Mass incidence of gout in a breeding colony of Milos vipers (Macrovipera schweizeri)


János Gál*, Tamás Tóth2, Viktor Molnár2, Miklós Marosán3, Endre Sós2



1 Szent István University, Faculty of Veterinary Medicine, Department of Pathology and Forensic Veterinary Medicine. István u. 2. H-1078 Budapest. *E-mail: Gal.Janos@aotk.szie.hu
2 Budapest Zoo and Botanical Garden
3 Department of Zoology, University of West Hungary


Summary.
The authors describe lethal pathological alterations because of mal-management during controlled breeding program in case of the imperiled snake species, the milos viper (Macrovipera schweizeri), that is found under natural conditions in small island-populations at limited areas of Greece. The humidity in the terrarium was too low for the snakes participating in the breeding program, which resulted in severe exsiccation through the respiratory process. The consequence of the fluid-loss was hypovolemia on the first place, than secondary retention type uricosis (gout) because of the decreased perfusion of the kidney, abnormal excretion and accumulation of uric acid. The authors draw attention to the point that the milos viper must be kept at certain humidity level in artificial environment to avoid lost of this precious animal. The moisture content of the terrarium should be also carefully monitored during the hybernation to maintain the required conditions of the species.

Milos viper (Macrovipera schweizeri) is a venomous snake species that is found only in a few points of Greece, such as some islands of the West Cyclads (Milos, Sifnos, Polynos and Kimolos) in south Europe (9, 10). In the small area, the populations are unstable, therefore the Budapest Zoo and Botanical Garden has proposed to start a breeding and reservation program and to establish a breeding stock, aiming to save the species. The studied breeding stock contained four male and three female animals.

Milos viper (Figure 1) belongs to the large true vipers. Adults males can exceed 100 cm in length, however, the average length of the species ranges between 65 and 75 cm (5, 9). Within his living area, the snake prefers the regions with dry mezoclimate, nevertheless in such regions he spends the hot hours of day-time in humid caves and pits, underground holes, empty gullets or in the shade of a bush (9, 10). Nevertheless it must be noted, that on the Cyclad Islands, the air humidity is around 70% during the whole year, due to the closeness of the sea.
Only a limited number of experiences were published on the indoor keeping of this species, moreover the few publications report inconsistent data in many of the cases. Schweiger kept his vipers at 24–26 ºC in the spring and at 26–35 ºC in the summertime (8). In other papers the terrarium was reported to be heated occasionally over 40 ºC (7). Concerning the best keeping temperature, recently the authors agreed, that the most favourable is if the snakes can choose the optimal places by themselves with the best temperature inside the terrarium. Thus a hot (with the temperature of 30–33 ºC) and a cool (with the temperature of 20–25 ºC) corner was established in the terrarium for the daytime hours (3, 6). Each authors agrees, that by the night the temperature of the terrarium must drop (to 10–18 ºC). The minimal air humidity of the terrarium must be 70(–80)% (3, 6, 9, 10).
For their successful reproduction, milos vipers need a rest-period for dormancy during the winter. This can be achieved in a safely closed, airy box filled with fallen leaves or wet peat and supplied with a water pot (9, 10). The available publications report various values regarding the temperature and duration of the winter dormancy of the viper (Table).
Amongst the disorders of protein metabolism in snakes, the most common is gout which can be caused by different factors. One is the impairment of kidneys resulting from inadequate keeping conditions. Nevertheless, numerous factors can generate gout: substrates that damage kidneys and among them some medicines (e.g. gentamycin), the excessive consumption of proteins (especially in basically herbivorous reptiles), the lack of water, and occasionally the lack of vitamin A. As a result of kidney impairment, crystals of uric acid salts encrust in the kidney tubules. Later, as the failure of the kidney function worsens, uric acid precipitates out on different mucous membranes, on the serous membranes and also in the parenchymal organs such as the liver, the spleen and the lung. This phenomenon is followed by the cell inflammation of the tissues. Therefore granulomas (tophi) appear in the different organs showing a specific tissue structure (1, 2, 4).

Case report
Four of our seven milos vipers (3 males and one female) died between 2001 and 2004 in the Budapest Zoo and Botanical Garden. The vipers were kept separately in terrariums of 100X50X60 cm, made of laminated plates. The bolster of the terrarium was ground larch bark. Artificial plants and rocks were also applied to give shelter to the animals. Fresh drinking water was provided for the animals in twice a week in a 10 cm deep vessel which was 15 cm in diameter. The terrarium was exposed 12 hours a day by a bulb of 60 W and also by UV lamps. The room heating and the bulbs provided a daytime temperature of 25–32 ºC in the terrariums which dropped to 22–28 ºC during the night. The air humidity of the room in which the snakes were kept ranged from 30 to 60%. The wintering of snakes was performed at 5–12 ºC for 3 months. During the wintering the snakes were supplied with drinking water.
In each case the vipers perished at the end of the wintering or right after wintering, often without showing any characteristic changes or showing only general clinical symptoms. The carcasses were dissected at the Department of Pathology and Forensic Veterinary Medicine, Faculty of Veterinary Medicine, Szent István University. In vitro bacteriologic investigation was performed in an incubator at 25–26 ºC for 48 hours. The condition of animals was estimated according to the size of fat bodies in the body cavity.
Three of the adult, mature snakes that were dissected were males (marked with number 1, 2 and 3) and one was a female (marked with number 4).
The spleen of each dissected animals had normal size and shape. The initial part of the digestive system (the stomach and the small intestine) was empty in each cases. The liver was red-brownish with normal shape (elongated, cigar-like shape) and size. However on the liver-covering serous membrane greyish-white effaceable settlings of the size of a pinhead were observed
(Figure 2). The kidneys of each snakes were normal in size and shape, however with a greyish-white pattern (Figure 3). The urinary channels were filled with stretching greyish-white, fragmentary uric acid. In the pericardium of the female and one of the male vipers (male number 1) greyish-white, mortar-like/gypsum-like detritic material was observed (Figure 4). In the coat of the lung of the male snake number 3, chalk dust-like foyers of a size of a pin-prick were detected (Figure 5). In case of snake number 2 and 4, multiple greyish-white effaceable settlings were observed on the mucous membrane of the mouth and the pharyngeal cavity. After the removal of the pseudomembranes the bottom part of the area was red because of acute inflammatory processes (Figure 6).
During the in vitro bacteriological investigation, no infective bacteria were detected from the liver.

Discussion
In each cases of the four dissected milos vipers, serious kidney and visceral gout was identified, despite of the good condition of the animals.
In the snakes the most common reasons of gout is known to be the uptake of kidney impairing substrates, while the second reason is supposed to be the dehydration caused by the lack of drinking water.
In our case the appearance of gout is suspected to be related to exsiccation, consequential hypovolemia and thus the decreased kidney perfusion, although the animals had free access to drinking water all the time.
Traditional bulbs were used to illuminate the snakes, decreasing more the low relative air humidity (30–60%) in the terrariums during the daytime hours. In the nature, milos vipers live in dry mezoclimate areas, nevertheless, in their natural habitat these snakes spend the hot daytime hours in underground holes and caves, where air humidity is much higher than that of the terrariums. We suggest, that in our case the impairment of kidneys were generated by the high haemoconcentration (caused by the low humidity in the terrarium) and the insufficient blood supply (perfusion) of the kidneys. Enhancing the emergence of gout, after feeding, the metabolates released from the digestion of the pray’s tissues also burdened the kidneys, which has usually slow blood support. Regarding, that in the present study the animals were observed every day routinely, fed on pray animals (mice) of controlled origin and that kidney compromising medicines (such as gentamycin) were not used, the appearance of gout can be explained only with the keeping conditions.
Our study confirms the high sensitivity of milos vipers to the changes (decrease) of air humidity, thus the relative air humidity of their terrarium should never drop below 70–75% (3, 6, 9, 10). Therefore during the keeping of M. schweizeri the regular control of air humidity and the spraying of tap water in the terrarium at least once a day are necessary. Besides, it is expedient to change their drinking water in every 2 or 3 days because these animals don’t drink stale, warm water willingly.

Figure 1.

Figure 1. Milos viper (Macovipera schweizeri)
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Figure 2.

Figure 2. Uric-acid salt precipitated on the serous membrane of the liver
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Figure 3.
Figure 3. Uric acid deposits in the kidneys
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Figure 4.
Figure 4. Settlings of uric acid salts in the pericardium and blood vessels
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Figure 5.
Figure 5. Tophi in the lungs
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Figure 6.
Figure 6. Uric-acid precipitated in the mouth and pharyngeal cavity
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Author Wintering temperature (ºC) 
Duration of wintering
(days)
3
13-15
-
6
4-10
-
7
13
-
8
12,2-14,5
45-73

Table. Data on the indoor wintering of Milos viper
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