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VAGINAL

BLEEDING

IN GONADAL

DYSGENESIS

Stephen Kaufman, M.D.

Department of Pediatrics, University of California-San Francisco Medical Center, San Francisco, California

Ftc. 1. Case 1 at 12% years (without therapy).

(Submitted February 3; accepted for publication March 29. 1965.)

ADDRESS: Department of Pediatrics, University of California-San Francisco Medical Center, San

Francisco 22, California.

26

PEDIATRICS, Vol. 37, No. 1, Part I, January 1966

S

POBADIC CASES which probably represent

ovarian dysgenesis have been described since the first decade of the twentieth c’n-tury. This syndrome was first thoroughly described, however, by Turner in 1938,1

when he reported 7 females with short sta-tune, cuhitus valgus, webbed neck, and sexual infantilism. Since that time, the lit-erature has been replete with cases which represent variations of this syndrome. A review of all published cases which are called “Turner’s syndrome” includes

pa-tients who are of either 2 short or of

average height,4 with or without cubitus valgus and pterygium colli,” and who may be sexually immature or sexually mature and fertile.6 Chromosomal studies suggest

an abnormality which involves the

X-chromosome,’5 although even this may not be constant.

This paper presents two unusual cases of females with several of the physical stig-mata associated with Turner’s syndrome. These are the fourteenth and fifteenth pa-tients reported in the world literature who

have been studied by chromosomal karyo-typing that have both the physical stigmata of Turner’s syndrome and repeated spon-taneous episodes of vaginal bleeding.

CASE REPORTS

CASE 1, whose parents were 35 and 38 years old,

was born at term, weighed 5 lb 14 oz and was

17 inches long. By contrast, the birth weight of

her 2 siblings was 7 lb 8 oz and 9 lb 10 oz.

Lymphedema of the extremities was noted in the

newborn period and a slight puffiness of the

dor-sum of the hands and feet still persists. Psoriasis,

diagnosed at age 3, is still active and a mild

hear-ing deficit, first noted at the age of 4 years, also

persists. Although growth velocity is normal, her

height has remained below the 3rd percentile.

s’Ienarche, without other secondary sexual

char-acteristics, occurred at 11 years 11 months and

vaginal bleeding, lasting from 3 to 4 days, with 1

to 2 pads per period, has persisted at monthly

intervals since then.

On physical examination at 12h years she was a

short stocky child with a masculine habitus (Fig. 1), a height of 49% in., weight 68% lb, span 48%

in., upper segment 26%, lower segment 23%, ratio

1:13; blood pressure: right arm supine 115/85;

left leg prone 125/80; pulse 80, respirations 18.

Pertinent positive physical findings included a high-arched palate, 12-year molars on the left but

not on the right side, and a mild bilateral hearing

loss. The neck was minimally broadened at the

base with a low posterior hairline. Pectus

(2)

ARTICLES 27

tissue was palpable. The nipples were infantile but

not widely spaced or inverted. The external

geni-talia were immature except for a slight rugation of the labia majora. Pubic and axillary hair was

absent and the clitoris was not enlarged. There

was mild cubitus valgus bilaterally, with

fore-shortening of the fourth and fifth knuckles on the

left hand and the fifth knuckle of the right hand.

The third and fourth toes of both feet were

ab-normally short and webbed at their bases. There

were multiple pigmented nevi on the skin, active

psoriatic lesions, and healed scars from past lesions.

On three occasions, buccal smears stained with

orscein revealed between 15 and 17% Barr bodies/

100 cells (normal values in our laboratory: less

than 4% for males; more than 20% for females).

Peripheral blood smears demonstrated 8

drum-sticks/500 neutrophils in our patient and 7/500

in her mother.9 Karyotyping showed 45

chrorno-somes in all 30 cells counted, with an XO

idio-gram in each of 5 cells. In a second chromosomal

count 1 year later, 45 chromosomes in all 50 cells

counted and idiograrns of 15 cells were consistent

with an XO pattern. A chromosomal count on the

mother showed 46 chromosomes in 28 out of 30

cells, with idiograms of 2 cells yielding an XX

pattern. The father and the siblings were

unavail-able for study.

FSH was positive at both 5 and 80 mouse units,

urinary estrogens were negative at 3 and 1 ?% and

a vaginal smear at approximately mid-cycle was

negative for estrogen effect. Urinary

17-hydroxy-corticosteroids were 4.0 mg/24 hr and 17

keto-steroids were 1.4 mg/24 hr.

Because of the known relationship between

ovarian dysgenesis and

pseudopseudohypoparathy-roidism, investigation of the serum calcium and

phosphorus and the renal tubular response to

para-thyroid extract was undertaken. Serum calcium was

10.5 mg/100 ml, serum phosphorus 4.3 mg/100 ml,

alkaline phosphatase 14 SJR units, total proteins

7.0 gm/100 ml. Following intramuscular injection

of 500 units of parathormone (Lilly) every 12 hours

for 4 doses, serum calcium rose to 15.5 mg/100 ml,

serum phosphorus fell to 3.4 mg/100 ml, and

alka-line phosphatase to 10 SJR units.

X-ravs revealed a disproportionate shortening of

the fourth and fifth metacarpal of the left hand

and the fifth metacarpal of the right hand, with

fusion of the epiphysis typical of

pseudopseudo-hypoparathyroidism rather than Turner’s syndrome.

Beaking of the middle aspect of the tibial

meta-physis was present bilaterally with an inclination

of the medial epiphyseal cartilage typical of Turn-er’s syndrome. The third and fourth metatarsals showed premature closure of the epiphyses, and

bone age was equivalent to the chronological age.

Estrogen therapy was inaugurated just prior to

the patient’s thirteenth birthday. In the subsequent

6 months she grew 1.75 in. and gained 8 ib;

bud-Fic. 2. Case 2 at 2 ears.

ding of breasts and pigmentation of the nipples

occurred, and the body habitus became more

feminine. Periodic vaginal bleeding has continued

and at the present time is more profuse. Sexual

hair has appeared and occasional acneiform lesions

have been noted.

CASE 2 was born of a pregnancy complicated

by maternal hyperemesis. The parents were 36

and 38 years old at the time of her birth, which

was 2 weeks prior to term. Her birth weight was

4 lb, 13 Oz; the height was unrecorded. Mild

lymphedema of the distal extremities and bilateral

ptosis were noted in the nursery. The posterior

fontanelle did not close until 14 months and the

anterior fontanelle was still widely patent at 2

years. At 2 years she was below the 3rd percentile

in height and weight, with pinched facial features,

a short frenulum, bilateral ptosis and hyperopic

astigmatism (Fig. 2). Laboratory studies suggested

normal thyroid function and normal intelligence;

gonadotropin assays were negative; bone age was

1 year retarded and an electroencephalogram

dem-onstrated a generalized irregularity.

At the age of 13 she was seen because of her

short stature. The intervening 1 1 years had been

complicated only by 2 nocturnal grand mal

seiz-ures. Vaginal bleeding occurred for the first time at age 13 and has continued irregularly

approxi-mately every 2 weeks since then with a moderate

flow for 5 to 7 days accompanied by mild

ab-dominal cramping and weakness. When she was 14

(3)

Ftc. 3. Case 2 at 14 years.

On physical examination at age I 4, she was

52% in. tall, weighed 67 Ib, had a blood pressure

of 120/80, pulse 84, and a head circumference of

20 in. A pinched facies and bilateral ptosis gave

her a dull vacant expression. The cars were small

and low-set with abnormally narrow external

audi-tory canals. The palate was high arched, the teeth

irregularly placed, and the mandible recessed. Her

neck was short, mildly webbed, with a low

pos-tenor hairline (Fig. 3). Her chest was

shield-shaped with widely spaced hut not inverted nipples and without palpable breast tissue. A small

amount of straight black pubic and axillary hair

was evident; mild cubitus valgus was present; the skin was dry and several raised brown nevi were apparent.

Follicle-stimulating hormone levels were

border-line at 160 mouse units, positive at 80; vaginal

smears for estrogen effect produced 38% basal,

60% intermediate and 2% superficial cells. Buccal

smears were consistently positive and a chromo-somal count revealed a mosaicism of 16 cells with 45 chromosomes and 37 cells with 46. Idiograms

suggested an XO/XX mosaicism. The bone age

was between 11 and 13 years at a chronological

age of 13 years, 6 months, and the abnormal

knuckle sign associated with gonadal dysgenesis was present.’#{176}An electroencephalogram revealed

an inactive focus in or deep to the left temporal

region . w\’ith the institi itioii of estrogen tllIral)\’

breast buds Ll)Pet1rel within 1 month; 2 months

later, site refused all medications and has

con-tiflu((l to do so until the l)rcsetlt time. At 14 ears,

6 months she weighed 74 Ibs, was 53 1/16 in. tall,

had luxuriant pubic and axillary hair and scanty

vaginal bleeding at monthly intervals which lasted

7 days without dysmennorhea.

REVIEW OF THE LITERATURE

Prior to the development of the tech-niques for interpreting buccal smears for sex chnomatin and chromosomal karyotyp-ing, the diagnosis of ovarian dysgenesis with vaginal bleeding was difficult to make with certainty. Available data listed in the

table suggest that the first 20 cases (in-cluding our 2 cases) are highly probable examples of the syndrome, whereas the evidence is not as conclusive in the remain-ing cases. Several other vaguely

docu-mented cases have been reported but are

(4)

ARTICLES 29

cases reported by Bahner, Haddad,’4 Lem-ii,” and Lindsten.15 With the exception of our Case 2, Haddad’s Case 3,14 and Lind-sten’s Cases 51, 53 all other patients with mosaic karyotypes

XX/XO,

XX/XXX

/xO,

and XO/XY have been amennorheic. There have been 4 reports of pseudopseudo-hypoparathyroidism with ovarian dysgene-sis-1 case by Archibald’o and 3 by Wenif

Ten “ None of these had

chromo-somal analysis or investigation of the re-sponse of the renal tubule to parathynoid hormone.

The table shows the wide variation of physical and laboratory data reported in these patients. Several had no evidence of cubitus valgus or ptenygium colli, some were of average height, 2 had normal breast de-velopment, 1 was fertile, 2 had positive buc-cal smears for sex chromatin, and 1 had a

normal excretion of gonadotropins.

COMMENT

Our report describes the fourteenth and fifteenth cases in the world literature of patients with ovarian dysgenesis and ne-peated spontaneous episodes of vaginal bleeding who have had chromosomal karyo-ty ping. The usual order of sexual maturation was disrupted; both girls had vaginal bleed-ing prior to the onset of sexual hair or

changes in the breasts and nipples. With the

institution of exogenous estrogen therapy, breast buds quickly became visible and palpable but a normal degree of mammary tissue has not occurred yet. The etiology of the underdevelopment of the mammary tissue is not clean. We are investigating the possibility that minute amounts of

circulat-ing estrogen during childhood can prime

the mammary tissue for more adequate re-sponse during puberty.

Case 1 reveals a 45

XO

chromosomal karyotype without evidence of mosaicism in the lymphocytes; however, the presence

of 15 to 17% Barr bodies in the buccal smear, a figure compatible with previously described patients with mosaicism, and a

chromatin pattern of 8 dnumsticks/500

neu-trophils, strongly suggests mosaicism. The

mother, with a typical 46 XX chromosomal

karyotype, has the same percentage of

drumsticks, further emphasizing the likeli-hood of mosaicism in our Case 1. Our in-ability to demonstrate two or more differ-ent chromosomal cell lines may be due to our present inability to culture other tissues.

Pseudopseudohypopanathyroidism and

ovarian dysgenesis may both exhibit

abnor-malities of the fourth metacarpal, short sta-tune, and a tendency to reduced intelli-gence. The cases of Werf Ten Boschl2 and Archibald0 suggest that this relationship

may not be entirely fortuitous. Further-more, the response of the renal tubules to parathyroid hormone becomes important if we consider the current theory that pseudo-and pseudopseudohypoparathyroidism are

part of the same continuum of disease.28

Our Case 1 had shortened fourth and fifth

metacarpals of the left hand, a shortened fifth metacarpal on the right hand, and foreshortened third and fourth metacarpals bilaterally. Radiologically, these bones are typical of

pseudopseudohypoparathyroid-ism rather than ovarian dysgenesis (Fig. 4) for the following reasons. In Turner’s syn-drome the metacarpals tend to be normally shaped with a normal or retarded fusion of the epiphysis and minimal degree of

short-ening of the fourth metacarpal. In pseudo-pseudohypoparathynoidism the abnormality

often involves the first and fifth metacarpal as vell as the fourth, which is abnormally broadened and significantly foreshortened, with a premature closure of the epiphysis

and lack of normal 2930

Since the patients described by Werif Ten Bosch” and Archibald’#{176} had normal levels of serum calcium and phosphorus and the renal tubular response to parathyroid hormone was not tested in them, investiga-tion of the calcium and phosphorus

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(7)

Ftc. 4. The foreshortening of the fourth metacarpal (Case 2) is demonstrated by the line which connects

the distal epiphysis of the fifth, fourth, and third metacarpals. In the normal hand, a line from the fourth and fifth metacarpals would not touch the third. The differences between the metacarpal abnormality in ovarian dysgenesis as opposed to

Patients with

pseudopseudohypoparathy-roidism have 46 chromosomes with a nor-mal karyotype,3’ suggesting that if there is

a genetic relationship between the two syn-dromes it is more subtle than our present

chromosomal evaluation techniques can demonstrate.

Case 2 is clearly a chromosomal mosaic and is unusual because of the physical re-semblance of the mother and daughter. The

sudden death of the mother of an aontic

aneurysm, an anomaly occasionally seen in

Turner’s syndrome, raises the possibility of

an inherited chromosomal aberration.

SUMMARY

Two cases of ovarian dysgenesis with pe-riodic vaginal bleeding are presented, with evidence which suggests chromosomal

mo-saicism. In a review of the world literature

our cases are the fourteenth and fifteenth

described with vaginal bleeding and

chromosomal analysis. Our first case also demonstrates the foreshortened metacarpals

of pseudo- and

pseudopseudohypoparathy-is dpseudopseudohypoparathy-iscussed in text.

noidism. It is the fourth case reported with ovarian dysgenesis and brachymetacarpal dwarfism and the first in which renal tubular sensitivity to parathynoid hormone has been determined. It is suggested that the clinical

term, Turner’s syndrome, be replaced by a

classification based on chromosomal karyo-type.

ADDENDUM

Rothenbuchner et al. (Human

Chromo-some Newsletter, 14:20, 1964) report a 17-year-old girl, 132 cm tall, 31 kg, with poor breast development, no sexual hair and no physical stigmata of ovarian dysgenesis who had one episode of vaginal bleeding. Sex chromatin studies revealed 4% Barr bodies and a chromosome count of 45/46 XO/XX in the blood and 45/46/47 XO/XX/XXX

in the fibroblasts.

REFERENCES

1. Turner, H. H.: Syndrome of infantilism,

con-genital webbed neck, and cubitus valgus.

Endocrinol., 23:566, 1938.

(8)

ARTICLES

33 A. M., and Eberlein, W. R. : Turner’s

syn-drome in the male. J. Pediat., 58:321, 1961.

3. Fraccaro, M., Ikkos, D., Lindsten, J., Luft, R.,

and Tillinger, K. G.: Testicular germinal

dysgenesis (male Turner’s syndrome). Report of a case with chromosomal studies and

review of the literature. Acta Endocr., 36:

98, 1961.

4. Engstrom, W. W., and Stoddard, F. J.:

Con-adal dysgenesis : Ovaries in association with

chromatin-negative pattern in somatic cells.

Metabolism, 20:780, 1960.

5. Hoffenberg, R., Jackson, W. P. U., and Muller, W. H.: Gonadal dsgenesis with

menstruation: Report of 2 cases. J. Clin.

Endocr. Metab., 17:902, 1957.

6. Bahner, F., Schwartz, G., Heinz, H. A., and

Walter, K.: Turner syndrome with fully

developed secondary sex characteristics and

fertility. Acta Endocr., 35:397, 1960.

7. Becker, K. L., Sprague, R. G., and Albert, A.:

Chromosomal spectrum of gonadal

dysgene-sis. Mayo Clin., 38:490, 1963.

8. Parsons, L., and Sommers, S. C.: Gynecology,

Philadelphia: W. B. Saunders, 1962, p. 65. 9. Murthy, M. S. N., and von Haam, E. : The

occurrence of the sex chromatin in white

blood cells of young adults. I. Study of normal peripheral blood. Amer. J. Clin.

Path., 30:216, 1958.

10. Archibald, R. M., Finby, N., and de Vito, F.:

Endocrine significance of short metacarpals.

J. Clin. Endocr. Metab., 19:1312, 1959. ii. Lemli, L., and Smith, D. W. : The XO

syn-drome: A study of the differentiated

pheno-type in 25 patients. J. Pediat., 63:577, 1963.

12. Stewart, J. S. S.: Gonadal dysgenesis: the genetic significance of unusual variants. Acta

Endocr., 33:89, 1960.

13. Bricaire, H., Tourneur, R., Leprat, J.. and de Gennes, L. : Gonadal dysgenesis with

pseudo-menstrual genital hemorrhages.

Apropos of 3 personal cases. Presse Med., 69:425, 1961.

14. Haddad, J. G.: Turner’s syndrome: Case

re-ports and review of clinical and cytogenetic

aspects. Bull. Tulane Med. Fac., 21:139,

1962.

15. Lindsten, J.: The Nature and Origin of Chromo-some Abberations in Turner’s Syndrome, Stockholm, Almquest and Wiksell, 1963. 16. Guisti, C., Borghi, A., Begozzi, V., and

Toe-cafondi, R.: Rass. Neurol. \Teg., 15:253, 1960.

17. Varney, R. F., Kenyon, A. T., and Koch, F. C.:

Association of short stature, retarded sexual

development and high urinary gonadotropin

titers in women: Ovarian dwarfism.

J.

Clin. Endocr. Metab., 2:137, 1942.

18. Lisser, H., Curtis, L. E., Escamilla, R. F., and

Goldberg, M. B. : Syndrome of congenitally

aplastic ovaries with sexual infantilism, high

urinary gonadotropins, short stature and other congenital abnormalities. Tabular pre-sentation of 25 previously unpublished cases. J. Clin. Endocr. Metab., 7:665, 1947. 19. Albright, F., Smith, P. H., and Fraser, R.:

Syndrome characterized by primary ovarian

insufficiency and decreased stature. Report of 1 1 cases with digression on hormonal control of axillary and pubic hair, Amer.

J.Med. Sci.,204:625, 1942.

20. Briggs, D. K., and Kupperman, H. S. : Sex

differentiation by leukocyte morphology.

J.

Clin. Endocr. Metab., 16:1163, 1956. 21. Perloff, W. H., Stein, R. 0. : Stigmata of

Turner’s syndrome in woman with regular

menstrual rhythm, J. Clin. Endocr. Metab.,

13:1548, 1953.

22. Werif Ten Bosch, van der: The syndrome of

brachymetacarpal dwarfism

pseudo-pseudo-hypoparathyroidism) with and without

go-nadal dysgenesis. Lancet, 1 :69, 1959.

23. Michelin, R. : Le syndrome de Turner-Albright.

Rapport de deux case. These de Paris, 1949,

No. 417, quoted in La Presse Medicale 69:

427, 1961.

24. Netter, A. : Fonction endocrine der testicule.

Paris: Mal Masson, 1957.

25. Guinet, P., and Putelat, R. : Le syndrome de

Turner. Vie Med., 37:441, 1956.

26. Perrault, M., Klotz, B., and Housset, E. : Deux

cas de syndrome de Turner avec

surdi-mutite dans une meme fratrie. Bull Mem. Soc. Med. HOp. Paris, 67:79, 1951.

27. del Castillo, E. B., and Argonz,

J.:

Syndrome

of rudimentary gonad: Report of four cases with unusual alterations of the gonad. Acta Endocr., 24:379, 1957.

28. Cordan, C. : Introduction, Year Book of

En-docrinology, 1960-61, Chicago: Year Book

Publishers, 1961, p. 5.

29. Steinbach, H. : Personal communication, 1964.

30. Kosowicz, J.: Changes in the medial tibial condyle: A common finding in Turner’s syn-drome. Acta Endocr., 31:321, 1959. 31. Schwarz, C., and Walter, K.: Chromosomal

analysis in gonadal dysgenesis with

pseudo-pseudohypoparathyroidism. Lancet, 1:1075,

1962.

Acknowledgment

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1966;37;26

Pediatrics

Stephen Kaufman

VAGINAL BLEEDING IN GONADAL DYSGENESIS

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1966;37;26

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Stephen Kaufman

VAGINAL BLEEDING IN GONADAL DYSGENESIS

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