be conside ed when de eloping
guidelines o educe ca le anspo s ess and sh inkage:
he ype o ca le, ambien empe a u e, anspo du a ion,
d i ing quali y, and ime and o igin o loading (González e
al., 2012a).
Conclusion
Bee ca cass ai s can be a ec ed by ca cass weigh and ma-
u i y, bu only o a limi ed ex en . The hypo hesis ha long
dis ances would signi ican ly a ec bee quali y was no con-
i med o he Nello e b eed in he condi ions s udied. This
could be because o low s ess du ing anspo , as well as he
physical cha ac e is ics o he Nello e b eed ha a o g ea e
esis ance o opical clima ic condi ions.
In addi ion, he s a egy o pu chasing animals wi hin a a-
dius o 300 km, equi alen o a maximum o 8 h o anspo
ime, is consis en wi h he li e a u e on changes in he quali y
o bo ine ca casses due o anspo ime. This is an obse a-
ion bene icial o he company and con o ms o he s anda ds
equi ed by he B azilian ma ke and o hose ma ke s, o
which B azil expo s.
An expe imen al s udy on a much smalle scale, wi h
an assessmen o s ess indica o s, such as lac a e, glucose
concen a ions, co isol concen a ion and c ea ine kinase,
no epineph ine and epineph ine, o b uise sco e shee o e al-
ua e he consequences on bee ea ing quali y, is necessa y o
unde s and any in e ac ion be ween hese pa ame e s and
he bene i s o he supply chain so ha he mea indus y
can u he imp o e animal wel a e and mea quali y du ing
p e-slaugh e comme cial ope a ions. This s udy which used a
da ase p o ided by a slaugh e house can se e as a sou ce o
use ul indica o s on a la ge scale. Al hough mea p oduc ion
has become mo e e icien and line speed has inc eased, he e
Table 4. Poin es ima e o a iance componen s o andom e ec s and model e o espec i ely, using he es ic ed maximum likelihood me hod.
Lowe and uppe bounds o 95% con idence in e als o he a iance componen s o andom e ec s and model e o
Va iances Poin es ima e Lowe limi Uppe limi
Random e ec s 0.02979055 0.02698031 0.0328935
Random e o 0.06518885 0.06466902 0.06571286
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