Use of high-frequency ultrasonography for evaluation of skin thickness in relation to hydration status and fluid distribution at various cutaneous sites in dogs

Alessia Diana Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Alma Mater Studiorum, University of Bologna, Via Tolara di Sopra 50, I-40064 Ozzano Emilia (BO), Italy.

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Carlo Guglielmini Department of Veterinary Clinical Sciences, School of Veterinary Medicine, University of Teramo, Viale Crispi 212, I-64100 Teramo, Italy.

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Federico Fracassi Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Alma Mater Studiorum, University of Bologna, Via Tolara di Sopra 50, I-40064 Ozzano Emilia (BO), Italy.

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Marco Pietra Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Alma Mater Studiorum, University of Bologna, Via Tolara di Sopra 50, I-40064 Ozzano Emilia (BO), Italy.

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Erika Balletti Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Alma Mater Studiorum, University of Bologna, Via Tolara di Sopra 50, I-40064 Ozzano Emilia (BO), Italy.

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Mario Cipone Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Alma Mater Studiorum, University of Bologna, Via Tolara di Sopra 50, I-40064 Ozzano Emilia (BO), Italy.

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Abstract

Objective—To assess the usefulness of high-frequency diagnostic ultrasonography for evaluation of changes of skin thickness in relation to hydration status and fluid distribution at various cutaneous sites in dogs.

Animals—10 clinically normal adult dogs (6 males and 4 females) of various breeds.

Procedures—Ultrasonographic examination of the skin was performed before and after hydration via IV administration of an isotonic crystalloid solution (30 mL/kg/h for 30 minutes). A 13-MHz linear-array transducer was used to obtain series of ultrasonographic images at 4 different cutaneous sites (the frontal, sacral, flank, and metatarsal regions). Weight and various clinicopathologic variables (PCV; serum osmolality; and serum total protein, albumin, and sodium concentrations) were determined before and after the infusion. These variables and ultrasonographic measurements of skin thickness before and after hydration were compared.

Results—Among the 10 dogs, mean preinfusion skin thickness ranged from 2,211 μm (metatarsal region) to 3,249 μm (sacral region). Compared with preinfusion values, weight was significantly increased, whereas PCV; serum osmolality; and serum total protein, albumin, and sodium concentrations were significantly decreased after infusion. After infusion, dermal echogenicity decreased and skin thickness increased significantly by 21%, 14%, 15%, and 13% in the frontal, sacral, flank, and metatarsal regions, respectively.

Conclusions and Clinical Relevance—Cutaneous site and hydration were correlated with cutaneous characteristics and skin thickness determined by use of high-frequency ultrasonography in dogs. Thus, diagnostic ultrasonography may be a useful tool for the noninvasive evaluation of skin hydration in healthy dogs and in dogs with skin edema.

Abstract

Objective—To assess the usefulness of high-frequency diagnostic ultrasonography for evaluation of changes of skin thickness in relation to hydration status and fluid distribution at various cutaneous sites in dogs.

Animals—10 clinically normal adult dogs (6 males and 4 females) of various breeds.

Procedures—Ultrasonographic examination of the skin was performed before and after hydration via IV administration of an isotonic crystalloid solution (30 mL/kg/h for 30 minutes). A 13-MHz linear-array transducer was used to obtain series of ultrasonographic images at 4 different cutaneous sites (the frontal, sacral, flank, and metatarsal regions). Weight and various clinicopathologic variables (PCV; serum osmolality; and serum total protein, albumin, and sodium concentrations) were determined before and after the infusion. These variables and ultrasonographic measurements of skin thickness before and after hydration were compared.

Results—Among the 10 dogs, mean preinfusion skin thickness ranged from 2,211 μm (metatarsal region) to 3,249 μm (sacral region). Compared with preinfusion values, weight was significantly increased, whereas PCV; serum osmolality; and serum total protein, albumin, and sodium concentrations were significantly decreased after infusion. After infusion, dermal echogenicity decreased and skin thickness increased significantly by 21%, 14%, 15%, and 13% in the frontal, sacral, flank, and metatarsal regions, respectively.

Conclusions and Clinical Relevance—Cutaneous site and hydration were correlated with cutaneous characteristics and skin thickness determined by use of high-frequency ultrasonography in dogs. Thus, diagnostic ultrasonography may be a useful tool for the noninvasive evaluation of skin hydration in healthy dogs and in dogs with skin edema.

Mammalian skin is a complex multicellular organ that provides protection from physical, chemical, and microbiologic injury and, at the same time, preserves the internal environment of all other organs by functioning as an effective barrier against the loss of water, electrolytes, and, macromolecules.1,2 The skin is a living and complex system composed of different heterogeneous and anisotropic tissue layers, each of which has distinctly different mechanical properties.3 Skin hydration is an important characteristic of the skin itself, and water content influences various characteristics of the skin such as barrier function, drug penetration, and mechanical properties.3,4 Thus, the degree of hydration plays an important role in cutaneous architecture and function. In the skin, numerous chemical processes occur within an aqueous environment, and many of these processes are dependent on the skin's tissue water concentration.4 Furthermore, the skin is an important reservoir of water, as well as electrolytes, vitamins, fat, carbohydrates, proteins, and other materials, and participates in the fluid content of the whole body.3,4 In healthy domestic animals, the subcutis and dermis are always moist and contain approximately 70% to 80% water.3 Conversely, lipids contained in the stratum corneum of epidermis provide the major barrier against water loss from the skin.5

In vivo determination of cutaneous water content plays an important role both in clinical settings (aiding in the characterization of cutaneous disorders associated with changes of skin hydration6) and in research investigations of the mechanisms of skin irritation or evaluation of the efficacy of topically applied drugs.7 A large amount of data are available regarding the noninvasive evaluation of skin hydration in humans. Various electrical (eg, measurements of dermal capacitance, dermal conductance, and dermal impedance) and mechanical methods have been used for such evaluations8; diagnostic imaging and, particularly, high-frequency ultrasonography are also commonly applied to evaluate the skin in humans.9 Via cutaneous ultrasonography, cutaneous layers can be differentiated and skin water content can be estmated.10 However, few data regarding the noninvasive evaluation of skin hydration in dogs are available. The measurement of the skin hydration by use of electrical capacitance in healthy dogs and in dogs with cutaneous disorders has been reported.4 The use of corneometry to evaluate transepidermal water loss in 2 breeds of dog was more recently described by Hester et al.11 In a study12 by our group, we investigated the usefulness of high-frequency ultrasonography for the noninvasive evaluation of the skin of clinically normal dogs. In that investigation, a 2-layered echoic pattern of the skin was evident in 11 of 26 clinically normal dogs, which was possibly related to a large amount of dermal fluid storage. Thus, we hypothesized that ultrasonography may be useful for the evaluation of dermal fluid storage in dogs, as it is in humans.13 The purpose of the study reported here was to assess the usefulness of high-frequency diagnostic ultrasonography for evaluation of changes of skin thickness in relation to hydration status and fluid distribution at various cutaneous sites in dogs.

Materials and Methods

Animals—Ten clinically normal client-owned dogs (6 Italian Bloodhounds, 1 English Setter, and 3 mixedbreed dogs) were used in the study (designated as dogs 1 through 10); this group included 6 males and 4 females. The ages of the dogs ranged from 1 to 13 years (mean ± SD age, 5.1 ± 3.6 years); the dogs' weights ranged from 14.3 to 26.2 kg (mean weight, 18.1 ± 3.4 kg). Dogs were considered clinically normal on the basis of results of physical examination, a CBC, routine serum biochemical analyses, and urinalysis. Prior to study commencement, informed consent of owners was obtained and the protocol of the study was approved by the Ethical Committee of the University of Bologna.

Hydration protocol—A 20-gauge catheter was inserted in the left cephalic vein of each dog. An isotonic crystalloid solution composed of lactated Ringer's solutiona and 5% dextrose solutionb (1:1 [vol/vol]) was administered IV. The composition of the colloid solution was as follows: sodium (66 mEq/L), potassium (20 mEq/L), chloride (56 mEq/L), calcium (2 mEq/L), lactate (14.5 mEq/L), and dextrose (27.5 g/L). The osmolality of the colloid solution was 279 mOsm/kg. The solution was administered for 30 minutes at a rate of 30 mL/kg/h by use of an infusion pump.c In each dog, weight; PCV; serum osmolality; and serum total protein, albumin, and sodium concentrations were assessed immediately before (baseline) and after the infusion.

Ultrasonography of the skin—B-mode real-time ultrasonographic examination of the skin was conducted by use of a real-time ultrasound machine equipped with a high-frequency (13 MHz) linear-array transducerd immediately before (baseline) and immediately after infusion in all dogs; all examinations were performed by the same experienced sonographer (AD). Four cutaneous sites were examined: frontal, sacral, metatarsal, and the left flank regions. For examination of the frontal region, the transducer was placed slightly caudal to a line joining the supraorbital processes. For examination of the sacral region, the transducer was placed on a line joining the right and left tuber coxae. For examination of the metatarsal region, the transducer was placed on the dorsal surface of the metatarsal portion of the left hind limb. For examination of the flank region, the transducer was positioned ventral to the transverse processes of the lumbar vertebrae. The frontal, sacral, and metatarsal regions were examined while dogs were maintained in sternal recumbency; the flank region was examined while the dogs were maintained in right lateral recumbency.

Each cutaneous region was clipped, and the skin surface was gently cleaned with 70% isopropyl alcohol to remove cutaneous debris and sebum. Copious amounts of coupling gele were applied between the transducer and skin surface. The ultrasound beam was maintained strictly perpendicular to the skin surface, and direct contact between the probe and the skin surface was avoided. The scanning technique has been reported previously.12

A series of images of the skin were obtained and stored on a magnetic optical disc for subsequent offline evaluation by use of imaging software.f Measurements of the skin (from the outer side of the skin surface to the clearly recognizable acoustic interface) were made by use of the electronic calipers of the ultrasound machine. For each region, the mean value of 3 measurements obtained from each ultrasonographic image was used for statistical analysis.

Statistical analysis—Data were analyzed by use of a commercial statistical software package.g Baseline and postinfusion weight and clinicopathologic variables and results of ultrasonographic skin measurements are reported as mean ± SD values. Pre- and postinfusion weight, clinicopathologic variables, and echocardiographic measurements of skin thickness were compared by use of a Student t test for paired data. Values of P < 0.05 were considered significant.

Results

Effect of hydration on weight and clinicopathologic findings—Values of weight and clinicopathologic variables before and after hydration were recorded for all 10 dogs (Table 1). The infusion resulted in a significant (P < 0.001) increase in weight; however, a change in weight was not detected in 2 dogs (dogs 3 and 6) because of micturition prior to the postinfusion assessment. Compared with baseline values, significant decreases in PCV (P < 0.001); serum osmolality (P = 0.021); and serum total protein (P < 0.001), albumin (P < 0.001), and sodium (P = 0.007) concentrations were evident after infusion.

Table 1—

Mean ± SD (range) weight and clinicopathologic variables immediately before (baseline) and after infusion of an isotonic crystalloid solution (lactated Ringer's solution and 5% dextrose solution* [1:1 {vol/vol}]) via a cephalic vein in 10 clinically normal dogs.

VariableBaselineAfter infusion
Weight (kg)18.1 ± 3.4 (14.3–26.2)18.4 ± 3.5 (14.7–26.8)
PCV(%)43 ± 4 (36–48)36 ± 4 (29–40)
Serum osmolality (mmol/kg)301 ± 4 (297–313)297 ± 3 (290–302)
Total protein (g/dL)6.7 ± 0.6 (6.0–8.1)5.9 ± 0.8 (5.3–7.9)
Albumin (g/dL)3.0 ± 0.3 (2.3–3.3)2.7 ± 0.2 (2.2–3.0)
Sodium (mmol/L)148 ± 3 (145–154)145 ± 3§ (138–148)

The composition of the mixed solution was as follows: sodium (66 mEq/L), potassium (20 mEq/L), chloride (56 mEq/L), calcium (2 mEq/L), lactate (14.5 mEq/L), and dextrose (27.5 g/L). The osmolality of the mixed solution was 279 mOsm/kg. The solution was administered at a rate of 30 mL/kg/h by use of an infusion pump for 30 minutes.

Value after infusion is significantly different from baseline value (†P < 0.001, ‡ P < 0.05, and § P < 0.01).

Ultrasonographic findings—Ultrasonographically, the skin was characterized by 3 distinct and recognizable layers in each dog (Figure 1). Most superficially, there was a well-defined and regular echoic line (epidermal entry echo), followed by a less echogenic layer of varying intensity (epidermis and dermis). At greater depth, there was a thicker layer characterized by an inhomogeneous hypoechoic (compared with the overlying layers) pattern containing thin linear hyperechoic areas (subcutaneous tissue). In 2 dogs, 2 different echogenic patterns were detected in the intermediate layer (epidermis and dermis) of the sacral, flank, and metatarsal regions (dog 4) and of the sacral region (dog 6); the deeper layer had decreased echogenicity, compared with the appearance of the upper layer. After infusion, decreased echogenicity of the skin was evident in each cutaneous region in all dogs. Furthermore, a 2-layered appearance of the epidermis plus dermis layer was appreciable in 4 dogs (Figure 2); this was apparent in all cutaneous regions in 1 dog (dog 4), in the sacral and flank regions in a second dog (dog 6), in the frontal region of a third dog (dog 7), and in the flank region of a fourth dog (dog 8).

Figure 1—
Figure 1—

Ultrasonographic appearance of the skin in the frontal region of a dog (dog 4) before (A) and after infusion of an isotonic crystalloid solution (lactated Ringer's solution and 5% dextrose solution [1:1 {vol/vol}]) via a cephalic vein (B). The mixed solution was composed of sodium (66 mEq/L), potassium (20 mEq/L), chloride (56 mEq/L), calcium (2 mEq/L), lactate (14.5 mEq/L), and dextrose (27.5 g/L); osmolality of the solution was 279 mOsm/kg. The solution was administered by use of an infusion pump at a rate of 30 mL/kg/h for 30 minutes. After the infusion, there is an overall decrease in echogenicity of the dermis and an increase in skin thickness. Measurement of skin thickness is illustrated by the dotted line. E = Epidermal entry echo. D = Epidermis and dermis. F = Frontal bone. S = Subcutaneous tissue. Bar = 5 mm.

Citation: American Journal of Veterinary Research 69, 9; 10.2460/ajvr.69.9.1148

Figure 2—
Figure 2—

Ultrasonographic appearance of the skin in the sacral region of a dog (dog 6) after hydration via IV infusion of an isotonic crystalloid solution. Notice the 2 distinct bands with different echogenicity in the dermis (D) that were associated with dermal fluid storage. Measurement of skin thickness is illustrated by the dotted line. Bar = 5 mm. See Figure 1 for key.

Citation: American Journal of Veterinary Research 69, 9; 10.2460/ajvr.69.9.1148

Measurements of skin thickness in ultrasonographic images were performed before and after infusion in all 10 dogs (Table 2). At baseline, mean ± SD values of skin thickness (epidermis plus dermis) ranged from 2.211 ± 0.409 mm to 3.249 ± 1.017 mm; skin thickness was greatest in the sacral region, followed by the frontal, flank, and metatarsal regions (in decreasing order). After infusion, skin thickness increased significantly in all cutaneous regions; these increases were apparent in all dogs. Among the cutaneous regions examined, the largest increase (from the baseline value) in skin thickness was evident in the frontal region (21% increase; P < 0.001), with lesser but similar increases in the sacral (14% increase; P < 0.001), flank (15% increase; P = 0.002), and metatarsal (13% increase; P = 0.005) regions.

Table 2—

Mean ± SD (range) skin thickness (epidermis plus dermis) measured on ultrasonographic images obtained at 4 cutaneous sites immediately before (baseline) and after infusion of an isotonic crystalloid solution* via a cephalic vein in 10 clinically normal dogs.

Cutaneous regionSkin thickness (mm)
BaselineAfter infusion
Frontal2.457 ± 0.551 (1.487–3.247)2.977 ± 0.622† (1.910–3.837)
Sacral3.249 ± 1.017(1.997–4.087)3.696 ± 1.079† (2.327–5.667)
Metatarsal2.211 ± 0.409(1.580–3.120)2.489 ± 0.521§ (1.763–3.413)
Flank2.239 ± 0.580 (1.707–2.863)2.567 ± 0.433§ (1.927–3.343)

See Table 1 for key.

Discussion

Physiologically, skin thickness varies among species and among animals of the same species, according to breed, age, sex, and area of the body surface.1,14–16 In domestic animals, skin thickness typically decreases dorsally to ventrally on the trunk and proximally to distally on the limbs.1 The reported mean thickness of canine skin is 0.5 to 5.0 mm; the thickest skin is located over the head, dorsum of the neck, back, and sacrum.1,14 Skin thickness depends on the amount of collagen fibers and cellular substances and on interstitial fluid content; therefore, increased fluid content leads to a greater skin thickness. Furthermore, diurnal variations in skin thickness secondary to dermal fluid translocation are known to occur in humans.17

Results of the present study confirmed that skin thickness varies at different cutaneous sites within an individual dog and that skin hydration is positively correlated with skin thickness in this species. In particular, among the cutaneous sites examined in our study, the epidermis-dermis zone of the sacral region had the greatest thickness (mean value, 3.2 mm); skin was less thick in the frontal, flank, and metatarsal regions (in decreasing order). Nevertheless, for each examined site, considerable interindividual variation in skin thickness was evident. All of the aforementioned physiologic features of skin thickness were detectable in the study dogs by use of noninvasive, high-frequency ultrasonography. After completion of the baseline ultra sonographic evaluation, a state of hyperhydration was induced by IV infusion of an isotonic crystalloid solution in each dog; the efficacy of the procedure was confirmed by an increase in weight and decreases in PCV; serum osmolality; and serum concentrations of total protein, albumin, and sodium. The change of hydration status was rapidly reflected in the ultrasonographic appearance of the skin, and skin thickness increased and echogenicity of the dermis decreased at all 4 cutaneous sites after infusion. The infusion-associated volume shift from the intravascular compartment to the interstitial compartment occurred rapidly because the postinfusion ultrasonographic examination of the skin was performed immediately after completion of the infusion of fluid. Increased capillary hydrostatic pressure and decreased colloid osmotic pressure or increased permeability of the capillary walls lead to increased fluid shift from the intravascular space to the interstitial tissue, and following the Starling mechanism, this is in balance with lymphatic flow.18,19

The connective tissues of the skin are characterized by a low cell density and an abundance of extracellular macromolecular material and are regarded as the water stores of the body.19,20 In the skin, water storage takes place in the dermis because of its rich arteriolar and venular supply.13 In particular, the dermis contains a third of the interstitial fluid volume and is mainly responsible for changes in skin thickness via increased net capillary filtration.19 A double-layered ultrasonographic appearance of the dermis was evident before and after infusion in 2 and 4 dogs of the present study, respectively. Furthermore, the number of cutaneous sites that had a 2-layered appearance of the dermis increased after infusion. These findings confirm the hypothesis that dermal fluid storage can be detected via high-frequency ultrasonography in dogs. Moreover, dermal echogenicity and the double-layered appearance of the dermis (the deeper layer of which is less echogenic than the more superficial layer) are correlated with cutaneous fluid content. Disarrangement of the collagen bundles is likely responsible for decreased dermal echogenicity as a consequence of interstitial edema.21 Similar to findings in humans, accumulation of fluid takes place in the deeper portion of the dermis in dogs, where water accumulates in the papillary skin compartment.6,22 The efficiency of ultrasonography for assessment of dermal water changes in humans has been validated by use of a nuclear magnetic resonance technique to precisely determine skin water content.10 In clinical settings, highfrequency ultrasonographic examination has been used to investigate the distribution of intradermal fluid in patients with edema associated with lipodermatosclerosis, lymphedema, and cardiac insufficiency.6 Results indicated that dermal echogenicity associated with any type of edema is decreased, compared with findings in healthy individuals, and that the characteristic patterns of dermal echogenicity differ according to the type of edema.6 On the basis of results of our investigation, it appears that high-frequency ultrasonography may also be a useful tool for the evaluation of cutaneous edema in dogs.

At the cutaneous sites examined in the dogs of the present study, the increase in skin thickness of the frontal region after hydration was the greatest (21% increase from the preinfusion baseline value); a lesser increase (ranging from 13% to 15%) was evident in the sacral, flank, and metatarsal regions. The effect of gravity may insufficiently explain those differences because the position in which dogs were placed during site examinations varied (ie, sternal recumbency for examinations of the frontal, sacral, and metatarsal regions and lateral recumbency for examination of the flank region). Differences in distribution of collagenous bundles and elastic reticular fibers in the dermis of various cutaneous sites may likely explain the relatively higher fluid storage in the frontal region, compared with the other examined regions.14

Evaluation of skin hydration in dogs currently relies on clinical palpation (ie, picking up the skin with the fingers) and instrumental techniques (eg, evaluation of electrical capacitance and corneometry).4,11,23 The former has low sensitivity, and the latter techniques are time-consuming and not readily available in clinical settings. As a tool for the evaluation of skin hydration status in dogs, ultrasonographic examination of the skin is noninvasive and appears to be accurate and easy to perform. Additionally, this technique may also prove to be useful in evaluation of pathologic modifications of skin hydration (eg, skin edema) in dogs as it is in humans.

ABBREVIATIONS

a.

Ringer lattato, Fresenius Kabi, Isola della Scala (Vr), Italy.

b.

Glucosio (5 g/100 mL), Fresenius Kabi, Isola della Scala (Vr), Italy.

c.

Infusomat fm, Braun, Meldungen, Germany.

d.

AU5 Epi, Esaote Biomedica, Genova, Italy.

e.

Aquasonic 100, Parker Laboratories Inc, Fairfield, NJ.

f.

Imagelab, version 7.0 C, Esaote Biomedica, Genova, Italy.

g.

Statistica for Windows, version 4.5, StatSoft, Tulsa, Okla.

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  • Figure 1—

    Ultrasonographic appearance of the skin in the frontal region of a dog (dog 4) before (A) and after infusion of an isotonic crystalloid solution (lactated Ringer's solution and 5% dextrose solution [1:1 {vol/vol}]) via a cephalic vein (B). The mixed solution was composed of sodium (66 mEq/L), potassium (20 mEq/L), chloride (56 mEq/L), calcium (2 mEq/L), lactate (14.5 mEq/L), and dextrose (27.5 g/L); osmolality of the solution was 279 mOsm/kg. The solution was administered by use of an infusion pump at a rate of 30 mL/kg/h for 30 minutes. After the infusion, there is an overall decrease in echogenicity of the dermis and an increase in skin thickness. Measurement of skin thickness is illustrated by the dotted line. E = Epidermal entry echo. D = Epidermis and dermis. F = Frontal bone. S = Subcutaneous tissue. Bar = 5 mm.

  • Figure 2—

    Ultrasonographic appearance of the skin in the sacral region of a dog (dog 6) after hydration via IV infusion of an isotonic crystalloid solution. Notice the 2 distinct bands with different echogenicity in the dermis (D) that were associated with dermal fluid storage. Measurement of skin thickness is illustrated by the dotted line. Bar = 5 mm. See Figure 1 for key.

  • 1.

    Scott DW, Miller WH, Griffin CE. Structure and function of the skin. In: Scott DW, Miller WH, Griffin CE, eds. Muller and Kirk's small animal dermatology. 6th ed. Philadelphia: WB Saunders Co, 2001;170.

    • Search Google Scholar
    • Export Citation
  • 2.

    Gniadecka M, Nielsen OF, Christensen DH, et al. Structure of water, proteins, and lipids in intact human skin, hair, and nail. J Invest Dermatol 1998;110:393398.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Chesney CJ. Water: its form, function and importance in the skin of domestic animals. J Small Anim Pract 1993;34:6571.

  • 4.

    Chesney CJ. Measurement of skin hydration in normal dogs and in dogs with atopy or a scaling dermatosis. J Small Anim Pract 1995;36:305309.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Friberg SE, Kayali IW, Rhein LD, et al. Water permeation of the reaggregated stratum corneum with model lipids. J Invest Dermatol 1990;94:377380.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Gniadecka M. Localization of dermal edema in lipodermatosclerosis, lymphedema, and cardiac insufficiency. J Am Acad Dermatol 1996;35:3741.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Lebwohl M, Herrmann LG. Impaired skin barrier function in dermatologic disease and repair with moisturization. Cutis 2005;76:712.

  • 8.

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