Abstract
Azoospermia is a rare, irreversible complication in the UK resulting from heavy infection of schistosomiasis of the male genital tract. Adequate anti-bilharzial treatment and close follow-up with urological assessments should reduce the risk of chronic ill health. This patient contracted schistosomiasis following swimming in lakes in Uganda, Africa, which resulted in azoospermia and reversible loss of libido. The couple underwent treatment at our assisted conception programme with testicular sperm extraction and intracytoplasmic sperm injection (ICSI). The female partner conceived in her second stimulated ICSI cycle and had a spontaneous vaginal delivery at term.
BACKGROUND
Severe manifestation of schistosomiasis can cause intense granulomatous epididymitis and inhibition of spermatogenesis causing male infertility. Where the cause of azoospermia is due to schistosomiasis, surgical sperm retrieval followed by intracytoplasmic sperm injection (ICSI) should be considered.
CASE PRESENTATION
Presenting features
The couple were referred to our assisted conception unit by their general practioner following two azoospermic semen analyses and 9 months of primary infertility. The male partner had normal general and abdominal examination. Examination of his testes showed testicular volumes of 10 ml on right and 8 ml on the left, with no epididymal swelling or tenderness. After investigations for the female partner, the couple were keen for ICSI treatment cycle.
Past history
The male partner had heavy infestation of schistosomiasis at the age of 28 years after swimming in lakes in Uganda, which resulted in reduction of testicular volume that was confirmed clinically and from ultrasound examination of his testes. He had significant loss of libido during his illness. He had three courses of praziquantel to treat his schistosoma infection.
INVESTIGATIONS
The female partner had normal fertility investigations. The male partner’s semen analyses demonstrated persistence of azoospermia with normal levels gonadotropins and normal testosterone suggestive of obstructive azoospermia.
Endoscopic rectal biopsy at the time of his clinical diagnosis in 1994 confirmed heavy infestation with ova of schistosoma.
His testicular ultrasound examination revealed normal testicular morphology with no upper tract dilatation and flexible cystoscopy examination showed normal bladder findings. The investigations confirmed no active schistosoma infection. He had screening for sexually transmitted diseases and the results were negative. His karyotype was 46 XY.
DIFFERENTIAL DIAGNOSIS
Azoospermia with normal gonadotropins and normal testosterone was suggestive of obstructive azoospermia. The differential diagnosis was non-obstructive azoospermia because of incomplete recovery of changes in testicular volume but this was unlikely because of normal gonadotropins.
TREATMENT
The couple underwent two cycles of stimulated fresh cycles of ICSI and two cycles of frozen embryo thaw cycles. A right scrotal exploration and surgical sperm retrieval was undertaken on the day of egg recovery during fresh cycles of treatment. On both occasions it was difficult to gain access to the right epididymis because of dense peritoneal adhesion to his testicular tunica and testicular biopsy was taken from two sites from his right testicle. Although the number of sperm was low from the testicular biopsy, this was adequate for ICSI. However, this was deemed of too poor quality for cryopreservation.
The female partner had a miscarriage with her first stimulated cycle, unsuccessful outcome with her first frozen embryo cycle and spontaneous early miscarriage with her second frozen embryo cycle. In her second stimulated fresh ICSI cycle, she had ovarian stimulation using Puregon (recombinant follicle stimulating hormone) and Cetrorelix (gonadotropin antagonist). She had two good quality embryos for transfer.
OUTCOME AND FOLLOW-UP
The female partner conceived with her second stimulated ICSI cycle. Her pregnancy was uneventful and she delivered a healthy child at term. The couple are planning to use their cryopreserved embryos for a thaw cycle in the next 12 months.
DISCUSSION
Azoospermia resulting from schistosomiasis is rare in the UK. In the above case, a testicular biopsy (TESE) and ICSI offered the only chance of fertility treatment for this couple. The success rate from ICSI treatment depends on the age of the women during treatment. Women less than 35 years old have a higher success rate.1 There is no significant difference in fertilisation rates when ICSI is carried out using testicular sperm compared with ICSI using epididymal sperm in obstructive azoospermia.2
Schistosomiasis, also known as bilharziasis, is a parasitic disease that can lead to chronic ill health. Causal agents of the disease are fluke worms (schistosomes). A person infected with schistosomiasis expels eggs in their faeces or urine. On contact with water, the eggs hatch and release larvae called miracidia. If the miracidia find the right type of fresh water snail they use it to multiply in several cycles, eventually producing thousands of new parasites, called cercariae, which the snail then releases into the surrounding water. Humans become infected when they come into contact with contaminated water (during wading, swimming, washing). Cercariae penetrate the skin and make their way into the person’s bloodstream. Over the next 30–45 days, the parasite transforms itself into a long worm—either male or female—which makes its way to the intestine or bladder. In their final location, the female lays between 200 and 2000 eggs per day over an average of 5 years. Only half of the eggs produced are excreted in the faeces or urine. The rest become trapped in the body tissues and this causes major damage.3
Urogenital schistosomiasis, caused by schistosoma haematobium, is a major health problem in many parts of Africa. Infertility may develop in males with schistosoma haematobium infection of the genital organs. Occlusion of the spermatic venous plexus by ova and subsequent granuloma formation may result in testicular infarction. Azoospermia with a chronic inflammatory eosinophilic infiltrate in the interstitium of the testes may develop. Infertility may be prevented by treatment with praziquantel and early diagnosis of schistosomiasis is essential to avoid the development of infertility.4
Aal H et al reported presence of anti-sperm antibodies in sera of 35% of the patients compared with none of the control group and showed evidence of autoimmune response in individuals with bilharziasis.5 Once the disease has progressed to the granuloma stage, the damage is irreversible. Because schistosomas do not multiply in the human host, reinfection is always the result of new contact with an infected environment.3
Seminal vesiculitis can cause haematospermia, painful ejaculation, burning micturition and low backache. Patients with bilharzial prostatitis often complain of diminished sexual libido, weak erection or rapid ejaculation.6 Toresi et al suggested that microscopic examination of semen might provide additional means of diagnosing infection with schistosoma haematobium in addition to routine urine microscopy.4 Transrectal and transscrotal ultrasound examination can be offered in men with schistosoma haematobium infection to check for involvement of the prostate and seminal vesicles.7 Ghoneim proposed that severity of manifestation and relative incidence of complications would change significantly with mass treatment using the new and safe orally administered anti-bilharzial agent praziquantel.6
It is highly likely that severe infestation with schistosomiasis has caused severe inflammation of the epididymis leading to obstructive azoospermia. In the case of the male partner, reduction in testicular volume and incomplete recovery of changes in the testicular volume together with findings of dense adhesions during the scrotal exploration are highly suggestive of causal link between this patient’s obstructive azoospermia and previous infection with schistosomiasis.
In conclusion, schistosomiasis resulting in infertility is rare in the UK. Infertile men with a history of schistosomiasis should be referred to a secondary/tertiary centre for assessment and treatment.
LEARNING POINTS
Physicians should be aware of possibility of schistosomiasis in holidaymakers who have been to endemic areas.
Schistosomiasis is an important cause for sub-fertility in endemic areas.
Early diagnosis and treatment with praziquantel can potentially prevent infertility.
Infertile men with complications resulting from schistosomiasis should be referred to an infertility clinic for assessment and assisted conception treatment.
Clinicians and travellers should be aware that although complications from schistosomiasis are not common, they can be devastating and irreversible.
Acknowledgments
The authors would like to acknowledge all the staff at Assisted Conception Unit at Edinburgh for their continued support.
Footnotes
Competing interests: none.
Patient consent: Patient/guardian consent was obtained for publication.
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