Figure 1. (a) A focal moderate ventral edema. Note the smooth skin structure with reduced wrinkles in the edematous region. (0.1 African elephant, 33yrs.) (b) Focal moderate ventral edema in lateral view. (0.1 African elephant, 22yrs., 2.5 months before giving birth) (c) A moderate ventral edema extending to the external genital region. (0.1 African elephant, 46yrs., advanced pregnancy >18 months).
Figure 2. Ventral edema in a 7 yr-old Asian elephant bull suffering of Salmonellosis (Photo: Willem Schaftenaar). Click here to read this case report.
Figure 3. A 45 yr-old female African elephant with ventral edema showing signs of irritation (left) and sloughing of skin (right, arrow).
Differential diagnosis of ventral edema
In the young elephant a swelling around the umbilicus can be an indication of an umbilical hernia, sometimes accompanied by local edema.
A blunt trauma of the abdominal wall can result in an abdominal hernia. Intestines can be visualized using ultrasound examination.
Figure 4. Asian elephant (>35yrs) with traumatic ventral hernia. Movement of the intestines and fecal balls in the subcutaneous space could be visualized during transcutaneous ultrasound examination. Photo: Willem Schaftenaar
Pathogenesis
In general
The body always tries to maintain the balance between intravascular and interstitial fluid, driven by four different pressures acting in the capillary bed (Fig. 5). In addition, the capacity of the lymphatic system is critical for the physiologic reabsorption of interstitial fluid and its return transport into the blood circulation (Fig. 5). Beside an increased permeability of the capillary wall, any alteration in each of these five factors can cause edema. In particular an increase in the capillary hydrostatic pressure and a decrease in the plasma oncotic pressure (= osmotic pressure induced by the plasma proteins) lead to an increased shift of fluid towards the interstitial space. If this fluid load exceeds the lymphatic capacity, fluid will accumulate and edema will develop. The aforementioned parameters do vary across different body regions, leading to a locally varying susceptibility to edema development. Therefore, edema can occur both multifocal (e.g. EEHV-HD) or focal (e.g. ventral edema) with respect to the predisposition of certain body regions and the underlying cause. The latter can be systemic or focal. The localization of edema is also determined by gravity forces and species-specific anatomical characteristics. Extracellular fluid will have the tendency to migrate downwards due to gravity. Extracellular spaces that are surrounded by tightly fitting, non-elastic tissue, are not prone to show edema, even if they are at the lowest point of the body: in humans edema can easily develop in the feet, while in elephants edema has never been reported in the distal parts of the limbs.
Figure 5. Four critical parameters are determining fluid shift in the capillary bed through the semipermeable capillary wall. An increase in capillary hydrostatic pressure and interstitial oncotic pressure leads to an increased fluid shift towards the interstitial space, as well as a decrease in plasma oncotic pressure and interstitial hydrostatic pressure. The lymphatic vessels are running in parallel to the blood vessels and are collecting the interstitial fluid according to their transport capacity.
In elephants
According to Mikota (2006), no single underlying etiology for ventral edema in elephants has been identified so far. More likely, it presents a non-specific response to a variety of physiological stressors (Mikota 2006). In our opinion these stressors or pathological alterations can be categorized based on the general pathogenesis of an edema (Fig. 5). With this approach, each condition reported to be associated with edema in elephants so far, can be ascertained to one of the four defined etiologic categories (Fig. 6). Fowler & Mikota (2006) consider the ventral distribution of an edema in elephants caused by the gravitation of fluids into this area. But if gravitation alone would present the critical parameter for the characteristic ventral occurrence of an edema in the elephant, one would expect the swelling to occur primarily in the distal limb regions. The very thigh skin surrounding the legs with minimal elasticity may prevent this pattern. Apart from this, we assume the anatomy and physiology of the lymphatic system to explain the specific distribution pattern of ventral edema in elephants (Fig. 7). Unfortunately, anatomical knowledge on the lymphatic system in elephants is limited to one incomplete description in a fetal Asian elephant (Mariappa 1986). In this individual, a peculiarity was reported with the Cisterna chyli located in the thoracic cavity (Mariappa 1986). In humans, the horse, dogs & cats the Cisterna chyli is located in the abdominal cavity (Berens von Rautenfeld 2000, Herpertz 2013, Salomon et al. 2008). We do rather question the validity of the report for the fetal Asian elephant, than expect a significant peculiarity in the anatomy of the lymphatic system in the elephant.
Figure 6. Four defined etiologic categories for edema in elephants, each with examples reported in the existing literature. Note that underlying alterations may vary extremely but result in the same clinical sign of accumulated interstitial fluid.
Therefore, due to the lack of solid evidence, our line of arguments is largely based on the anatomy of the lymphatic system in horses and extrapolated to the elephant (Berens von Rautenfeld 2000, Salomon et al. 2008; Fig. 7). Assuming that the lymphatic watersheds in the elephant are running similar to the situation in the horse, it becomes obvious that the characteristic location of a ventral edema presents the region between the major transversal and horizontal watershed (Fig. 7). In this proximal part of the lymphatic territory VII, the lymphatic vessels drain towards the deep abdominal lymphatic centers and have no connection to a relevant superficial lymphocentrum. Therefore, it seems reasonable that increased abdominal pressure (e.g. during late pregnancy) may reduce the drainage of this territory. At the same time, interstitial hydrostatic pressure in the subcutaneous tissue of this body region may be low compared to the limb or the thoracic wall where bony and muscular structures are supporting the lymphatic capacity. These factors together with gravitation can serve as an explanation for the specific distribution of ventral edema in elephants. In contrast, the limbs may rarely be affected by edema, because the relatively rigid skin in combination with the underlying musculoskeletal apparatus will result in kind of a physiologic compression bandage as reported for the horse (Aurenz 2020).
Figure 7. Hypothesized lymphatic territories in the elephant. The seven distinct lymphatic territories with their specific drainage areas were extrapolated from the situation in the horse (Berens von Rautenfeld et al. 2000) and numbered accordingly. The blue lines indicate the lymphatic watersheds. Note the proximal part of area VII is lacking a connection to a relevant superficial lymphocentrum.
Treatment of ventral edema
Given the wide diversity of underlying causes (Fig. 6) no general treatment protocol can be defined. In the literature, hot and cold pressure bandages (du Toit 2001) and increasing protein in the diet (Fowler & Mikota 2006) have been recommended. The administration of Furosemide (1mg/kg i.m.) has been unsuccessful (Martelli 2006).
Considering the different etiological pathways leading to an edema, we strongly encourage the treatment of the underlying cause. To do so, an underlying cause needs to be determined or at least a classification according to Figure 6 should be strived for. The latter seems realistic by a thorough anamnesis and clinical examination. For example in cases of heart failure, positive inotropic agents may reduce the capillary hydrostatic pressure and simultaneously support the lymphatic capacity, as shown in humans (Scallan et al. 2016). In less severe cases of assumed cardiorespiratory insufficiency, which has been observed to repeatedly cause ventral edema in geriatric Asian females during hot summer days, herbal medicine can present a helpful approach (Crataegus Dilution vet.®, DHU-Arzneimittel GmbH & Co. KG, Karlsruhe, Germany; three times a day, 6.0-8.0ml orally) (personal observation in four cases). In addition to the treatment of the underlying cause, or in cases where only a symptomatic treatment is realizable, the following methods may facilitate the reabsorption of an edema. Moderate walking will centrally activate the lymphatic flow and subsequently increase the lymphatic capacity. Hence locomotion is considered a critical part of edema therapy in horses (Aurenz 2020). A sufficient amount of satisfying recumbent rest will also support the reabsorption of interstitial fluid by reducing the negative impact of gravitation. Moderate pressure washing may have a positive effect similar to manual lymph drainage in horses (Aurenz 2020). Under the assumption of a similar anatomy of the lymphatic system, adhering to the protocols established in equine lymph drainage seems a reasonable approach (Berens von Rautenfeld 2000). Given that the selectively applied pressure for manual lymph drainage could be applied by a water jet, even treating from a safe distance might become an option. Further research is needed to base such an approach on scientific findings and formulate a detailed practical guidance.
Additional note
With respect to our very limited knowledge on the anatomy of the lymphatic system in elephants and the corresponding physiological pathways, a major part of this compilation is very hypothetical. Although we based these hypotheses on evidence from other mammalian species, they remain to a certain amount speculative and should be interpreted with caution.
References
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Edema
by Christian & Linda Schiffmann
Definition
A local or general swelling due to excessive accumulation of fluid in the interstitial space of tissues. This condition can be caused by various underlying alterations. Depending on the composition of the fluid (in particular the protein content), an edema can be further categorized.
Relevance of edema in elephants
In elephants the occurrence of the so-called ventral edema is a well-known and quite common clinical symptom (Mikota 1994) (Fig. 1 and 2). Ventral edema is defined as edematous swelling in the ventral abdominal wall and tissues surrounding the external genitalia (Mikota 2006). Although the clinical impact of ventral edema is often not visible, the underlying mechanism indicates a disturbance of the internal fluid balance. In addition, edema in the submandibular region and multifocal has been described in cases of hemorrhagic disease due to herpes virus infection (EEHV-HD) (Fuery et al. 2020, Howard & Schaftenaar 2019).
Clinical signs
The characteristic swelling in edema may develop immediately or over the course of several days, depending on the underlying cause. Edemas caused by a local inflammatory response may be warm and painful upon palpation. The swelling in case of ventral edema without any underlying inflammatory process may feel slightly cooler compared to other body regions. Palpation is not painful and moderate pressure with the thumb may result in a dent. Such dent may also be produced if the edema is the result of an inflammatory process, in which case the pressure will provoke a pain reaction. Compared to non-edematous areas, the skin will look smoother with reduced wrinkles (Fig. 1a). If ventral edema extends from the umbilical to the genital area (Fig. 1c), the skin may become irritated through the repeated contact with the medial hind legs while walking. In severe cases, this irritation may lead to pressure necrosis and sloughing (Mikota 2006). In cases without such complications, edema may resolve without treatment within months (Mikota 1994), although this will heavily depend on the underlying cause, which should be treated accordingly.
Prevention
Depending on the underlying cause, the occurrence of ventral edema in elephants can be prevented. A continuous health monitoring program with focus on individuals at peculiar risk such as geriatric elephants, pregnant females or individuals suffering from cardio-respiratory or renal insufficiency will enable early supportive and/or curative treatment. Is ventral edema bad? Although ventral edema as such may not necessarily present a serious condition in an elephant, it is often associated with serious health issues and bears the risk for complications. Therefore this symptom should be investigated thoroughly and its development monitored closely.