Enzootic Geophagia of Calves and Lambs in the Northern Cape And

SA-ANIM SCI 2001, vol 2: http://www.sasas.co.za/Popular/Popular.html 9

Enzootic geophagia of calves and lambs in the Northern Cape and North-West Provinces of the Republic of South Africa, and the possible role of chronic manganese poisoning

J.A. Neser Pathology Section, Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort 0110, RSA e-mail: [email protected]

Enzootic geophagia Geophagia, the deliberate ingestion of soil, has been classified as a form of pica. Geophagia in mammals has been associated with deficiencies of elements such as phosphorus, sodium, magnesium, sulphur, copper, cobalt and manganese (Kreulen & Jaeger, 1984). Geophagia may also be an instinctive behavioural response to gastro-intestinal disturbances (Kreulen, 1985; Johns & Duquette, 1991; Reid, 1992). In this presentation a specific enzootic form of geophagia is described which occurs in young beef calves and lambs born under ranching conditions at very specific locations in the Northern Cape and North-West Provinces of South Africa.

Symptoms, age susceptibility and incidence Young calves display an insatiable appetite for the manganese-rich soil. Some calves lick iron poles. Severe constipation and dehydration develop and death occurs within 7 to 14 days of age. Calves older than ± 2 months are rarely affected. However, morbidity and mortality rates have been difficult to determine accurately. The farmers managed to control the occurrence of the geophagia by keeping their cows with young calves on deep litter in pens, allowing cows limited grazing during the day. They were also successful in suppressing the symptoms by injecting their calves shortly after birth with commercial iron-dextran compounds.

Geographical distribution, geology and topography The Enzootic geophagia occurs on a limited number of farms in the Vryburg, Postmasburg and Barkley West districts of the Northern Cape and North-Western Provinces. The affected farms are found in an arid region of the provinces, known as the Ghaap Plateau. All farms have one characteristic in common, a manganese-rich soil with superficial outcrops of manganese-rich dolomite rock. According to the Official Geological Map (1:1000000) of South Africa (Council for Geoscience, Private Bag X112, Pretoria 0001, RSA), the affected area is underlain by manganese-rich dolomitic or carboniferous rock of the Reivilo Formation (Astrup & Tsikos, 1998). The area has a unique geological composition of limestone, dolomite and chert. The affected areas are characterized by wide, shallow pans. Rainwater tends to drain slowly from the pans. The soil contains numerous densely distributed, round to ovoid, black-grey carboniferous concretions of ca. 1-10 mm, derived from the superficial weathering of parent rock under warm moist conditions in the pans. The soil contains an average of 8% manganese, 3% iron and 0.0024% cobalt.

Ingestion of manganese-rich concretions by calves and lambs The stimuli prompting the ingestion of the manganese-rich soil by calves and lambs are unknown. Evidence of the ingestion of small quantities of soil by calves and lambs is frequently observed during routine post mortem examinations. Graham et al. (1994) associated consumption of soil by calves with a deficiency of minerals especially iron in their dams’ milk. It may also be a displaced reaction to hunger when the calves are temporarily deserted by their dams when grazing. Such calves were observed to start licking soil. In our investigations calves and lambs reared in confinement voluntarily ingested small quantities of soil from both affected and unaffected farms in the affected area, as well as soils from experimental farms where geophagia is unknown. In all cases the dams were not deficient in phosphorus or sodium, thus excluding these as possible causes of geophagia in their calves. The ingestion of the manganese-rich soil was SA-ANIM SCI 2001, vol 2: http://www.sasas.co.za/Popular/Popular.html 10

found to aggravate the initial ingestion of this soil and produced severe geophagia experimentally in a high proportion of young calves. The tendency apparently disappears when the rumen becomes functional. The mechanism through which the intake of manganese initiates geophagia in calves and lambs is unclear and apparently rather complex. It is known that manganese interferes with iron absorption by competitively binding to sites for absorption (Thomson & Valberg, 1972; Hurley & Keen, 1987). Manganese has been shown to interfere with the availability of zinc in the digestive tract, as well as with the uptake of cobalt by micro-organisms in the rumen (Pfander et al., 1966). A deficiency in cobalt has been associated with pica in cattle (Kreulen & Jaeger, 1984; Valli & Parry, 1993) and a zinc deficiency has been implicated as a cause of geophagia in children (Hambidge et al., 1987). It is hypothesized that the ingestion of manganese-rich soil has a perpetual effect in the gastro- intestinal tract of the calf, thereby causing progressive deficiencies of iron and/or zinc. This prompts a vicious cycle of increasing consumption of the manganese-rich soil that ultimately leads to the demise of the calf. In our investigation geophagia could be prevented in the calves exposed to manganese-rich soil from the affected area by prophylactic injections of commercial iron- and vitamin B12 compounds at birth, and at 10 days of age.

Hepatotoxic effect of manganese The main characteristic of the problem is liver damage. Macroscopical pathological changes consist of moderate to severe jaundice and a marked enlargement and yellow discolouration of the liver. The ingestion of soil leads to varying degrees of constipation and colic. This probably causes the cessation of suckling which contributes to occurrence of death within 7 – 14 days after the commencement of geophagia. Dark- brown to black soil, largely consisting of manganese-rich concretions, is usually found in the abomasum and small intestine of the animal. Liver specimens from calves and a lamb with soil in their digestive tracts or a history of geophagia revealed high concentrations of manganese, ranging from 10 – 1800 mg/kg wet liver mass compared to the normal range of 2 – 3 mg/kg wet mass (Hurley & Keen, 1987). A preliminary investigation showed that the concentrations of manganese and iron in the livers of yearlings and culled cows from two severely affected farms were within normal ranges for cattle. The histopathological changes in the liver were consistently characterized by a chronic cholangiohepatitis with marked portal fibrosis and bile duct proliferation. Similar histopathological changes could be induced in the liver of laboratory rodents through the experimental dosing of manganese compounds (Findlay, 1924; Witzleben et al., 1968). The concentrations of the other elements in the liver did not show any specific pattern which could be related to soil ingestion. The manganese concentration in the livers of full-term bovine foetuses from cows in the affected areas as well as from new-born calves before milk was ingested, were within the normal range. Transplacental transmission of manganese with its accumulation in the livers of calves, rabbits and mice has been reported where the dams were supplemented with manganese (Hurley & Keen, 1987). However, our observations were based on a limited number of animals, and further cases will have to be examined to arrive at more definite conclusions on the possible role of transplacental transmission of manganese on the occurrence of geophagia in calves in the affected area. The contribution of a possible manganese-induced vitamin B12 deficiency in the mothers which is transferred to their offspring has not been investigated. This seems unlikely because the geophagia could be induced in calves at experimental stations where their mothers were not subjected to an overexposure of manganese.

Final conclusions The ultimate cause of the geophagia is still uncertain. The characteristic lesions in the liver can be attributed to a subacute to chronic form of manganese poisoning caused by an abnormally high intake of manganese-rich soil. Our findings suggested that the accumulation of manganese in their livers occurs mainly after birth. Therefore, the occurrence of geophagia in the calf seems to be independent of the habitation of their mothers in the affected area, though the beef production practices on the farms seem to contribute to the occurrence of the problem.

References SA-ANIM SCI 2001, vol 2: http://www.sasas.co.za/Popular/Popular.html 11

Astrup, J. & Tsikos, H., 1998. Mineral Resources of South Africa. In: Handbook of Geological Survey of South Africa. Eds. Wilson, M.G.C. & Annhauser C.R., 6th ed. pp, 450 – 460. Council for Geoscience, Private Bag X112, Pretoria 0001, South Africa. Findlay, G.M., 1924. The production of biliary cirrhosis by salts of manganese. Br. J. Exp. Path. 5, 92–99. Graham, T.W., Thurmond, M.C., Mohr, F.C., Holmberg, M.L. & Keen, C.L., 1994. Relationships between maternal and foetal liver copper, iron, manganese and zinc concentrations and fetal development in California Holstein dairy cows. J. Vet. Diag. Investig. 6, 77–87. Hambidge, K.M., Casey, C.E. & Krebs, N.F., 1987. Zinc. In: Trace elements in human and animal nutrition. Mertz, W. (ed.). 5th ed. Academic Press Inc., San Diego, U.S.A., Vol. 2, 50–51. Hurley, L.S. & Keen, C.L., 1987. Manganese. In: Trace elements in human and animal nutrition. Mertz, W. (ed.). 5th ed. Academic Press Inc., San Diego, U.S.A. Vol. 1, 185–223. Johns, T. & Duquette, M., 1991. Detoxification and mineral supplementation as functions of geophagy. Am. J. Clin. Nutr. 53, 448–456. Kreulen, D.A. & Jagger, T., 1984. The significance of soil ingestion in the utilization of arid rangelands by large herbivores with special reference to natural licks on the Kalahari pans. In: Herbivore Nutrition in the Tropics and Subtropics. Eds: Gilchrist, F.M.C. & Mackie, R.I. The Science Press, Craighall, South Africa. pp. 204-221. Kreulen, D.A., 1985. Lick use by large herbivores:A review of benefits and banes of soil consumption. Mammal Rev. 15, 107–23. Morris, E.R., 1987. Iron. In: Trace elements in animal and human nutrition Mertz, W. (ed.). 5th ed. Academic Press Inc., San Diego, U.S.A. Vol. 1, 79–142. Neser, J.A., de Vries, M., de Vries, M.A., Van der Merwe, A.J., Loock, A.H., Smith, H.J.C., Van der Vyver, F.H., Elsenbroek, J.H. & Delport, R., 1997. The possible role of manganese poisoning in enzootic geophagia and hepatitis of calves and lambs. J. S. Afr. Vet. Assoc. 68, 2–7. Pfander, W.H., Beck, H. & Preston, R.L., 1966. The interactions of manganese, zinc and cobalt in ruminants. Fed Proc. 25, 1362. Reid, R.M., 1992. Cultural and medical perspectives on geophagy. Med. Anthropol. 13, 337–351. Thomson, A.B.R. & Valberg, L.S., 1972. Intestinal uptake of iron, cobalt and manganese in the iron deficient rat. Am. J. Phys. 223, 1327-1329. Valli, V.E. & Parry, B.W., 1993. Anemia. In: Pathology of Domestic Animals. Eds. Jubb, K.V.F., Kennedy, P.C. & Palmer, N., 4th ed. Academic Press Inc., San Diego, U.S.A. Vol. 3, 72. Witzleben, C.L., Pitlick, O.P., Bergmeyer, J. & Benoit, P., 1968. Acute manganese overload – A new experimental model of intrahepatic cholestasis. Am. J. Path. 53, 409–423. ENZOOTICENZOOTIC GEOPHAGIAGEOPHAGIA OFOF CALVESCALVES ANDAND LAMBSLAMBS ININ THETHE NORTHERNNORTHERN CAPECAPE ANDAND NORTH-WESTNORTH-WEST PROVINCESPROVINCES OFOF THETHE REPUBLICREPUBLIC OFOF SOUTHSOUTH AFRICA,AFRICA, ANDAND THETHE POSSIBLEPOSSIBLE ROLEROLE OFOF CHRONICCHRONIC MANGANESEMANGANESE POISONINGPOISONING

J.A. Neser1, M.A. De Vries2, Mandy De Vries2, A.J. Van der Merwe3, A.H. Loock3, H.J.C. Smith3, F.H Van der Vyver4 & J.H. Elsenbroek5 1Pathology Section, Onderstepoort Veterinary Institute, P/Bag X05, Onderstepoort 0110, RSA 2State Veterinary Laboratory, P/Bag X36, Vryburg 8600 3Institute for Soil, Climate and Water, P/Bag X70, Pretoria 0001 4Directorate of Animal Health, P/Bag X369, Pretoria 0001 5Council for Geoscience, P/Bag X112, Pretoria 0001

1. ENZOOTIC GEOPHAGIA 7. THE HEPATOXIC EFFECT OF MANGANESE 1 7 · Geophagia or the deliberate ingestion of soil has been classified · The main feature of the disease is liver damage, although as a form of pica. the ingestion of soil also leads to variable degrees of · Geophagia can also be symptomatic for deficiencies of nutrient constipation and colic which probably causes the calf to stop elements such as P, Na, Mg, S, Cu, Co or Mn (Kreulen & Jaeger, suckling and contributes to death within c. 7-14 days after 1984). the commencement of geophagia. · Geophagia may also be an instinctive behavioural response to · Macroscopical pathological changes consisted of moderate gastro-intestinal disturbances (Kreulen 1985; Johns & Duquette to severe jaundice, marked enlargement and yellow 1991; Reid 1992). discolouration of the liver, as well as the presence of variable · In this illustration, a specific enzootic form of geophagia is amounts of dark-brown to black soil, largely composed of described. manganese-rich concretions in the stomach and intestines. · Enzootic geophagia occurs in young calves and lambs on · Liver specimens from calves and a lamb with soil in their manganese-rich soil with superficial outcrops of manganese-rich Calves eating soil digestive tracts, or a history of geophagia, revealed high dolomite rock in restricted areas of the Vryburg, Postmasburg and concentrations of manganese ranging from 10-1800 ppm wet Concretions on the surface Barkley West districts of the Northern Cape- and North-West Provinces of the RSA. mass [(normal range 2-3 ppm)(Hurley and Keen 1987)]. · The results of the analyses for the other mineral elements in the liver were inconclusive. · Manganese levels in liver specimens from full-term bovine fetuses that had died during dystocia, as well as new- 2. SYMPTOMS, AGE SUSCEPTIBILITY AND INCIDENCE 2 born calves that had not yet ingested milk, were within normal limits. · Manganese and iron levels were within normal limits in liver specimens from yearling tollies and culled cows from · Young calves born under ranching conditions display an insatiable two severely affected farms. appetite for the manganese-rich soil. · Some calves lick iron poles. · Severe constipation, dehydration and death occur within 7-10 days. 8. HISTOPATHOLOGICAL CHANGES IN THE LIVER 8 · The highest frequency occurs at 7-14 days, calves older than ±2 months, rarely being affected. · The histopathological changes in the liver were consistently · Morbidity and mortality rates are difficult to determine accurately. characterised by a chronic cholangiohepatitis with marked · Geophagia can be prevented by keeping cows with young calves portal fibrosis and bile duct proliferation. on deep litter in pens, allowing cows limited grazing during the · Similar histopathological changes could be induced in the day time. liver of laboratory rodents by the experimental dosing of · Farmers claim successful prevention of geophagia by injecting manganese compounds (Findlay 1924; Pitlick, Bergmeyer calves with commercial iron-dextran compounds shortly after birth. Calf licking iron pole et. al. 1968).

3. GEOGRAPHICAL DISTRIBUTION 3 9. EXPERIMENTS WITH SOIL FEEDING AND MINERAL SUPPLIMENTATION · Enzootic geophagia occurs on a limited number of farming units Concretions in the stomach in the Vryburg, Postmasburg and Barkley West districts of the · Fatal geophagia could be caused in young calves at the PVL Northern Cape and North-Western Provinces. at Vryburg and at the OVI by offering manganese-rich soil · Affected farms are situated on an extensive area known as the from the affected area to calves purchased from locations Ghaap Plateau. other than the affected area. 9 · Geophagia could be prevented in calves exposed to manganese- rich soil from the affected area by the prophylactic injection 4. GEOLOGY OF THE AFFECTED AREA of commercial iron- and vitamin B12 compounds at birth, and at 10 days of age on farms in the affected area, as well · According to the Official Geological Map (1:1000000) of South as at the OVI. Africa (Council for Geoscience, P/B X112, PTA., 0001) the area Map of Southern Africa is underlain by manganese-rich dolomitic or carboniferous rock of the Reivilo Formation (Astrup & Tsikos 1998). The area 10. FINAL CONCLUSIONS has a unique geological composition of limestone, dolomite and 4 chert. · The cause of geophagia is not yet certain. · This area is designated by a peculiar blue-grey colour and the letter · The characteristic lesions in the liver can be attributed to a code of VGH. subacute to chronic form of manganese poisoning. · The area is characterised by superficial outcrops of manganese- · The occurrence of geophagia in the calf is not dependent on Enlarged yellow liver rich dolomitic rocks. the habitation of the maternal animal in the affected area. · Our findings suggested that manganese mainly accumulated in the liver of affected calves after birth, after the ingestion 5. TOPOGRAPHY OF THE AFFECTED AREA of manganese-rich soil or milk. 10 · We could not demonstrate significant increases of manganese · The affected area is also characterised by wide, low-lying shallow levels in the liver of fetuses and newborn calves on the affected pans in which rainwater takes longer to drain. farms, although transplacental transmission of manganese · The soil contains numerous densely distributed small, round to with accumulation in the liver of calves, rabbits and mice ovoid, black-gray carboniferous concretions of c. 1-10mm derived Geological map of SA has been reported in maternal animals supplemented with from the superficial weathering of parent rock under moist warm manganese (Hurley and Keen 1987). conditions in these pan areas. · Our observations were based on a limited number of animals, · On analysis, the soil contains an average of c. 8% manganese, 5 and further cases need to be examined in order to make more 3% iron and 0.0024% cobalt. definite conclusions on the possible role of transplacental transmission of manganese in the occurrence of geophagia in calves from the affected area. 6. INGESTION OF MANGANESE-RICH CONCRETIONS BY CALVES AND LAMBS Histopathological section of liver 11. REFERENCES Portal fibrosis and bile duct proliferation · The initial stimulus for the ingestion of manganese-rich soil by calves and lambs is not known. Astrup, J. & Tsikos H., 1998. In: Wilson, MGC & Annhauser · The ingestion of relatively small quantities of soil by calves and C.R. (eds.) Mineral Resources of South Africa. Handbook 11 lambs from diverse unaffected areas has been observed frequently of Geological Survey of South Africa, No. 16, 6th edn. pp.450- during routine post mortem examinations. 460. Council for Geoscience, P/B X 112, Pretoria, 0001, South · Soil licking may be an instinctive mechanism to secure necessary Manganese rich dolomitic rocks Africa. mineral nutrients in the soil, especially iron, as calves on Findlay, G.M., 1924. The production of biliary cirrhosis by salts unsupplemented whole milk diets have been shown to develop of manganese. Br. J. Exp. Path., 5: 92 99. iron deficiency in the absence of soil (Graham, Thurmond, Mohr 6 Graham T.W., Thurmond M.C., Mohr F.C. et.al., 1994. et. al. 1994). Relationships between maternal and foetal liver copper, iron, · Calves may also ingest soil due to displaced appetitive behaviour manganese and zinc concentrations and foetal development due to hunger, while temporarily deserted by their dams persuing in California Holstein dairy cows. J. Vet. Diag. Investig., 6: green growth in the pans.Calves have been observed to start 77-87. licking small amounts of soil around them which may often include Hambidge, K.M., Casey C.E. and Krebs, N.F., 1987. Zinc. In: manganese-rich concretions in areas where they are prevalent. Mertz, W. (ed.) 5th Edn. Academic Press Inc., San Diego, · We have shown that calves and lambs reared in close confinement USA, Vol. 2: 50 51. voluntarily ingest limited amounts of soil from both affected and Hurley, L.S. & Keen, C.L., 1987. Manganese. In: Mertz, W. (ed.), Experimental reproduction of geophagia unaffected farms near Vryburg, as well as soil from Irene and 5th Edn. Academic Press, Inc. San Diego, USA, Vol. 1: 185 Onderstepoort where geophagia is not known to occur. - 223. · Phosphate and sodium deficiency were disregarded as possible Johns,T. & Duquette, M., 1991. Detoxification and mineral supplementation as functions of geophagy. Am. Jl. Clin. causes of geophagia in these calves, since cows and calves on Wide shallow pans Nutr., 53: 448 456. all affected farms had free access to licks which contained both Reid, R.M., 1992. Cultural and medical perspectives on geophagy. Med. Anthropol. 13: 337 351. these ingredients in sufficient quantities. Kreulen, D.A. & Jager, T., 1984. The significance of soil ingestion in the utilization of arid rangelands by large herbivores · According to our experiments at the Onderstepoort Veterinary Institute (OVI), as well as at the Provincial Veterinary with special reference to natural licks on the Kalahari pans. In: Gilchrist F.M.C. & Mackie R.I. (eds.), Herbivore Laboratory (PVL) at Vryburg, it was clear that the ingestion of manganese-rich soil aggravated the initial ingestion Nutrition in the Tropics and Subtropics. The Science Press, Craighall, South Africa: 204- 221. of this soil to produce severe geophagia in a high percentage of young calves. Kreulen, D.A., 1985. Lick use by large herbivores: a review of benefits and banes of soil consumption. Mammal Rev. · The tendency apparently disappears when the calf becomes a ruminant. 15 (3): 107- 123. · The way in which high intake of manganese produces disease seen in calves and lambs appears to be complex. Morris, E.R., 1987. Iron. In: Mertz, W.(ed.), 5th Edn. Academic Press, Inc. San Diego, USA, Vol. 1:-79-142. · Manganese interferes with iron and cobalt absorption by competitively binding to sites for absorption (Thomson Neser, J.A., de Vries, M., De Vries, M.A., van der Merwe, A.J., Loock, A.H., Smith, H.J.C., van der Vyfer, Elsenbroek, and Valberg, 1972; Hurley and Keen 1987). J.H. and Delport R. 1997. The possible role of manganese poisoning in enzootic geophagia and hepatitis of calves · Manganese has been shown to interfere with the availability of zinc in the digestive tract, as well as with the uptake and lambs. Jl. SA. Vet. Assoc., 68(1):2-7. of cobalt by micro-organisms in the rumen (Pfander, Beck and Preston, 1966). Pfander W.H., Beck H. and Preston R.L., 1966. The interaction of manganese, zinc and cobalt in ruminants. Federation · Deficiencies of cobalt have been associated with pica in cattle (Kreulen and Jaeger, 1984; Valli and Parry 1993) Proceedings. 25: 1362. and zinc deficiency has been implicated as a cause of geophagia in children (Hambidge, Casey & Krebs 1987). Valli, V.E. & Parry B.W., 1993. Anemia. In: Jubb, K.V.F., Kennedy P.C. and Palmer, N. (eds.) Pathology of Domestic · It is therefore hypothesized that the ingestion of manganese-rich soil has a perpetual effect in the gastro-intestinal Animals, 4 th edn., Academic Press Inc., San Diego, USA, Vol. 3: 72. tract of the calf, thereby causing a progressive deficiency of iron, cobalt and zinc, and leading to a vicious cycle Witzleben C.L., Pitlick P., Bergmeyer, J. et. al., 1968. Acute manganese overload A new experimental model of of increasing geophagia of the manganese-rich soil which ultimately leads to the demise of the calf. intrahepatic cholestasis. Am. Jl. Path. 53 (3): 409423.

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