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New concepts in Klinefelter syndromeDarius A. PaduchRonnie G. Alexander Bolyakoand Joseph Kiper aDepartment of Urology and Reproductive Medicine, Weill Medical College of Cornell University and Klinefelter syndrome, 47,XXY and its variants, is the most common chromosomal Population Council, Center for Biomedical Research, aberration among men, with estimated frequency of 1 : 500 among newborns. Men withKlinefelter syndrome present with sequels of hormonal and spermatogenic testicular Correspondence to Darius A. Paduch, MD, PhD,Department of Urology, Weill Medical College of failure like infertility, low testosterone, erectile dysfunction, and low bone mineral Cornell University, 525 East 68th Street F-924A, density. This review is aimed to provide the practicing urologist with an important source New York, NY 10065, USATel: +1 212 746 5309; fax: +1 212 746 7287; of clinically relevant information about Klinefelter syndrome.
Current Opinion in Urology 2008, 18:621–627 Sperm can be found in over 50% of men with Klinefelter syndrome, thus men withKlinefelter syndrome are not sterile. Recent evidence suggests that children withKlinefelter syndrome are born with spermatogonia and lose large numbers of germ cellsduring puberty. Early diagnosis and treatment can improve the quality of life and theoverall health of men with Klinefelter syndrome.
SummaryGrowing interest in Klinefelter syndrome among translational scientists and clinicianswill result in better understanding of the pathophysiology of testicular failure. In somestates, screening programs for Klinefelter syndrome are already in place, which willincrease the number of patients with Klinefelter syndrome seen by practicing urologistsin the near future. Diagnosis and management of patients with Klinefelter syndrome iswithin the scope and training of urologists. Development of randomized clinical trialscomparing different forms of interventions in men and children with Klinefelter syndromewill allow us to standardize the care of these patients.
Keywordshypogonadism, Klinefelter syndrome, meiosis, spermatogenesis Curr Opin Urol 18:621–627ß 2008 Wolters Kluwer Health | Lippincott Williams & Wilkins translational scientists with an update on pathophysiol- ogy and management of Klinefelter syndrome. This Klinefelter syndrome, despite its high prevalence and study focuses on new developments in reproductive plethora of urological symptoms, has drawn marginal biology and medicine in men with Klinefelter syndrome.
attention among urologists. However, over the last 10years, with advancements in artificial reproductive tech-niques and the successful delivery of healthy children from men with Klinefelter syndrome, the involvement of Klinefelter syndrome is the most common numerical urologists in the care of patients with Klinefelter syn- chromosomal aberration among men, with an estimated drome is increasingly important. In the past, Klinefelter frequency of 1 : 500–1 : 1000 of live deliveries Kline- syndrome was managed mostly by endocrinologists; how- felter syndrome is characterized by X chromosome polys- ever, successful sperm recovery from men with Kline- omy with X disomy being the most common variant felter syndrome indicating that adolescents with Kline- (47,XXY). Ninety percent of men with Klinefelter syn- felter syndrome have spermatogonia has stimulated drome have nonmosaic X chromosome polysomy growing interest in Klinefelter syndrome .
Although the classic description of men with Klinefelter Urologists are in a unique position to address long-term syndrome emphasized tall eunuchoid body proportions, care of patients with Klinefelter syndrome in respect to low testosterone, sparse facial and pubic hair, small hard their reproductive and sexual function. Thus, we feel it is testicles, micropenis, sterility, and mild-to-moderate important to provide practicing practitioners as well as cognitive deficits, it is now well known that this original 0963-0643 ß 2008 Wolters Kluwer Health | Lippincott Williams & Wilkins Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Andrology, sexual dysfunction and infertility Figure 1 The classic descriptions of men with Klinefelter syndrome are based on the most severe cases of phenotypic abnormalities Most teenagers and young adults seen in our practice have typical body proportions, arm span and penile length as their peers. The only obviousdifference that is seen in all men with Klinefelter syndrome is clearly visible difference in testicular size between men with Klinefelter syndrome (verysmall testes) and men with 46,XY karyotype (normal size). The photograph shows two 21-year-old men seen in our practice. The 46,XY had history ofconstitutionally delayed puberty. Both of them required testosterone treatment early during puberty. The patient with Klinefelter syndrome continuestestosterone replacement therapy. Both of them are top of the class college students.
description is not accurate and men with Klinefelter syndrome represent a broad spectrum of phenotypes, professions, incomes and socioeconomic status The 47,XXY karyotype of Klinefelter syndrome arises Severe intellectual deficits are rare. Often, the auditory spontaneously when paired X chromosomes fail to processing delay and language dysfunction seen in men separate – nondisjunction in stage I or II of meiosis, with Klinefelter syndrome are misdiagnosed as cognitive during oogenesis or spermatogenesis Less than 3% of deficits Most commonly, men with Klinefelter syn- X chromosome polysomy occurs during early divisions of drome will present to their urologist with infertility: the fertilized egg. However, postfertilization nondisjunc- azoospermia or severe oligospermia, low testosterone tion is responsible for mosaicism, which is seen in and complications of low testosterone such as erectile approximately 10% of Klinefelter syndrome patients.
dysfunction and poor libido. Boys will present with con- Men with mosaicism are less affected and often are cerns about genital and pubertal development Sper- not diagnosed. Advanced maternal age and possibly matogenic and steroidogenic dysfunction are cardinal and paternal age have been linked to increased risk of the most prevalent signs of Klinefelter syndrome. Harder testes, with volume less than 10 ml, in older adolescentand younger men should always be evaluated furtherregardless of penile size, body proportions, or level of The X chromosome carries genes that play roles in many body systems including testis function, brain develop- chromosomes (48,XXXY; 49,XXXXY) are more affected ment and growth Men with Klinefelter syndrome are than men with the classic 47,XXY karyotype usually infertile because of primary testicular failure. A Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
New concepts in Klinefelter syndrome Paduch et al.
typical patient with Klinefelter syndrome will present from boys with Klinefelter syndrome who were biopsied with low serum testosterone, high LH and FSH level, and at different ages and development stages indicated that often elevated estradiol; however, the decline in testos- boys with Klinefelter syndrome have spermatogonia at terone production is progressive over the life span and not birth but that damage to the germinal epithelium occurs early during puberty Three potential mechan-isms have been suggested to explain spermatogenic fail- Men with Klinefelter syndrome are at a higher risk of ure in Klinefelter syndrome: intratesticular hormonal autoimmune diseases; diabetes mellitus, leg ulcers, osteo- imbalance with hypersensitivity to increasing intratesti- penia and osteoporosis, tumors (breast and germ cells), cular testosterone and estradiol concentrations, Sertoli and historically have increased mortality It is cell dysfunction, and defects in spermatogonial stem cell unknown if the morbidity associated with Klinefelter renewal. A less likely although possible explanation of syndrome is a result of hypogonadism and hyperestrogen- spermatogenic failure would be a loss of spermatocytes ism or rather due to abnormal function of X chromosome- during meiosis as a result of abnormal pairing of X and It is well accepted that the X chromosome bears over Low testosterone and elevated estradiol levels are cardi- 1100 genes that are critical for the normal function of the nal symptoms of Klinefelter syndrome. In most men, LH testis and brain Inactivation of additional X chromo- some is initiated within the X chromosome inactivation center (XIC) by activation of the XIST promoter. Many boys with Klinefelter syndrome have abnormally elev- genes on the X chromosome are highly expressed in the ated FSH and LH at Tanner stage III. The most likely testis, ovaries and brain; thus, it is not surprising that causes of hypogonadism seen in men with Klinefelter these organs are affected by X chromosome polysomy syndrome are aberrant expression of steroidogenic Understanding the molecular mechanisms of X enzymes and/or negative effects of elevated intratesticu- chromosome inactivation has important clinical appli- lar estradiol levels. Hyperestrogenism is commonly seen cations, because at this point, we do not have a clinical in Klinefelter syndrome, with increased estrogen-to-tes- or molecular test that can predict an extent of reproduc- tosterone ratios and delayed increase in testosterone tive or cognitive failure in an individual patient levels during puberty being responsible for the charac-teristic body proportions and gynecomastia Treat- In the last decade, developments in microsurgical tech- ment with aromatase inhibitors can lower intratesticular niques and advances in artificial reproductive technol- estradiol levels and have beneficial effect on testosterone ogies (ART) allowed over 50% of patients with Kline- production and spermatogenesis in men with Klinefelter felter syndrome to have their own children through the combination of microsurgical testicular sperm extraction(TESE) and use of freshly retrieved sperm for in-vitro Sperm found in testes of men with Klinefelter syndrome fertilization (IVF) The fact that sperm can be have only a slightly increased frequency of sex chromo- found in the testes of men with Klinefelter syndrome some polysomies, and most boys born from fathers with has challenged the previous assumption that men with Klinefelter syndrome have a normal karyotype Klinefelter syndrome are always sterile. This has raised These findings indicate that during early stem-cell pro- the mechanistic question whether children with Kline- liferation or meiotic division, the checkpoint mechanisms felter syndrome are born with a severely depleted num- are able to overcome X chromosome polysomy resulting ber of spermatogonia or whether there is a period in life in sperm with a single X (or Y) chromosome Data by when the spermatogonia undergo massive apoptosis that Bergere et al. and Yamamoto et al. suggest that results in depletion of the spermatogonial population and the most likely explanation for normal haploid sperm in men with Klinefelter syndrome is the presence of a repairmechanism that, during spermatogonial renewal, allows for Based on the current data, it is reasonable to assume that the loss of the additional X chromosome. Alternatively, most men with Klinefelter syndrome are born with sper- rare errors in mitotic proliferation of spermatogonia in matogonia However, during early puberty – which the ‘error’ actually results in a normal karyotype most likely after initiation of the first wave of spermato- could explain the development of normal sperm.
genesis – the spermatogonia appear to undergo massiveapoptosis , Fig. 4). This hypothesis is based primarily Klinefelter syndrome can be diagnosed prenatally by on three observations: testicular sperm can be identified amniocentesis and in the postnatal period by karyotyp- and recovered from at least half of adult men with ing, fluorescence in-situ hybridization (FISH) and molec- Klinefelter syndrome; in rare cases, sperm can be found ular techniques. Karyotyping is a gold standard in in ejaculates of men with Klinefelter syndrome; and data Klinefelter syndrome diagnosis; however, the test is Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Andrology, sexual dysfunction and infertility Figure 2 Changes in hormonal level in 85 adolescents and young men seen over 3 years FSH and LH measured in serum (mIU/ml), total testosterone level converted to nmol/l to facilitate combining all hormone levels to be presented on onegraph. Thick black line represents upper normal levels of LH and FSH, which in fertile men should be below 10 mIU/ml, and low normal level oftestosterone, which should remain above 10 nmol/l in adolescents and adult men. The damage to testis occurs within the 2-year window at earlypuberty and by 16 years of age most boys have similar levels of FSH as adult men who presented with infertility. ( ) FSH; ( ) LH; ( ) T (nmol/l).
expensive, labor intensive and has relatively low sensi- management of men with Klinefeltersyndrome Management of men with Klinefelter syndrome is challen- All men with Klinefelter syndrome should have a full ging because one’s reproductive goals have to be included hormonal evaluation including FSH, LH, testosterone, in optimal medical treatment. Most men present with estradiol, prolactin and IGF-1. Cortisol levels should be infertility and seek therapeutic interventions, specifically routinely measured, because there is growing evidence microsurgical TESE with IVF. Treatment options in that adrenal steroidogenic deficiency may be seen in adolescents and adults differ, and especially in younger 47% of men with Klinefelter syndrome Because adolescents, fertility preservation should be discussed with decreased testosterone significantly increases the risk of parents. Currently, fertility preservation in adolescents osteopenia and osteoporosis, bone density is routinely should be reserved to large academic centers, as each team performed to diagnose these conditions. Men with needs to solve complex ethical, legal and logistics issues Klinefelter syndrome have an increased risk of deep vein that arise when a child with a genetic defect is subjected to thrombosis, and in 85 adult men we have seen over the a surgical procedure. The benefits of sperm retrieval, last 3 years, three had pulmonary embolism and deep although very likely, are not certain at this point. Because vein thrombosis. At this point, it is unclear whether recovery of sperm through TESE combined with intracy- screening for mutations leading to hypercoagulability is toplasmic sperm injection (ICSI) has led to successful live indicated in all men with Klinefelter syndrome. Regard- births of children, it is critical that reproductive endocri- less, all patients with Klinefelter syndrome should be nologists and reproductive urologists are familiar with the informed about the increased risk of deep vein throm- current literature and success rates. The best success rate bosis and have their hematocrit checked to avoid of IVF in Klinefelter syndrome seems to be obtained through the use of fresh sperm through testicular biopsyperformed the same day as egg retrieval. In the largest Patients with Klinefelter syndrome have an increased risk study reported so far, Schiff et al. reported a retrieval of extratesticular germ cell tumors and possibly increased rate of 69% (29/42), much higher than the 42% (5/12) pub- lished by Friedler et al. In addition, the fertilization Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
New concepts in Klinefelter syndrome Paduch et al.
rate was higher: 85% using fresh sperm in the study by in many oncological centers and is becoming a standard of Schiff et al. compared with 58% using cryopreserved care in adolescents and young adults undergoing che- sperm. Although no statistical difference between fresh motherapy or radiation despite the fact that not all forms and cryopreserved sperm has been reported, there was a of chemotherapy result in sterility. Klinefelter syndrome trend toward a lower rate of fertilization and implantation results in infertility in over 97% of men and thus every in the study by Friedler et al. Even with conservative effort should be considered for preservation of fertility in estimates, at least 50% of adult men with Klinefelter children diagnosed with Klinefelter syndrome syndrome will yield viable sperm that can be used success-fully for IVF. This represents a remarkable success in Our own experience, together with published reports, reproductive medicine. So far, the follow-up of boys born indicate that the loss of spermatogonial cells in men with from fathers with Klinefelter syndrome has not shown any Klinefelter syndrome occurs progressively and that most phenotypic abnormalities or increased risk of Klinefelter boys with Klinefelter syndrome are born with spermato- syndrome Optimal timing of sperm retrieval as gonia, which undergo massive apoptosis most likely well as optimal hormonal treatment prior to sperm retrieval during early puberty It is highly likely that during has not been established so far. Injectable testosterone early puberty there is a period during the development of may lower sperm recovery rate; however, this may simply the adolescent when spermatogenesis starts to occur and reflect that often men with Klinefelter syndrome who had sperm is present in the ejaculate. Preservation of ejacu- to be treated with testosterone injections early may have lated sperm not only offers clear benefits to our patients more severe testicular failure with delayed puberty and in respect to their biological reproductive options but also poor development during puberty. Much more data are might have important positive impact on the psychologi- needed to establish optimal hormonal treatment of men cal development of an adolescent faced with a diagnosis with Klinefelter syndrome. In our practice, we cease that for years has been synonymous with sterility. This injectable testosterone in men with Klinefelter syndrome prospect of storing the sperm facilitates the discussion of prior to any treatment for infertility. Some of the men who the impact of fertility in young men with Klinefelter are used to very high levels of circulating testosterone are syndrome, who in our practice seem to have an easier placed on topical testosterone, most commonly AndroGel time accepting the diagnosis knowing that they are not (Solvay, Marietta, Georgia, USA), which achieves physio- sterile. Having sperm available simplifies the IVF pro- logical levels of testosterone and does not suppress FSH cedure itself, avoids general anesthesia and reduces the and LH as much as injectable testosterone does. An cost to procure associated with procurement of sperm in aromatase inhibitor like Arimidex (AstraZeneca, Wilming- ton, Detroit, USA) is used in all patients for a minimum of 6months to decrease intratesticular estradiol levels and There are significant regulatory, logistic and develop- increase testosterone production. Aromatase inhibitors mental physiology issues faced by the male reproductive have been shown to increase testosterone and improve specialist offering gamete preservation. For example, it is sperm recovery rates Some practitioners use hCG to not yet established when the loss of spermatogonia occurs stimulate intratesticular testosterone and sperm pro- and if all boys undergo adequate spermatogenesis to have duction. It is possible that increasing intratesticular tes- sperm in ejaculated semen or in testicular biopsy tosterone may increase the chances of sperm recovery, but material. There is no recognized and well accepted set because of concern about concomitant increase in estradiol of markers that would allow us to decide on the best levels, the hCG should be used with aromatase inhibitors timing for the cryopreservation. If no sperm are found in ejaculate but the FSH continues to increase, then micro-surgical testicular sperm retrieval is offered. The micro- In patients who are not interested in fertility treatment, surgical biopsy is preferred because it offers the the focus is on testosterone replacement therapy, health advantage of minimal testicular damage and small maintenance, adequate bone health and decreasing the volume of testis to be obtained. The sample is examined in the operating room and the testicular tissue is cryo-preserved if spermatogonia are found. This approach Because sterility is often a main concern of parents and the allows for the highest chance for preservation of fertility.
adolescent patient, several centers including our own havedeveloped programs for the preservation of fertility in boys Several new technologies such as testis xenografting and with chromosomal aberrations using similar principals of spermatogonial stem cell transplantation are being inves- practice that are used for children and adolescents who will tigated to work around the current lack of an in-vitro undergo chemotherapy or radiation treatment culture system that would support full spermatogenesis.
We currently have an ongoing research program devoted Sperm cryopreservation in postpubertal adolescents and to maturing spermatogonia from boys with Klinefelter adults faced with the need for chemotherapy is common syndrome. Optimal time of testicular biopsy would be at a Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Andrology, sexual dysfunction and infertility time when spermatogenesis progresses through com- Thomas NS, Hassold TJ. Aberrant recombination and the origin of Klinefeltersyndrome. Hum Reprod Update 2003; 9:309–317.
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This paper brings important insight into the differences between Klinefeltersyndrome and other disorders of development and sexual differentiation.
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