FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Animals : an open access journal from MDPI2020; 10(11); 1963; doi: 10.3390/ani10111963

An Unusual Case of Testicular Disorder in Sex Development of Arabian Mare (64,XX SRY-Negative).

Abstract: A 3-year-old Arabian mare underwent medical examinations due to the presence of abnormalities of the reproductive apparatus and stallion behavior (nervous temperament, aggressiveness, masculine attitude). During the clinical visit, an anovulvar distance shorter than normal was observed; moreover, vulvar lips were dorsally fused except for the lower neckline, showing a blind ending from which a penis-like structure protruded. The ultrasound examination revealed the presence of a cervix and corpus of a uterus, hypoplastic uterine horns, and small gonads with an echogenicity similar to a testis. Blood testosterone levels ranged from 0.4 to 0.6 ng/mL. Cytogenetic analysis showed a normal female karyotype (2n = 64,XX), while PCR amplification of SRY and ZFY genes revealed the absence of a Y chromosome. At necroscopic examination, internal genitalia arising from the genital ridge in the form of masculine type structures were found, while those deriving from the Mullerian ducts were of feminine type. In addition, an infundibular portion of the salpinx at the cranial pole of the gonads was found. This is the first case in equine species of DSD 2n = 64,XX -negative, with the simultaneous presence of male (hypoplastic testicles, epididymal portions, and a penis-like structure) and female (cervix, horn and body of a hypoplastic uterus) genital structures.
Get Full Text
Publication Date: 2020-10-25 PubMed ID: 33113813PubMed Central: PMC7693820DOI: 10.3390/ani10111963Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Case Reports

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper deals with the peculiar case of an Arabian mare that showed both male and female sexual characteristics, a condition known as ‘disorder of sex development’, despite having a normal female chromosome set (64,XX) but no Y chromosome.

Background and Introduction

  • The study revolves around a unique case of a 3-year-old Arabian mare exhibiting male-like behaviors such as aggressiveness and a masculine posture, despite having a female genetic makeup (64, XX chromosomes).
  • In addition to behavior, the mare also had abnormal physical features such as a shorter anovulvar distance and a penis-like structure protruding from a fused vulvar lip.
  • This intrigued the researchers, leading to further investigations to understand this anomaly using various diagnostic techniques.

Clinical and Cytogenetic Analysis

  • The mare underwent clinical examination, which revealed physical abnormalities such as a short anovulvar distance, dorsally fused vulvar lips, and a penis-like protrusion.
  • Ultrasound examination further revealed a complex internal structure that included elements of both male (testis-like gonads) and female (cervix, uterus) reproductive systems, coupled with unusually low blood testosterone levels.
  • The cytogenetic analysis discovered a strictly female chromosome set (64,XX), contradicting the mare’s mixed physical features and behaviors. Moreover, PCR amplification of SRY and ZFY genes revealed the absence of a Y chromosome, which is essential for male development.

Necroscopic Examination and Findings

  • Following the cytogenetic analysis, a necroscopic examination was carried out which revealed an even more complex picture. The internal genitalia had elements deriving from both male and female embryonic structures.
  • The mare had a masculine developmental structure arising from the genital ridge as well as feminine structures deriving from the Mullerian ducts. An infundibular portion of the salpinx at the cranial pole of the gonads was also found.
  • The mishmash of male and female characteristics observed in this case qualifies as a disorder of sex development (DSD). What makes this case peculiar is that the DSD had a negative 2n = 64,XX condition, i.e., simultaneous presence of both male and female genitals while having a female karyotype.
  • This case is the first of its kind in equine species, shedding new light on DSD and its manifestation in horses.

Cite This Article

APA
Peretti V, Satué K, Ciotola F, Cristarella S, De Majo M, Biondi V, D'Anza E, Albarella S, Quartuccio M. (2020). An Unusual Case of Testicular Disorder in Sex Development of Arabian Mare (64,XX SRY-Negative). Animals (Basel), 10(11), 1963. https://doi.org/10.3390/ani10111963

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 10
Issue: 11
PII: 1963

Researcher Affiliations

Peretti, Vincenzo
  • Department of Veterinary Medicine and Animal Production, University of Naples Federico II, via Delpino 1, 80137 Naples, Italy.
Satué, Katiuska
  • Department of Animal Medicine and Surgery, Faculty of Veterinary Medicine, CEU-Cardenal Herrera University, 46115 Valencia, Spain.
Ciotola, Francesca
  • Department of Veterinary Medicine and Animal Production, University of Naples Federico II, via Delpino 1, 80137 Naples, Italy.
Cristarella, Santo
  • Department of Veterinary Sciences, University of Messina, Polo Universitario Annunziata, 98168 Messina, Italy.
De Majo, Massimo
  • Department of Veterinary Sciences, University of Messina, Polo Universitario Annunziata, 98168 Messina, Italy.
Biondi, Vito
  • Department of Veterinary Sciences, University of Messina, Polo Universitario Annunziata, 98168 Messina, Italy.
D'Anza, Emanuele
  • Department of Veterinary Medicine and Animal Production, University of Naples Federico II, via Delpino 1, 80137 Naples, Italy.
Albarella, Sara
  • Department of Veterinary Medicine and Animal Production, University of Naples Federico II, via Delpino 1, 80137 Naples, Italy.
Quartuccio, Marco
  • Department of Veterinary Sciences, University of Messina, Polo Universitario Annunziata, 98168 Messina, Italy.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 50 references
  1. Ali A, Derar DR, Alshahed M. Management strategies, reproductive performance and causes of infertility in sheep flocks in the central region of Saudi Arabia.. Trop Anim Health Prod 2020 Jul;52(4):1691-1697.
    doi: 10.1007/s11250-019-02182-9pubmed: 31858370google scholar: lookup
  2. Dash S, Chakravarty AK, Singh A, Upadhyay A, Singh M, Yousuf S. Effect of heat stress on reproductive performances of dairy cattle and buffaloes: A review.. Vet World 2016 Mar;9(3):235-44.
    doi: 10.14202/vetworld.2016.235-244pmc: PMC4823282pubmed: 27057105google scholar: lookup
  3. Prete CD, Ciani F, Tafuri S, Pasolini MP, Valle GD, Palumbo V, Abbondante L, Calamo A, Barbato V, Gualtieri R, Talevi R, Cocchia N. Effect of superoxide dismutase, catalase, and glutathione peroxidase supplementation in the extender on chilled semen of fertile and hypofertile dogs.. J Vet Sci 2018 Sep 30;19(5):667-675.
    doi: 10.4142/jvs.2018.19.5.667pmc: PMC6167334pubmed: 29649854google scholar: lookup
  4. Tafuri S, Cocchia N, Vassetti A, Carotenuto D, Esposito L, Maruccio L, Avallone L, Ciani F. Lepidium meyenii (Maca) in male reproduction.. Nat Prod Res 2021 Nov;35(22):4550-4559.
    doi: 10.1080/14786419.2019.1698572pubmed: 31805775google scholar: lookup
  5. Tafuri S, Cocchia N, Carotenuto D, Vassetti A, Staropoli A, Mastellone V, Peretti V, Ciotola F, Albarella S, Del Prete C, Palumbo V, Esposito L, Vinale F, Ciani F. Chemical Analysis of Lepidium meyenii (Maca) and Its Effects on Redox Status and on Reproductive Biology in Stallions (†).. Molecules 2019 May 23;24(10).
    doi: 10.3390/molecules24101981pmc: PMC6571579pubmed: 31126050google scholar: lookup
  6. Bugno M, Klukowska J, Słota E, Tischner M, Switoński M. A sporadic case of the sex-reversed mare (64,XY; SRY-negative): molecular and cytogenetic studies of the Y chromosome.. Theriogenology 2003 Apr 1;59(7):1597-603.
    doi: 10.1016/S0093-691X(02)01197-4pubmed: 12559464google scholar: lookup
  7. Lear TL, McGee RB. Disorders of sexual development in the domestic horse, Equus caballus.. Sex Dev 2012;6(1-3):61-71.
    doi: 10.1159/000334048pubmed: 22095202google scholar: lookup
  8. Albarella S, Ciotola F, D'Anza E, Coletta A, Zicarelli L, Peretti V. Congenital Malformations in River Buffalo (Bubalus bubalis).. Animals (Basel) 2017 Feb 10;7(2).
    doi: 10.3390/ani7020009pmc: PMC5332930pubmed: 28208595google scholar: lookup
  9. De Lorenzi L, Arrighi S, Rossi E, Grignani P, Previderè C, Bonacina S, Cremonesi F, Parma P. XY (SRY-positive) Ovarian Disorder of Sex Development in Cattle.. Sex Dev 2018;12(4):196-203.
    doi: 10.1159/000489869pubmed: 29902792google scholar: lookup
  10. Albarella S, D'Anza E, Galdiero G, Esposito L, De Biase D, Paciello O, Ciotola F, Peretti V. Cytogenetic Analyses in Ewes with Congenital Abnormalities of the Genital Apparatus.. Animals (Basel) 2019 Oct 10;9(10).
    doi: 10.3390/ani9100776pmc: PMC6826438pubmed: 31658596google scholar: lookup
  11. Vaiman D, Koutita O, Oustry A, Elsen JM, Manfredi E, Fellous M, Cribiu EP. Genetic mapping of the autosomal region involved in XX sex-reversal and horn development in goats.. Mamm Genome 1996 Feb;7(2):133-7.
    doi: 10.1007/s003359900033pubmed: 8835530google scholar: lookup
  12. Pailhoux E, Popescu PC, Parma P, Boscher J, Legault C, Molteni L, Fellous M, Cotinot C. Genetic analysis of 38XX males with genital ambiguities and true hermaphrodites in pigs.. Anim Genet 1994 Oct;25(5):299-305.
    doi: 10.1111/j.1365-2052.1994.tb00362.xpubmed: 7818163google scholar: lookup
  13. Krzemińska P, D'Anza E, Ciotola F, Paciello O, Restucci B, Peretti V, Albarella S, Switonski M. Polymorphisms of MAMLD1, SRD5A2, and AR Candidate Genes in Seven Dogs (78,XY; SRY-Positive) Affected by Hypospadias or Cryptorchidism.. Sex Dev 2019;13(2):92-98.
    doi: 10.1159/000500219pubmed: 31055572google scholar: lookup
  14. De Lorenzi L, Banco B, Previderè C, Bonacina S, Romagnoli S, Grieco V, Parma P. Testicular XX (SRY-Negative) Disorder of Sex Development in Cat.. Sex Dev 2017;11(4):210-216.
    doi: 10.1159/000479175pubmed: 28848109google scholar: lookup
  15. D’Ovidio D, Melidone R, Rossi G, Albarella S, Noviello E, Fioretti A, Meomartino L. Multiple Congenital Malformations in a Ferret (Mustela putorius furo). J. Exot. Pet. Med. 2015;24:92–97.
    doi: 10.1053/j.jepm.2014.11.005google scholar: lookup
  16. Villagómez DA, Lear TL, Chenier T, Lee S, McGee RB, Cahill J, Foster RA, Reyes E, St John E, King WA. Equine disorders of sexual development in 17 mares including XX, SRY-negative, XY, SRY-negative and XY, SRY-positive genotypes.. Sex Dev 2011;5(1):16-25.
    doi: 10.1159/000322811pubmed: 21196712google scholar: lookup
  17. Albarella S, De Lorenzi L, Catone G, Magi G.E, Petrucci L, Vullo C, D’Anza E, Parma P, Raudsepp T, Ciotola F. Diagnosis of XX/XY Blood Cell Chimerism at a Low Percentage in Horses. J. Equine Veter. Sci. 2018;69:129–135.
    doi: 10.1016/j.jevs.2018.06.016google scholar: lookup
  18. Blaschko SD, Cunha GR, Baskin LS. Molecular mechanisms of external genitalia development.. Differentiation 2012 Oct;84(3):261-8.
    doi: 10.1016/j.diff.2012.06.003pmc: PMC3443292pubmed: 22790208google scholar: lookup
  19. Pujar S, Meyers-Wallen VN. Sequence variations in equine candidate genes For XX and XY inherited disorders of sexual development.. Reprod Domest Anim 2012 Oct;47(5):827-34.
    doi: 10.1111/j.1439-0531.2011.01976.xpubmed: 22239239google scholar: lookup
  20. Mäkinen A, Hasegawa T, Mäkilä M, Katila T. Infertility in two mares with XY and XXX sex chromosomes.. Equine Vet J 1999 Jul;31(4):346-9.
    doi: 10.1111/j.2042-3306.1999.tb03829.xpubmed: 10454097google scholar: lookup
  21. Kuiper H, Distl O. [Intersexuality in horses].. Dtsch Tierarztl Wochenschr 2007 Feb;114(2):50-6.
    pubmed: 17341020
  22. Peer M, Neuhauser S, Klaus C, Kuiper H, Gruber A.D, Distl O, Lischer C, Handler J. Laparoscopic Gonadectomy in Two Intersex Warmblood Horses. J. Equine Veter. Sci. 2012;32:117–122.
    doi: 10.1016/j.jevs.2011.08.011google scholar: lookup
  23. Pieńkowska-Schelling A, Becker D, Bracher V, Pineroli B, Schelling C. [Cytogenetical and molecular analyses in a horse with SRY-negative sex reversal].. Schweiz Arch Tierheilkd 2014 Jul;156(7):341-4.
    doi: 10.1024/0036-7281/a000604pubmed: 24973322google scholar: lookup
  24. Raudsepp T, Durkin K, Lear TL, Das PJ, Avila F, Kachroo P, Chowdhary BP. Molecular heterogeneity of XY sex reversal in horses.. Anim Genet 2010 Dec;41 Suppl 2:41-52.
    doi: 10.1111/j.1365-2052.2010.02101.xpubmed: 21070275google scholar: lookup
  25. Switonski M, Chmurzynska A, Szczerbal I, Lipczynski A, Yang F, Nowicka-Posłuszna A. Sex reversal syndrome (64,XY; SRY-positive) in a mare demonstrating masculine behaviour.. J Anim Breed Genet 2005 Apr;122 Suppl 1:60-3.
    doi: 10.1111/j.1439-0388.2005.00510.xpubmed: 16130458google scholar: lookup
  26. Eggers S, Ohnesorg T, Sinclair A. Genetic regulation of mammalian gonad development.. Nat Rev Endocrinol 2014 Nov;10(11):673-83.
    doi: 10.1038/nrendo.2014.163pubmed: 25246082google scholar: lookup
  27. Parma P, Radi O, Vidal V, Chaboissier MC, Dellambra E, Valentini S, Guerra L, Schedl A, Camerino G. R-spondin1 is essential in sex determination, skin differentiation and malignancy.. Nat Genet 2006 Nov;38(11):1304-9.
    doi: 10.1038/ng1907pubmed: 17041600google scholar: lookup
  28. Bodvarsdottir S.K, Imsland F, Thorisson B, Steinarsdottir M, Eyfjord J.E. 64,XX, SRY-, and ZFY-Negative Icelandic Horse Likely to Be True Hermaphrodite. J. Equine Veter. Sci. 2009;29:734–738.
    doi: 10.1016/j.jevs.2009.08.007google scholar: lookup
  29. Jaszczak K, Sysa P, Sacharczuk M, Parada R, Romanowicz K, Kawka M, Jarmuż W. SRY-negative, 64, XX sex reversal in a Konik Polski horse: A case report. Anim. Sci. Papers Rep. 2010;28:381–388.
  30. Vaughan L, Schofield W, Ennis S. SRY-negative XX sex reversal in a pony: a case report.. Theriogenology 2001 Mar 15;55(5):1051-7.
    doi: 10.1016/S0093-691X(01)00465-4pubmed: 11322233google scholar: lookup
  31. Moreno-Millán M, Demyda S.E, Saleno D.R. Sex Chromosomes Abnormalities in Purebred Spanish Horses with Reproductive Problems: Cases Report. Bullet. UASMV Vet. Med. 2012;69:1–7.
  32. Buoen LC, Zhang TQ, Weber AF, Ruth GR. SRY-negative, XX intersex horses: the need for pedigree studies to examine the mode of inheritance of the condition.. Equine Vet J 2000 Jan;32(1):78-81.
    doi: 10.2746/042516400777612071pubmed: 10661390google scholar: lookup
  33. Ciotola F, Albarella S, Pasolini MP, Auletta L, Esposito L, Iannuzzi L, Peretti V. Molecular and cytogenetic studies in a case of XX SRY-negative sex reversal in an Arabian horse.. Sex Dev 2012;6(1-3):104-7.
    doi: 10.1159/000331480pubmed: 22025175google scholar: lookup
  34. Torres A, Silva JF, Bernardes N, Sales Luís J, Lopes da Costa L. 64, XX, SRY-negative, testicular DSD syndrome in a Lusitano horse.. Reprod Domest Anim 2013 Jun;48(3):e33-7.
    doi: 10.1111/rda.12094pubmed: 23057740google scholar: lookup
  35. Iannuzzi L, Di Meo G, Perucatti A, Incarnato D, Peretti V, Ciotola F, Barbieri V. An improved characterization of horse (Equus caballus, 2n = 64) chromosomes by using replicating G and R banding patterns. Caryologia 2003;56:205–211.
    doi: 10.1080/00087114.2003.10589326google scholar: lookup
  36. Vilar J.M, Batista M, Carrillo J.M, Rubio M, Sopena J, Álamo D. Histological, cytogenetic and endocrine evaluation in twenty-five unilateral cryptorchid horses. J. Appl. Anim. Res. 2017;46:441–444.
    doi: 10.1080/09712119.2017.1333435google scholar: lookup
  37. Han SH, Yang BC, Ko MS, Oh HS, Lee SS. Length difference between equine ZFX and ZFY genes and its application for molecular sex determination.. J Assist Reprod Genet 2010 Dec;27(12):725-8.
    doi: 10.1007/s10815-010-9467-7pmc: PMC2997947pubmed: 20809415google scholar: lookup
  38. Kent MG, Shoffner RN, Hunter A, Elliston KO, Schroder W, Tolley E, Wachtel SS. XY sex reversal syndrome in the mare: clinical and behavioral studies, H-Y phenotype.. Hum Genet 1988 Aug;79(4):321-8.
    doi: 10.1007/BF00282169pubmed: 3410457google scholar: lookup
  39. Meyers-Wallen VN, Hurtgen J, Schlafer D, Tulleners E, Cleland WR, Ruth GR, Acland GM. Sry-negative XX true hermaphroditism in a Pasa Fino horse.. Equine Vet J 1997 Sep;29(5):404-8.
    doi: 10.1111/j.2042-3306.1997.tb03148.xpubmed: 9306070google scholar: lookup
  40. Bannasch D, Rinaldo C, Millon L, Latson K, Spangler T, Hubberty S, Galuppo L, Lowenstine L. SRY negative 64,XX intersex phenotype in an American saddlebred horse.. Vet J 2007 Mar;173(2):437-9.
    doi: 10.1016/j.tvjl.2005.11.008pubmed: 16386440google scholar: lookup
  41. Li TF, Wu QY, Zhang C, Li WW, Zhou Q, Jiang WJ, Cui YX, Xia XY, Shi YC. 46,XX testicular disorder of sexual development with SRY-negative caused by some unidentified mechanisms: a case report and review of the literature.. BMC Urol 2014 Dec 22;14:104.
    doi: 10.1186/1471-2490-14-104pmc: PMC4289540pubmed: 25529318google scholar: lookup
  42. Rossi E, Radi O, De Lorenzi L, Vetro A, Groppetti D, Bigliardi E, Luvoni GC, Rota A, Camerino G, Zuffardi O, Parma P. Sox9 duplications are a relevant cause of Sry-negative XX sex reversal dogs.. PLoS One 2014;9(7):e101244.
    doi: 10.1371/journal.pone.0101244pmc: PMC4091935pubmed: 25010117google scholar: lookup
  43. Xiao B, Ji X, Xing Y, Chen YW, Tao J. A rare case of 46, XX SRY-negative male with approximately 74-kb duplication in a region upstream of SOX9.. Eur J Med Genet 2013 Dec;56(12):695-8.
    doi: 10.1016/j.ejmg.2013.10.001pubmed: 24140641google scholar: lookup
  44. Benko S, Gordon CT, Mallet D, Sreenivasan R, Thauvin-Robinet C, Brendehaug A, Thomas S, Bruland O, David M, Nicolino M, Labalme A, Sanlaville D, Callier P, Malan V, Huet F, Molven A, Dijoud F, Munnich A, Faivre L, Amiel J, Harley V, Houge G, Morel Y, Lyonnet S. Disruption of a long distance regulatory region upstream of SOX9 in isolated disorders of sex development.. J Med Genet 2011 Dec;48(12):825-30.
    doi: 10.1136/jmedgenet-2011-100255pubmed: 22051515google scholar: lookup
  45. Albarella S, Lorenzi L, Rossi E, Prisco F, Riccardi MG, Restucci B, Ciotola F, Parma P. Analysis of XX SRY-Negative Sex Reversal Dogs.. Animals (Basel) 2020 Sep 16;10(9).
    doi: 10.3390/ani10091667pmc: PMC7552623pubmed: 32947906google scholar: lookup
  46. Sukumaran A, Desmangles JC, Gartner LA, Buchlis J. Duplication of dosage sensitive sex reversal area in a 46, XY patient with normal sex determining region of Y causing complete sex reversal.. J Pediatr Endocrinol Metab 2013;26(7-8):775-9.
    doi: 10.1515/jpem-2012-0354pubmed: 23612644google scholar: lookup
  47. Mizuno K, Kojima Y, Kamisawa H, Moritoki Y, Nishio H, Kohri K, Hayashi Y. Gene expression profile during testicular development in patients with SRY-negative 46,XX testicular disorder of sex development.. Urology 2013 Dec;82(6):1453.e1-7.
    doi: 10.1016/j.urology.2013.08.040pubmed: 24149105google scholar: lookup
  48. Moalem S, Babul-Hirji R, Stavropolous DJ, Wherrett D, Bägli DJ, Thomas P, Chitayat D. XX male sex reversal with genital abnormalities associated with a de novo SOX3 gene duplication.. Am J Med Genet A 2012 Jul;158A(7):1759-64.
    doi: 10.1002/ajmg.a.35390pubmed: 22678921google scholar: lookup
  49. Polanco JC, Wilhelm D, Davidson TL, Knight D, Koopman P. Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development.. Hum Mol Genet 2010 Feb 1;19(3):506-16.
    doi: 10.1093/hmg/ddp520pubmed: 19933217google scholar: lookup
  50. Jeays-Ward K, Dandonneau M, Swain A. Wnt4 is required for proper male as well as female sexual development.. Dev Biol 2004 Dec 15;276(2):431-40.
    doi: 10.1016/j.ydbio.2004.08.049pubmed: 15581876google scholar: lookup

Citations

This article has been cited 2 times.
  1. Bugno-Poniewierska M, Raudsepp T. Horse Clinical Cytogenetics: Recurrent Themes and Novel Findings. Animals (Basel) 2021 Mar 16;11(3).
    doi: 10.3390/ani11030831pubmed: 33809432google scholar: lookup
  2. Li Y, Shi J, Yang Y, Ruan D, Wu J, Lin D, Liao Z, Hong X, Zhou F, Liu L, Yang J, Yang M, Zheng E, Wu Z, Cai G, Zhang Z. Genome-Wide Association Study Reveals Genetic Mechanisms Underlying Intersex and Aproctia in Large White Pigs. Animals (Basel) 2025 Apr 10;15(8).
    doi: 10.3390/ani15081094pubmed: 40281928google scholar: lookup
Subscribe to our newsletter
Join 99,850 horse owners like you who receive our email updates on horse health and nutrition.