Crooked Calf - Lupine Induced Arthrogryposis
Collaborative research FDIU and USDA PPRL Utah
Crooked calf is the colloquial name given to a pattern of congenital anomalies that occurs in the offspring of range-grazed cows in certain areas of the western United States. The anomalies are characterized by the presence of arthrogryposis (flexure of a joint) of the forelimbs typically involving both the elbow and the carpal joints, and by the variable presence of torticollis (wryneck, twisting of the neck), scoliosis, (lateral curvature of the spinal column) kyphosis (humpback, dorsal curvature of the spinal column), and cleft palate. The problem results when cows in early pregnancy ingest lupines (Lupinus spp.) that contain high concentrations of teratogenic alkaloids. A wide spectrum of severity is observed in affected calves. Calves with severe deformities cannot stand to suckle or follow the dam and must be destroyed for humane reasons. Less severely affected calves (bent limbs) can stand and walk and are viable but are not suited to range conditions.
Crooked calf has been reported from several areas in the western continental United States, British Columbia in Canada, and Kodiak Island in Alaska. In Washington State, it occurs sporadically in several areas east of the Cascades but it is particularly prevalent and recurrent in parts of the Channeled Scablands in the central part of the State. This is a semi-arid area of extensive rangeland and large ranches, which is unsuitable for agricultural use other than grazing. The severity of the problem in all affected regions varies from year to year, both with respect to the number of calves born affected and to the severity of the deformities in affected calves. In the scablands, ranches at risk for this disease commonly experience an incidence of moderate deformity in a small percentage of calves but periodically there are years in which a large proportion of calves born are affected with severe deformity. The 1997 spring calving was such a year and several hundred calves were born deformed. Since 1980, there have been 7 years with high prevalence and severity.
Crooked calf occurs when cows in early pregnancy consume lupines that contain high concentrations of teratogenic alkaloids. Experimental studies indicate that these alkaloids exert their effect by producing a sedating effect on the fetus that depresses normal fetal movements in utero. The calf may be in an abnormal position when its movements become depressed from the sedative effect of the ingested alkaloid and it remains fixed in that abnormal position while it still continues to grow. The resultant growth is deformed and the severity of the deformity may rest with the duration of sedation associated with the length of time of lupine ingestion by the dam and the concentration of teratogenic alkaloid ingested. The bovine fetus is susceptible to the sedative effects of the teratogenic alkaloids during the early stages of its development. Based on challenge studies and epidemiological studies this period appears to extend from approximately 40 to 110 days of gestational age with a period of high susceptibility between 40 and 70 days.Lupines are widely distributed across the western United States and Canada and there are many species. Most are perennial and produce a hard seed that is viable for many years. Speciation within the genus is extensive and complicated by the fact that hybridization occurs among the species. Like other legumes they have a high protein content and high nutritive value but many species contain toxic or inhibitory substances. These include over 100 different alkaloids each with differing biological activities. The types and concentrations of these alkaloids vary between the species and between collections of the same species. Lupines with high alkaloid content are termed "alkaloid "rich" or "bitter" lupines, which terminology includes the majority of the western range lupines. There are also "alkaloid poor" or "sweet" lupines that are used for animal and human feed. Some lupines produce alkaloids which are teratogenic while others do not.
The quinolizidine alkaloid anagyrine was the first alkaloid identified as a teratogen in lupines. Native lupines commonly found on the rangeland of western America that contain potentially teratogenic concentrations of anagyrine include L.albicus, L. alpestris, L. andersonii, L . argenteus, L, bakeri, L. burkei, L. caudatus, L erectus, L. evermannii, L. latifolius, L. laxiflorus, L. leucophyllus, L. littoralis, L. montigenus, L. polyphyllus, L. sericeus and L. sulphureus. More recently certain piperidine alkaloids in lupines have also been shown to be teratogenic and to produce congenital deformities. Lupine species producing teratogenic piperidine alkaloids include L. formosus and L. arbustus.
Within the lupine the alkaloid concentration varies according to the stage of growth. It is moderately high in the young growing leaf material, decreases in concentration in the more mature leaf growth, is high in the flower bud and highest in the seed. Alkaloid concentration in lupines may be influenced by environmental factors, plant nutrition and the mineral status of the growing medium and by climate. In the scablands lupines are in flower as early as mid-May with flowering continuing throughout the remainder of the spring and summer. The bulls are turned in for mating in March through early May.
Research and findings to date
Our initial approach to the problem has been to define its descriptive epidemiology on the Channelled Scablands. Current and historical prevalence data for the affected range indicates that there are areas of high risk, moderate risk and low risk for crooked calf. Areas of high and low risk exist within a few miles of each other and with different pastures on the same range. Both areas have lupines. There are also areas with no history of crooked calf, which also have lupines. We have established 98 Global Positioning System--identified transects on ranches representing pastures from low to high risk for crooked calf to address whether area differences in risk relate to area differences in lupine species or alkaloid content. Lupine species identification, lupine density estimates and collections for alkaloid analysis and soil analysis have been made at each transect. Data is entered in a Geographic Information System.
There are two major lupine species on the problem range L. leucophyllus and L. sericeus. L. leucophyllus is the dominant of the two and is present in high, moderate and low risk areas. L. sericeus is more restricted in occurrence but is present in high and low risk range.
There are differences in grazing of lupines, which varies between pastures and between and within lupine species. L. leucophyllus is grazed in preference to L. sericeus.
In this region L leucophyllus contains the teratogenic alkaloid anagyrine and L sericeus does not.
We have examined for differences in soil type and trace element composition and stocking density on high risk and low risk pastures and found no significant difference.
In affected herds, all cows have not given birth to crooked calves even though all cows in the group have been at equal risk grazing the same pasture. Blood alkaloid concentrations in challenge studies of cows that have had crooked calves paired with cows from the same ranch that had normal calves not indicate that this difference in occurrence is not due to differences in the absorption and metabolism of anagyrine.
This is strongly suggestive of the occurrence of preference/aversion grazing of lupines by individual cows. The low stocking density, the extent and difficult terrain of the range, the widespread distribution of the lupines and the length of the period of susceptibility during the grazing season, are a challenge to research on lupine consumption during nthe grazing period. Research headed by range scientists at the USDA PPRL is currently examining the grazing behavior of cattle on this range by daily bite count studies.