Small Ruminant Research 152 (2017) 86–99

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Small Ruminant Research

journal homepage: www.elsevier.com/locate/smallrumres

Ultrasonographic examination of the udder in sheep

M.S. Barbagianni, V.S. Mavrogianni, N.G.C. Vasileiou, G.C. Fthenakis, I.G. Petridis ∗
Veterinary Faculty, University of Thessaly, 43100, Karditsa, Greece

a r t i c l e i n f o a b s t r a c t

Article history: Objective of the paper is to review work relevant to ultrasonographic examination of the udder of ewes.
Available online 21 December 2016 Udder structures that can be readily imaged ultrasonographically (B-mode or Doppler examination)
are mammary parenchyma, the gland cistern, the lactiferous ducts, the mammary vessels, the teat and
Keywords: the supramammary lymph nodes. Conventional diagnostic approaches for mastitis (i.e., combination of
Cistern clinical, bacteriological and cytological examinations) provide a good means for diagnosis of mastitis;
Diagnosis
hence, in diagnosis of mastitis, use of ultrasonographic examination has, in general, an ancillary role, for
Ewe
example during investigation of cases, in which clinical diagnosis alone can prove of little help, e.g., in
Mammary gland
Mammary parenchyma
animals with small-sized, deep mammary nodules. The technique can be used at the end of a lactation
Mastitis period as part of routine udder examination performed at that point, which would provide additional
Milk yield useful information, e.g., regarding presence of abcesses or of increased quantity of fibrous tissue. Further,
Sheep estimation of the dimensions of gland cistern of ewes in a flock would support decisions regarding milking
Teat frequency to be applied. Finally, examination of the teat can provide indications regarding optimising
Ultrasonography use of the milking machine by applying the appropriate settings.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction review work relevant to ultrasonographic examination of the udder

of ewes.
The importance of the mammary glands in the profitability of
ewes, especially in dairy flocks, makes early and accurate diagno-
2. Methodology of ultrasonographic examination
sis of its disorders necessary. This will, in turn, support efficient
management of cases of diseased animals. The matter is of signifi-
2.1. Principles of ultrasonographic examination of the udder of
cance for the welfare of the affected animals (European Food Safety
ewes
Authority, 2014), as well for their productivity in terms of quantity
and quality of milk produced.
Ultrasonographic examination can be used to explore the struc-
The diagnosis of clinical or subclinical mastitis in ewes has been
ture of the udder of ewes, as well as to study functional parametres
recently reviewed by Fragkou et al. (2014). Various approaches can
of the organ (Ruberte et al., 1994; Caja et al., 1999; Nudda et al.,
be employed, which more often include clinical, bacteriological
2000; Petridis et al., 2014; Barbagianni et al., 2015). By using
and/or cytological techniques and methodologies. Use of ultra-
ultrasonographic examination, monitoring of the udder can be per-
sonography has also been advocated and various publications have
formed and information may be obtained regarding its internal
indicated the usefulness of the technique in the diagnosis of mam-
structures, as ultrasonographic images of the mammary gland cor-
mary diseases of ewes. Further, the technique can be employed
respond well to its anatomical structure (Ruberte et al., 1994).
in management practices in healthy animals, e.g., for selection of
The technique can be used for examination of the mammary
animal for increased milk production, based on the volume of the
parenchyma, the gland cistern and/or the teat (Franz et al., 2001)
gland cistern. Finally, other workers have used the methodology
and the supramammary lymph nodes (Hussein et al., 2015), as
for research purposes to support the study of various mechanisms
well as for evaluation of blood flow disorders (Petridis et al.,
in healthy or diseased animals. Objective of the current paper is to
2014; Barbagianni et al., 2015; Barbagianni, 2016). Further, dur-
ing ultrasonographic examination details are collected in real time,
as processes are developing.
Udder structures that can be readily imaged ultrasonographi-
∗ Corresponding author. cally are the body of the mammary gland (corpus mammae) with
E-mail address: ipetridis@hotmail.com (I.G. Petridis). the mammary parenchyma, the gland cistern (sinus lactiferous),

http://dx.doi.org/10.1016/j.smallrumres.2016.12.009
0921-4488/© 2016 Elsevier B.V. All rights reserved.
 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99 87

Fig. 1. B-mode ultrasonographic presentation of mammary parenchyma; image taken at the 6th month of lactation period, along the long axis of the udder; mildly echogenic
®
mammary parenchyma and section of the external pudendal artery with its echogenic wall and its three branches. Image taken and processed on a MyLab 30 ultrasonography
system (ESAOTE SpA, Genova, Italy) with microconvex transducer, imaging frequency: 3.3 MHz – scanning depth: 120 mm.

Table 1
Summary of references regarding use of transducers during ultrasonographic examination of various structures of the udder of ewes.

Reference Details of transducer employed Part of udder examined

Ruberte et al. (1994) 5.0 MHz sector Gland cistern

Nudda et al. (2000) 3.5 MHz convex sector Gland cistern
Franz et al. (2001) 12.0 MHz linear Teat (examination through water filled plastic cup)
Franz et al. (2003) 8.5 MHz Teat, gland cistern, mammary parenchyma
Mavrogianni et al. (2004) 6.0 MHz sector Teat (direct application)
Wójtowski et al. (2006) 10.0 MHz linear Teat (examination through water filled plastic cup)
Castillo et al. (2008) 5.0 MHz sector Gland cistern
Rovai et al. (2008) 5.0 MHz sector Gland cistern
Alejandro et al. (2014b) 5.0 and 7.5 MHz linear Teat (examination through water filled plastic cup)
Petridis et al. (2014) 10.0 MHz linear Mammary parenchyma
3.3 MHz Gland cistern
microconvex
Barbagianni et al. (2015) 10.0 MHz linear Mammary parenchyma
Hussein et al. (2015) 7.5 MHz linear and Teat, mammary parenchyma, supramammary lymph nodes
4.0 MHz convex
Barbagianni (2016) 12.0 MHz linear Teat (direct application)

the lactiferous ducts (ducti lactiferi), the mammary vessels [espe-
cially the external pudendal artery (arteria pudenda externa) with
the three branches: caudal mammary artery (arteria mammaria
caudalis), mid mammary artery (arteria mammaria media), cra-
nial mammary artery (arteria mammaria cranialis) (Fig. 1), as well
as the larger mammary veins: mid mammary vein (vena mam-
maria media), cranial mammary vein (vena mammaria cranialis),
external pudendal vein (vena pudenda externa)], the teat (papilla
mammae) with the teat duct (ductus papillaris), the teat cistern
(sinus papillaris) and the teat arteries (arteriae papillares), and the
supramammary lymph nodes (lymphonodi inguinalis superficialis).
Benefits from using udder ultrasonographic examination depend
strongly on the operator’s experience; more experienced opera-
tors would produce better images, with increased repeatability, and
leading to more accurate interpretation (Klein et al., 2005; Díaz et
al, 2013).
The ultrasonographic examination of the mammary glands in
sheep can be performed with the animal in the standing position,
under mild restraint by an assistant. Wherever there is availabil-
ity, the examination can take place in the milking parlour, which
would improve work-flow and ease of work for the operator and
also decrease time required for the examination. Hairs on the
udder should be clipped, to facilitate the procedure and to obtain
improved image. Coupling gel should be applied on the udder and
the examination starts by placing the transducer on the caudal
surface of the udder.
The type of transducer employed for the examination differs
depending on the available equipment, the structure of the udder
and the specific structure under examination. Types of transducers
referenced in the literature are summarised in Table 1.
2.2. Ultrasonographic examination of mammary parenchyma
For ultrasonographic examination of the parenchyma, a linear
transducer is used most often. This should be placed transcuta-
neously, in a position perpendicular to the long axis of the udder.
Initially, dorsal sections of the mammary parenchyma are taken,
starting from the upper part downwards; then, the transducer is
moved around the axis of the udder. The images can be evaluated
immediately or can be saved for further processing and detailed
88 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99

Fig. 2. B-mode ultrasonographic presentation of gland cistern; image taken at the 6th month of lactation period, in an inclined sagittal scan towards the teat; presence of
®
small clots (arrow) floating inside the cistern. Images taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with microconvex transducer,
imaging frequency: 3.3 MHz – scanning depth: 120 mm.

Fig. 3. B-mode ultrasonographic presentation of the gland cistern; image taken at the 6th month of lactation period, in an inclined sagittal scan towards the teat; presence of a
®
large clot (arrow) floating inside the cistern. Images taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with microconvex transducer,
imaging frequency: 3.3 MHz – scanning depth: 120 mm.

evaluation later. Scanning depth and frequency employed vary and
depend on the size of the udder examined, as well as on the avail-
able equipment. A frequency of 7.5–10.0 MHz can be used in most
cases (Petridis et al., 2014; Barbagianni et al., 2015); a smaller fre-
quency may be occasionally needed in animals with a larger udder.
One mammary gland is imaged initially, which is followed by imag-
ing of the contralateral gland.
There is particular scope for analysis of grey-scale intensity of
images of mammary parenchyma (Petridis et al., 2014; Barbagianni
et al., 2015). This would provide indirect information regarding
amount of fluids (i.e., lacteal secretions) into the parenchyma and
also, possibly, about the amount of glandular tissue. In an image
processing context, grey-scale analysis refers to the image’s overall
pixel grey intensity values (Ojala et al., 2002) and can be performed
by means of various image processing softwares (e.g., ImageJ;
National Institutes of Health, Rockville Pike, MD, USA). For analysis
of grey-scale of the whole parenchyma, it is recommended to eval-
uate intensity values of at least three images of the parenchyma,
each presenting a different part of the parenchyma with the median
value calculated at the end; areas with vessels or ductal formations
should not be taken into account for the grey-scale analysis (Petridis
et al., 2014; Barbagianni et al., 2015). In analysis of grey-scale inten-
 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99
Fig. 4. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the penultimate week of pregnancy, at a level immediately above the gland
cistern; non-homogeneous mammary parenchyma, due to incomplete development
during lactogenesis (for fully developed mammary parenchyma: Fig. 5). Image taken
®
and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy)
with linear transducer, imaging frequency: 10.0 MHz – scanning depth: 60 mm.
Fig. 5. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the last week of pregnancy, at a level immediately above the gland cistern;
homogeneous, mildly echogenic fully developed mammary parenchyma, with no
abnormalities evident therein (for underdeveloped mammary parenchyma: Fig. 4).
®
Image taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA,
Genova, Italy) with linear transducer, imaging frequency: 10.0 MHz – scanning
depth: 60 mm (Barbagianni et al., 2015).
sity of images, results are expressed on a 0 (black) to 255 (white)
scale.
2.3. Ultrasonographic examination of gland cistern
After examination of the parenchyma, the gland cistern can be
examined. The gland cistern can be better visualised by means of
a microconvex or sector transducer. An inclined sagittal imaging
plane should be taken, starting from the upper part of the inter-
mammary groove (sulcus intermammarius) towards the teat, which
should be used as the scanning axis. That way, the size of the cistern
can be initially estimated; then, by moving the transducer to the
left and the right, upwards and downwards, after a 90◦ rotation, it
is possible to check for clots, fibrous tissue development/formation
and/or lactoliths (Figs. 2, 3). By means of the inclined sagittal image,
the whole cistern can be visualised in one scan (Ruberte et al., 1994).
Nudda et al. (2000) have proposed the application of the transducer
on the inguinal-abdominal fold at the side of the udder and, by hav-
89
Fig. 6. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the last week of pregnancy, at a level immediately above the gland cistern;
homogeneous, mildly echogenic fully developed mammary parenchyma, with pres-
ence of well-developed lactiferous ducts. Image taken and processed on a MyLab
®
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer,
imaging frequency: 10.0 MHz – scanning depth: 60 mm.
Fig. 7. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the last week of pregnancy at the level of the gland cistern; presence
of well-developed lactiferous ducts and gland cistern. Image taken and processed
®
on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear
transducer, imaging frequency: 10.0 MHz − scanning depth: 60 mm.
ing the teat as a scan axis, to take cross sections of the contralateral
gland cistern. Bruckmaier and Blum (1992) have created vertically-
cut images with the scanning plane longitudinally through the teat
canal; cross sections of the entire udder, including the parenchyma
and teat cisternal cavities, were examined vertically through the
teat from below. However, the approach would be time-consuming
and difficult to perform in field conditions (Bruckmaier and Blum,
1992; Bruckmaier et al., 1997). In animals with large cisterns, a
decreased frequency, e.g. 3.5 MHz, would be required and an ade-
quate scanning depth should be selected, in order for the entire
cistern to be visualised (Castillo et al., 2008; Rovai et al., 2008).
Measurement of the volume of the cistern can be difficult, because
of the irregular shape of the structure; hence, only measurements
of the area of one or more cross sections can be taken (Nudda et al.,
2000); nevertheless, there is scope for use of three-dimensional
ultrasonography, which might possibly improve direct evaluation
of the volume of gland cistern. In any case, if such an examination
90 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99
Fig. 8. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the 3rd week of lactation period at the level of the branching of the external
pudendal artery; homogeneous, mildly echogenic mammary parenchyma, with no
abnormalities evident therein; the external pudendal artery and the external puden-
® ®
dal vein are imaged vertically sectioned. Image taken and processed on a MyLab
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer,
imaging frequency: 10.0 MHz – scanning depth: 60 mm.
Fig. 9. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the 3rd week of lactation period at the level of the branching of the external
pudendal artery; homogeneous, mildly echogenic mammary parenchyma, with no
abnormalities evident therein; vertical sections of the external pudendal artery and
®
its branches are imaged. Image taken and processed on a MyLab 30 ultrasonogra-
phy system (ESAOTE SpA, Genova, Italy) with linear transducer imaging frequency:
10.0 MHz – scanning depth: 60 mm.
would be undertaken, it has been indicated that an interval of 8 h
between milking and imaging should be maintained, as this leads
to improved results in analysis of the relevant data (Castillo et al.,
2008).
2.4. Ultrasonographic examination of teat
The teat can be immersed into a plastic cup filled with warm
water, to avoid its deformation during imaging and visualisation
(Franz et al., 2001), with the transducer placed outside the cup.
Alternatively, the teat could be filled with milk and the transducer
Fig. 10. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the 3rd week of lactation period at the level immediately after the branch-
ing of the external pudendal artery; homogeneous, mildly echogenic mammary
parenchyma, with no abnormalities evident therein. Image taken and processed
on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear
transducer, imaging frequency: 10.0 MHz – scanning depth: 60 mm.
Fig. 11. B-mode ultrasonographic presentation of mammary parenchyma; image
taken on the 2nd month of lactation period at the level immediately after the
branching of the external pudendal artery; homogeneous, sub-echogenic mammary
parenchyma, with no abnormalities evident therein. Image taken and processed
®
on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear
transducer, imaging frequency: 10.0 MHz – scanning depth: 60 mm (Petridis et al.,
2014).
placed directly on the teat skin after gel has been applied on it
(Mavrogianni et al., 2004; Barbagianni, 2016). Franz et al. (2001)
have indicated that a high frequency of 12.0 MHz is necessary for
good imaging of the teat structures, although Díaz et al. (2013) have
reported that, for imaging of the layers of the teat wall, a 7.5 MHz
transducer would be more useful. Scanning starts from the base of
the teat and continues towards its orifice (Mavrogianni et al., 2004;
Fragkou et al., 2014). Scanning depths of 20–30 mm can be used
during the examination.
2.5. Ultrasonographic examination of supramammary lymph
nodes
For examination of the supramammary lymph nodes, the trans-
ducer is placed on the area dorsal and lateral to the caudal aspect
of udder halves. The lymph nodes can be easily identified from
 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99 91

Fig. 12. B-mode ultrasonographic presentation of mammary parenchyma; image taken on the 2nd month of mammary involution at the level immediately after the branching
of the external pudendal artery; homogeneous, significantly sub-echogenic mammary parenchyma, with no abnormalities evident therein. Image taken and processed on a
®
MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer, imaging frequency: 10.0 MHz – scanning depth: 60 mm (Petridis et al., 2014).

Fig. 14. B-mode ultrasonographic presentation of mammary parenchyma; image

Fig. 13. B-mode ultrasonographic presentation of mammary parenchyma; image
taken 3 days after development of mastitis associated with Mannheimia haemolytica,
at the level immediately before branching of the external pudendal artery; non-
homogeneous mammary parenchyma with areas of increased echogenicity. Image
®
taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Gen-
ova, Italy) with linear transducer, imaging frequency: 10.0 MHz – scanning depth:
60 mm.
their well-demarcated echogenic capsule and their echogenic lin-
ear structure that runs longitudinally through their centre (Kofler
et al., 1998; Hussein et al., 2015). The two lymph nodes can be
easily distinguished between them, if the ipsilateral branch of the
mammary artery is followed.
2.6. Ultrasonographic examination of udder blood vessels
The mammary blood vessels are best imaged by using Doppler
ultrasonographic examination. In Doppler examination, blood ves-
sels would appear blue or red, in accord to the movement of the red
cells within the vessels (moving towards or away from the probe)
taken 3 days after development of mastitis associated with Mannheimia haemolyt-
ica, at the level immediately before the gland cistern; non-homogeneous mammary
parenchyma with areas of increased echogenicity and foci of early stage of devel-
®
opment of fibrous tissue (arrows). Image taken and processed on a MyLab 30
ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer, imag-
ing frequency: 10.0 MHz – scanning depth: 60 mm.
and the settings implemented in the ultrasound machine. That way,
the external pudendal artery and its branches can be easily identi-
fied. Initially, the transducer is placed perpendicular to the long axis
of the gland near its attachment to the abdomen; once the external
pudendal artery has been localised, the transducer is rotated 90◦
and moved gently to the left and the right, in order to get a lon-
gitudinal/lengthwise cross-section of the vessel and its branches
(Fig. 1). Then, the colour Doppler gate is positioned within the ves-
sel examined, with no contact to the wall; when optimal flow is
achieved, a spectral mode waveform is taken. Uniform waveforms
from three consecutive cardiac cycles of the animal under exami-
nation should be considered for calculations (Petridis et al., 2014;
Barbagianni et al., 2015). The technique can also be applied in the
subcutaneous vessels of the teat. In Doppler mode examination
92 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99

Fig. 17. B-mode ultrasonographic presentation of mammary parenchyma, into

which a hard formation was palpated at clinical examination; presence of nodular-
type formation full with hypoechogenic material; arrows indicate artefact caused by
the difference in echogenicity between the content of the formation (liquid) and the
Fig. 15. B-mode ultrasonographic presentation of mammary parenchyma; image
neighbouring parenchyma (when sound waves pass through fluid-filled formations,
taken 1 day after development of mastitis associated with Mannheimia haemolytica;
decrease of reflectance occurs, leading to acoustic enhancement thereafter). Image
normal ultrasonographic appearance lost in the imaged fields; non-homogeneous ®
taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Gen-
mammary parenchyma with areas of increased or reduced echogenicity indicative
ova, Italy) with linear transducer, imaging frequency: 10.0 MHz – scanning depth:
of the extensive parenchymal damage; presence of hypoechoic oedematous foci
60 mm.
(red arrows), as well as hyperechogenic areas and foci of early stage of development
of fibrous tissue around the external pudendal artery (yellow arrow). Image taken
®
and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy)
with linear transducer, imaging frequency: 10.0 MHz – scanning depth: 60 mm. (For
interpretation of the references to colour in this figure legend, the reader is referred
to the web version of this article.)

Fig. 18. B-mode ultrasonographic presentation of mammary parenchyma, into

which a hard formation was palpated at clinical examination; presence of
nodular-type formation full with hypoechogenic material, also with areas of hyper-
echogenicity; likely a mammary abscess (same artefact as in Fig. 17). Image taken
®
and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy)
with linear transducer, imaging frequency: 10.0 MHz – scanning depth: 60 mm.

Fig. 16. B-mode ultrasonographic presentation of mammary parenchyma, into

which a hard formation was palpated at clinical examination; presence of nodular-
type formation full with hypoechogenic material, surrounded by a hyperechogenic
area; image intentionally cropped to avoid presentation of an artefact, caused by the
difference in echogenicity between the content of the formation and the neighbour-
®
ing parenchyma (for full image: Fig. 17). Image taken and processed on a MyLab
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer,
imaging frequency: 10.0 MHz – scanning depth: 60 mm.

Fig. 19. B-mode ultrasonographic presentation of mammary parenchyma, into

of the udder blood vessels, scanning frequency can vary from 5.0
to 6.6 MHz (Barbagianni, 2016). Further details regarding Doppler
ultrasonography are available in another paper of this special issue
(Petridis et al., 2017).
which hard formations were palpated at clinical examination; presence of two for-
®
mations full with hypoechogenic material. Image taken and processed on a MyLab
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer,
imaging frequency: 10.0 MHz – scanning depth: 60 mm.
 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99 93

Fig. 20. B-mode ultrasonographic presentation of gland cistern; image taken on the 2nd month of lactation period at an inclined sagittal imaging plane, from the upper part
®
of the intermammary groove towards the teat, used as the scanning axis; gland cistern at full size (for cistern at reduced size: Fig. 21). Image taken and processed on a MyLab
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with microconvex transducer, imaging frequency: 3.3 MHz – scanning depth: 120 mm (Petridis et al., 2014).

Fig. 21. B-mode ultrasonographic presentation of gland cistern; image taken on the 2nd month of mammary involution at an inclined sagittal imaging plane, from the upper
part of the intermammary groove towards the teat, used as the scanning axis; gland cistern at reduced size (for cistern at full size: Fig. 20). Image taken and processed on a
®
MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with microconvex transducer, imaging frequency: 3.3 MHz – scanning depth: 120 mm (Petridis et al., 2014).

3. Findings during ultrasonographic examination of the
udder
3.1. Findings in the mammary parenchyma
The normal mammary parenchyma is imaged as a homoge-
neous, granular structure with medium echogenicity; anechoic
structures identified therein correspond to lactiferous ducts and
vessels. The image is the result of even distribution of more echoic
connective tissue and less echoic mammary epithelial tissue; it also
depends on the filling degree of the gland, as anechoic material
(milk and lacteal secretions in general) would reduce the over-
all echogenicity of the image (Floeck and Winter, 2006; Franz
et al., 2009; Barbagianni et al., 2015). Differences in the appear-
ance of the parenchyma according to reproductive status of the
animals, i.e., pregnancy or after cessation of lactation, have been
documented, which reflected changes occurring during lactoge-
nesis or mammary involution, respectively (Figs. 4–12) (Petridis
et al., 2014; Barbagianni et al., 2015). Various systemic disorders can
have an effect in the echogenicity of the parenchyma; Barbagianni
et al. (2015) have described that grey-scale intensity of mammary
parenchyma in ewes with pregnancy toxaemia was increased in
comparison with that in healthy individuals, but the echotexture
of the image had not been altered.
Ultrasonographic images of udders with mastitis reveal non-
homogenous regions in the mammary gland, in which hyper- and
hypo-echogenic areas alternate (Franz et al., 2003), although, in
some animals, echogenicity of the parenchyma may appear nor-
94 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99
Fig. 22. B-mode ultrasonographic presentation of teat; the teat cistern, which is full
of milk, is imaged as anechoic cavity, with the teat duct marginally obvious at the
right apex of the cavity, as a hyperechoic line; the hypoechoic parallel bands present
in the teat wall, represent blood vessels. Image taken and processed on a MyLab
®
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer,
imaging frequency: 12.0 MHz – scanning depth: 30 mm.
Fig. 23. Colour Doppler ultrasonographic presentation of teat; the teat cistern,
which is full of milk, is imaged as anechoic cavity, with the teat duct marginally
obvious at the right apex of the cavity; presence of very few vessels in the subcuta-
®
neous tissue. Image taken and processed on a MyLab 30 ultrasonography system
(ESAOTE SpA, Genova, Italy) with linear transducer, imaging frequency: 6.6 MHz –
scanning depth: 20 mm.
mal, especially if only mild inflammation has developed. Further,
milk can often be imaged into the gland cistern with the char-
acteristic form of flakes; changes in the echogenicity of milk can
also be evident, as milk becomes more echogenic and has the
form of snow (Franz et al., 2009). In cases of severe mastitis,
the normal ultrasonographic appearance is lost; the mammary
parenchyma appears non-homogeneous with areas of increased
or reduced echogenicity indicative of the extensive parenchymal
damage; presence of hypoechoic oedematous foci, as well as of
hyperechogenic areas may also be evident (Figs. 13–15). During
infections with gas-forming bacteria, hyperechoic spots or bands
casting dirty shadows in a homogeneous parenchyma could be
found; in infections caused by Trueperella pyogenes, presence of
hypoechoic spots with a hyperechogenic centre has been reported
(Floeck and Winter, 2006; Franz et al., 2009). In cases of mastitis,
mammary secretion, normally anechoic, can appear with increased
echogenicity, as the result of increased cellular content therein
(Floeck and Winter, 2006). Further, development of connective tis-
sue, a feature of long-standing mastitis, might result in increase of
Fig. 24. B-mode ultrasonographic presentation of teat of a ewe with mastitis; the
wall of the teat is imaged with increased echogenicity, with presence of particularly
hyperechoic foci within the tissue; some flakes are also visible within the content of
®
the teat cistern. Image taken and processed on a MyLab 30 ultrasonography system
(ESAOTE SpA, Genova, Italy) with linear transducer, imaging frequency: 12.0 MHz –
scanning depth: 30 mm.
Fig. 25. Colour Doppler ultrasonographic presentation of teat; the teat cistern,
which is full of milk, is imaged as anechoic cavity; presence of markedly increased
blood flow into the teat vessels; image compatible with early stage of bacterial
infection through the teat duct; teat duct imaged as an hyperechoic line with bor-
ders clearly defined as hypoechoic parallel bands. Image taken and processed on a
®
MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear trans-
ducer, imaging frequency: 6.6 MHz – scanning depth: 30 mm.
the echogenicity of the mammary parenchyma (Trostle and O’Brien,
1998).
Ultrasonographic examination may also support diagnosis of
mammary abscesses, when these have small size and are located
deeply, thus not readily palpable (Hiepler et al., 2009) (Figs. 16–18).
The technique can also help in the differentiation of mammary
abscesses from haematomas or cysts, in which the image taken
indicates thin hyperechoic septae or large clots floating in ane-
choic fluid. In cases of oedema located subcutaneously in the udder,
apparent fluid-filled spaces are more extended than similar struc-
tures in haematomas; the former are also imaged as ‘the skin of the
onion’, because of the alternating hyperechoic connective tissue
and hypoechoic fluid (Floeck and Winter, 2006; Franz et al., 2009).
In contrast, mammary abscesses are imaged as round structures
with capsule and hypoechoic content (Floeck and Winter, 2006;
Fasulkov, 2012). Depending on the stage of abscess formation, a
hypoechoic capsule with hyperechoic content can also be found.
Ultrasonographic evidence of gas shadowing within an encapsu-
lated mass should be taken as supportive of the diagnosis of an
 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99 95

Fig. 26. Colour Doppler ultrasonographic presentation of teat; the content of the teat cistern is imaged with increased echogenicity and disorderly appearance, with presence
®
of hyperechoic foci; teat wall with increased echogenicity; development of neovascularisation in teat wall. Image taken and processed on a MyLab 30 ultrasonography
system (ESAOTE SpA, Genova, Italy) with linear transducer, Doppler imaging frequency: 6.6 MHz – scanning depth: 20 mm.

abscess, although mixed echogenicity images can be obtained with

both abscesses and haematomas (George et al., 2008) (Fig. 19).

3.2. Findings in the gland cistern

The size of the gland cistern has been found to correlate well
with milk production, hence ultrasonographic evaluation of its size
has been proposed for the identification of animals with increased
milk yield potential (Figs. 20, 21). That way, the technique may be
used for selection of animals for improving milk production and
milkability of ewes in a flock (Nudda et al., 2000; Castillo et al.,
2008; Ayadi et al., 2011).
Rovai et al. (2008) have concluded that selection of ewes for
increased milk yield has resulted ultimately in breeding of animals
with large gland cisterns (as confirmed by results of ultrasono-
graphic examination), which indicates that greater volumes of milk
can be accommodated therein. These animals can be more tolerant
to long intervals between milkings (Rovai et al., 2008). Therefore,
estimation of the size of the gland cistern can be used in choos-
ing appropriate intervals between milkings, which would improve
overall productivity in a flock (Labussiere, 1988; Nudda et al., 2000;
Castillo et al., 2008).

3.3. Findings in the teat

The teat wall has a three layer construction; below the external
hyperechoic skin, there are the less echoic muscle and connective
tissue layer and the hyperechoic mucosa layer. The teat cistern
appears as a uniformly anechoic structure, better visualised when
filled with milk (Franz et al., 2001); hypoechoic parallel bands, rep-
resenting blood vessels may also be imaged therein (Figs. 22–24).
During ultrasonographic examination of teats removed from dead
ewes, the teat duct was imaged as a hyperechoic line around
8.0–9.0 mm in length and 0.2 mm in width, with borders clearly
defined as hypoechoic parallel bands (Franz et al., 2001). The hyper-
echogenicity of the teat duct has been attributed to the stratified
keratinised squamous epithelium (Franz et al., 2001).
In cases of mastitis, the content of the teat cistern often con-
tains hyperechogenic foci (Fig. 24). Increased vascularisation in
the teat wall may become evident during Doppler examination
(Figs. 25, 26). Ultrasonographic examination may also be useful in
identifying the cause of teat stenosis (e.g., injury, lactoliths, polyps,
papillomas, foreign body, congenital disorder) and establishing a
prognosis in ewes with ensuing milk flow disorders. It may also sup-
port diagnostic differentiation between suspected conjoined teats
Fig. 27. B-mode ultrasonographic presentation of a teat, into which a hard, cord-like
structure had been palpated lengthwise; presence of a long hyperechoic line under
the mucosa of the teat cistern (S: skin; T: subcutaneous teat tissues; M: mucosa of
the teat cistern; TC: teat cistern). Image taken and processed on an AMI B7 ultra-
sonography system (Alliance Medical, Quebec, Canada) with a sector transducer,
imaging frequency: 6.0 MHz – scanning depth: 40 mm (Mavrogianni et al., 2004).
from teat fistulas (Franz et al., 2009). Imaging can reveal presence
of haematomas or abscesses into the teat, as well as development
of fibrous tissue within the teat, leading in stenosis. In experimen-
tally induced teat stenosis, a hyperechoic line running lengthwise
under the mucosa of the teat cistern has been observed; it has
been hypothesised that this was the result of extensive fibrosis
(Fig. 27) (Mavrogianni et al., 2004). Less often, foreign bodies may
be observed into a teat, whilst the post-operative process after teat
surgery may also be evaluated by ultrasonographic observation
(Franz et al., 2009).
Ultrasonographic examination has been used to evaluate effects
of inappropriate milking technique in the health of teats (Alejandro
96 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99
Fig. 28. B-mode ultrasonographic presentation of mammary lymph node; image
taken 25 days after development of mastitis associated with Staphylococcus chro-
mogenes; marked enlargement of the lymph node, with thickening of the cortex
®
(arrows). Image taken and processed on a MyLab 30 ultrasonography system
(ESAOTE SpA, Genova, Italy) with linear transducer, imaging frequency: 12.0 MHz –
scanning depth: 40 mm.
et al., 2014a), as changes in dimensions of the teat, as well as in its
condition, might adversely affect with local defence mechanisms,
leading in increased likelihood of infections (Mavrogianni et al.,
2005, 2006). Overmilking may lead in increased teat wall thick-
ness, due to congestion and oedema, which ultrasonographically
is imaged as increase of the line perpendicular to the mid axis of
the teat wall, when comparing findings before and after milking
(Alejandro et al., 2014b). Inappropriate milking conditions can lead
in significant increase in teat dimensions, most markedly 4 h after
milking, which would not return to normal even 6 h later (i.e., 10 h
after milking) (Wójtowski et al., 2006). Hence, ultrasonographic
examination of teats can be employed to optimise milking con-
ditions in dairy flocks, especially after installation of a new milking
system.
In a field investigation, Franz et al. (2003) have indicated a pos-
itive association between increased California Mastitis Test scores
(reflecting cell content in a milk sample; Fthenakis, 1995) and
increased diametre of teat canal (as measured during ultrasono-
graphic examination). Therefore, ultrasonographic examination of
the teat might be used to identify and select dairy ewes with long
and narrow teat canals, which have been considered as factors min-
imising chances of mammary infection (Gelasakis et al., 2015), that
way improving udder health in a flock.
3.4. Findings in the supramammary lymph nodes
The supramammary lymph nodes have an anechoic or hypoe-
choic parenchyma, with the hilar area imaged as a highly echogenic
linear structure. Their dimensions can vary, in accord with the
health status of the ipsilateral mammary gland; in cases of mam-
mary infection, their dimensions can be significantly increased
(Figs. 28 and 29).
According to Hussein et al. (2015), ultrasonographic exami-
nation of supramammary lymph nodes might possibly support
diagnosis of subclinical mastitis in field conditions. It has been pos-
tulated that in ewes with subclinical mastitis, the supramammary
lymph nodes had increased dimensions during ultrasonographic
examination, leading to a conclusion that ewes in which length
of these lymph nodes was ≥11.5 mm and width ≥7.8 mm, were 6.5
Fig. 29. B-mode ultrasonographic presentation of mammary lymph node; image
taken 25 days after development of mastitis associated with Staphylococcus chro-
mogenes in the contralateral side of the udder; homogeneous parenchyma, with no
abnormal features (when compared with contralateral lymph node: Fig. 28). Image
®
taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Gen-
ova, Italy) with linear transducer, imaging frequency: 12.0 MHz – scanning depth:
40 mm.
Fig. 30. B-mode ultrasonographic presentation of mammary parenchyma, showing
the external pudendal artery and the external pudendal vein vertically sectioned;
the larger section, appearing with more echogenic wall, represents the artery, whilst
the smaller section, with less echogenic wall, represents the vein. Image taken and
®
processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Genova, Italy) with
linear transducer, imaging frequency: 12.0 MHz – scanning depth 40 mm.
times more likely to have subclinical mastitis (Hussein et al., 2015).
Further, it has also indicated that in cases of staphylococcal infec-
tions, the architecture of lymph nodes might change, with a loss
of the normally highly echogenic hilus central area (Hussein et al.,
2015).
3.5. Findings in the udder blood vessels
The mammary vessels can be imaged as anechoic structures
inside the mammary parenchyma (Fig. 30). Doppler examination
helps to differentiate them from lactiferous ducts. There is little
work with Doppler examination in mammary vessels of ewes.
Blood flow into the mammary gland through the external
pudendal artery has been found to decrease progressively during
involution, with the speed of the decrease depending on the pro-
cedure followed for drying-off (i.e., progressive or abrupt cessation
of lactation period) (Figs. 31, 32) (Petridis et al., 2014). Blood flow
into the mammary gland increases progressively with lactogene-
sis at the last stage of pregnancy (Figs. 33–35) (Barbagianni et al.,
2015). Further, blood flow into mammary glands of ewes with preg-
nancy toxaemia has been found to be greatly reduced (Barbagianni
et al., 2015), as well as blood flow into mammary glands of lactat-
ing ewes that had developed pregnancy toxaemia at the preceding
pregnancy (Barbagianni, 2016). Possibly, an association of blood
 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99 97

Fig. 31. Spectral waveforms of the external pudendal artery (Doppler ultrasonography) obtained 2 days after start of the drying-off procedure; increased blood input into
®
the, still wide, vessel (for comparison with image obtained later during the involution process: Fig. 32). Image taken and processed on a MyLab 30 ultrasonography system
(ESAOTE SpA, Genova, Italy) with linear transducer, Doppler imaging frequency: 6.6 MHz – scanning depth: 60 mm (Petridis et al., 2014).

Fig. 32. Spectral waveforms of the external pudendal artery (Doppler ultrasonography) obtained on the 5th week after start of the drying-off procedure; markedly reduced
®
blood input into the vessel, which has a small diametre (for comparison with image obtained at start of involution process: Fig. 31). Image taken and processed on a MyLab
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer, Doppler imaging frequency: 6.6 MHz – scanning depth: 60 mm (Petridis et al., 2014).

input into the udder during late gestation with milk production
during the subsequent lactation period could support a method to
identify in advance ewes with increased milk yield in the forth-
coming lactation period (Barbagianni et al., 2015). After infection,
the diametre of the external pudendal artery has been found to
increase, coupled with an abrupt and excessive increase in blood
input into the mammary gland and increase of mean blood velocity
(Barbagianni, 2016).
4. Ultrasonographic examination of the udder in sheep
health management
Application of ultrasonographic examination of the udder in
sheep flocks might be employed as a complementary method in the
diagnosis of mammary disorders (Fragkou et al., 2014). However,
we consider that, at the moment, despite the difficulties in inter-
preting the results of somatic cell counts in ewes’ milk (Berthelot
et al., 2005), the combination of bacteriological and cytologi-
98 M.S. Barbagianni et al. / Small Ruminant Research 152 (2017) 86–99
Fig. 33. Spectral waveforms of the external pudendal artery (Doppler ultrasonog-
raphy) obtained 3 weeks before lambing; markedly reduced blood input into the
vessel, which has a smaller diametre (for comparison with images obtained later in
® phy) obtained the first week after lambing; markedly increased blood input into the
pregnancy or during lactation: Figs. 34, 35). Image taken and processed on a MyLab
30 ultrasonography system (ESAOTE SpA, Genova, Italy) with linear transducer,
Doppler imaging frequency: 6.6 MHz – scanning depth: 60 mm.
Fig. 34. Spectral waveforms of the external pudendal artery (Doppler ultrasonog-
raphy) obtained 2 days before lambing; increase of blood input into the vessel
(for comparison with images obtained earlier in pregnancy or during lactation:
®
Figs. 33,35). Image taken and processed on a MyLab 30 ultrasonography system
(ESAOTE SpA, Genova, Italy) with linear transducer, Doppler imaging frequency:
6.6 MHz – scanning depth: 60 mm.
cal examinations provides an acceptable diagnostic methodology
(Fragkou et al., 2014), which, for diagnosis of subclinical mastitis,
cannot be replaced by the ultrasonographic examination alone. The
technique can have only an ancillary role in the diagnosis of the
disease, for example during investigation of cases, in which clin-
ical diagnosis alone can prove of little help, e.g., in animals with
small-size, deep mammary nodules.
The ultrasonographic examination of the udder of ewes at the
end of a lactation period, as part of routine udder examination
performed at that point (Fthenakis et al., 2012), would provide
Fig. 35. Spectral waveforms of the external pudendal artery (Doppler ultrasonogra-
vessel (for comparison with images obtained during pregnancy: Figs. 33, 34). Image
®
taken and processed on a MyLab 30 ultrasonography system (ESAOTE SpA, Gen-
ova, Italy) with linear transducer, Doppler imaging frequency: 6.6 MHz – scanning
depth: 60 mm.
additional information, e.g., regarding presence of abcesses or of
increased quantity of fibrous tissue consequently to long-standing
mastitis. Such findings can be useful in deciding the management of
animals that are found with reduced milk production. Estimation of
the dimensions of gland cistern of ewes in the flock would support
decisions regarding milking frequency to be applied in a flock. Iden-
tification of ewes with gland cistern with increased capacity can
be also incorporated in the selection process of animals for even-
tual improvement of milk production of the flock (Nudda et al.,
2000; Castillo et al., 2008; Rovai et al., 2008; Ayadi et al., 2011).
Finally, examination of the teat can provide indications regarding
optimising use of the milking machine by applying the appropriate
settings.
5. Concluding remarks
The ultrasonographic examination of the udder of ewes is a use-
ful ancillary technique for in depth study of disorders of the udder.
The technique has many uses and can support decisions during a
diagnostic and/or health management procedures. However, the
technique should be used in combination with established diag-
nostic methods, including clinical, bacteriological and cytological
techniques. This, of course, does not preclude the use of the tech-
nique in sheep udder health management; it only underlines that
limitations of the technique do occur and these should be taken
into account during its application.
Conflict of interest
The authors have nothing to disclose.
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