PERINATAL LAMB MORTALITY IN WESTERN AUSTRALIA 7. Congenital Defects S . M. DENNIS*,B.V.Sc., Ph.D., F.R.C.V.S., M.R.C. Path., M.A.C.V.Sc. Department of Agriculture, Jarrah Road, Perth, Western Australia Inhwluction
Congenital defects are caused by genetic or environmental factors, or their interaction. External factors implicated in sheep include copper deficiency (Bennetts and Beck 1942), bluetongue virus (Schultz and Delay 1955), and ingestion of Verutrurn californicurn (Binns et al 1959). The incidence of congenital defects in lambs is unknown. New Zealand workers reported lethal defects to be responsible for about 1% of dead lambs autopsied (Hartley and Kater 1964); they commented that there were also several common non-lethal defects. Hughes et al (1964) reported an incidence of 1.5 to 2.1% defects in 3,503 lambs autopsied from three districts in New South Wales. In a later survey involving 4,408 lambs from 79 flocks they found a 1.8% incidence (Hughes et al 1972). In calves, for comparison, the incidence of congenital defects appears to range from 0.5 to 3.0% ; 40 to 50% are born dead and only a small fraction of the defects are not externally visible (Leipold et al 1972). In pigs, a New Zealand survey attributed 2.3% of preweaning deaths to congenital defects (O'Hara and Shortridge 1965). In man, gross defects are detectable in 1.5% of infants at births (Carrington 1966). Outbreaks of multiple congenital defects occurred in scattered flocks in the southern agricultural area of Western Australia during the 1960 autumn lambing season (J. M. Armstrong, personal communication, 1964). The cause was not determined but there was evidence that it was due to ingestion of a plant or plants by ewes in early pregnancy following summer rains. A sheep abortion questionnaire completed by farmers in 1963 revealed a surprising incidence of congenital defects; 36.6% reported malformed lambs and the incidence of defects ranged up to 20% (Dennis 1965). As a result it was decided to determine the types of congenital defects present in the sheep population (92% Merino) of the agricultural area of Western Australia. This paper records observations of congenital ovine defects during a 3-year investigation in 1963-65 into 'Present Address: College of Veterinary Medicine Kansas State. University, Manhattan, Kansas, United States of h e r i c a , 66506.
83
causes of perinatal lamb mortality in Western Australia. Materials and Methods
The general procedures followed were described previously (Dennis 1974). During 1964 and 1965, farmers were requested to submit malformed lambs for examination. Each dead lamb was subjected to a standardised autopsy and the time-of-death was assessed (McFarlane 1965). Sex, dry weight, degree of predator damage, and decomposition together with a description of each defect were recorded. Each defect was classified on the basis of the principally defective body system. Information was sought on breed, time of lambing, type of pasture, and clover disease status. Results
Of the 4,417 lambs examined, 401 (9.1%) were congenitally malformed; the defects included lethal and non-lethal conditions. Twelve malformed lambs were submitted in 1963, 162 in 1964, and 227 in 1965. The various defects are listed in Table 1. The body systems principally involved were: musculo-skeletal 55.4%; digestive 12.7%; cardiovascular 9.7%; uro-genital 7.1%; nervous 6.0% ; special senses 3.5% ; integument 3.2% and endocrine 1.5%. One-third of the defects (32.9%) were multiple and involved two or more systems; the remaining 67.1% involved one system. The common defects in order of frequency were: agnathia, atresia ani, cardiac defects, arthrogryposis, micrognathia scrota1 bifurcation, embryonic duplications, hernias, meningocele, and perosomus elumbis. The time-of-death of the 401 malformed lambs examined was: ante-parturient 1.5%, parturient 15.5%, post-parturient 82% (immediate 36.9%, delayed 7.5%, and late 37.6%), unclassified 0.5%, and alive 0.5%. Breed distribution was: Merino 77.3%, Merino crossbred 16.5%, Southdown 2.5%, Corriedale 2.0%, Border Leicester 1.0% , Suffolk 0.5%, and Shropshire 0.2%. There was a marked sex difference: male 56.4%, female 36.2% and hermaphrodite 0.7%. The sex was not recorded in 6.7% of the lambs. dustralicrn Vererinary Journal, Vol. 51, February. 1975
TABLE 1 Congenital Defects Found in 401 Malformed Lurnbs Autopsied in Western Australiri % Total
No.
Defect
52.4
210
Skeletal System Acephalus Adactylia Agnathia Amelia Aprosopia Arthrogryposis Bowed forelegs Brachycephalus Brachyury Campylognathia Cebocephalus Cephalomelia Conjoined twinning Dicephalus Diprosopus Dwarfism Fused ribs Hemignathia Kyphosis Kyphosicoliosis Micrognathia Missing ribs Notomelia Perocephalus Perosomus elumbis Phocomelia Polymelia Prognathia Polyury Py gomelia Schistosomus reflexus Scoliosis Syndactyly Torticollis Wrytail
0.2 1.2 17.5 0.5 0.7 8.0 1.2 0.7 0.3 0.5 0.3 0.3 2.0 0.5 0.5 1.2 0.3 0.3 0.3 0.7 5.2 0.3 0.5 0.3 2.0 0.7 0.3 0.5 0.3 0.7 0.5 0.5 0.3 1.5 1.7
1 5 70 2 3 32 5 3 1 2 1 1 8
2 2 5 1 1 1 3 21 1 2 1 8 3 1 2 1 3 2 2 1 6 7 7 1 2 1 1
11.0
I
0.2
2
0.5 0.3 0.7
3
9.7
39 2 2 4 1
Nervous System Anencephaly Arnold Chiari defect Ataxia Cerebellar hypoplasia Hydrocephalus M eningocele Meningo-encephalocele Micrencephaly Spina bifida
12.7
44 1
Cardiovascular System Anasarca Cardiomegaly Cor triloculare biatriatum Endocardia1 fibroclastosis
Genital System Cryptorchidism Diphallia Hermaphroditism Hypospadias Pseudohermaphroditism Scrotal bifurcation Partial scrota1 bifurcation
1.7 0.2 0.5 0.3 0.3 51
Digestive System Atresia ani Atresia ilei Erupted incisors Otognathia Palatoschisis
Urinary System Renal agenesis Hydronephrosis Patent urachus Polycystic kidneys
3.0
12
Muscular System Diaphragmatic hernia Hypertrophy Patent umbilical ring Perineal hernia Scrotal hernia
Defect Persistent umbilical haemorrhage Septa1 defect
0.5 0.5
1.o 0.2
A third of the carcasses (31.4%) had predator damage post mortem. Discussion
Definitive aetiological knowledge of congenital defects in sheep is scarce, Environment is now Australian Veterinary Journal. Vol. 51, February, 1975
Special Senses Anophthalmia Cyclopia Entropion Macrophthalmia Microphthalmia Microtia Polyotia Integument Black coat Black patches Epitheliogenesis imperfect a Excessive horn buds Excessive skin fold, base tail Lustre mutant Small polyp, adjacent to anus Endocrine System Goitre Thyroid dystopia
No. 3 27
% Total
0.7 6.7 6
2 2 1 1
1.5 0.5 0.5 0.2 0.3
26
5.6
1 2 1 4 1 2
0.3 0.5 0.3 1.o 0.3 0.5
15
3.7 24
1 1
6.0 0.3 0.2 0.5 0.3 1.2 1.7
7
I
1 5 7 2 1 4
0.5
0.3 1.o 14
1 2 5 1 2 2 1
3.5 0.3 ~. 0.5
1.2 0.3 0.5 0.5
0.3 13
3.2
2 6
0.5
1 1
0.2 0.2
1 1
0.2
1.5
0.3
1
0.2 6
5
1
401 -
1.5 1.2 0.2 100.0
recognised as a major cause. Although a wide variety of environmental factors have produced congenital defects in laboratory animals, only a few have been incriminated as teratogenic for sheep. The need to identify environmental teratogenic agents in sheep is emphasised by the Vera81
lrum califoraicum studies by Binns et a1 (1959) in Utah, United States of America, and by the undiagnosed outbreaks in the south-west of Western Australia during autumn lambing in 1960. There was little evidence from the investigation reported here to suggest whether the defects were environmentally or genetically induced, or both. Agnathia, atresia ani and persistent umbilical haemorrhage, however, appeared to be hereditary. Neither was there any relationship between congenital defects and the time of lambing and clover disease involvement. Unimproved pastures were suspected to be involved in two flocks. Phytooestrogens were logical suspects as teratogenic agents particularly with intersex defects; the incidence of genital malformations, however, appeared to be unaffected by the presence or absence of clover varieties with relatively high concentrations of oestrogenic compounds. Identification of aetiological agents in ovine defects is often extremely difficult because defects occur many months after exposure, and usually it is not possible to investigate the breeding records, pedigrees, diet, management and disease status of the flocks involved, as most owners do not keep adequate records. The prevalence of 9.1% congenital defects in the lambs autopsied was misleading and biased as malformed lambs were requested in 1964 and 1965. The results in 1963, and on individual properties in 1964-65 suggested that the incidence was probably 1-2%. The types of congenital defects examined and reported were considered representative of those present in the sheep population of Western Australia. There was no evidence that any one breed was affected more with congenital defects; the higher percentage in Merinos reflected the predominance of the breed in Western Australia. Collectively, there was a marked sex difference of 3 males : 2 females. For many individual defects, however, including agnathia, there was no sex difference. Hughes et a1 (1972) confirmed this finding with agnathia. The musculo-skeletal system was involved in 55.4% of the 401 malformed lambs. The most common defects involved the jaws, primarily the mandibles, which were hypoplastic to aplastic, hyperplastic or twisted: seventy lambs had agnathia. Agnathia was also found to be the most common lethal defect in a large survey in eastern Australia (Hughes et al 1972). The other com-
82
mon defects they reported involved the musculoskeletal system, central nervous system, cardiovascular system and imperforate intestinal tract. Although this investigation identified the types of congenital defects commonly observed in sheep in Western Australia, more information on the incidence, cause and nature of the various defects is needed. In addition, environmental agents that are teratogenic to sheep under existing methods of husbandry require identification. summary
Four hundred and one malformed lambs were examined during a 3-year investigation into the causes of perinatal lamb mortality. Frequency of involvement of the various body systems was: musculo-skeletal 55.4% , digestive 12.7%, cardiovascular 9.7%, uro-genital 7.1 % , nervous 6.0% , special senses 3.5 % , integument 3.2% , and endocrine 1.5%. A third of the defects (32.9%) involved more than one body system. There was a sex difference of 3 males : 2 females. The common defects in the lambs autopsied in order of frequency were: agnathia, atresia ani, cardiac defects, arthrogryposis, micrognathia, scrota1 bifurcation, embryonic duplications, hernias, meningocele, and perosomus elumbis. Agnathia, atresia ani and persistent umbilical haemorrhage appeared to be hereditary. There was no relationship between congenital defects and the time of lambing and phytoestrogens. References Bennetts, H. W., and Beck, A. B. (1942)-Comm. Sci. Ind. Res. Bull. 147. Binns, W., Thacker, E. J., James, L. F. and Huffman, W. T. (1959)-I. A m . vet. med. Ass. 134: 180. Carrington, E. R. (1966+Clin. Obst. and Gynec. 9: 595.
Dennis, S. M. ( 1 9 6 5 w . Dept. Agric., West Aust. 6: 221.
Dennis, S . M. (1974)-.4ust. vet. I . 50: 443. Hartley, W. J. and Kater, J. C . (1964)-N.Z. vet. J. 12: 49. Hughes, K. L., Hartley, W. J., Haughey, K. G. and McFarlane, D. (1964)-Proc. Aust. SOC. Anim. Prod. 5: 92. Hughes, K. L., Haughey, K. G., and Hartley, W. J. (1972)--Teratology 5: 5. Lcipold, H. W., Dennis, S. M. and Huston, K. (1972)Adv. vet. sci. comp. Med. 16: 103. McFarlane, D. (1965)-N.Z. vet. I . 13: 116. O’Hara, P. J., and Shortridge, E. H. ( 1 9 6 5 b N . Z . vet. 1. 14: 13. Schultz, G., and Delay, P. D. (1955)-J. Am. vet. med. Ass. 127: 224. (Received f o r publication 24 August 1971)
Australian Veterinary Journal, Vol. 51, February, 1975
Congenital defects are caused by genetic or environmental factors, or their interaction. External factors implicated in sheep include copper deficiency (Bennetts and Beck 1942), bluetongue virus (Schultz and Delay 1955), and ingestion of Verutrurn californicurn (Binns et al 1959). The incidence of congenital defects in lambs is unknown. New Zealand workers reported lethal defects to be responsible for about 1% of dead lambs autopsied (Hartley and Kater 1964); they commented that there were also several common non-lethal defects. Hughes et al (1964) reported an incidence of 1.5 to 2.1% defects in 3,503 lambs autopsied from three districts in New South Wales. In a later survey involving 4,408 lambs from 79 flocks they found a 1.8% incidence (Hughes et al 1972). In calves, for comparison, the incidence of congenital defects appears to range from 0.5 to 3.0% ; 40 to 50% are born dead and only a small fraction of the defects are not externally visible (Leipold et al 1972). In pigs, a New Zealand survey attributed 2.3% of preweaning deaths to congenital defects (O'Hara and Shortridge 1965). In man, gross defects are detectable in 1.5% of infants at births (Carrington 1966). Outbreaks of multiple congenital defects occurred in scattered flocks in the southern agricultural area of Western Australia during the 1960 autumn lambing season (J. M. Armstrong, personal communication, 1964). The cause was not determined but there was evidence that it was due to ingestion of a plant or plants by ewes in early pregnancy following summer rains. A sheep abortion questionnaire completed by farmers in 1963 revealed a surprising incidence of congenital defects; 36.6% reported malformed lambs and the incidence of defects ranged up to 20% (Dennis 1965). As a result it was decided to determine the types of congenital defects present in the sheep population (92% Merino) of the agricultural area of Western Australia. This paper records observations of congenital ovine defects during a 3-year investigation in 1963-65 into 'Present Address: College of Veterinary Medicine Kansas State. University, Manhattan, Kansas, United States of h e r i c a , 66506.
83
causes of perinatal lamb mortality in Western Australia. Materials and Methods
The general procedures followed were described previously (Dennis 1974). During 1964 and 1965, farmers were requested to submit malformed lambs for examination. Each dead lamb was subjected to a standardised autopsy and the time-of-death was assessed (McFarlane 1965). Sex, dry weight, degree of predator damage, and decomposition together with a description of each defect were recorded. Each defect was classified on the basis of the principally defective body system. Information was sought on breed, time of lambing, type of pasture, and clover disease status. Results
Of the 4,417 lambs examined, 401 (9.1%) were congenitally malformed; the defects included lethal and non-lethal conditions. Twelve malformed lambs were submitted in 1963, 162 in 1964, and 227 in 1965. The various defects are listed in Table 1. The body systems principally involved were: musculo-skeletal 55.4%; digestive 12.7%; cardiovascular 9.7%; uro-genital 7.1%; nervous 6.0% ; special senses 3.5% ; integument 3.2% and endocrine 1.5%. One-third of the defects (32.9%) were multiple and involved two or more systems; the remaining 67.1% involved one system. The common defects in order of frequency were: agnathia, atresia ani, cardiac defects, arthrogryposis, micrognathia scrota1 bifurcation, embryonic duplications, hernias, meningocele, and perosomus elumbis. The time-of-death of the 401 malformed lambs examined was: ante-parturient 1.5%, parturient 15.5%, post-parturient 82% (immediate 36.9%, delayed 7.5%, and late 37.6%), unclassified 0.5%, and alive 0.5%. Breed distribution was: Merino 77.3%, Merino crossbred 16.5%, Southdown 2.5%, Corriedale 2.0%, Border Leicester 1.0% , Suffolk 0.5%, and Shropshire 0.2%. There was a marked sex difference: male 56.4%, female 36.2% and hermaphrodite 0.7%. The sex was not recorded in 6.7% of the lambs. dustralicrn Vererinary Journal, Vol. 51, February. 1975
TABLE 1 Congenital Defects Found in 401 Malformed Lurnbs Autopsied in Western Australiri % Total
No.
Defect
52.4
210
Skeletal System Acephalus Adactylia Agnathia Amelia Aprosopia Arthrogryposis Bowed forelegs Brachycephalus Brachyury Campylognathia Cebocephalus Cephalomelia Conjoined twinning Dicephalus Diprosopus Dwarfism Fused ribs Hemignathia Kyphosis Kyphosicoliosis Micrognathia Missing ribs Notomelia Perocephalus Perosomus elumbis Phocomelia Polymelia Prognathia Polyury Py gomelia Schistosomus reflexus Scoliosis Syndactyly Torticollis Wrytail
0.2 1.2 17.5 0.5 0.7 8.0 1.2 0.7 0.3 0.5 0.3 0.3 2.0 0.5 0.5 1.2 0.3 0.3 0.3 0.7 5.2 0.3 0.5 0.3 2.0 0.7 0.3 0.5 0.3 0.7 0.5 0.5 0.3 1.5 1.7
1 5 70 2 3 32 5 3 1 2 1 1 8
2 2 5 1 1 1 3 21 1 2 1 8 3 1 2 1 3 2 2 1 6 7 7 1 2 1 1
11.0
I
0.2
2
0.5 0.3 0.7
3
9.7
39 2 2 4 1
Nervous System Anencephaly Arnold Chiari defect Ataxia Cerebellar hypoplasia Hydrocephalus M eningocele Meningo-encephalocele Micrencephaly Spina bifida
12.7
44 1
Cardiovascular System Anasarca Cardiomegaly Cor triloculare biatriatum Endocardia1 fibroclastosis
Genital System Cryptorchidism Diphallia Hermaphroditism Hypospadias Pseudohermaphroditism Scrotal bifurcation Partial scrota1 bifurcation
1.7 0.2 0.5 0.3 0.3 51
Digestive System Atresia ani Atresia ilei Erupted incisors Otognathia Palatoschisis
Urinary System Renal agenesis Hydronephrosis Patent urachus Polycystic kidneys
3.0
12
Muscular System Diaphragmatic hernia Hypertrophy Patent umbilical ring Perineal hernia Scrotal hernia
Defect Persistent umbilical haemorrhage Septa1 defect
0.5 0.5
1.o 0.2
A third of the carcasses (31.4%) had predator damage post mortem. Discussion
Definitive aetiological knowledge of congenital defects in sheep is scarce, Environment is now Australian Veterinary Journal. Vol. 51, February, 1975
Special Senses Anophthalmia Cyclopia Entropion Macrophthalmia Microphthalmia Microtia Polyotia Integument Black coat Black patches Epitheliogenesis imperfect a Excessive horn buds Excessive skin fold, base tail Lustre mutant Small polyp, adjacent to anus Endocrine System Goitre Thyroid dystopia
No. 3 27
% Total
0.7 6.7 6
2 2 1 1
1.5 0.5 0.5 0.2 0.3
26
5.6
1 2 1 4 1 2
0.3 0.5 0.3 1.o 0.3 0.5
15
3.7 24
1 1
6.0 0.3 0.2 0.5 0.3 1.2 1.7
7
I
1 5 7 2 1 4
0.5
0.3 1.o 14
1 2 5 1 2 2 1
3.5 0.3 ~. 0.5
1.2 0.3 0.5 0.5
0.3 13
3.2
2 6
0.5
1 1
0.2 0.2
1 1
0.2
1.5
0.3
1
0.2 6
5
1
401 -
1.5 1.2 0.2 100.0
recognised as a major cause. Although a wide variety of environmental factors have produced congenital defects in laboratory animals, only a few have been incriminated as teratogenic for sheep. The need to identify environmental teratogenic agents in sheep is emphasised by the Vera81
lrum califoraicum studies by Binns et a1 (1959) in Utah, United States of America, and by the undiagnosed outbreaks in the south-west of Western Australia during autumn lambing in 1960. There was little evidence from the investigation reported here to suggest whether the defects were environmentally or genetically induced, or both. Agnathia, atresia ani and persistent umbilical haemorrhage, however, appeared to be hereditary. Neither was there any relationship between congenital defects and the time of lambing and clover disease involvement. Unimproved pastures were suspected to be involved in two flocks. Phytooestrogens were logical suspects as teratogenic agents particularly with intersex defects; the incidence of genital malformations, however, appeared to be unaffected by the presence or absence of clover varieties with relatively high concentrations of oestrogenic compounds. Identification of aetiological agents in ovine defects is often extremely difficult because defects occur many months after exposure, and usually it is not possible to investigate the breeding records, pedigrees, diet, management and disease status of the flocks involved, as most owners do not keep adequate records. The prevalence of 9.1% congenital defects in the lambs autopsied was misleading and biased as malformed lambs were requested in 1964 and 1965. The results in 1963, and on individual properties in 1964-65 suggested that the incidence was probably 1-2%. The types of congenital defects examined and reported were considered representative of those present in the sheep population of Western Australia. There was no evidence that any one breed was affected more with congenital defects; the higher percentage in Merinos reflected the predominance of the breed in Western Australia. Collectively, there was a marked sex difference of 3 males : 2 females. For many individual defects, however, including agnathia, there was no sex difference. Hughes et a1 (1972) confirmed this finding with agnathia. The musculo-skeletal system was involved in 55.4% of the 401 malformed lambs. The most common defects involved the jaws, primarily the mandibles, which were hypoplastic to aplastic, hyperplastic or twisted: seventy lambs had agnathia. Agnathia was also found to be the most common lethal defect in a large survey in eastern Australia (Hughes et al 1972). The other com-
82
mon defects they reported involved the musculoskeletal system, central nervous system, cardiovascular system and imperforate intestinal tract. Although this investigation identified the types of congenital defects commonly observed in sheep in Western Australia, more information on the incidence, cause and nature of the various defects is needed. In addition, environmental agents that are teratogenic to sheep under existing methods of husbandry require identification. summary
Four hundred and one malformed lambs were examined during a 3-year investigation into the causes of perinatal lamb mortality. Frequency of involvement of the various body systems was: musculo-skeletal 55.4% , digestive 12.7%, cardiovascular 9.7%, uro-genital 7.1 % , nervous 6.0% , special senses 3.5 % , integument 3.2% , and endocrine 1.5%. A third of the defects (32.9%) involved more than one body system. There was a sex difference of 3 males : 2 females. The common defects in the lambs autopsied in order of frequency were: agnathia, atresia ani, cardiac defects, arthrogryposis, micrognathia, scrota1 bifurcation, embryonic duplications, hernias, meningocele, and perosomus elumbis. Agnathia, atresia ani and persistent umbilical haemorrhage appeared to be hereditary. There was no relationship between congenital defects and the time of lambing and phytoestrogens. References Bennetts, H. W., and Beck, A. B. (1942)-Comm. Sci. Ind. Res. Bull. 147. Binns, W., Thacker, E. J., James, L. F. and Huffman, W. T. (1959)-I. A m . vet. med. Ass. 134: 180. Carrington, E. R. (1966+Clin. Obst. and Gynec. 9: 595.
Dennis, S. M. ( 1 9 6 5 w . Dept. Agric., West Aust. 6: 221.
Dennis, S . M. (1974)-.4ust. vet. I . 50: 443. Hartley, W. J. and Kater, J. C . (1964)-N.Z. vet. J. 12: 49. Hughes, K. L., Hartley, W. J., Haughey, K. G. and McFarlane, D. (1964)-Proc. Aust. SOC. Anim. Prod. 5: 92. Hughes, K. L., Haughey, K. G., and Hartley, W. J. (1972)--Teratology 5: 5. Lcipold, H. W., Dennis, S. M. and Huston, K. (1972)Adv. vet. sci. comp. Med. 16: 103. McFarlane, D. (1965)-N.Z. vet. I . 13: 116. O’Hara, P. J., and Shortridge, E. H. ( 1 9 6 5 b N . Z . vet. 1. 14: 13. Schultz, G., and Delay, P. D. (1955)-J. Am. vet. med. Ass. 127: 224. (Received f o r publication 24 August 1971)
Australian Veterinary Journal, Vol. 51, February, 1975
