Cistus salvifolius

ARTICLE ORIGINAL
A urinary retention syndrome in beef cows
probably caused by ingestion of Cistus
salvifolius
° I. YERUHAM*, °° U. ORGAD, °° Y. AVIDAR, °° S. PERL, °°° M. LIBERBOIM, °°° H. ADLER
and °° A. SHLOSBERG
° «Hachaklait» Gedera and the Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, POB 12, Rehovot 76100, Israel;
°° The Kimron Veterinary Institute, POB 12, Bet Dagan 50250, Israel
°°° «Hachaklait» Zichron Yakov, Israel
°°°° The Regional laboratory Western Gallilee
* Correspondance : I. YERUHAM, 4 Hagoren St., Gedera 70700, Israel
Fax : 972-8-869983 - E-mail : [email protected]
SUMMARY
RESUMÉ
Two outbreaks of a urinary retention syndrome in beef cattle grazing in
northern Israel and probably caused by ingestion of the shrub Cistus salvifolius are described. Consumption of Cistus shrubs occurred during a period of pasture scarcity in the years 1998-2000. A progressive syndrome of
wasting, apathy, anorexia, distention of the urinary bladder, dysuria, nephrosis, constipation and recumbency, culminating in death, was seen. In one
herd, a high mortality rate of 58.8% (20/34) in first and second calving cows
in comparision to 5.4% (4/74) in adult cows was noted. Typical clinicalpathological findings revealed increases in blood urea, creatinine, aspartate
aminotransferase (AST), creatine kinase (CPK) and lactate dehydrogenase
(LDH). Decreases were found in alkaline phosphatase (ALP), total serum
protein, albumin (ALB), potassium (K), sodium (Na) and chloride (Cl). No
significant changes were noted in levels of gamma glutamyl transferase
(GGT), calcium, triglyceride and cholestrol levels. The main pathological
findings were severe cystitis, pyelonephritis and a great increase in urine
bladder wall thickness. On the basis of epidemiology, clinical signs, clinical-pathological, and pathological and histopathological findings, a diagnosis of Cistus salvifolius toxicosis was made.
Un syndrome de rétention urinaire chez des bovins dû à l’ingestion de
Cistus salvifolius. Par I. YERUHAM, U. ORGAD, Y. AVIDAR, S.
PERL, M. LIBERBOIM, H. ADLER et A. SHLOSBERG.
KEY-WORDS : urinary retention - beef cows - Cistus salvifolius - toxicosis.
MOTS-CLÉS : rétention urinaire - bovins - Cistus
Salvifolius - intoxication.
Trees and shrubs in arid environments are often important
feedstuffs for ruminants, but their usefulness to grazing animals is often limited by the presence of toxins, such as phenolic compounds including tannins, which can adversely
affect feed intake, digestibility and or even cause toxicosis.
Twenty Cistus spp. shrubs (Cistaceae, rockrose family) grow
in the Mediterranean region, but only two species, Cistus salvifolius (sage-leafed cistus) and C. creticus, are found in the
eastern Mediterranean.
Cistus spp. toxicosis in ruminants is an uncommon phenomenon. There are few reports on Cistus (C. laurifolius, C.
psilopsepalus, C. monspeliensis, C. ladaniferus) toxicosis in
sheep and goats in France and Italy [3, 14], and only one
other recent report in cattle [15]. Various flavonoids accumulate during leaf development in Cistus spp. [7, 8, 18, 25]. It
seems that one of the most likely toxic constituents, in the
various species of Cistus are tannins (derivatives of flavonols). Tannin content of plants may change dramatically
Revue Méd. Vét., 2002, 153, 10, 627-632
Cette étude décrit deux épisodes d’un syndrome de rétention urinaire
chez des bovins qui paissent dans le nord d’Israël, dus probablement à l’ingestion d’un arbuste, Cistus salvifolius.
La consommation d’arbuste du genre Cistus s’est produite au cours d’une
période de pénurie d’herbe dans les années 1998-2000.
Il a été observé un syndrome progressif de dépérissement avec apathie,
anorexie, distention de la vessie, dysurie, néphrose, constipation et décubitus conduisant à la mort.
Dans un troupeau, un taux de mortalité élevé de 58,8 % (20 animaux sur
34) a été enregistré sur des vaches au premier ou second vêlage par rapport
à 5,4 % de mortalité (4 animaux sur 74) sur des bovins adultes.
Les analyses biochimiques sanguines montrent une augmentation de
l’urée, de la créatinine, de l’aspartate aminotransférase (AST), de la créatine kinase (CK) et de la lactate déshydrogénase (LDH) et une diminution de
l’alkaline phosphatase (ALP), des protéines totales du sérum, de l’albumine
(ALB), du potassium (K), du sodium (Na) et du chlore (Cl).
Aucun changement significatif n’est noté dans les taux de gamma glutamyl transférase (GGT), de calcium, de triglycérides et de cholestérol.
Les lésions révélées par l’autopsie sont : une sévère cystite, une pyélonéphrite, un important épaississement de la paroi vésicale.
Sur la base de l’épidémiologie, des signes cliniques, de la pathologie et
de l’anatomie pathologique, le diagnostic d’intoxication par Cistus salvifolius fut établi.
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within a single plant species according to seasonal changes in
leaf morphology, moisture content, and chemical composition [4, 11]. Tannins are a very complex group of plant antinutritional metabolites that are distinguished from other
polyphenolic compounds by their ability to precipitate proteins. Their major negative effect results from either direct
inhibition of digestive enzymes, or from formation of indigestible complexes with endogenous proteins [22]. Tannins
are converted by bacterial fermentation in the rumen to gallic
acid and pyrogallol, both known to be nephrotoxic [10, 19,
20].
In ruminants ingesting tannins, supplementation of polyethylene glycol (PEG) increased digestible organic matter
intake, which was associated with a marked improvement in
protein and cell wall digestibility [22]. PEG is a polymer that
binds tannins irreversibly over a wide range of pH (2-8.5)
and its presence reduces the formation of protein-tannin complexex [12]. The present report describes the clinical, laboratory, and pathological findings concerning presumed Cistus
salvifolius toxicosis in 2 beef cattle herds grazing in the northern hills of Israel.
Case report
A) HISTORY
One herd (Herd A) comprised an average of 54 mixedbreed beef cattle kept in a natural hilly pasture in the Carmel
hills in Israel. The heifers were kept in barns until post-calving, and than were transferred to the pasture. During the
summer months (June-November), the owner supplemented
the drinking water with Polyethylene glycol (PEG) at a
dosage of 40 g/head per day. During 2 observation years
(1998-1999, 1999-2000) animals started to show clinical
signs and mortality in the autumn-winter months (NovemberFebruary). The syndrome was only seen in females. In the
course of the illness, clinical examinations were conducted
and blood samples were collected from 6 animals exhibiting
the syndrome. Blood samples taken from grazing clinically
healthy grazing animals in a neighboring herd [2] serve as a
comparison.
The second herd (Herd B) grazed for the first time, on a
rocky, hilly area in the far north of Israel and after several
months the clinical syndrome was seen from about
December-April.
B) LABORATORY PROCEDURES
Clinical-pathological, urine analysis and haematological
examinations were performed on affected animals, and postmortem examinations were carried out on 4 cows in Herd A.
Specimens of liver, lung, kidney and alimentary tract were
collected in 10 % neutral buffered formalin. Sections were
stained with haematoxylin-eosin and examined by light
microscopy.
The blood samples were collected by means of jugular
venipuncture, into plain evacuated tubes for recovery of
serum and into EDTA-containing tubes for complete blood
count (CBC). The serum was separated and analyzed within
YERUHAM (I.) ET COLLABORATEURS
24 h. Enzymes, metabolites and minerals were analyzed
spectrophotometrically with a Kone Selective Chemistry
Autoanalyser (Kone Corporation, Finland) at 30°C, according to standard methods. The following enzymes were
determined: aspartate aminotransferase EC 2.6.1.1 (AST);
lactate dehydrogenase EC 1.1.1.27 (LDH); alkaline phosphatase EC 3.1.3.1 (ALP); creatine kinase EC 2.7.3.2 (CPK);
gamma-glutamyltransferase EC 2.3.2.2 (GGT). The following metabolites were determined as indicated: urea, enzymatically; creatinine colorimetrically; albumin and protein,
colorimetrically; globulin by subtracting albumin from total
protein; and triglyceride, colorimetrically. Sodium (Na),
potassium (K) and chloride (Cl) were determined by means
of a Kone Selective Ion Analyzer (Kone Corporation,
Finland). Calcium (Ca) and inorganic phosphorus (Pi) were
determined colorimetrically, respectively, [26]. Urine
samples were collected via free catch in specimen cups and
stored as 4°C awaiting analysis for urinary calculi and bacteriological examination. The urine samples were inoculated
onto 5 % sheep blood agar, nutrient agar and McConkey agar
(Difco laboratories) and incubated overnight at 37°C. CBC
and differential counts were performed by standard procedures, with the Technicon H1 System (Miles Inc; Diagnostics
Division, Tarrytown, NY).
Statistical analysis was performed with the SAS software
(21), with differences between the comparison group and
affected group being considered significant at p < 0.05.
C) CLINICAL FINDINGS
In Herd A, the condition of the first and second calving
cows deteriorated markedly, and ultimately the mortality rate
reached 58.8 % (20/34) in comparison to 5.4 % (4/74) in
adult cows (Table I). The progressive syndrome seen in both
herds comprised manifestations of apathy, anorexia, decreased rumen motility and cessation of rumination. Persistent
elevation of the tail head in many cows was often accompanied by difficulty in urination, with dribbling of drops of
urine, or a persistant low volume stream of urine, with no
straining, being typical; rectal examination invariably revealed a full urinary bladder. Dehydration was seen with moderate subcutaneous oedema under the jaw and on the ventral
abdomen. Dry rough coats, crust on muzzle and constipation
were also observed. Rectal temperature of all examined animals was normal, but heart and respiratory rates were usually
elevated (95-110 beats/min and 50-70 breaths/min). Once
severe urinary difficulties were apparent, there was a rapid
weight loss, culminating in recumbency, severe cachexia and
death.
Examination of the pasture in Herd A revealed very high
consumption of both Cistus salvifolius and C. creticus
bushes. In the pasture of Herd B, only C. salvifolius was present.
D) BIOCHEMICAL, BACTERIOLOGICAL AND HAEMATOLOGICAL FINDINGS
The biochemical findings of the affected animals in Herd
A are presented in Figures 1-5, and with data from clinically
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A URINARY RETENTION SYNDROME IN BEEF COWS PROBABLY
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Mortality
Year
First & second calving cows
Adult cows
1998/1999
10/14 (71,4 %)
2/36 (5,5 %)
1999/2000
10/20 (50 %)
2/38 (5.3 %)
1998/2000
20/34 (58,8 %)
4/74 (5,4 %)
TABLE I. — Mortality in Herd A, caused apparently by Cistus toxicosis
healthy animals at the same age, and breed from a neighboring herd for comparison. Marked increases in LDH
(3070 ± 476 SD compared with 2307 ± 34 in the normal herd)
(P < 0.05), CPK (1486 ± 1918 vs 219 ± 73 U/L) (P < 0.001)
(Fig. 1), and AST (133 ± 76 vs 76 ± 17) (P < 0.001) (Fig. 2).
A decrease was found in ALP (118 ± 43 vs 286 ± 147 U/L)
(P<0.01) (Fig. 2). Increase in blood urea (105 ± 53.3 mg/dl)
in comparison with the normal herd (49.4 ± 12.2 mg/dl)
(P<0.001) (Fig. 3), and the same pattern was noted also with
creatinine (3.89 ± 1.94 vs 1.22 ± 0.15 mg/dl) (P < 0.001)
(Fig. 4). Decreases in total proteins (72 ± 2 vs 81.7 ± 3 gr/dl
in the normal herd) (P<0.01); albumin (33±1 vs 36.5±2 gr/dl)
(P < 0.01); and globulin (39 ± 3 vs 45.2 ± 4.5 gr/dl) (P < 0.01)
(Fig. 5) were noted. Calcium decreased slightly (8.6 ± 1.0 vs
9.57 ± 0.54 mg/dl in the normal herd). No significant changes
were noted in the GGT, triglyceride and cholesterol levels.
Comparison among the levels of minerals and electrolytes
revealed decreases in K, Na, and Cl compared with the normal herd (4.66 ± 0.46 vs 5.69 ± 0.15; 139 ± 4.0 vs 142 ± 2.1;
93.7 ± 4.3 vs 107.6 ± 4.3 mmol/l, respectively) (P < 0.01) and
increase in Pi (9.33 ± 0.82 vs 7.24 ± 0.3 mg/dl) (P < 0.01)
(Fig. 4). Urine samples were dark yellow and of moderate
specific gravity (1.025 on average) and urine pH was 7.6 on
average. The urine contained 100-300 mg/100ml protein.
Microscopic examination of the urine sediment revealed
crystals of triple phosphate and moderate quantity of erythrocytes. Bacterial cultures of urine samples were negative.
Haematology did not reveal any consistent abnormalities.
FIGURE 1. — Serum LDH and CK of control and affected animals caused by
intake of Cistus.
E) PATHOLOGICAL AND HISTO-PATHOLOGICAL FINDINGS
The most prominent pathological findings at necropsy
were consistently an urinary bladder that was greatly distended and filled with a turbid haemorrhagic urine. The bladder
wall was thickened and very hyperaemic with a irregular
mucosal surface (Fig. 6). Kidneys were slightly enlarged, had
an irregular surface with yellow, pale foci randomly scattered
over the surface but more abundant in the poles of the kidneys and showed a mild interstitial nephritis. Histopathology
of the kidneys revealed a severe, subacute, diffuse neutrophilic pyelonephritis (Fig 7). In the urinary bladder the transitorial epithelium was absent in most areas and was replaced by
necrosis and inflammation. The propria mucosa was infiltrated by mixed inflammatory cells mainly lympho-plasmocytes, some histiocytes and a few neutrophils (Fig. 7).
In the mucosa of the small intestine a moderate, diffuse,
subacute to chronic enteritis was observed. The majority of
FIGURE 2. — Serum ALP and AST of control and affected animals caused by intake of Cistus.
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YERUHAM (I.) ET COLLABORATEURS
inflammatory cells were lympho-plasmocytes and numerous
eosinophils were also present. No significant histopathological lesions were seen in all the other tissues examined including the brain and entire length of the spinal cord.
Discussion
Despite the relatively high widespread of Cistus spp. in the
Mediterranean basin there has been only one other case of
suspect Cistus toxicosis in cattle [15]. The flowering period
of C. salvifolius is between March and June. The Habitat is
on garigue, rocky places on limestone soils. All Cistus spp.
should be regarded as potentially toxic because of their relative high tannin concentration. The tannin concentration in
Cistus spp. in Israel is about 25 % of the dry matter
(GILBOA, personal communication). The effects of heavy
consumption of Cistus spp. apparently due to the supplement
FIGURE 3. — Serum urea of control and affected animals caused
by intake of Cistus spp.
of PEG in the drinking water [22], in the late autumn and at
the beginning of the winter (October-December), when pasture was sparse, aggravated by insufficient supplemental feeding, may have been the cause of the toxicosis in Herd A.
The daily supplementation of PEG increase the intake and
digestion of tannin-containing leaves [22]. The affected animals developed a chronic course of debilitating disease. This
disease lasted for several weeks after removal of the animals
from the Cistus source. The condition was not diagnosed as
having any involvement with an infectious or metabolic
diseases.
The duration of the toxicosis seemed to vary with the
amount of toxin ingested, as reported in a previous toxicosis
[26]. The cattle in the present study were suspected of having
been exposed to a toxic agent, and the pastures were thoroughly examined for the presence of known toxic annual
and perennial plants, chemicals or non-made artifacts, but no
FIGURE 4. — Serum creatinine and phosphorus of control and affected animals caused by intake of Cistus.
FIGURE 5. — Serum proteins of control and affected animals caused by
intake of Cistus.
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A URINARY RETENTION SYNDROME IN BEEF COWS PROBABLY
631
Figure 6. (ci-dessus) — Glomerulo-interstitial nephritis with proteinaceous
tubular casts (H & E x 40).
FIGURE 7. (ci-contre) — Cystitis, epithelial necrosis and submucosa infiltration with inflammatory cells (H & E x 10).
plausible cause was found. As Herd A was on sparse pasture
and no supplementary feed had been given, except the PEG
in drinking water, it is believed that the herd lacked access to
sufficient feed and thus were forced to eat native shrubs and
bushes. Only Cistus spp. were considered to be sufficiently
toxic to induce such a syndrome, especially when the climatic conditions during 1998-2000, possibly caused on
increase of tannins concentrations in the Cistus. The mode of
elimination of PEG - tannin complexes from the intestine are
still uncertain. Possibly these complexes may contribute also
to the nephrotoxicosis. The condition of affected animals
deteriorated markedly, and the mortality rate reached 58.8 %
for the first and second calving cows and only 5.4 % for the
adult cows. It seems that young cattle are more susceptible to
oak toxicosis [5, 6, 16, 26]. Urinary retention, the incomplete
emptying of the bladder, may be caused by failure of contractile function, inappropriate outlet resistance, or both [13]. No
evidence was found for physical or anatomical causes, unlikely anyway in many cows simultaneously. No histopathological lesions were found in the spinal cord to indicate a central effect. Phenolic compounds may block pudendal nerves
[13], and manipulation of pudendal nerve activity has been
attempted to reduce striated urethral muscle resistance. This
is probably the reason for the urinary retention and distended
urinary bladders found in the affected animals.
The clinical signs, macrosopic and microscopic lesions
closely corresponded to those described in cattle succumbing
to oak toxicosis [5, 6, 16, 26]. The nephrotoxicosis might be
attributed to a peracute decrease in glomuralar filtration rate
and oliguria [24] caused by renal changes elicited by ischaemia and the nephrotoxic nature of tannins and their metabolites [1, 28], or secondary to the pathological accumulation of
urine in the bladder.
Our findings provide evidence that renal demage, paralysis
of the urinary bladder and uremia may be the cause of death
Revue Méd. Vét., 2002, 153, 10, 627-632
in Cistus toxicosis since striking elevations of the urea and
creatinine levels, like those associated with nephrosis, were
found. It has been stated that only after extensive loss of 5060 % of glomerular function will serum urea and creatinine
concentrations increase [24], which means that increases in
serum concentrations of creatinine and urea are sensitive
indicators of partial renal dysfunction [23]. Serum creatinine
concentration is usually considered a more accurate indicator
of renal function in ruminants than urea concentration,
because the normally functioning rumen recycles urea by
using it a nitrogen source for bacterial protein synthesis [17].
This microbial activity decreases or disappeared as a secondary effect of renal diseases and prolonged anorexia [17].
The marked increase in urea concentration found in the affected cattle in the present outbreak is an important finding,
implying decreased urea clearance by rumen and kidneys,
and it supports the role of renal failure in the pathogenesis of
Cistus toxicosis similar to the condition in oak toxicosis.
Blood urea and creatinine estimations have also been of prognostic value [17, 24]. Decreases in sodium and chloride also
occur in renal disease [26]; decreases in plasma concentrations of these electrolytes are a result of excessive loss
through kidney or decreased reabsorption in the glomerulus.
In the present survey decreases in sodium and chloride
concentration were moderate, compared with the normal
group. Polyuria, low urine specific gravity and proteinuria
also contributed to clinical deterioration and ultimately to
death.
Elevations of AST, CPK and LDH were apparently due to
muscle damage consequent to recumbency of the affected
animals [2]. The decrease in total protein concentration was
due to hypoalbuminaemia resulting from albumin loss in the
kidney («nephrotoxic syndrome») [2]. Malabsorption was
most probably the reasons for the decreases in alkaline phosphatase and albumin levels [2]. Inorganic phosphorus was
reabsorbed from the glomerular filtrate by the renal tubules,
632
even though the increase in serum concentration was not
significant. It can indicated tubular dysfunction and it is a
useful diagnostic indicator of the development of renal
disease [2, 23]. Hypocalcaemia has been reported in cases of
chronic renal failure [2], and could also be a result of hypoalbuminaemia.
Supplementary feeding with hay and further consideration
of supplemention with PEG may be beneficial and cost effective especially when there is pasture scarcity. Presumptive
diagnosis of Cistus toxicosis was made, based on a herd history of exposure to Cistus shrubs, physical findings of the
sick animals, clinico-pathological data consistent with renal
dysfunction, results of urine analysis, and gross and microscopic kidney lesions (renal tubular necrosis).
This clinical diagnosis indicates that these should be an
increased awareness that Cistus toxicosis may occur in cattle
in the Mediterranean region. It is strange that such an obvious
clinical syndrome had not been recorded previously in the
Mediterranean basin, apart from one report from Portugal, at
the opposite, far side of the Mediterranean [15]. The cases in
Portugal occurred in the same years as these cases, but were
more chronic in nature, and were not always fatal; probably
less tannins or some other toxic components were ingested.
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