RESEARCH Open Access
E alua ion o pulmona y hype ension and
clinical s a us in dogs wi h hea wo m by
Righ Pulmona y A e y Dis ensibili y Index
and o he echoca diog aphic pa ame e s
B. Se ano-Pa eño
1
, E. Ca e ón
1*
, A. Ca o-Vadillo
2
, Y. Falcón-Co dón
1
, S. Falcón-Co dón
1
and J. A. Mon oya-Alonso
1
Abs ac
Backg ound: Pulmona y hype ension (PH) is a equen and se e e phenomenon in hea wo m disease caused by
Di o ila ia immi is, mainly caused by in imal p oli e a ion o he a e ies and pulmona y h omboembolisms.
T ans ho acic echoca diog aphy is he me hod o choice o diagnosing PH in dogs al hough he diagnosis is o en
based on indi ec and subjec i e pa ame e s. The Righ Pulmona y A e y Dis ensibili y Index (RPAD Index) is a me hod
ha has been ecen ly alida ed o es ima e he p esence and se e i y o PH in hea wo m-in ec ed dogs. This s udy
compa ed some echoca diog aphic pa ame e s commonly used o es ima e PH in 93 dogs in ec ed by D. immi is and
e alua ed he impac o he pa asi e bu den, mic o ila emia, sex o o igin o he dog (clien -owned/shel e ).
Resul s: None o he s udied echoca diog aphic a iables seemed use ul in he es ima ion o he e alua ed clinical
aspec s, excep o he PA/Ao a io o pa asi e bu den. The RPAD Index was de e mined in 88 o he dogs; o hese, 70.
4% had PH (mild: 37.5%, mode a e: 19.3%, se e e: 13.6%). This Index showed non-signi ican di e ences acco ding o
mic o ila emia, sex, o igin o pa asi e bu den. Symp oma ic dogs showed PH mo e o en and displayed mo e se e e
PH, in addi ion he p esence o symp oms was g ea e among dogs wi h high bu den; on he o he hand 64.4% o
asymp oma ic dogs had some deg ee o PH acco ding o he RPAD Index. Apa om he PA/Ao a io, he o he
e alua ed echoca diog aphic a iables we e no use ul in e alua ing o he hype ensi e s a us o he hea wo m-
in ec ed dog compa ed o he RPAD Index.
Conclusions: The es ima ion o mos common indi ec pa ame e s is no use ul in p edic ing PH in hea wo m-
in ec ed dogs. The esul s con i m he RPAD Index as an objec i e and suppo i e es in he moni o ing and
e alua ion o PH in he hea wo m-in ec ed dog, and show a po en ial diagnos ic alue o he de ec ion o PH in
asymp oma ic animals.
Keywo ds: Hea wo m, Di o ila ia immi is, Echoca diog aphy, Pulmona y hype ension, Pulmona y a e y, Enda e i is
* Co espondence: [email p o ec ed]
1
In e nal Medicine, Facul y o Ve e ina y Medicine, Resea ch Ins i u e o
Biomedical and Heal h Sciences (IUIBS), Uni e si y o Las Palmas de G an
Cana ia, Las Palmas de G an Cana ia, Spain
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Se ano-Pa eño e al. Pa asi es & Vec o s (2017) 10:106
DOI 10.1186/s13071-017-2047-2
Backg ound
Hea wo m disease caused by Di o ila ia immi is is a
cosmopoli an, wo ldwide dis ibu ed ec o -bo ne disease,
endemic in a eas wi h high empe a u es and humidi y
which in u n a o he p oli e a ion o he mosqui o ec-
o o he in ec ion [1]. Di o ila ia immi is mainly a ec s
pulmona y a e ies, causing in imal p oli e a ion o he oc-
cupied a e ies and pulmona y h omboembolisms caused
by embolic wo m agmen s. These e en s ch onically lead
o pulmona y hype ension (PH) which is one o he main
causes o induce clinical signs and, i no ea ed, ch onic-
ally leads o ca diac disease [2].
T ans ho acic Dopple echoca diog aphy p o ides a
nonin asi e and eadily a ailable me hod o es ima ing
pulmona y a e ial p essu e in conscious animals and is
he me hod o choice o diagnosing na u ally occu ing
PH in e e ina y pa ien s [3]. Howe e , he diagnosis o
PH is o en based on indi ec and subjec i e pa ame e s,
speci ically when icuspid egu gi a ion and/o pulmon-
a y insu iciency a e no p esen , which only help o pa -
ially quan i y he disease se e i y. Recen ly, he Righ
Pulmona y A e y Dis ensibili y Index (RPAD Index),
which is calcula ed as he di e ence in diame e o he
igh pulmona y a e y in sys ole and dias ole as mea-
su ed by M-mode, was alida ed as a aluable me hod
o es ima ing he p esence and se e i y o PH in
hea wo m-in ec ed dogs [4]. Howe e , his index has
no been compa ed in dogs wi h D. immi is o o he in-
di ec measu emen s commonly used o es ima e PH in
e e ina y pa ien s; no has i s use ulness in e alua ing
di e en aspec s o he clinical s a us o in ec ed dogs
been es ablished.
On his basis, he aims o his s udy we e (i) o e alu-
a e se e al common echoca diog aphic measu emen s in
2D mode, M-mode and Dopple in dogs in ec ed wi h D.
immi is, o de e mine he sensi i i y o he echoca dio-
g aphic changes in in ec ed dogs in compa ison wi h he
RPAD Index, and (ii) o assess he use ulness o he clas-
sic echoca diog aphic measu emen s and/o RPAD
Index in ela ion o some clinical aspec s o he in ec ed
dogs. These a e p esence/absence o symp oms, pa asi e
bu den and p esence o mic o ila emia.
Me hods
In he p esen s udy, 93 dogs p esen ed o he Ve e in-
a y Teaching Hospi al o he Uni e si y o Las Palmas
de G an Cana ia we e included. The dogs li ed in a
hype -endemic a ea o D. immi is [5, 6]. O hese, 62
we e clien -owned and 31 we e om a local shel e .
None o he animals had ecei ed p e ious ea men
o hea wo m in ec ion. A comple e eco d was kep o
each animal, including iden i ica ion (age, sex, and b eed),
clinical his o y, and demog aphic da a. The e we e 51 e-
males and 42 males, wi h a mean age o 5.3 yea s.
All es ed posi i e o ci cula ing D. immi is an igens
using a comme cial immunoch oma og aphic es ki
(U ano es Di o ila ia®, U ano Ve SL, Ba celona, Spain).
Dogs we e u he e alua ed o he p esence o absence
o mic o ila iae using a modi ied Kno es .
Dogs unde wen echoca diog aphic examina ion, using
an ul asound machine wi h spec al and colo Dopple
and mul i equency p obes (5.5–10 MHz) (Logic P5,
Gene al Elec ic, New Yo k, USA). The dogs we e placed
in igh la e al ecumbence wi h he ansduce placed
in he hi d in e cos al space. Dogs we e conscious and
unde elec oca diog aphic moni o ing du ing he whole
es . Fo each measu emen , six con inuous ca diac cy-
cles we e eco ded. All he echoca diog aphic eco ds
we e ca ied ou by he same esea che .
The p esence o wo ms isible in he pulmona y a e ies
and igh ca diac chambe s was assessed. The wo m bu -
den was classi ied acco ding o Venco e al. [7]; a low o
high wo m bu den sco e anging om 1 o 4 was assigned
as ollows: (i) no wo ms isualized; (ii) ew wo m echoes
in he dis al pa o he igh pulmona y a e y; (iii) wo m
echoes occupying he igh pulmona y a e y and ex end-
ing o he main pulmona y a e y; and (i ) wo m echoes
occupying he whole igh pulmona y a e y and he main
pulmona y a e y o he le el o pulmona y al e.
The ollowing pa ame e s we e de e mined by means
o spec al Dopple : pulmona y low accele a ion ime
(AT), pulmona y low ejec ion ime (ET), AT/ET a io,
and maximum eloci y o he blood low h ough he
pulmona y a e y (PAVmax). P esence o absence o i-
cuspid egu gi a ion (TR) and pulmona y egu gi a ion
(PR) as well as he di e ence g adien be ween RV/RA
and PA/RV we e also assessed. By s anda d wo-
dimensional mode, he ollowing was de e mined: main
pulmona y a e y/ao a a io (PA/Ao a io), le a ial
(LAV) and igh a ial (RAV) olumes, le a ial (LAA)
and igh a ial (RAA) a eas. By M-mode, he measu ed
pa ame e s we e: ac ional sho ening (FS), ejec ion
ac ion (EF), igh en icula in e nal diame e in ele-
dias ole (RVIDD) and le en icula in e nal diame e
in eledias ole (LVIDD), RVIDD/LVIDD a io, igh en-
icle wall hickness (RVWT), le en icle pos e io wall
hickness (LVPWT), RVWT/LVPWT a io, and icuspid
annula plane sys olic excu sion (TAPSE). The RPAD
Index was de e mined as desc ibed by Venco e al. [4]
and was pe o med in 88 dogs o he p esen s udy.
The 88 dogs e alua ed by he RPAD Index we e u -
he classi ied in o wo g oups acco ding o p esence o
absence o symp oms. Dogs we e conside ed as symp-
oma ic when he e was p esence o one o mo e symp-
oms ela ed o hea wo m disease (dyspnea, cough,
exe cise in ole ance, weakness, loss o weigh , syncope).
Theda awe eanalyzedusing heSPSSBase19.0
so wa e o Windows. Con inuous a iables we e
Se ano-Pa eño e al. Pa asi es & Vec o s (2017) 10:106 Page 2 o 6
exp essed as median ± s anda d de ia ion acco ding o
he Kolmogo o -Smi no es . Quali a i e a iables
a e exp essed as pe cen ages. The non-pa ame ic
Mann–Whi ney U- es was used o de e mine he
associa ion be ween quan i a i e and ca ego ical a i-
ables, along wi h he Chi squa e es . In all cases, a P
alue < 0.05 was de e mined as signi ican .
Resul s
O he 93 dogs, 52 (55.9%) we e mic o ila emic and 41
(44.1%) we e amic o ila emic. When pa asi e bu den was
e alua ed, 75 (80.6%) dogs we e conside ed o ha e a low
pa asi e bu den (sco e 1 and 2) and 18 (19.4%) we e clas-
si ied as ha ing a high pa asi e bu den (sco e 3 and 4).
When he p esence o absence o mic o ila iae was
compa ed, he e we e no s a is ically signi ican di e -
ences in any o he e alua ed echoca diog aphic measu e-
men s. When he dogs we e compa ed by pa asi e bu den,
i was obse ed ha only he echoca diog aphic alues o
PA/Ao a io showed s a is ically signi ican di e ences be-
ween bo h g oups o dogs (Z= -2.004, P=0.045).
Compa ed by sex, s a is ically signi ican di e ences
we e ound in RVIDD (Z= -2.089, P= 0.037), LVIDD (Z
= -2.131, P= 0.033), RVIDD/LVIDD (Z= -2.563, P= 0.01)
and LAA (Z= -2.803, P= 0.005). By o igin o he dog
(clien -owned/shel e ), signi ican di e ences we e ound
in AT (Z= -2.228, P= 0.026) and ET (Z= -2.965, P=
0.003). The mean alues o he measu ed pa ame e s by
ca ego y a e shown in Table 1.
Absence o p esence o PH, as well as he se e i y, was
based on he de e mina ion o he RPAD Index. Acco d-
ing o Venco e al. [4], a RPAD Index be ween 35% and
28% was co ela ed wi h mild PH (30–55 mm Hg), be-
ween 27% and 23% wi h mode a e PH (56–79 mm Hg)
and be ween 22% o less wi h se e e PH (> 79 mm Hg).
O he dogs measu ed (n= 88), 29.6% (26/88) did no
ha e PH, and 70.4% (62/88) we e hype ensi e, showing
mild PH 37.5% (33/88), mode a e PH 19.3% (17/88) and
se e e PH 13.6% (12/88).
When he dogs we e compa ed by PH s a us (no mo-
ensi e s hype ensi e), none o he echoca diog aphic
pa ame e s showed s a is ically signi ican di e ences be-
ween g oups, excep he PA/Ao a io (Z= -2.310, P=
0.02). On he o he hand, when he dogs whe e compa ed
by se e i y o PH, no s a is ically signi ican di e ences
we e ound in any o he s udied pa ame e s. The TAPSE
alue was abno mal in all animals, ega dless o he p es-
ence o absence o PH.
TR and/o PR we e p esen in 27 dogs. The g adien s
we e no consis en wi h pulmona y hype ension whe he
his be sys olic o dias olic. PR was p esen in 25 dogs
(mean eloci y low: 1.24 ± 0.87 m/s; mean g adien : 9.16
± 12.76 mm Hg) and TR was p esen in 11 dogs (mean
eloci y low: 1.35 ± 0.93 m/s; mean g adien : 11.25 ±
14.88 mm Hg). The mean RPAD Index o dogs wi h TR
was 29.9 ± 7.8%, and o dogs wi h PR was 27.9 ± 7.9%.
The RPAD Index showed no s a is ically signi ican
di e ences acco ding o pa asi e bu den, mic o ila emic
s a us, sex o o igin o he animals. When p esence/ab-
sence o symp oms was e alua ed, a s a is ically signi i-
can di e ence was obse ed in he RPAD Index
be ween symp oma ic dogs (n= 29; mean RPAD Index:
26.8 ± 9.3%) and asymp oma ic dogs (n= 59; mean
RPAD Index: 35.4 ± 8.3%) (Z= -3942, P< 0.0001)
(Table 2). Fu he mo e, a signi ican di e ence was
ound be ween p esence/absence o symp oms and he
pa asi e bu den (χ
2
= 8.394, d =1,P= 0.005) (Table 3).
Discussion
In hea wo m disease, embolism o dead hea wo ms
can cause acu e clinical signs o PH, while p oli e a i e
in imal changes lead o i e e sible s uc u al damage o
he ascula u e and sus ained PH [2, 8]. An objec i e de-
e mina ion o PH is impo an gi en ha i is a equen
and se e e phenomenon in hea wo m disease.
Excep o he PA/Ao a io, he esul s showed no signi i-
can di e ences in he s udied echoca diog aphic pa ame-
e s be ween dogs wi h PH and wi hou PH measu ed by
RPAD Index; mo eo e , he e we e no signi ican di e -
ences in any pa ame e by deg ees o PH. T adi ionally, he
e alua ion o he p esence o PH in dogs has been de e -
mined om clinical and indi ec echoca diog aphic indings
when icuspid egu gi a ion and/o pulmona y insu i-
ciency we e no p esen [3]. P e ious epo s ha e s udied
he diagnos ic alue o AT, AT: ET, and PA/Ao a io in p e-
dic ing PH [9–11]; al hough some accu acy was ound, he
au ho s indica ed ha he desc ibed a iables we e hin-
de ed by ela i ely low sensi i i y and speci ici y alues (PA/
Ao a io) o echnical and alignmen limi a ions (AT, AT/
ET a io); s udies also concluded ha he RPAD Index may
be use ul and p edic i e o PH in dogs when icuspid e-
gu gi a ion is absen [11]. These obse a ions a e in acco d-
ance wi h he esul s om he p esen s udy, which showed
ha only he PA/Ao a io p esen ed some signi icance
when compa ing no mo ensi edogs e sushype ensi e
dogs, bu his signi icance disappea ed when hype ensi e
dogs we e e alua ed by se e i y o PH. Fu he mo e, based
on he esul s, he es ima ion o mos common indi ec pa-
ame e s was no use ul in p edic ing PH in hea wo m-
in ec ed dogs agains he RPAD Index and showed ha he
es ima ion o he s udied echoca diog aphic measu emen s
p esen ed li le use ulness when compa ing pa asi e bu den,
p esence o mic o ila emia, sex o o igin o he animal.
The PA/Ao a io was also signi ican ly g ea e in dogs
wi h high pa asi e bu den in compa ison wi h dogs wi h
low bu den; howe e , he pa asi e bu den seems o ha e
no e ec in he RPAD Index. This di e ence could be
due o he mechanical p essu e caused by he p esence
Se ano-Pa eño e al. Pa asi es & Vec o s (2017) 10:106 Page 3 o 6
Table 1 Echoca diog aphic pa ame e s measu ed in he p esen s udy
Mic o ila emia Pa asi e bu den Sex O igin P esence/Absence PH
Amic o ila emic Mic o ila emic High
bu den
Low
bu den
Male Female Clien -owned Shel e RPAD
Index ≥36%
RPAD
Index ≤35%
RPAD
Index 28–35%
RPAD
Index 23–27%
RPAD
Index ≤22%
n41 52 18 75 42 51 62 31 26 62 33 17 12
AT (ms) 0.08 ± 0.02 0.08 ± 0.02 0.08 ± 0.02 0.08 ± 0.02 0.08 ± 0.02 0.08 ± 0.02 0.08 ± 0.02
c
0.09 ± 0.02
c
0.08 ± 0.02 0.08 ± 0.02 0.07 ± 0.02 0.09 ± 0.02 0.07 ± 0.02
ET (ms) 0.21 ± 0.04 0.22 ± 0.11 0.23 ± 0.05 0.21 ± 0.09 0.22 ± 0.12 0.21 ± 0.05 0.21 ± 0.10
c
0.22 ± 0.03
c
0.23 ± 0.15 0.21 ± 0.05 0.20 ± 0.03 0.22 ± 0.05 0.21 ± 0.08
AT/ET 0.40 ± 0.10 0.37 ± 0.11 0.37 ± 0.11 0.39 ± 0.11 0.40 ± 0.11 0.38 ± 0.11 0.38 ± 0.12 0.39 ± 0.08 0.40 ± 0.09 0.38 ± 0.12 0.37 ± 0.08 0.41 ± 0.14 0.38 ± 0.17
PAVmax 0.80 ± 0.17 0.90 ± 0.31 0.87 ± 0.29 0.82 ± 0.20 0.85 ± 0.20 0.84 ± 0.28 0.85 ± 0.13 0.83 ± 0.22 0.89 ± 0.23 0.83 ± 0.26 0.82 ± 0.19 0.85 ± 0.18 0.84 ± 0.47
PA/Ao 1.02 ± 0.13 1.02 ± 0.15 1.03 ± 0.15
a
1.01 ± 0.13
a
1.02 ± 0.17 1.03 ± 0.12 1.01 ± 0.13 1.05 ± 0.17 0.97 ± 0.09
d
1.05 ± 0.15
d
1.03 ± 0.12 1.06 ± 0.17 1.09 ± 0.21
LAV (cm) 7.68 ± 5.79 7.60 ± 5.95 7.85 ± 5.58 7.89 ± 5.90 8.54 ± 5.44 7.17 ± 5.79 7.50 ± 5.56 8.28 ± 5.85 6.98 ± 5.45 8.00 ± 5.68 8.76 ± 6.70 6.30 ± 2.46 8.61 ± 6.13
RAV (cm) 6.16 ± 4.53 5.59 ± 3.64 5.80 ± 3.45 5.86 ± 3.86 6.13 ± 3.60 5.82 ± 4.22 5.83 ± 4.10 6.20 ± 3.68 4.69 ± 3.22 6.43 ± 4.17 6.50 ± 4.07 6.03 ± 3.57 6.91 ± 5.57
LAA (cm
2
) 4.69 ± 2.19 4.33 ± 2.25 4.53 ± 2.10 4.75 ± 2.21 5.20 ± 1.94
b
4.13 ± 2.18
b
4.52 ± 2.17 4.74 ± 2.09 4.44 ± 2.23 4.63 ± 2.09 4.93 ± 2.37 4.42 ± 0.97 4.10 ± 2.58
RAA (cm
2
) 4.33 ± 2.23 4.02 ± 2.28 4.09 ± 2.08 4.20 ± 2.24 4.40 ± 1.70 4.04 ± 2.43 4.27 ± 2.39 4.07 ± 1.62 3.69 ± 1.91 4.42 ± 2.25 4.54 ± 2.52 4.34 ± 1.84 4.22 ± 2.25
FS (%) 39.69 ± 10.64 40.80 ± 7.09 39.85 ± 7.56 39.69 ± 9.26 39.98 ± 9.82 39.61 ± 8.37 39.84 ± 9.13 39.67 ± 8.92 38.13 ± 7.29 40.73 ± 9.71 38.5 ± 7.57 42.73 ± 13.41 44.22 ± 8.27
EF (%) 68.96 ± 12.98 72.37 ± 8.35 71.05 ± 8.86 69.77 ± 11.22 69.64 ± 11.49 70.53 ± 10.43 70.11 ± 10.85 70.14 ± 11.12 69.06 ± 9.11 70.83 ± 11.70 68.84 ± 9.38 70.98 ± 16.52 76.09 ± 8.74
RVIDD (cm) 1.03 ± 0.53 0.92 ± 0.42 0.93 ± 0.43 0.96 ± 0.46 0.85 ± 0.39
b
1.07 ± 0.51
b
0.94 ± 0.49 1.04 ± 0.45 0.91 ± 0.42 1.02 ± 0.50 0.98 ± 0.49 1.09 ± 0.40 1.06 ± 0.65
LVIDD (cm) 2.84 ± 0.87 2.99 ± 0.80 3.00 ± 0.75 3.00 ± 0.79 3.14 ± 0.82
b
2.76 ± 0.76
b
2.91 ± 0.82 2.98 ± 0.8 2.79 ± 0.80 2.99 ± 0.81 3.00 ± 0.86 2.96 ± 0.65 3.01 ± 0.92
RVIDD/LVIDD 0.40 ± 0.30 0.33 ± 0.18 0.33 ± 0.17 0.34 ± 0.17 0.30 ± 0.17
b
0.42 ± 0.27
b
0.36 ± 0.27 0.37 ± 0.17 0.35 ± 0.18 0.37 ± 0.27 0.35 ± 0.19 0.38 ± 0.15 0.44 ± 0.50
RVWT (cm) 0.60 ± 0.15 0.57 ± 0.20 0.55 ± 0.19 0.56 ± 0.17 0.56 ± 0.16 0.59 ± 0.18 0.57 ± 0.18 0.59 ± 0.16 0.56 ± 0.15 0.58 ± 0.18 0.57 ± 0.18 0.61 ± 0.16 0.56 ± 0.23
LVPWT (cm) 0.87 ± 0.23 0.85 ± 0.23 0.85 ± 0.24 0.87 ± 0.24 0.86 ± 0.25 0.86 ± 0.22 0.88 ± 0.26 0.82 ± 0.18 0.82 ± 0.23 0.88 ± 0.24 0.89 ± 0.22 0.82 ± 0.21 0.92 ± 0.33
RVWT/LVPWT 0.72 ± 0.20 0.68 ± 0.21 0.66 ± 0.20 0.67 ± 0.21 0.68 ± 0.21 0.69 ± 0.20 0.67 ± 0.22 0.72 ± 0.16 0.72 ± 0.21 0.68 ± 0.20 0.66 ± 0.19 0.76 ± 0.19 0.66 ± 0.22
TAPSE (cm) 1.34 ± 0.38 1.39 ± 0.32 1.36 ± 0.30 1.35 ± 0.33 1.35 ± 0.34 1.36 ± 0.33 1.38 ± 0.36 1.29 ± 0.26 1.43 ± 0.36 1.32 ± 0.32 1.34 ± 0.36 1.35 ± 0.24 1.23 ± 0.27
RPAD
Index (%)
32.77 ± 8.67 32.42 ± 10.22 32.96 ± 12.2 32.73 ± 8.85 32.67 ± 9.50 32.51 ± 9.62 32.48 ± 9.54 32.77 ± 9.64 43.58 ± 6.58
d
27.97 ± 6.19
d
32.71 ± 2.19
d
25.87 ± 1.42
d
17.89 ± 3.21
d
S a is ically signi ican di e ences (P< 0.05) compa ed by pa asi e bu den (
a
), sex (
b
), o igin (
c
) and p esence/absence o pulmona y hype ension (
d
)
Abb e ia ions:AT pulmona y a e y low accele a ion ime, ET pulmona y a e y low ejec ion ime, PAVmax maximum eloci y o he blood low h ough pulmona y a e y, PA/Ao main pulmona y a e y/
ao a a io, LAV le a ial olume, RAV igh a ial olume, LAA le a ial a ea, RAA igh a ial a ea, FS ac ional sho ening, EF ejec ion ac ion, RVIDD igh en icula in e nal diame e in eledias ole,
LVIDD le en icula in e nal diame e in eledias ole, RVWT igh en icula wall hickness, LVPWT le en icula pos e io wall hickness, TAPSE icuspid annula plane sys olic excu sion, RPAD Index
Righ Pulmona y A e y Dis ensibili y Index, PH pulmona y hype ension
Se ano-Pa eño e al. Pa asi es & Vec o s (2017) 10:106 Page 4 o 6
o a la ge amoun o pa asi es in he pulmona y a e ies.
Howe e u he s udies should be ca ied ou o e alu-
a e his conclusion.
Signi ican di e ences we e ound in he AT and ET
pa ame e s as ega ds he o igin o he animal (clien
owned/shel e ). The e is no a clea explana ion o his;
some au ho s epo ed ha , in addi ion o he pulmon-
a y p essu e, he ET and AT can be in luenced by o he
ac o s like hea a e, ca diac ou pu o unc ion o he
igh en icle [12]. Also, he ET can be in luenced be-
cause he accu acy o he low eloci ies can be a ec ed
by i s ana omical displacemen in pa ien s wi h dila ed
pulmona y a e ies and high pulsed-wa e Dopple gain
which migh unde es ima e exac ime measu emen s
[13]. Fu he mo e, Visse e al. [11] desc ibed ha co -
ec measu emen s o AT and ET can be di icul o ac-
qui e in dyspneic dogs.
The di e ences ound in he esul s o RVIDD, LVIDD,
RVIDD/LVIDD and LAA by sex could be a ibu ed o
physiological di e ences in he size o he animals.
All s udied dogs showed an abno mal TAPSE alue, an
echoca diog aphic measu emen ha allows he assess-
men o he igh en icula sys olic unc ion which is a
s ong p edic o o ou come in human pa ien s wi h PH
[14]. I has also been desc ibed ha pa ien s wi h ei he
le o igh en icula sys olic dys unc ion had s a is i-
cally smalle TAPSE han pa ien s wi h no mal bi en i-
cula sys olic unc ion [15].
I was obse ed ha he dogs showing any symp om
compa ible wi h hea wo m disease showed PH mo e
o en and in gene al mo e se e ely han he asymp oma ic
dogs. Simila ly, he p esence o symp oms was mo e
p e alen among dogs wi h high pa asi e bu den. I seems
easonable o associa e he p esence o some symp oms
wi h he consequences o high pulmona y p essu e; also, a
high pa asi e bu den has been linked o high le els o
se um bioma ke s o ca diopulmona y and in lamma o y
damage in dogs wi h D. immi is [16–18]. Mo e impo -
an ly, jus as no all he symp oma ic dogs om he
p esen s udy we e hype ensi e, he esul s showed ha a
high pe cen age o asymp oma ic dogs had some deg ee
o PH. This highligh s he impo ance o ea ly de ec ion o
his condi ion by objec i e me hods, which could allow
app op ia e he apeu ic measu es aimed a minimizing
he e olu ion o he ascula damage.
Mo eo e , he RPAD Index can be seen as a mo e sen-
si i e ma ke o PH since, al hough 27 o he 62 hype -
ensi e dogs showed p esence TR and/o PR, none o
hem showed alues consis en wi h pulmona y
hype ension.
No signi ican changes we e obse ed in he RPAD
Index ega ding he mic o ila emic s a us, sex o o igin
o he dog. In addi ion, he pa asi e bu den did no sig-
ni ican ly a ec he RPAD Index. Fu he mo e, he e-
sul s showed a high pe cen age o dogs wi h PH and low
wo m bu den, which is in acco dance wi h p e ious ob-
se a ions made by o he au ho s who epo ed ha he
se e i y o hype ension does no co ela e wi h he
numbe o pa asi ic wo ms and ac o s such as in ensi y
o exe cise and lowe pa asi e bu den in olde dogs, his
being due o na u al dea h o he wo ms [7, 19]. O he
ac o s ha may con ibu e o he ascula enda e i is
and he e o e de elopmen o hype ension a e cu en ly
being s udied [20].
Conclusions
Based on hese esul s, none o he classic echoca -
diog aphic pa ame e s s udied seemed use ul in es i-
ma ing he se e i y o PH and o he clinical aspec s.
Table 2 Dogs classi ied by he RPAD Index and acco ding o he p esence/absence o symp oms and by pa asi e bu den. Da a a e
shown as numbe o dogs (n). Animals we e conside ed ha ing mild pulmona y hype ension (30–55 mm Hg) wi h a RPAD Index
be ween 28% and 35%, mode a e pulmona y hype ension (56–79 mm Hg) wi h a RPAD Index be ween 23% and 27% and se e e
pulmona y hype ension (> 79 mm Hg) wi h a RPAD Index ≤22%. When he RPAD Index was ≥36% he dog was conside ed
no mo ensi e
Symp oma ic Asymp oma ic High bu den Low bu den
No mo ensi e (n= 26) 5 21 8 18
Hype ensi e (n= 62) 24 38 17 45
Mild PH (n= 33) 5 28 8 25
Mode a e PH (n= 17) 8 9 4 13
Se e e PH (n= 12) 11 1 5 7
TOTAL (n= 88) 29 59 25 63
Abb e ia ion:PH pulmona y hype ension
Table 3 Dogs compa ed by p esence/absence o symp oms
and by pa asi e bu den (high bu den/low bu den). Da a a e
shown as numbe o dogs (n)
Symp oma ic Asymp oma ic
High bu den (n= 25) 14 11
Low bu den (n= 63) 15 48
To al (n= 88) 29 59
Se ano-Pa eño e al. Pa asi es & Vec o s (2017) 10:106 Page 5 o 6

Mo eo e , hese echoca diog aphic a iables did no
seem o o e any addi ional bene i s in he e alua ion
o he hype ensi e s a us o he hea wo m-in ec ed
dog compa ed o he RPAD Index, which p e iously
showed a s ong co ela ion wi h in asi e pulmona y
a e ial p essu es demons a ing i s po en ial diagnos-
ic alue in dogs [4]. The esul s con i m he RPAD
Index as an objec i e and suppo i e es in he mon-
i o ing and e alua ion o he hea wo m-in ec ed dog
and show i s diagnos ic alue in he ea ly de ec ion
o PH in asymp oma ic animals, which could acili a e
app op ia e he apeu ic measu es aimed a minimizing
he e olu ion o he ascula damage. Al hough add-
i ional s udies would be necessa y o consolida e
hese conclusions, hese esul s encou age he use o
he RPAD Index as a s anda dized me hod o asses-
sing he hype ensi e s a us o he hea wo m-in ec ed
dogs.
Abb e ia ions
AT: Pulmona y low accele a ion ime; EF: Ejec ion ac ion; ET: Pulmona y
low ejec ion ime; FS: F ac ional sho ening; LAA: Le a ial a ea; LAV: Le
a ial olume; LVIDD: Le en icula in e nal diame e in eledias ole;
LVPWT: Le en icle pos e io wall hickness; PA/Ao a io: Main pulmona y
a e y/ao a a io; PAV max: Maximum eloci y o he blood low h ough he
pulmona y a e y; PH: Pulmona y hype ension; PR: Pulmona y egu gi a ion;
RA: Righ a ium; RAA: Righ a ial a ea; RAV: Righ a ial olume; RPAD
Index: Righ Pulmona y A e y Dis ensibili y Index; RV: Righ en icle;
RVIDD: Righ en icula in e nal diame e in eledias ole; RVWT: Righ
en icle wall hickness; TAPSE: T icuspid annula plane sys olic excu sion;
TR: T icuspid egu gi a ion
Acknowledgemen s
No applicable.
Funding
This esea ch was pa ially suppo ed by he Mexican Na ional Council on
Science and Technology (CONACYT) - G an 314686.
A ailabili y o da a and ma e ial
All da a gene a ed o analyzed du ing his s udy a e included in his
published a icle.
Au ho s’con ibu ions
EC, ACV and JAMA designed he s udy, analyzed he da a and w o e he
manusc ip . BSP, YFC and SFC o ganized he ieldwo k and pa icipa ed in
he da a collec ions. All au ho s ead and app o ed he inal manusc ip .
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Consen o publica ion
No applicable.
E hics app o al and consen o pa icipa e
All he owne s ga e hei consen o pa icipa e in his s udy. The s udy was
app o ed by he e hical commi ee o he Ve e ina y Medicine Se ice o he
Uni e si y o Las Palmas de G an Cana ia and was ca ied ou in acco dance
wi h he cu en Eu opean legisla ion on animal p o ec ion.
Au ho de ails
1
In e nal Medicine, Facul y o Ve e ina y Medicine, Resea ch Ins i u e o
Biomedical and Heal h Sciences (IUIBS), Uni e si y o Las Palmas de G an
Cana ia, Las Palmas de G an Cana ia, Spain.
2
Depa men o Animal Medicine
and Su ge y, Ve e ina y Facul y, Complu ense Uni e si y o Mad id, Mad id,
Spain.
Recei ed: 28 Oc obe 2016 Accep ed: 18 Feb ua y 2017
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