Disorders of sex development in the dog-Adoption of a new nomenclature and reclassification of reported cases

Animal Reproduction Science

Volumn 121, Issue 3-4, 2010, Pages 197-207

  Poth, T ^a   Breuer, W ^a   Walter, B ^a   Hecht, W ^b   Hermanns, W ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Disorders of sex development; Dog; Ovotestis; Pseudohermaphroditism; Sex reversal; True hermaphroditism

Indexed keywords

ANIMAL; ANIMAL DISEASE; CHROMOSOME DISORDER; CLASSIFICATION; DOG; DOG DISEASE; FEMALE; MALE; NOMENCLATURE; OVARY; PHENOTYPE; REVIEW; SEX DIFFERENTIATION DISORDER; SEXUAL MATURATION; TESTIS;

ANIMALS; DISORDERS OF SEX DEVELOPMENT; DOG DISEASES; DOGS; FEMALE; MALE; OVARY; PHENOTYPE; SEX CHROMOSOME DISORDERS; SEXUAL MATURATION; TERMINOLOGY AS TOPIC; TESTIS;

ANIMALIA; CANIS FAMILIARIS; CAPRA HIRCUS; EQUIDAE; SUIDAE;

EID: 77956175191     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2010.04.011     Document Type: Review

References (83)

1. Alam M.R., Cho Y.G., Cho S.J., Lee J.I., Lee H.B., Tae H.J., Kim I.S., Kim N.S. Male pseudohermaphroditism in dogs: three case reports. Vet. Med. (Praha) 2007, 52:74-78.
2. Allen W.E., Daker M.G., Hancock J.L. Three intersexual dogs. Vet. Rec. 1981, 109:468-471.
3. Axelson R.D. Pseudohermaphroditism in a dog. J. Am. Vet. Med. Assoc. 1978, 172:584-585.
4. Barch M.J. The ACT Cytogenetics Laboratory Manual 2 1991, Raven Press, New York.
5. Bosu W.T.K., Chick B.F., Basrur P.K. Clinical, pathologic and cytogenetic observations on two intersex dogs. Cornell Vet. 1978, 68:375-390.
6. Buijtels J.J.C.W.M., de Gier J., van Haeften T., Kooistra H.S., Spee B., Veldhuis Kroeze E.J.B., Zijlstra C., Okkens A.C. Minimal external masculinization in a SRY-negative XX male Podenco dog. Reprod. Dom. Anim. 2009, 44:751-756.
7. Chaffaux S., Mailhac J.M., Cribiu E.P., Popescu C.P., Cotard J.P. L'intersexualité chez le chien (canis familiaris). A propos de quatre cas. Rec. Méd. Vét. 1980, 156:179-192.
8. Chaffaux S., Cribiu E.P., Crespeau F. Un cas rare d'hermaphrodisme vrai latéral chez une chienne 78,XY. Rec. Méd. Vét. 1986, 162:463-470.
9. Chaffaux S., Nudelmann N., Durand V., Cribiu E.P. Le pseudohermaphrodisme mâle, a propos du cas d'un chien intersexué 78,XX. Rec. Méd. Vét. 1990, 166:125-132.
10. Clough E., Pyle R.L., Hare W.C.D., Kelly D.F., Patterson D.F. An XXY sex-chromosome constitution in a dog with testicular hypoplasia and congenital heart disease. Cytogenetics 1970, 9:71-77.
11. Cotinot C., Pailhoux E., Jaubert F., Fellous M. Molecular genetics of sex determination. Sem. Reprod. Med. 2002, 20:157-168.
12. Dain A.R., Walker R.G. Two intersex dogs with mosaicism. J. Reprod. Fert. 1979, 56:239-242.
13. De Lorenzi L., Gropetti D., Arrighi S., Pujar S., Nicoloso L., Molteni L., Pecile A., Cremonesi F., Parma P., Meyers-Wallen V. Mutations in the RSPO1 coding region are not the main cause of canine SRY-negative XX sex reversal in several breeds. Sex. Dev. 2008, 2:84-95.
14. De Rooster H., Vercauteren G., Görtz K., Saunders J., Polis I., Rijsselaere T. True hermaphroditism in six female littermates after administration of synthetic androgens to a pregnant bitch. Reprod. Dom. Anim. 2006, 41:22-26.
15. Feldman E.C., Nelson R.W. Infertility, associated breeding disorders, and disorders of sexual development. Canine and Feline Endocrinology and Reproduction 2004, 893-898. Saunders. third ed. E.C. Feldman, R.W. Nelson (Eds.).
16. Fischer K. Pseudohermaphroditism in a dog. Vet. Med. Small. Anim. Clin. 1983, 78:683-685.
17. Fitzgerald A.L., Murphy D.A. Bilateral ovotestes in an intersex, mixed-breed dog. Lab. Anim. Sci. 1990, 40:647-650.
18. Fredholm M., Winterø A.K. Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm. Genome 1995, 6:11-18.
19. Genero E.R., Moreno-Millán M., Ocaña-Quero J.M. XX/XY chromosome chimaerism in an intersex dog. Vet. Rec. 1998, 142:340.
20. Goldschmidt B., El-Jaick K.B., Souza L.M., Carvalho E.C.Q., Moura V.L.S., Benevides Filho I.M. Cryptorchidism associated with 78,XY/79,XXY mosaicism in dog. Israel J. Vet. Med. 2001, 56:56-58.
21. Hare W.C.D. Intersexuality in the dog. Can. Vet. J. 1976, 17:7-15.
22. Hayes H.M., Wilson G.P. Hospital incidence of hypospadias in dogs in North America. Vet. Rec. 1986, 118:605-607.
23. Hinsch G.W. Intersexes in the dog. Teratology 1979, 20:463-468.
24. Holt P.E., Long S.E., Gibbs C. Disorders of urination associated with canine intersexuality. J. Small. Anim. Pract. 1983, 24:475-487.
25. Hughes I.A. Disorders of sex development: a new definition and classification. Pract. Res. Clin. Endocrinol. Metab. 2008, 22:119-134.
26. Johnston S.D. Premature gonadal failure in female dogs and cats. J. Reprod. Fertil. Suppl. 1989, 39:65-72.
27. Jurka P., Galanty M., Zielinska P., Max A., Sysa P. Hypospadias in six dogs. Vet. Rec. 2009, 164:331-333.
28. Kelly D.F., Long S.E., Strohmenger G.D. Testicular neoplasia in an intersex dog. J. Small. Anim. Pract. 1976, 17:247-253.
29. Kothapalli K., Kirkness E., Pujar S., Van Wormer R., Meyers-Wallen V.N. Exclusion of candidate genes for canine SRY-negative XX sex reversal. J. Hered. 2005, 96:759-763.
30. Kuiper H., Distl O. Intersexuality in dogs: causes and genetics. Dtsch. Tierärztl. Wschr. 2004, 111:251-258.
31. Löfstedt R.M., Buoen L.C., Weber A.F., Johnston S.D., Huntington A., Concannon P.W. Prolonged proestrus in a bitch with X chromosomal monosomy (77,X0). J. Am. Vet. Med. Assoc. 1992, 200:1104-1106.
32. Marshall L.S., Oehlert M.L., Haskins M.E., Selden J.R., Patterson D.F. Persistent Müllerian duct syndrome in miniature schnauzers. J. Am. Vet. Med. Assoc. 1982, 181:798-801.
33. Mayenco-Aguirre A.M., Padilla J.A., Flores J.M., Daza M.A. Canine gonadal dysgenesis syndrome: a case of mosaicism (77,X0-78,XX). Vet. Rec. 1999, 145:582-584.
34. McElreavey K., Rappaport R., Vilain E., Abbas N., Richaud F., Lortat-Jacob S., Berger R., Le Coniat M., Boucekkine C., Kucheria K., Temtamy S., Nihoul-Fekete C., Brauner R., Fellous M. A minority of 46,XX true hermaphrodites are positive for the Y-DNA sequence including SRY. Hum. Genet. 1992, 90:212-215.
35. Medleau L., Johnson C.A., Perry R.L., Dulisch M.L. Female pseudohermaphroditism associated with mibolerone administration in a dog. J. Am. Anim. Hosp. Assoc. 1983, 19:213-215.
36. Melniczek J.R., Dambach D., Prociuk U., Jezyk P.F., Henthorn P.S., Patterson D.F., Giger U. Sry-negative XX sex reversal in a family of Norwegian Elkhounds. J. Vet. Intern. Med. 1999, 13:564-569.
37. Meyers-Wallen V.N., Patterson D.F. Disorders of sexual development in the dog. Current Therapy in Theriogenology: Diagnosis, Treatment and Prevention of Reproductive Diseases in Animals 1986, 567-574. WB Saunders. second ed. D.A. Morrow (Ed.).
38. Meyers-Wallen V.N., Donahoe P.K., Manganaro T., Patterson D.F. Müllerian inhibiting substance in sex-reversed dogs. Biol. Reprod. 1987, 37:1015-1022.
39. Meyers-Wallen V.N., Patterson D.F. Sexual differentiation and inherited disorders of sexual development in the dog. J. Reprod. Fertil. Suppl. 1989, 39:57-64.
40. Meyers-Wallen V.N., Bowman L., Acland G.M., Palmer V.L., Schlafer D., Fajt V. Sry-negative XX sex reversal in the German Shorthaired Pointer dog. J. Hered. 1995, 86:369-373.
41. Meyers-Wallen V.N., Schlafer D., Barr I., Lovell-Badge R., Keyzner A. Sry-negative XX sex reversal in purebred dogs. Mol. Reprod. Dev. 1999, 53:266-273.
42. Meyers-Wallen V.N. Inherited abnormalities of sexual development in dogs and cats. Recent Advances in Small Animal Reproduction 2001, International Veterinary Information Service, Ithaca, New York. P.W. Concannon, G. England, J. Verstegen (Eds.).
43. Nickel R.F., Ubbink G., Van der Gaag I., Van Sluijs F.J. Persistent Müllerian duct syndrome in the Basset Hound. Tijdschr. Diergeneeskd 1992, 117(Suppl. 1):31S.
44. Nie G.J., Johnston S.D., Hayden D.W., Buoen L.C., Stephens M. Theriogenology question of the month. Azoospermia associated with 79,XXY chromosome complement (canine Klinefelter's syndrome). J. Am. Vet. Med. Assoc. 1998, 212:1545-1547.
45. Nowacka J., Nizanski W., Klimowicz M., Dzimira S., Switonski M. Lack of the SOX9 gene polymorphism in sex reversal dogs (78,XX; SRY negative). J. Hered. 2005, 96:797-802.
46. Nowacka-Woszuk J., Nizanski W., Klimowicz M., Switonski M. Normal male chromosome complement and a lack of the SRY and SOX9 gene mutations in a male pseudohermaphrodite dog. Anim. Reprod. Sci. 2007, 98:371-376.
47. Nowacka-Woszuk, J., Switonski, M., 2009. Variability of CAG tandem repeats in exon 1 of the androgen receptor gene is not related with dog intersexuality. Anim. Reprod. Sci., doi:10.1016/j.anireprosci.2009.05.001.
48. Olson P.N., Seim H.B., Park R.D., Grandy J.L., Freshman J.L., Carlson E.D. Female pseudohermaphroditism in three sibling Greyhounds. J. Am. Vet. Med. Assoc. 1989, 194:1747-1749.
49. Pailhoux E., Vigier B., Chaffaux S., Servel N., Taourit S., Furet J.-P., Fellous M., Grosclaude F., Cribiu E.P., Cotinot C., Vaiman D. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat. Genet. 2001, 29:453-458.
50. Peter A.T., Markwelder D., Asem E.K. Phenotypic feminization in a genetic male dog caused by nonfunctional androgen receptors. Theriogenology 1993, 40:1093-1105.
51. Pujar S., Kothapalli K.S., Kirkness E., Van Wormer R.H., Meyers-Wallen V.N. Exclusion of Lhx9 as a candidate gene for SRY-negative XX sex reversal in the American Cocker Spaniel model. J. Hered. 2005, 96:452-454.
52. Pujar S., Kothapalli K.S.D., Göring H.H.H., Meyers-Wallen V.N. Linkage to CFA29 detected in a genome-wide linkage screen of canine pedigree segregating SRY-negative XX sex reversal. J. Hered. 2007, 98:438-444.
53. Pullen C.M. True bilateral hermaphroditism in a Beagle: a case report. Am. J. Vet. Res. 1970, 31:1113-1117.
54. Randolph J.F., Center S.A., McEntee M., Goldberg E.H. H-Y antigen-positive XX true bilateral hermaphroditism in a German Shorthaired Pointer. J. Am. Anim. Hosp. Assoc. 1987, 24:417-420.
55. Redden B. Clinical snapshot. A vulvar mass in a dog. True hermaphrodite. Compend. Contin. Educ. Vet. 2007, 29. 240, 245.
56. Reimann-Berg N., Murua Escobar H., Nolte I., Bullerdiek J. Testicular tumor in an XXY dog. Cancer Genet. Cytogenet. 2008, 183:114-116.
57. Röcken H. Über Hermaphroditismus beim Hund. Berl. Münch. Tierärztl. Wschr. 1988, 101:55-57.
58. Sarafoglou K., Ostrer H. Familial sex reversal: a review. J. Clin. Endocrinol. Metab. 2000, 85:483-493.
59. Schelling C., Pienkowska A., Arnold S., Hauser B., Switonski M. A male to female sex-reversed dog with a reciprocal translocation. J. Reprod. Fertil. Suppl. 2001, 57:435-438.
60. Schlafer D.H., Miller R.B. Pathology of the genital system of the nongravid female. Jubb, Kennedy, and Palmer's Pathology of Domestic Animals 2007, vol. 3:431-444. Elsevier Saunders. fifth ed.
61. Schneck G.W. Letter: hermaphroditism in a Shetland sheepdog. Vet. Rec. 1975, 96:323.
62. Selden J.R., Wachtel S.S., Koo G.C., Haskins M.E., Patterson D.F. Genetic basis of XX male syndrome and XX true hermaphroditism: evidence in the dog. Science 1978, 201:644-646.
63. Selden J.R., Moorhead P.S., Koo G.C., Wachtel S.S., Haskins M.E., Patterson D.F. Inherited XX sex reversal in the cocker spaniel dog. Hum. Genet. 1984, 67:62-69.
64. Simpson G., England G., Harvey M. BSAVA Manual of Small Animal Reproduction and Neonatology 1998, Iowa State University Press, Ames.
65. Smith F.W.K., Buoen L.C., Weber A.F., Johnston S.D., Randolph J.F., Waters D.J. X-chromosomal monosomy (77,X0) in a Doberman Pinscher with gonadal dysgenesis. J. Vet. Intern. Med. 1989, 3:90-95.
66. Sonne C., Dietz R., Born E.W., Leifsson P.S., Andersen S. Is there a link between hypospadias and organochlorine exposure in East Greenland sledge dogs (Canis familiaris)?. Ecotoxicol. Environ. Saf. 2008, 69:391-395.
67. Stewart R.W., Menges R.W., Selby L.A., Rhoades J.D., Crenshaw D.B. Canine intersexuality in a Pug breeding kennel. Cornell Vet. 1972, 62:464-473.
68. Stünzi B., Stünzi H. Hermaphroditus verus unilateralis beim Hund mit blastomatöser Entartung des rudimentären Ovars. Schweiz. Arch. Tierheilkd. 1950, 92:67-82.
69. Svendsen C.K., Thomsen P.D., Basse A. Two cases of male pseudohermaphroditism in the dog. Clinical, macroscopic, karyotypic, and therapeutic features. Nord. Vet. Med. 1985, 37:358-363.
70. Switonski M., Godynicki S., Jackowiak H., Pienkowska A., Turczuk-Bierla I., Szymas J., Golinski P., Bereszynski A. X trisomy in an infertile bitch: cytogenetic, anatomic, and histologic studies. J. Hered. 2000, 91:149-150.
71. Switonski M., Szczerbal I., Grewling J., Antosik P., Nizanski W., Yang F. Two cases of infertile bitches with 78,XX/77,X mosaic karyotype: a need for cytogenetic evaluation of dogs with reproductive disorders. J. Hered. 2003, 94:65-68.
72. Switonski M., Nowacka J., Skorczyk A., Chmurzynska A., Nizanski W. Hereditary sex-reversal syndrome (78,XX; SRY-negative) in German Shepherd puppies. Medycyna weterynaryjna 2004, 60:705-707.
73. Tammer I., Herzog A., Bostedt H. Disorders of sexual development in the dog: two case reports. Tierärztl. Prax. 1998, 26 (K):390-395.
74. Tangner C.H., Breider M.A., Amoss M.S. Lateral hermaphroditism in a dog. J. Am. Vet. Med. Assoc. 1982, 181:70-71.
75. Thomas T.N., Olson P.N., Hoopes P.J. Lateral hermaphroditism and seminoma in a dog. J. Am. Vet. Med. Assoc. 1986, 189:1596-1597.
76. Van Schouwenburg S.J., Louw G.J. A case of dysuria as a result of a communication between the urinary bladder and corpus uteri in a Cairn Terrier. J. S. Afr. Vet. Assoc. 1982, 53:65-66.
77. Volpe P., Izzo B., Pia Di Meo G., Perucatti A., Iannuzzi L. Male pseudohermaphroditism in a dog: a clinical case. Vet. Rec. 2000, 146:532-533.
78. Weaver A.D., Harvey M.J., Munro C.D., Rogerson P., McDonald M. Phenotypic intersex (female pseudohermaphroditism) in a Dachshund dog. Vet. Rec. 1979, 105:230-232.
79. Wernham B.G.J., Jerram R.M. Male pseudohermaphroditism in a Labrador Retriever, and a review of mammalian sexual differentiation. N. Z. Vet. J. 2006, 54:248-252.
80. Whyte A., Monteagudo L.V., Díaz-Otero A., Lebrero M.E., Tejedor M.T., Falceto M.V., Whyte J., Gallego M. Malformations of the epididymis, incomplete regression of the mesonephric tubles and hyperplasia of Leydig cells in canine persistence of Müllerian duct syndrome. Anim. Reprod. Sci. 2009, 115:328-333.
81. Williams J., Partington B.P., Smith B., Hedlund C.S., Law J.M. Pyovagina and stump pyometra in neutered XX sex-reversed beagle: a case report. J. Anim. Hosp. Assoc. 1997, 33:83-90.
82. Williamson J.H. Intersexuality in a family of Kerry Blue Terriers. J. Hered. 1979, 70:138-139.
83. Wu X., Wan S., Pujar S., Haskins M.E., Schlafer D.H., Lee M.M., Meyers-Wallen V.N. A single base pair mutation encoding a premature stop codon in the MIS type II receptor is responsible for canine Persistent Müllerian Duct Syndrome. J. Androl. 2009, 30:46-56.