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Table of Contents
REVIEW ARTICLE
Year : 2018  |  Volume : 1  |  Issue : 1  |  Page : 17-23

Testicular dysfunction and cancer: The current status


1 HOD, Army Hospital (R & R), New Delhi, India
2 B.Tech Biotechnology, Uttar Pradesh Technical University (UPTU), Lucknow, Uttar Pradesh, India

Date of Web Publication13-Feb-2018

Correspondence Address:
Pankaj Talwar
Army Hospital (R & R), Delhi Cantt, New Delhi - 110 010
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tofj.tofj_3_17

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  Abstract 


Anticancer treatments have increased the survival rates in young cancer patients in the past 15 years due to early detection. These cytotoxic therapies affect spermatogenesis temporarily or permanently because of detrimental effect they have on germ cells. Chemotherapy impairs spermatogenesis depending on the additive dose of the drugs and the combination of the drugs used for the cancer treatment. Alkytlating agents such as Cyclophosphamide has the most detrimental effect on germ cells. Radiation therapy is also associated with the risk of permanent sterility. Cryopreservation of semen and testicular tissue in the postpubertal and adult males before the cancer treatment is the only nonexperimental and efficient method to preserve future male fertility. With the advancements in cryopreservation and assisted reproductive technologies, surviving cancer patients can use their frozen sperms to raise a family.

Keywords: Cancer, chemotherapy, male infertility, radiation therapy, semen cryopreservation


How to cite this article:
Talwar P, Yadav S. Testicular dysfunction and cancer: The current status. Onco Fertil J 2018;1:17-23

How to cite this URL:
Talwar P, Yadav S. Testicular dysfunction and cancer: The current status. Onco Fertil J [serial online] 2018 [cited 2018 Oct 19];1:17-23. Available from: http://www.tofjonline.org/text.asp?2018/1/1/17/225414




  Introduction Top


Cancer is the leading cause of death in the world. The common cancers in patients of reproductive age in the males are Hodgkin's and non-Hodgkin's lymphoma, leukemia, and testicular cancer which can affect the testicular functions. The effective antimalignancy treatments (i.e., surgery, chemotherapy, and radiotherapy) have improved the survival rates of cancer patients by up to 70%–90%, making it possible for them to reproduce.[1] Early detection and type of treatment followed can help in curing one-third of cancer cases. However, anticancer treatments can cause testicular damage in men,[2] with 15%–20% of them remaining sterile in the long term up to 5 years.[3] The chances of recovery of spermatogenesis posttreatment and the speed of the recovery are dependent on the dose received and the agent used. Few studies also suggested that germinal epithelium of the adult testis is more prone to damage than the prepubertal testis,[4] implying that the factors such as maturation of testis and patient's age may greatly influence the damage at the time of cytotoxic insult.[3] Regular sperm cryopreservation, surgical sperm retrieval, and testicular tissue freezing are the most efficient methods opted for fertility preservation in male cancer patients.


  the Influence of Cancer on Spermatogenesis Top


Cancer can affect spermatogenesis through many complex interactions. It can influence hormonal alterations along with deficiencies in vitamins, minerals, and trace elements, resulting in impaired spermatogenesis.[5] Tumor-related fever or hypermetabolism and antisperm antibodies produced by autoimmune responses may also affect spermatogenesis negatively.[6] In Hodgkin's lymphoma and germ cells tumors, the hypothalamus–pituitary–gonadal function might be altered due to inappropriate endocrine secretions, resulting in impaired spermatogenesis.[7] Testicular tumors affect spermatogenesis by destroying surrounding tissue, local secretion of human chorionic gonadotropin (HCG) and other paracrine factors, intrascrotal temperature elevation, and variations in local blood flow.[8] Furthermore, alterations in β-HCG and α-fetoprotein and inhibin B levels might be responsible for the decline in sperm quality.[9]


  the Influence of Surgery on Spermatogenesis Top


Cancer surgery affects the genital or pelvic organs. It also has adverse effects on fertility by reducing sperm concentration (following unilateral orchiectomy for testicular cancer), erectile dysfunction (postprostatectomy performed for prostate cancer), or dry ejaculation, following radical retroperitoneal lymph node dissections (RPLNDs).[3] RPLND for testicular cancer patients may result in injury to the lumbar splanchnic nerves and hypogastric plexus, resulting in the permanent loss of emission and ejaculation.[10]


  the Effect of Chemotherapy on Spermatogenesis Top


Chemotherapy uses different agents for the treatment of cancer. These agents interfere with DNA and RNA synthesis and protein synthesis and prevent microtubule functions, all important for cell division. The most harmful drugs are mustard derivatives, such as busulfan and melphalan, and alkylating drugs, such as cyclophosphamide and procarbazine.[11] Azoospermia was reported for up to 4 years in men treated with platinum-based chemotherapeutic agents. Permanent sterility was reported in men with Hodgkin's lymphoma when treated with cyclophosphamide, vincristine, procarbazine, and prednisolone with recovery of spermatogenesis in 50% men when treated with cisplatin.[12] Combination chemotherapy with or without radiation and additive cyclophosphamide dosages >9.5 g/m 2 results in permanent sterility in lymphoma patients when treated with cyclophosphamide, doxorubicin, vincristine, prednisolone, and bleomycin regimen,[13] whereas multi-agent chemotherapy, such as use of mustin, vincristine, procarbazine, and prednisolone for lymphomas and leukemia, or vinblastine, bleomycin, and cisplatin for testicular malignancies, is associated with complete germ cell loss and Leydig cell dysfunction with less chances of recovery [14] [Table 1] and [Table 2].[27]
Table 1: The effect of chemotherapeutic agents on spermatogenesis (adapted from Chiba and Fujisawa)[27]

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Table 2: Chemotherapeutic agents and risk for impairment of spermatogenesis and testicular damage

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Recovery of spermatogenesis depends on the drugs used and the additive dose given. Alkylating agents such as cyclophosphamide have gonadotoxic effect. Rivkees and Crawford [15] analyzed 30 studies and examined gonadal dysfunction postchemotherapy regimens, which included a total of 116 males who had been treated with cyclophosphamide alone. Of the 116 patients, 52 (45%) had testicular dysfunction and 80% had gonadal dysfunction in postpubertal patients when treated with large doses of alkylating agents.

Cytotoxic chemotherapy causes deterioration of spermatogenesis along with transmissible genetic damage. Patients with Hodgkin's disease and testicular cancer have shown increased aneuploidy frequency in human sperms after chemotherapy.[16],[17],[18]


  Effect of Radiotherapy on Spermatogenesis Top


Radiotherapy can be administered either by electromagnetic radiation (X-rays) or corpuscular radiation (electrons) produced by a linear accelerator or by rays generated by the decay of the cobalt 60 radioisotope.[19] Testis is a radiosensitive tissue, to which even a low dose of radiation can cause a significant impairment of its function. High dose (>2.5 Gy) can cause DNA damage and cell death caused directly by irradiation or from scattered radiation during treatment.

Single-dose irradiation with doses as low as 0.1 Gy to immature cells can cause morphological and quantitative changes to spermatogonia, whereas doses >0.8 Gy result in azoospermia and <0.8 Gy result in oligospermia. Doses of 2–3 Gy cause a clear damage to spermatocytes, resulting in reduction in spermatid numbers in 60–70 days, whereas doses of 4–6 Gy can cause permanent sterility.[2]

Fractionation of radiotherapy and total body radiation are associated with higher gonadal toxicity. The testicular dose of radiation of 1.2–3 Gy administered in 14–26 fractions for Hodgkin's disease can cause azoospermia.[20] Return of spermatogenesis after radiotherapy depends on the radiation dose. At doses of >400 cGy, recovery of spermatogenesis is possible in 5 years or more and in 9–18 months if <100 cGy is administered. Up to 25% of men receiving infradiaphragmatic radiotherapy might remain permanently sterile.[12] Leydig cells are more resistant to irradiation and a dose >20 Gy may lead to hypogonadism [13] [Table 3].
Table 3: Effect of radiation on spermatogenesis[2]

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[Table 4]">  Fertility in Cancer Survivors: Summary of Individual Studies [Table 4] Top


Agarwal et al.[21] completed a case–control study on effect of cryopreservation on semen quality in patients with testicular cancer. They compared the sperm quality of 34 patients with testicular cancer and 30 controls before and after cryopreservation for 7 years. Semen quality was worst in 71.4% of patients with mixed tumors having Stage III disease compared to patients with seminomas having Stage I disease. Difference in prefreeze motility of sperms and decreased percentage motility after cryopreservation were noticed in cancer patients and controls, but the effect of cryopreservation on sperm count and motility was similar in both cancer patients and controls.
Table 4: Descriptive studies with data on semen parameters in different cancer patients

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Rofeim and Gilbert [12] evaluated 214 men with cancer and 22 men without cancer. 22.6% men out of 214 had nonseminomatous primary testicular cancer, 20.8% had Hodgkin's lymphoma, 18.8% had testicular seminoma, 12.3% had non-Hodgkin's lymphoma, 5.2% had prostate cancer, 4.3% had acute leukemia, and 16.0% had other cancers. Semen samples for all 214 men with different cancer were cryopreserved. Among 22 men without cancer, 36.4% requested cryopreservation before vasectomy and remaining opted cryopreservation for other reasons. Prefreeze and postthaw semen parameters were compared, and it was observed that there was no significant difference in semen quality in cancer patients and controls.

Dohle [11] in his study concluded that malignancies, especially germ cell tumors, can itself impair sperm quality, and in approximately 12% of men also, no viable spermatozoa is present for cryopreservation before initiation of anticancer treatments. Furthermore, the effect of treatment on spermatogenesis depends on the combination of drug used and dose given which is associated with the risk of permanent sterility.

Di Bisceglie et al.[22] analyzed the effects of oncological treatments on semen quality in 261 patients with testicular neoplasia (TN) and 219 patients with lymphoproliferative disorders (LDs). Sperm and hormonal parameters such as follicle-stimulating hormone (FSH), luteinizing hormone, and inhibin B levels were also assessed before and 6, 12, 18, 24, and 36 months after the end of the treatment. The study showed that the baseline FSH levels and sperm concentration were impaired greatly in TN and LD patients. The significant decrease in sperm concentration was noticed at months 6 and 12 after treatment. The lowest baseline sperm concentration was observed in patients with nonseminomatous TN being treated with chemotherapy (TNCT group), while patients with seminoma being treated with radiotherapy (TNRT group) showed higher baseline FSH levels compared to TNCT group, whereas inhibin B levels were higher in patients with Hodgkin's lymphoma being treated with chemotherapy and patients with non-Hodgkin's lymphoma being treated with radiotherapy than TNCT and TNRT groups. Improved recovery of sperm concentration was observed after 18 months in patients who underwent cancer treatment.

Djaladat et al.[23] conducted a systematic review on the association between testis cancer and semen abnormalities before orchiectomy and observed that testicular germ cell tumors (TGCTs) are associated with the semen abnormalities before orchiectomy and the rise in semen abnormalities in TGCT patients even outside the treatment effects; orchiectomy, radiation, and chemotherapy.

Ku et al.[24] studied semen analysis in 66 cancer patients referred for sperm cryopreservation before chemotherapy. The types of cancer present were testicular cancer (31 cases, 47.0%), non-Hodgkin' disease (10 cases, 15.1%), Hodgkin's disease (5 cases, 7.61%), leukemia (8 cases, 12.1%), gastrointestinal malignancy (5 cases, 7.61%), and musculoskeletal malignancy (5 cases, 7.61%). A significant decrease in sperm concentration and viability among different types of cancer was observed, but no significant difference in semen volume or sperm motility and morphology was noticed. It was also suggested that sperm quality might be decreased even before the start of the chemotherapy.

Depalo et al.[25] investigated the fertility preservation in 721 males with cancer. Among 721 men studied, 196 has seminoma of the testis, 173 had Hodgkin's lymphoma, 108 had mixed testicular tumors, 89 had germ cell tumors, 67 had other tumors, 42 had non-Hodgkin's lymphoma, and 46 had hematological tumors. Lower volumes and sperm count were observed in Hodgkin's lymphoma, mixed testicular tumors, and hematological tumors. Significant postthaw decrease in motility and vitality and lower fertilization rates in patients affected by testicular tumor (35.42%) and lymphoma (50%) compared to other cancers (71.43%) were observed. No significant difference in cleavage and implantation rates was observed.

DiNofia et al.[26] analyzed the semen parameters in a young cohort of 399 patients. A total of 339 (85%) men opted to cryopreserve sperm, of which 265 (78%) were successful and 60 (15%) refused to participate. Anticancer therapy before the initiation of sperm banking significantly affected a successful collection. Results showed that only 16.9% of the untreated patients were azoospermic while 84.0% of the treated patients developed azoospermia. There were differences in quality of semen parameters across age and diagnostic groups.


  Cryobanking of Spermatozoa Top


Cryobanking of sperms is the cryopreservation of the sperms at subzero temperatures to maintain the cellular life for a prolonged period. The concept of cryobanking of sperms is not new. It is the extensively accepted and practiced method of infertility treatment. Many studies have reported that long-term cryopreservation does not affect the sperm motility, viability, and morphology.[28] The effect of snow on sperm, i.e., slowing of sperm motions wasfirst reported by Spallanzani in 1776.[29] An Italian scientist, Montegazzo in 1866,[30] described the possibility of establishing cryobanks for frozen human semen to continue the legal heir of soldiers dying on a battlefield. The major foundation in sperm preservation was laid by Polge et al. in 1949,[31] where they showed that glycerol (a permeating solute) can also be used as a cryoprotectant. In 1953, Sherman and Bunge [32] used dry ice for freezing and storing semen and reported thefirst successful human pregnancy, resulting from insemination with frozen human semen with 67% survival rates. On April 9, 1954, the Cedar Rapids Gazette [33] published a scoop named "Fatherhood after Death Has Now Been Proved Possible" declared the birth of three history-making babies using semen that had been frozen and preserved before use. In 1964, Sherman [34] in one of his discoveries suggested that preserving human sperm in liquid nitrogen at −196°C was much superior to storage at −75°C as there is no loss of motility for 1 year, whereas there was decline of motility after storage at −75°C. Before 1964, all pregnancies were produced from short-term preservation of sperms, whereas Perloff et al.[35] in 1964 reported pregnancies from frozen-thawed sperms stored for 1–5.5 months. Finally, in 1969, Behrman and Ackerman [36] described new and efficient method of freezing semen by immersing it into liquid nitrogen at −196.5°C which has improved the fertilizing capacity of frozen semen and led to the emergence of a number of commercial human sperms banks.


  Cryobanking of Testicular Tissue Top


Chemotherapeutic agents and radiation therapy used to treat cancers and other nonmalignant diseases result in loss of spermatogonial stem cells in the testis. Sperm cryopreservation is thefirst treatment suggested for the fertility preservation in adolescent males. In prepubertal boys, testicular tissue cryopreservation or harvesting and banking of isolated spermatogonial stem cells can be proposed to preserve their future fertility.[37] Cryoprotectants used for testicular tissue preservation were propanediol and glycerol. Spermatogenesis can be recovered by the transplantation of the frozen-thawed cells back to the testes.[38] First transplantation of the testicular tissue was performed in 1994 on mice where the recipient mice produced transgenic offspring. As many health risks and other factors were related to transplantation in mice as well as in humans, xenotransplantation or in vitro spermatogenesis could be one of the alternatives suggested to obtain malignant cell-free spermatozoa.[39] Spermatogonial stem cells depletion in mid-puberty occurs in Klinefelter syndrome which can lead to infertility, so to preserve fertility in such patients testicular tissue cryopreservation could be one of the proposals.[40] However, surgical sperm retrieval, i.e., microdissection testicular sperm extraction, could be the method used to treat infertility in cancer patients with persistent postchemotherapy azoospermia.[41]


  Conclusion Top


Currently, regular sperm cryopreservation, surgical sperm retrieval, and postpubertal testicular tissue freezing are the only effective methods of fertility preservation in males being treated for cancer and are recommended for cancer patients of reproductive age. A study in 2014 described that sperm motility decreases postcryopreservation but an increase in motility of sperms was illustrated as time progressed.[42] Therefore, oncologists should offer sperm banking to the adolescents and young adults who are at risk of infertility before initiation of therapy. Due to recent advances in ART technology and sperm cryopreservation procedures, even men with extremely reduced sperm count and motility can biologically father a child. It is recommended that sperm should be preserved prior the initiation of cancer therapy, because the quality of the sample and sperm DNA integrity may be compromised even after a single treatment session.[43]

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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