Stress and semen quality in an in vitro fertilization program*

FERTILITY AND STERILITY Copyright© 1987 The American Fertility Society

Vol. 48, No.4, October 1987 Printed in U.S.A.

Stress and semen quality in an in vitro fertilization program*

Keith L. Harrison, M.App.Sci. t Victor J. Callan, Ph.D.:j: John F. Hennessey, M.D.t Queensland Fertility Group, Brisbane, and University of Queensland, St. Lucia, Queensland, Australia

While a greater understanding is emerging of the psychological stresses of infertility treatment, little is known about the specific effects of these stresses upon the quality of the semen sample used at the fertilization stage in an in vitro fertilization and embryo transfer (IVF-ET) program. This study evaluated two semen profiles for each of 500 couples on IVF treatment. The first semen sample was collected in the couple's pre-IVF workup, and the second sample was given by husbands after ovum aspiration, and used to inseminate the eggs in vitro. Comparisons of samples revealed that sperm density, total sperm count, and both quantitative and qualitative sperm motility were significantly lower in the second sample presented for IVF. For 91% of cases, there was no change across samples in assigned fertility index categories. However, 14 cases revealed a deterioration, falling from normal to pathologic, while 21 cases changed in semen character from normal in IVF workup to severely pathologic in IVF treatment. For these cases, the incidence of total fertilization failure in the procedure also dramatically increased. Several steps are discussed in the better management of patients with such declines in semen quality. Fertil Steril 48:633, 1987

In dealing with infertility, the infertile couple is grappling with a problem that stresses them physically, financially, and emotionally. They are stressed by a loss of choice and control over the direction of their lives, some feeling damaged and defective over their personal and sexual identities.1-3 Little is known about the stresses experienced by couples within infertility treatment, or the possible effects of the stresses inherent in in vitro fertilization and embryo transfer (IVF-ET) treatment upon the quality of the semen sample, and the chances of fertilization.

Received September 18, 1986; revised and accepted June 3, 1987. * Presented at the second annual meeting of the European Society of Human Reproduction and Embryology, Brussels, Belgium, June 22 to 25, 1986. t Queensland Fertility Group, Wesley Hospital. :j: Reprint requests: Victor J. Callan, Ph.D., Department of Psychology, University of Queensland, St. Lucia, Queensland, Australia. Vol. 48, No.4, October 1987

As several reviews illustrate, stress does have negative effects on sperm count, motility, and morphology.4-6 Palti 7 listed impotence, sham ejaculation, retrograde ejaculation, and oligospermia as four types of disturbances associated with psychological factors in male infertility. A number of studies have shown the effect of stress upon testicular function. Depressed plasma testosterone levels are linked with stress in combat, combat training, and business activities. 5 •8 Nonhuman primates subjected to immobilization stress suffer spermatogenic arrest, 9 while similar spermatogenic damage occurs in condemned persons who have a prolonged wait before execution. 10 As Moghissi and W allach6 note, emotional stress either because of the experience of infertility or the evaluation and treatment of infertility may exert its influence through autonomic or neuroendocrine control of the male reproductive system and_ add to oligospermia. During an infertility evaluation, they remark that the stress of evaluation may result in variations in semen quality. 6 Harrison et al.

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633

To maximize the chances of infertile couples gaining a pregnancy, it is critical to any program's success to understand the couple's perception of critical procedures, and to examine the effects of stress from within the program upon the couple's chances of a successful outcome. The present study examines this latter issue through an analysis of the quality of semen samples taken at two stages of the IVF-ET program: in an early pre-IVF-ET workup when the stresses upon couples are low, and at the egg aspiration and fertilization stage of the actual treatment cycle. The task was to determine whether the second sample provided by husbands within the IVF treatment cycle differed from the earlier sample, and whether any change affected the chances of a couple's success with IVF treatment.

which provides four classifications of ejaculatesnormal, doubtful, pathologic, and severely pathologic-and the total normally motile sperm count obtained by applying the percentage of spermatozoa showing good progressive motility to the total sperm count. Other analyses involved comparisons of the samples with guidelines proposed for the minimal requirements for ejaculates for IVFY Performance of the sperm was judged on the percentage of ova fertilized in vitro (fertilization rate) and the incidence of total fertilization failure. Such a failure emerges when all ova obtained from a woman failed to be fertilized by her husband's spermatozoa. For the purposes of the study, ova showing immaturity by not having extruded the first polar body were excluded. RESULTS

MATERIALS AND METHODS. Subjects

For couples to enter the IVF-ET program, the infertility must have been fully investigated to determine its etiology, and other potential treatment regimes must have been exhausted. IVF-ET is perceived as then offering the couple's best chance of a pregnancy. In 1985, the IVF group performed 1000 laparoscopic ovum aspirations with a fertilization rate of around 65%, and an ongoing pregnancy level of 17%. At present, couples must wait at least 12 months before a first IVF attempt. Before commencing an IVF cycle, couples are counseled on details of the procedure and are offered literature summarizing this information. Sample Selection and Procedure

Two semen profiles were evaluated for each of 500 couples on IVF treatment between October 1985 and April 1986. The first semen sample was collected in their pre-IVF workup, usually in the cycle preceding the treatment cycle. The second semen sample was given after ovum aspiration and used to inseminate the eggs in vitro. The time difference between both samples was approximately 5 weeks. Comparisons between the two samples were made on parameters recommended by the World Health Organization. 11 These indices included semen volume, sperm density, total sperm count, sperm motility, grade of motility, and the number of morphologically abnormal forms. Additional parameters included the fertility index of Eliasson, 12 634

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Stress and semen quality in IVF program

Table 1 presents the mean values for the various semen parameters for the two groups. Mean differences were analyzed by t-tests, while simple chisquare was used to test differences between the frequencies reported within tables. As can be seen in Table 1, sperm density, total sperm count, and qualitative sperm motility were significantly lower in the second semen sample presented for IVF. Mean total normally motile sperm count and the mean fertility index were both significantly reduced in the IVF samples. Mean sperm morphology and mean semen volume were unchanged. The next step was to determine, according to the fertility index categories, whether a reclassification occurred with the second sample. In this analysis,

Table 1 Semen Parameters for Pretreatment and IVF Sample

n Volume Sperm density" Total sperm countb Motility (total)b Motility (grade)' Morphology(% abnormal) TNMSC"·d Fertility indexb

Mean values pretreatment sample

IVF sample (standard deviations)

500 3.6 ml (±1. 7) 69 X 106 /ml (±45) 265 X 106 (±148) 63% (±15%) 2.82 (±.42)

500 3.5 ml (±1.5) 61 X 106 /ml (±37) 225 X 106 (±172) 59% (±18%) 2.71 (±.52)

30.4% (±11.7%) 98 X 106 (±88) 2.97 (±5.68)

31.3% (±12.3%) 86 X 106 (±86) 4.11 (±6.41)

P < 0.05. p < 0.001. 'p < 0.01. a

b

d

TNMSC, total normally motile sperm count.

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Table 2

Change in Fertility Index with IVF Sample

Unchanged n(%) Fertilization rate-% Total fertilization failure-%

454 (91) 64 10

Improved pathologic to normal

Table 3

14 (3) 60 14

5 (1)

61

the category labeled doubtful was included within the normal category. Table 2 presents the fertilization rate and percentage of cases within each classification. In the vast majority of cases (91% ), there was no change in the index classification. There was an improvement in five cases. Fourteen cases, however, revealed a deterioration, falling from normal to pathologic. Nevertheless, their fertilization rate and incidence of total fertilization failure was not significantly different from the unchanged group. In 21 cases, there was a change in semen character from normal in the IVF workup to severely pathologic in the IVF treatment. While the fertilization rate did not significantly change, the incidence of total fertilization failure trebled. Similar results emerged for the six patients whose semen sample changed from pathologic to severely pathologic. However, these cases should be compared with patients who were classified as severely pathologic on both occasions. Their fertilization rate was 24% and the incidence of total fertilization failure was 52%. In their definition of minimal requirements for ejaculates to be used in IVF, Riedel et alY proposed a minimum sperm density of 5 X 106 /ml, with at least 30% showing normal motility: a normally motile sperm concentration of 1.5 X 106 /ml. When the two samples of semen were compared along these criteria (see Table 3) and both samples were above minimal requirements, the fertilization rate was 64%. There was only a 10% incidence of fertilization failure. In the 22 samples where there was evidence of deterioration, the fertilization rate was significantly reduced to 47%. As can be seen, there was a doubling of the rate of total fertilization fail-

Normal to severely pathologic

Normal to pathologic

Pathologic to severely pathologic

21 (4) 56

6 (1)

55 33

33

ure. When there was an improvement to above the 1.5 X 106 /ml level, fertilization results were marginally better. As would be expected, results were poor when both samples recorded concentrations below minimum requirements. DISCUSSION

Results from this study seem to indicate the need to monitor the emotional pressures upon couples as they enter infertility treatment. Our data suggest that the stress imposed upon some men by proceeding through IVF-ET appears to be associated with some reduction of their semen quality. This is shown in significant decreases in mean total sperm count, grade of motility, and fertility index. Although there is inherent variation in semen analysis parameters in any individual, deterioration in fertility index category was eight times more common than improvement between IVF workup and the IVF treatment cycle. Depending upon the criteria used, there is a more severe deterioration in about 4% to 8% of men. This reduction of sperm quality not only slightly reduces chances of fertilization of aspirated eggs, but more seriously doubles the incidence of total fertilization failure. However, while a decline in semen quality to a severely pathologic state negatively affects fertilization rates, the prognosis is still better than the poor chances of fertilization among men in whom both semen samples were severely pathologic. As the data suggest, the strongest indicator of a man's fertilizing potential is the best sample produced by him in recent times rather than the quality of the one produced for IVF. These interpretations, how-

Normally Motile Sperm Concentration Lower Limit: 1.5 X 106 /ml

n (%)

Fertilization rate-% Total fertilization failure-%

Vol. 48, No.4, October 1987

Both samples >1.5 X 106 /ml

Deterioration to <1.5 X 106 /ml

Both samples <1.5 X 106 /ml

Improvement to >1.5 X 106 /ml

451 (90) 64 10

22 (5) 47 23

21 (4) 19 62

6 (1) 52 16

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ever, must be considered in light of no objective criteria being used to assess the stress on husbands. Our findings need to be followed up with a design that incorporates stress measures that may be correlated with various semen parameters. At least from these initial findings, the most stressed men would be expected to demonstrate the greatest deteriorations in semen quality. A number of practical steps can be implemented within an IVF-ET program to better manage and minimize the emotional stresses upon couples, or to reduce the chances of treatment accentuating what is often labeled their "crisis of infertility." 2 There is little that can be done to alter the sense of drama surrounding an IVF treatment cycle. Everything is dependent upon the accurate timing of ovulation, so that, in a relatively short period, there are blood tests, hormone injections, and, when ovulation is expected, hospitalization, egg pickup, fertilization, and transfer of fertilized eggs. While the vast majority of husbands are able to provide the semen sample for IVF with apparent ease, a small number experience considerable difficulty. To reduce these problems, husbands could be allowed to return to their homes to collect the sample or to their motel room if they are from outside the city. There is also the need for hospitals with IVFET programs to provide a room that may be used by husbands either alone or with their wives to produce the semen sample. The object of all this is to obtain the best possible specimen with the greatest possible ease, as close as possible to the optimum insemination time. If major problems can be foreseen, a sample of frozen semen collected in the pre-IVF workup can be used. These pretreatment

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Stress and semen quality in IVF program

semen samples are often better along a number of parameters.

REFERENCES 1. Mazor MD: Emotional reactions to infertility. In Infertility: Medical, Emotional and Social Considerations, Edited by MD Mazor, HF Simons. New York, Human Sciences Press, 1984, p 23 2. Menning BE: The emotional needs of infertile couples. Fertil Steril 34:313, 1980 3. Seibel MM, Taymor ML: Emotional aspects of infertility. Fertil Steril 37:137, 1982 4. Bents H: Psychology of male infertility: a literature survey. Int J Androl 8:325, 1985 5. McGrady AV: Effects of psychological stress on male reproduction: a review. Arch Androl 13:1, 1984 6. Moghissi KS, Wallach EE: Unexplained infertility. Fertil Steril 39:5, 1983 7. Palti Z: Psychogenic male infertility. Psychosom Med 31:326, 1969 8. Steeno OP, Pangkahila A: Occupational influences on male fertility and sexuality. Andrologia 16:93, 1984 9. Cockett ATK, Elbadawi A, Zemjanis R, Adey WR: The effects of immobilization on spermatogenesis in subhuman primates. Fertil Steril 21:610, 1970 10. Stieve H: Der Einfluss des Nervensystems auf Bau und Tatigkect der Geschlec~tsorgane des Menschen. Stuttgart, Thieme, 1952 11. World Health Organization: Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction. Edited by MA Belsey, KS Moghissi, R Eliasson, CA Paulsen, AJ Gallegos, MRN Prasad. Singapore, Press Concern, 1980 12. Eliasson R: Parameters of male fertility. In Human Reproduction: Conception and Contraception, Edited by ESE Hafez, TN Evans. New York, Harper & Row, 1973, p 39 13. Riedel HH, Baukloh V, Mettler L: Minimal requirements for ejaculates used for in vitro fertilization. Arch Androl 12:69, 1984

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