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\begin{document}

\title{Doppler renal resistivity index in horses: a systematic review}



\author[1]{Nathalia dos Santos Rosse}%
\author[1]{Emily Reis}%
\affil[1]{Universidade Federal de Vicosa Departamento de Medicina Veterinaria}%


\vspace{-1em}



  
  \date{June 14, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
The renal resistivity index is a tool to evaluate the hemodynamics
through arterial resistance. Considering perfusion as one of the first
aspects to be affected upon kidney injury, alterations in renal blood
flow could be especially important for the early detection of kidney
damage. The aim of this systematic review was to retrieve published
studies on equine renal resistivity index (RI) in order to develop a
standardized method of renal ultrasound examination through a
transabdominal approach as well as to evaluate current reference range
for renal RI value in horses. An electronic search in Science Direct,
PubMed, Scopus and Web of Science databases was performed in February
2023 using the terms ``RI'' OR ``resistivity index'' OR ``IP'' OR
``pulsatility index'' AND (kidney OR renal) AND (equine OR horse) in
titles, keywords and abstracts. The studies were screened based on
inclusion criteria and variables of interest were extracted. To assess
the methodological quality, the SYRCLES`s risk of bias tool was used.
From the search, a total of 134 studies were identified and five of them
were considered eligible. The selected studies had been conducted in
healthy non-sedated horses through transabdominal technique. The upper
limit of normality for renal RI was 0.58 \selectlanguage{ngerman}± 0.06 for the right kidney of
untrained horses, which is considerably lower than the value of 0.70
currently used for humans, cats and dogs. There were heterogenous
outcomes among studies, where two out of the five demonstrated
difference between RI value of left and right kidneys and one out of the
five showed increased renal RI value in the elderly compared to foals
and adult animals. Data of RI in horses is still scarce; a normality
standard for renal RI studies in horses would greatly improve comparison
and good quality results to allow clinical application.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


Doppler renal resistivity index in horses: a systematic review

Abstract

The renal resistivity index is a tool to evaluate the hemodynamics
through arterial resistance. Considering perfusion as one of the first
aspects to be affected upon kidney injury, alterations in renal blood
flow could be especially important for the early detection of kidney
damage. The aim of this systematic review was to retrieve published
studies on equine renal resistivity index (RI) in order to develop a
standardized method of renal ultrasound examination through a
transabdominal approach as well as to evaluate current reference range
for renal RI value in horses. An electronic search in Science Direct,
PubMed, Scopus and Web of Science databases was performed in February
2023 using the terms ``RI'' OR ``resistivity index'' OR ``IP'' OR
``pulsatility index'' AND (kidney OR renal) AND (equine OR horse) in
titles, keywords and abstracts. The studies were screened based on
inclusion criteria and variables of interest were extracted. To assess
the methodological quality, the SYRCLES`s risk of bias tool was used.
From the search, a total of 134 studies were identified and five of them
were considered eligible. The selected studies had been conducted in
healthy non-sedated horses through transabdominal technique. The upper
limit of normality for renal RI was 0.58 \selectlanguage{ngerman}± 0.06 for the right kidney of
untrained horses, which is considerably lower than the value of 0.70
currently used for humans, cats and dogs. There were heterogenous
outcomes among studies, where two out of the five demonstrated
difference between RI value of left and right kidneys and one out of the
five showed increased renal RI value in the elderly compared to foals
and adult animals. Data of RI in horses is still scarce; a normality
standard for renal RI studies in horses would greatly improve comparison
and good quality results to allow clinical application.

\textbf{Keywords:} horse, ultrasonography, kidney, resistivity index

\par\null

\textbf{Introduction}

The kidneys are vital organs once they are responsible for homeostasis
as they play a main role in the hydric, acid-base and electrolyte
balance, help controlling blood pressure, and having endocrine function
as well {[}1{]}. Although renal diseases are reported as being
uncommonly diagnosed in horses, there are several published reviews and
case reports on different renal diseases {[}2-6{]} suggesting otherwise.
A study on the prevalence of acute kidney injury (AKI) in hospitalized
horses found that 14.8\% of studied horses developed AKI {[}7{]}.
Further, Knottenbelt e Pascoe {[}8{]} have noted that kidney injuries
are frequently found in \emph{post-mortem} examinations in horses and
so, we are probably dealing with a scenario where kidney diseases are
underdiagnosed.

Considering such possible underdiagnosed kidney damage and the
difficulties on treatment of kidney disease, it is very important to
stablish an early diagnosis due to its major impact on the body. There
are several hematological and urinary exams available nowadays, but it
is known that renal injuries up to 75\% can be compensated by nephrons
and possibly no relevant alterations would be seen in those exams
{[}9{]}. In that sense, when kidney injuries are detected using these
methods, effective treatment might be unattainable. In human medicine,
ultrasonography is being widely used as a tool to enhance the early
diagnosis of renal damage. It is an easy and non-invasive exam that
provides information about the morphology, shape, length, echogenicity
and even hemodynamics of the kidneys {[}10, 11{]}.

On top of the well-known B mode, the Doppler ultrasound can detect
alterations of reflected sound waves frequency when the object hit by
the wave is in movement and, by an equation, the velocity of that object
can be obtained {[}12{]}. The color Doppler shows the presence and
direction of the object towards the probe, it is majorly represented by
the blue and red colors, largely used for blood flow evaluation
{[}13{]}. Furthermore, the pulsed Doppler is responsible for reading the
sound pulses and generating a spectral wave that shows their number
within the same frequency {[}12{]}, being represented as velocity X
time. Two indexes can be calculated from de information acquired from
the spectral wave, the resistivity index (RI) and the pulsatility index
(PI). These indexes stand for (1) RI ({[}peak systolic velocity -- final
diastolic velocity{]}/peak systolic velocity) and (2) PI ({[}peak
systolic velocity -- final diastolic velocity{]}/average velocity),
according to Novellas et al. {[}14{]}. The RI and PI give information
about perfusion of the organ and its vascular resistance {[}15,16{]}.

Measurements of renal RI and PI are already being described in humans as
a method to investigate and follow the progression of various diseases,
not only related directly to the kidneys {[}17{]}, as well as a valuable
technique to evaluate the successfulness of renal transplantations
{[}18{]}. In small animals, it has been reported that RI and PI would be
advantageous to evaluate chronic renal disease in cats {[}19{]}, kidney
damage from inflammatory disease in cats {[}20{]}, acute renal disease
in dogs and cats {[}21{]}, cardiorenal syndrome in dogs {[}22{]} and a
number of other conditions. In addition, there are numerous studies
regarding the normal range for each species {[}14,23,24{]}.

For horses, however, there are only few studies in respect to RI,
consequently, limiting its clinical use. This review aimed to evaluate
standard RI values of normality in horses and analyze published studies
concerning their methodology, appraise and compare their results. In
addition, we were able to critically review possible limitations,
difficulties and methodological flaws in the selected studies along with
pointing achievable future directions on the subject.

\textbf{Materials and methods}

The present systematic review was conducted according to the premises of
PRISMA - Preferred Reporting Items for Systematic Reviews and
Meta-Analyses {[}25{]}.

\emph{Search strategy}

PubMed, Science Direct, Web of Science and Scopus were the databases
chosen for this research. An extensive search was driven applying the
following terms: RI OR ``resistivity index'' OR IP OR ``pulsatility
index'' AND (kidney OR renal) AND (equine OR horse) in titles, keywords
and abstracts. There were no limitations upon language, year or country
of publication and the last search was performed on February 9, 2023.

\emph{Eligibility criteria}

The studies screened in the searching were selected if they accomplished
the following features: (1) horses were the animal model, (2) conducted
in renal vessels, (3) at least the RI was measured. Further, the studies
were excluded if they were: (1) in another species other than equine,
(2) not performed in the kidneys, (3) book chapters, (4) not mentioning
RI or PI.

\emph{Data extraction}

Extraction was carried out by the same people and the variables
considered as being of interest were listed in an Excel table. Extracted
data were grouped according to articles information (authors, year and
country of publication), experimental model (horses' breed, age, body
weight and sex), methodology (animal grouping, sedated or non-sedated,
athletes or not athletes, comparing or not left and right kidney,
comparison between age groups, artery of interest), technical
information (type of equipment and probe, frequency of the last, wall
filter, sample volume) and the values obtained for RI and PI.

\emph{Risk of Bias assessment}

The quality assessment of the included studies was checked using the
SYRCLE`s risk of bias tool for animal studies {[}26{]}. This method is
based on ten signaling questions that can be adapted according to the
reviewer and the papers being reviewed so the analyses can be more
accurate.

\textbf{Results}

\emph{Selected studies}

From the initial search, 134 studies were identified. The screening
phase consisted of reading the titles and abstracts and evaluating if
they match the previously cited inclusion criteria, stage at which 14
studies were selected. A great number of studies were not included
because they were based on other animals rather than horses or because
they were not performed in kidneys. The selected records were downloaded
and fully read. One study was not available online, so it was necessary
to email the author, having a copy promptly sent. Finally, after
exclusion of duplicates and of one paper that did not address renal
arteries {[}27{]}, five studies were included in the present systematic
review. All steps from identification to inclusion were taken by two
examiners and there were no disagreements. It was not necessary to use a
specific program or software to evaluate data due to the small number of
eligible studies. The flow diagram on Figure 1 demonstrates how the
process of selecting the articles was conducted.

Figure 1 - Flow diagram showing the sequency of how studies were
selected to systematic review, according to PRISMA.

\emph{Study characteristics}

Two out of the five eligible studies were published in the 2010s
{[}11,28{]}, two in the 2020s {[}29,30{]} and one is dated back in the
1990s {[}31{]}. From those, two were carried out in Poland {[}28,30{]},
two in Italy {[}11,29{]} and one in Australia {[}31{]}.

According to the findings of this systematic review, Hoffmann and
colleagues {[}31{]} were the first research group to publish about RI
measurement in horses. They considered a group of 11 healthy animals,
being five of them sedated to ensure good ultrasonographic access to the
intrarenal arteries and seven of them not sedated so the pyelorenal
arteries were assessed. Although there were sedated horses in the study,
only the healthy non-sedated group was included in this review. The aim
of this pioneer research was to establish a reference range for peak
systolic and end diastolic velocities and for RI in the equine.

Furthermore, Macrì et al. {[}11{]} included 13 healthy Thoroughbred
horses aiming at determining a reference range for arterial renal RI in
healthy non-sedated horses and to compare the results of right and left
kidneys, mares and geldings as well as trained and untrained animals.
Siwinska and peers {[}28{]} selected 45 Warmbloods horses and compared
the renal RI among animals´ age groups (15 foals, 15 adults and 15
elderly), between the left and right kidneys, likewise the influence of
age, body weight, heart rate and blood pressure on the intrarenal
arteries RI. They also assessed repeatability by performing a second
ultrasound two hours after the first measurements.

In addition, Freccero et al. {[}29{]} aimed to obtain the renal RI value
of each kidney from 33 horses and nine donkeys, along with their breeds,
age, body mass and body condition and compare all this information
within itself. Since this systematic review is considering only horses,
the data including donkeys were excluded. Lastly, Siwinska and
colleagues {[}30{]} obtained the renal RI of 30 healthy horses (proven
healthy throughout complete clinical and laboratorial evaluation and
urinary tract ultrasonographic examination), 11 horses diagnosed with
acute kidney injury (AKI) and 30 horses under risk of developing AKI (10
horses with colic/gastrointestinal diseases; 10 horses on phenylbutazone
- 2.2 mg/kg twice a day orally for 10 days; 10 horses on gentamicin -
6.6 mg/kg intravenously for 5 days). She and her group aimed to
determine if animals with AKI would show a higher renal RI, as well as,
to measure renal RI in horses at risk for AKI and investigate if
potential nephrotoxic agents could impact renal RI. They compared the RI
data from right and left kidneys between groups and checked for
correlation between renal RI and blood and urine parameters. Also, the
group evaluated the sensitivity and specificity of renal RI to AKI
detection.

It is crucial to stablish that for this systematic review only the
healthy non-sedated group of each study was considered, so the baseline
characteristics and methodological features could be reliably compared
between papers. The Table 1 summarizes the characteristics of the
included information from the studies included in the review\selectlanguage{english}
\begin{longtable}[]{@{}lllllll@{}}
\toprule
\begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Reference\strut
\end{minipage} & \begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Country\strut
\end{minipage} & \begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Breed\strut
\end{minipage} & \begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Number of animals\strut
\end{minipage} & \begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Grouping\strut
\end{minipage} & \begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Body weight\strut
\end{minipage} & \begin{minipage}[b]{0.12\columnwidth}\raggedright\strut
Age\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Hoffmann et al., 1997\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Australia\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Thoroughbreds Standardbreds\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
7\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Non-sedated\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
NR\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
15 \selectlanguage{ngerman}± 4,6 years\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Macrì et al., 2015\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Italy\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Thoroughbreds\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
13\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Male (5) Female (8) Trained (5) Untrained (8)\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
420 -- 500kg\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
3 -- 24 years\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Siwinska et al., 2019\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Poland\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Warmbloods\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
45\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Foals (15) Adults (15) Elderly (15)\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
205 \selectlanguage{ngerman}± 38.8kg 558.4 ± 95.3kg 542.6 ± 74.6kg\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Up to 6 months 4 -- 10 years Above 18 years\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Freccero et al., 2020\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Italy\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Trotters Thoroughbreds Warmbloods\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
33\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Adults (18) Elderly (15) Trotters (23) Other breeds (10)\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Horses: 370 -- 645kg\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Horses: adults up to 15 years and elderly above 15 years\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Siwinska et al., 2021\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Poland\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Warmbloods\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
30\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Healthy (15F/15M)\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Healthy: 554 \selectlanguage{ngerman}± 80kg\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Healthy: 14.7 \selectlanguage{ngerman}± 8,4 years\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{ngerman}

Table 1 - Characterization of studies (n = 5) selected to the systematic
review

Abbreviations: NR not reported, F female, M male, AKI acute kidney
injury.

\par\null

\emph{Ultrasonographic examination}

In view of renal ultrasonography, all studies reported the performance
of the transabdominal approach with the horse standing and none of them
have selected the transrectal access. All studies also have described
the preparation of the animals prior to the examination (Table 2). This
stage was very similar between studies and consisted of clipping or
shaving the hair coat over the 14th or 15th to the 17th intercostal
space (ICS) and the paralumbar fossa on the right side and over the 15th
or 16th to the 17th ICS and the paralumbar fossa on the left side.
Siwinska et al. {[}28,30{]} opted for washing the horses` skin with
chlorhexidine and rinsing with alcohol, drying and applying
water-soluble coupling gel while Freccero et al. {[}29{]} chose to use
alcohol and coupling gel, similarly Hoffmann et al. {[}31{]} and Macrì
et al. {[}11{]} applied only ultrasound gel. Concerning the technical
information about the ultrasound machine and settings (Table 2.2), the
five studies have reported the type of probe and its range of frequency,
the sample volume (SV) and the wall filter (WF), except for Macrì et al.
{[}11{]} that did not demonstrate data on the last two and for Hoffmann
et al. {[}31{]} that reported only the WF. Freccero et al. {[}29{]} have
additionally presented information about the pulse repetition frequency
(PRF). Siwinska et al. {[}30{]} used the same ultrasound protocol as
Siwinska et al. {[}28{]}.

In order to avoid stressing the animals, Siwinska et al. {[}28{]} had
the foals included in their experiment kept together with mares during
the examination, also adults and elderly horses were examined near or in
front of their stalls. Freccero et al. {[}29{]} had the animals
restrained in a handling box that horses had already been acclimated. It
is important to minimize stress as it can affect the waveforms, and thus
the RI value {[}35{]}.\selectlanguage{english}
\begin{longtable}[]{@{}llll@{}}
\toprule
\begin{minipage}[b]{0.22\columnwidth}\raggedright\strut
Reference\strut
\end{minipage} & \begin{minipage}[b]{0.22\columnwidth}\raggedright\strut
Patient preparation\strut
\end{minipage} & \begin{minipage}[b]{0.22\columnwidth}\raggedright\strut
US characteristics\strut
\end{minipage} & \begin{minipage}[b]{0.22\columnwidth}\raggedright\strut
Equipment settings\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Hoffmann et al., 1997\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Hair shaving and coupling gel\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Opus 1 (Ausonics International). Split-crystal mechanical sector probe.
2.5MHz for B-mode and 1.9MHz for continuous wave Doppler\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
WF of 50Hz\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Macr\selectlanguage{ngerman}ì et al., 2015\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Hair clipping and coupling gel\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
MyLab 50 Vet (Esaote, Italy). 1.9MHZ to 3,0MHz phased-array probe.\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
NR\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
Siwinska et al., 2019\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
Hair clipping, skin washing with chlorhexidine soap and alcohol, use of
coupling gel\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
MyLab 30 Gold Vet (Esaote). 1MHz to 5MHz convex probe.\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
SV set at 5 to 10mm and decreased to small as possible WF of 50 or
100Hz\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
Freccero et al., 2020\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
Hair clipping, alcohol and coupling gel\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
MyLab 30 Gold (Esaote, Italy). Multifrequency curvilinear probe 3.5MHz
to 5MHz.\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
SV set at 2mm WF of 50Hz PRF set lowest possible values\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
Siwinska et al., 2021\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
Hair clipping, skin washing with chlorhexidine soap and alcohol, use of
coupling gel\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
MyLab 30 Gold Vet (Esaote). 1MHz to 5MHz convex probe.\strut
\end{minipage} & \begin{minipage}[t]{0.24\columnwidth}\raggedright\strut
SV set at 5 to 10mm and decreased to small as possible WF of 50 or
100Hz\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}

Table 2 - Characterization of patient preparation and ultrasound machine
and settings of the studies included (n = 5) in the systematic review.
Abbreviations: US ultrasonography, ICS intercostal space, PL paralumbar,
NR not reported, WF wall filter, SV sample volume, PRF pulse repetition
frequency

\par\null

\emph{RI measurements}

All five studies included in this review reported data on RI
measurements in healthy horses and none of them reported PI values. A
total of 128 healthy horses were assessed in the studies; data collected
are presented in Table 3. Among the five studies, one has reported a
mean value for both kidneys whereas the other four have presented the
values for left and right kidneys separately. Only Hoffmann et al.
{[}31{]} has used pyelorenal arteries, all other authors have chosen
intrarenal arteries, being those the arcuate and/or interlobar. All
writers presented the RI values as mean and standard deviation. The
higher value measured across studies was 0.58 \selectlanguage{ngerman}± 0.06 for the right
kidney of untrained horses {[}11{]} and the lowest value was 0.46 ± 0.04
for the left kidney of foals {[}28{]}. Hoffmann and colleagues {[}31{]}
accepted horses` RI normality value as being of the same order of
humans, cats and dogs, in which 0.70 is considered to be the upper
limit.

As a method to calculate a more reliable RI value, Hoffmann et al.
{[}31{]} reported that at least seven continuous-spectral waves
consisting of peak systolic and end diastolic velocities were attempted.
Macrì and colleagues {[}11{]} repeated measurements three times on each
kidney and Siwinska et al. {[}28,30{]} have acquired three adequate
waveforms. Lastly, Freccero and peers {[}29{]} have selected at least
one 8-second spectral tracing from each kidney.\selectlanguage{english}
\begin{longtable}[]{@{}llllllll@{}}
\toprule
\begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
Reference\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
Reference\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
Artery of interest\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
Artery of interest\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
Grouping (n)\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
Grouping (n)\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
RI\strut
\end{minipage} & \begin{minipage}[b]{0.10\columnwidth}\raggedright\strut
RI\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
Hoffmann et al., 1997\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
Hoffmann et al., 1997\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
Pyelorenal\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
Pyelorenal\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
Non-sedated (7)\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
Non-sedated (7)\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
0,512 \selectlanguage{ngerman}± 0,004\strut
\end{minipage} & \begin{minipage}[t]{0.10\columnwidth}\raggedright\strut
0,512 \selectlanguage{ngerman}± 0,004\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Macrì et al., 2015\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Interlobar and arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Interlobar and arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Male (5) Female (8) Trained (5) Untrained (8) Total: 13\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Male (5) Female (8) Trained (5) Untrained (8) Total: 13\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Male: 0.50 \selectlanguage{ngerman}± 0.05 Female: 0.50 ± 0.06 Trained: 0.52 ± 0.04
Untrained: 0.48 ± 0.06\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Male: 0.50 \selectlanguage{ngerman}± 0.05 Female: 0.50 ± 0.06 Trained: 0.52 ± 0.04
Untrained: 0.48 ± 0.06\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
RK: Male: 0.56 \selectlanguage{ngerman}± 0.03 Female: 0.57 ± 0.06 Trained: 0.55 ± 0.01
Untrained: 0.58 ± 0.06\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Siwinska et al., 2019\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Interlobar or arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Interlobar or arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Foals (15) Adults (15) Elderly (15) Total: 45\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Foals (15) Adults (15) Elderly (15) Total: 45\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Foals: 0.46 \selectlanguage{ngerman}± 0.04 Adults: 0.48 ± 0.05 Elderly: 0.52 ± 0.05\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Foals: 0.46 \selectlanguage{ngerman}± 0.04 Adults: 0.48 ± 0.05 Elderly: 0.52 ± 0.05\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
RK: Foals: 0.47 \selectlanguage{ngerman}± 0.05 Adults: 0.48 ± 0.05 Elderly: 0.52 ± 0.05\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Freccero et al., 2020\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Adults (18) Elderly (15) Trotters (23) Other breeds (10) Total: 33\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Adults (18) Elderly (15) Trotters (23) Other breeds (10) Total: 33\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Adults: 0.51 \selectlanguage{ngerman}± 0.01 Elderly: 0.51 ± 0.004 Trotters: 0.51 ± 0.01
Other breeds: 0.51 ± 0.003\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Adults: 0.51 \selectlanguage{ngerman}± 0.01 Elderly: 0.51 ± 0.004 Trotters: 0.51 ± 0.01
Other breeds: 0.51 ± 0.003\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
RK: Adults: 0.58 \selectlanguage{ngerman}± 0.004 Elderly: 0.59 ± 0.01 Trotters: 0.58 ± 0.01
Other breeds: 0.59 ± 0.01\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Siwinska et al., 2021\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Interlobar or arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Interlobar or arcuate\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Healthy (15F/15M) Total: 30\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
Healthy (15F/15M) Total: 30\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Healthy: 0.50 \selectlanguage{ngerman}± 0.05\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
LK: Healthy: 0.50 \selectlanguage{ngerman}± 0.05\strut
\end{minipage} & \begin{minipage}[t]{0.12\columnwidth}\raggedright\strut
RK: Healthy: 0.50 \selectlanguage{ngerman}± 0.04\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{ngerman}

Table 3 - Characterization of resistivity index of healthy horses'
groups of the studies (n = 5) included in the systematic review.

Abbreviations: RI resistivity index, LK left kidney, RK right kidney, F
female, M male.

\par\null

\emph{Other findings}

Macrì et al. {[}11{]} and Freccero et al. {[}29{]} reported differences
in the RI values from right and left kidneys of the horses evaluated in
their study. No study has found difference in the RI values related to
gender. Siwinska et al. {[}28{]} assessed repeatability in their study
and found a high correlation between measuring time-points. She and her
group also noted a higher RI value among the elderly horses compared to
adults and foals. They have also shown that RI is affected by the pulse
pressure. All studies have considered the renal ultrasonographic
examination for obtaining RI value as time consuming, dependent on the
horse´s willing to cooperate and dependent on the operator´s experience
to perform the exam.

\emph{Risk of Bias}

The risk analysis applied in this systematic review was adapted from the
SYRCLE tool {[}26{]} and the results are demonstrated in Table 4 below.

Concerning selection bias, allocation concealment was not included due
to the types of studies. For allocation sequence, it was considered a
high risk for all five studies {[}11,28,29,30,31{]} as the authors have
selected animals after taking laboratorial tests to ensure horses' good
health and so it cannot be considered as random allocation. In regard to
baseline characteristics, Hoffmann et al. {[}31{]} did not describe in
details the animals' conditions prior to ultrasound examinations as the
other four studies {[}11,28,29,30{]} did, so to his study the risk was
considered as unclear and to the others it was considered as low risk.

The performance bias of animal housing and management was addressed as
high risk for one study {[}31{]} that did not report any data on this
matter, as unclear risk for two studies {[}29,30{]} that informed
incomplete data and as low risk to two studies {[}11,28{]} that
described in details the housing, feeding, management, handling and
exercising routine of the horses. Another source of bias was the outcome
assessor and its randomness. In this matter, the experience level of the
evaluator was assessed and whether it was the same person to perform the
examinations in all horses during the research. The study that did not
report any information was considered as high risk, if there was at
least one information available, it was considered as unclear risk and
as low risk if there was enough data.

Regarding the risk of incomplete outcome data, we assessed it by
analyzing if the study has demonstrated the expected results, if all
proposed RI measurements were concluded and if they were achieved in
both kidneys and in all horses. Furthermore, to evaluate the risk of
selective outcome reporting, we analyzed if the study reported data
about all proposed outcomes and methods of animal evaluation, if they
mentioned the ethical committee protocol or equivalent and if it was
clear whether all expected results were demonstrated. For both
previously cited risks, the studies were considered as high risk if they
did show any of the cited characteristics, as unclear if they reported a
few information and as low risk if they presented all information
needed.

Other high risks assigned to the retrieved articles were related to a
small sample number {[}11,31{]}, one-time observation on renal RI
{[}11,29,30,31{]} and to not performing blood pressure measurement
{[}11,30{]}, as this parameter is known to potentially interfere with
the renal RI value.\selectlanguage{english}
\begin{longtable}[]{@{}lllllll@{}}
\toprule
& & HOFFMANN, 1997 & MACR\selectlanguage{ngerman}Ì, 2015 & SIWINSKA, 2019 & FRECCERO, 2020 &
SIWINSKA, 2021\tabularnewline
\midrule
\endhead
Selection bias & Allocation sequence & - & - & - & - & -\tabularnewline
& Baseline characteristics & ? & + & + & + & +\tabularnewline
Performance bias & Animal housing and management & - & + & + & ? &
?\tabularnewline
Detection bias & Outcome assessor & - & + & + & + & ?\tabularnewline
Attrition bias & Incomplete outcome data & - & ? & + & - &
-\tabularnewline
Reporting bias & Selective outcome reporting & ? & ? & + & + &
+\tabularnewline
Other sources of bias & Small sample number & - & - & + & + &
+\tabularnewline
& Single moment of evaluation & - & - & + & - & -\tabularnewline
& Blood pressure measurement & - & + & + & + & -\tabularnewline
\bottomrule
\end{longtable}

Table 4 - Assessment of methodological quality of reviewed reports.
Symbols were addressed to each bias regarding the five evaluated
studies, standing for high risk (- red), unclear risk (? yellow) and low
risk (+ green). MUST BE COLORED

\textbf{Discussion}

Despite B mode ultrasound being largely used in the equine veterinary
practice, its relevance to renal evaluation is limited as morphology
does not always relate to function {[}32{]}. On the other hand, the
noninvasive Doppler sonography is able to provide data in respect to
renal blood flow and vascular resistance {[}16{]}. The RI derives out of
the information given in the Doppler arterial waveforms and reflects the
hemodynamics of the targeted tissue {[}12,33{]}, which in turn, can
reflect its function and, as so, an impaired function {[}17{]}.

Although the RI is still not extensively used in veterinary medicine, it
is being considered as an important tool to assess renal
microcirculation in physiological and pathological situations {[}34{]},
most widely considered today for dogs and cats {[}14,20,22, 24{]}.
However, a number of elements can influence renal RI, such as arterial
characteristics (i.e. aortic stiffness), and systemic hemodynamics
factors (i.e. pulse pressure, hydration status) {[}17,33,34{]}. It is
crucial to keep that information in mind when undertaking a RI study.

Although renal RI relevance in humans and other animal species have been
demonstrated, the lack of information for equines and its physiological
range of value, motivated this systematic review. A compilation of renal
RI values obtained from healthy horses in five eligible studies was
made, as well as a description of study methodology, equipment
adjustments, technical information and patient preparation. All
information acquired was analyzed in order to develop a standardized
method to perform renal Doppler ultrasonography and to evaluate the
reference range for renal RI values in horses. Unfortunately, due to the
limited number of studies and the methodological variation between them,
a meta-analysis was not possible. This impaired the evaluation of the
reference range, making it clear that more studies are still needed in
horses.

Regarding patient preparation, the five selected studies
{[}11,28,29,30,31{]} described this step minutely and were consentaneous
about hair clipping, use of coupling gel and the location of
examination. Also, Siwinska et al. {[}28{]} and Freccero et al. {[}29{]}
described important strategies to minimize stress, as it can affect the
waveforms, and thus the RI value {[}35{]}, which should be observed in
future studies.

The transabdominal approach was a successful method in all studies,
using a 2 to 5MHz frequency curvilinear probe {[}11,28,29,30,31{]}. It
has been already described that this frequency range is more suitable
for abdominal ultrasound imaging in horses {[}36{]}, shown by these 5
studies to be also suitable for Doppler ultrasound and, thus, RI
measurements. For ultrasound examination, all operators first performed
the B mode evaluation of the kidneys, used the color Doppler to set the
artery and then got the Doppler waveforms on spectral Doppler. Another
important information concerns equipment settings as reason for better
image resolution, lowering occurrence of artifacts and, thus, providing
a more reliable result. In this light, pulse repetition frequency and
wall filter should be set as lower as possible to avoid aliasing
{[}37{]} and wall artifacts or clutter {[}38,39{]}, respectively. Sample
volume size should be adjusted to artery diameter and positioned in the
vascular lumen {[}35{]}, but it is still not standardized for horses.
These aspects described in the works included in this review should also
be observed in future studies.

Some authors {[}28,30,31{]} have found it difficult to retrieve a good
quality image from left kidney in comparison to right kidney. Siwinska
et al. {[}28{]} have attributed this difficulty to the anatomical
location of the organ, that lays under the spleen and is surrounded by
intestinal components. The target arteries (arcuate and interlobar) was
the same in four studies {[}11,28,29,30{]}, only Hoffmann and others
{[}31{]} used the pyelorenal artery due to the equipment they had
available. The ideal vessel for RI measurement is still not well
described for horses; however, it has been demonstrated that lower
caliber arteries suffer more from flow changes, thus producing a greater
variation in the RI value {[}14,40{]}. Also, it has been reported that
it is necessary to acquire three to five RI measures to properly get a
RI definitive value {[}41{]}. Two of the reviewed studies {[}11,31{]}
did not mention if they managed to get all desired waveforms and the
other three {[}28,29,30{]} have reached a lower number that they
expected. Yet, all five studies considered RI values to be reliable.
Based on studies in other species, we strongly suggest future works to
acquire at least 3 waveforms when conducting RI analysis and that future
studies may be done with such objective.

Macr\selectlanguage{ngerman}ì et al. {[}11{]} and Freccero et al. {[}29{]} have reported
different RI values for right and left kidneys, as showed in Table 3.
However, the other three studies {[}28, 29, 30{]} did not show RI
disparity, corroborating with cats, dogs and humans' findings {[}14, 18,
20{]}. No explanation is yet available for these divergent values
between kidneys, and so more research addressing this specific question
is still needed.

Siwinska et al. {[}28{]} found a higher RI value in the group of elderly
horses (0.52 ± 0.05 vs 0.48 ± 0.05 in adults; 0.52 ± 0.05 vs 0.47 ± 0.05
for right kidney and 0.46 ± 0.04 for left kidney in foals). For humans,
changes in the RI value according to age have been described, being
higher in infants and in the elderly population {[}44-47{]}. For dogs,
the age seems to influence the renal RI value as well, mostly during the
first three weeks of life, being higher in this period and then slowly
decreasing until adult values at 12 weeks {[}49{]}. RI changes according
to age are still unclear in cats {[}20{]} and should still be a subject
of study in horses.

Regarding the expected range of value for each species, it can be
noticed that they diverge from equine findings; for equine, the RI
values are mostly under 0.60 while for the other mentioned species the
upper limit is considered to be 0.70 {[}18,24,42{]}. For humans, a
normal renal RI value of 0.60 ± 0.01(mean and SD) and a threshold of
0,70 is being accepted nowadays {[}43,44{]}. For cats, the normal renal
RI values range has been reported to be between 0.64 and 0.72 {[}20{]}.
Further, the mean renal RI for dogs found in a study with 27 healthy
animals was 0.62 ± 0.04 {[}48{]} and the considered upper limit is the
same as for humans {[}22{]}.

Although at first it was not considered for appraisal by this systematic
review, Siwinska et al. {[}30{]} also evaluated two other groups that
can be interesting for our objectives: animals at risk of developing
acute kidney injury (AKI) and animals with clinical AKI. Siwinska and
her colleagues identified that even in the nonhealthy categories, the
renal RI values did not reach or pass 0.70, the RI value used for humans
and small animals, which brings the question whether this upper limit is
suitable for the equine species. In this regard, more studies on the
theme are still necessary to determine a reliable renal RI reference
range for horses.

Siwinska et al. {[}28{]} have analyzed their results in correlation to a
number of physiological parameters, such as age, heart rate, body weight
and blood pressure. They found no interaction among the RI and cited
parameters, however, there was an association between pulse pressure and
the obtained renal RI values. Therefore, for future studies, researchers
may include the measurement of pulse pressure in order to perform a
better evaluation of the renal RI results. Freccero et al. {[}29{]}
compared renal RI values to physiological parameters as well, being age,
breed, body weight and body condition and also did not find any
correlation.

\textbf{Conclusions and future directions}

Although renal RI has been stablished over the years as an efficient
tool in human medicine and has been a matter of interest for more than a
decade in regard to small animals, its usefulness in the equine medicine
is still not demonstrated. It is crucial that a variety of studies still
need to be conducted to ensure that renal RI has clinical utility in
horses. Determining a normal range for equine renal RI is still
necessary in a larger population, including comparisons with horses
proven to present kidney disease, once all studies enrolled in this
systematic review found a RI value between 0.50 and 0.64 (mean values)
in the 128 examined animals, much lower than the upper limit considered
for humans, cats and dogs of 0.70.

As future directions, we suggest a few patterns to be followed during
transabdominal renal ultrasound examination. For animal preparation,
hair clipping and use of coupling gel are very important, but if it is
not possible to trim the horse, the haircoat should be abundantly rinsed
with alcohol. A curvilinear probe is more suitable for the exam and the
frequency range should be between 2 and 5MHz. The wall filter should be
set at 50Hz, a sample volume of 2 to 4mm should be preferred and a lower
as possible pulse repetition frequency should be set. In order to locate
the artery to be assessed, the color or power Doppler must be employed.
All this information should be included on the description of the
material and methods. It is crucial that at least three waveforms are
acquired from each kidney, so the RI value could be more reliable. The
RI value can be presented as mean and standard deviation, separating
right and left kidney as there is still doubt that difference exist and
since upon disease, kidneys can be differently affected. Lastly, as the
pulse pressure have been shown to influence the RI results, it should
also be measured and taken into consideration when evaluating the
kidneys. We believe and hope that in a short future other works on the
topic will be presented and further evaluation will be made.

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