P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Archives of Sexual Behavior, Vol. 30, No. 1, 2001
Sexual Functioning After Treatment for Testicular Cancer—Review and Meta-Analysis of 36 Empirical Studies Between 1975–2000 Grieteke Jonker-Pool, M.A.,1,2,7 Harry B.M. Van de Wiel, M.A., Ph.D.,1,3 Harald J. Hoekstra, M.D., Ph.D.,4 Dirk Th. Sleijfer, M.D., Ph.D.,5 Mels F. Van Driel, M.D., Ph.D.,6 Jean P. Van Basten, M.D., Ph.D.,4 and Heimen Schraffordt Koops, M.D., Ph.D4
Literature concerning sexual functioning after treatment for testicular cancer from 1975–2000 is reviewed. After a literature search in Medline and Psylit was conducted, as well as a search for cross-references made, a meta-analysis was performed. To describe sexual functioning, several aspects of the sexual response cycle were used: sexual desire, sexual arousal, erection, and orgasm; ejaculatory function, sexual activity, and sexual satisfaction were used as well. The number of patients included in the studies as well as treatment modalities were taken into account. A total of 36 relevant studies was screened (28 retrospective and 7 prospective studies), concerning 2,786 cases of testicular cancer. Meta-analysis revealed that ejaculatory dysfunction was reported most frequently and was related to surgery in the retroperitoneal area. Erectile dysfunction was related to irradiation, but was reported least frequently. Other sexual functions were not related to treatment modality. Meta-analysis revealed no deterioration of sexual functioning in the course of time, except a decrease in sexual desire and an increase in sexual satisfaction. Retrospective studies reported more sexual dysfunction than did prospective studies. Detailed analysis of separate studies, however, revealed a wide variation in reported sexual morbidity, as well as in assessment methods. Somatic consequences of disease and treatment may reduce ejaculation; however, 1 Department
of Medical Psychology, Groningen University Hospital, The Netherlands. Centre for Health Care Research, Groningen, The Netherlands. 3 Dutch Institute for Social Sexological Research, Utrecht, The Netherlands. 4 Department of Surgical Oncology, Groningen University Hospital, The Netherlands. 5 Department of Medical Oncology, Groningen University Hospital, The Netherlands. 6 Department of Urology, Groningen University Hospital, The Netherlands. 7 To whom correspondence should be addressed at Department of Medical Psychology, Groningen University Hospital, PO Box 30.001, 9700 RB Groningen, The Netherlands; e-mail:
[email protected]. 2 Northern
55 C 2001 Plenum Publishing Corporation 0004-0002/01/0200-0055$19.50/0 °
P1: FZN Archives of Sexual Behavior [asb]
56
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
other aspects of sexual functioning are not clearly related to disease- or treatmentrelated factors and may instead refer to a psychological vulnerability caused by one’s confrontation with a life-threatening, genito-urinary disease, such as testicular cancer. KEY WORDS: testicular cancer; sexuality; literature review; meta-analysis.
INTRODUCTION In the western countries testicular cancer is the most prevalent malignancy in males aged between 20 and 40 (Wingo et al., 1995). Although the disease is relatively rare, its incidence has profoundly increased in the past half century (Harding et al., 1995; Hoff Wanderas et al., 1995). In northern Europe the incidence is 7.5/100,000 inhabitants per year (Adami et al., 1994). In The Netherlands the incidence is 4.7/100,000 inhabitants per year (Visser et al., 1996). Incidence rates in non-Western countries are much lower (Kenya 0.08/100,000 and India 0.2/100,000 inhabitants per year, respectively) (Zimmerman and Kung’u, 1978; Raina et al., 1995). Generally, two types of testicular cancer are distinguished: 40% concerns seminoma tumors (ST) and 60% concerns nonseminoma testicular germ cell tumors (NSGCT). The highest incidence rate of seminomas is between 30 and 35 years of age, whereas nonseminomas are mainly diagnosed between 25 and 29 years of age (Hadu, 1979; Hoff Wanderas et al., 1995). Treatment is based on the histology of the primary tumor and on the results of staging investigations (Fung and Garnick, 1988; Peckham et al., 1983). In the case of a seminoma tumor, hemi-orchiectomy is followed by radiation therapy (RT). A stage I nonseminoma, currently, is successfully treated by hemi-orchidectomy alone, followed by frequent surveillance, the so-called “Wait & See” policy (W&S) (Gels et al., 1995). Disseminated disease is currently treated with cisplatin-based PCT and the resection of only residual retroperitoneal tumor mass (RRRTM). It should be noted that formerly a more invasive resection in the abdominal of retroperitoneal lymph nodes (RPLND) was performed (Gels et al., 1997). With the introduction of cisplatin-based polychemotherapy, followed by tumor-reductive surgery, the survival rate has increased to almost 90% (Gels et al., 1997). This increase in the survival rate has advanced the awareness of the long-term sequelae of diagnosis and treatment. As the disease affects relatively young men, in their genital area, it may not be surprising that in the past decades, several authors have investigated aspects of sexual functioning and fertility after treatment for testicular cancer. Unfortunately, however, it is very difficult to make a clear picture based on the outcomes of the existing studies. For instance, in the literature, loss of sexual desire varies between 2 and 69% and ejaculatory dysfunction between 17 and 100%. This wide range of reported dysfunctioning makes it difficult to use empirical results as a sound basis for patient education and counselling. To create a more
P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
19:29
Sexuality and Testicular Cancer: Literature Review
Style file version Nov. 19th, 1999
57
comprehensive picture, it was decided to perform a meta-analysis on the existing data. METHODS Relevant literature was collected by performing a computer-based search (Medline, Psylit) of publications from 1975 to the end of 1999, with the following keywords: testicular cancer, cancer of the testicles, sexual functioning, sexuality, and sexual rehabilitation. As a second step all references given in the selected publications were examined. The following aspects of sexual functioning, based on Masters & Johnson (Masters and Johnson, 1966; Kaplan, 1979) and the DSM-IV (American Psychiatric Association [APA], 1994), were used to screen the literature: loss of sexual desire (libido); male erectile disorder; orgasmic dysfunction (in terms of delay or less intense orgasmic joy); and premature, delayed, or absent ejaculation. Some other relevant aspects of sexual functioning, frequently mentioned in the literature, were added: sexual activity and sexual satisfaction. A meta-analysis of the results was performed to obtain an insight into the ranges of outcomes of the reviewed field and into the eventual sources of heterogeneity. Means were weighted for number of patients included per study. To identify trends, outcomes of dependent (and co-) variables were simply interrelated across studies. RESULTS Entire Patient Population In the literature from 1975, a total of 29 retrospective and 7 prospective studies was found (see Appendix), which concerned, respectively, 2,437 and 338 cases that could be used for meta-analysis. Statistical analysis of the reported data, weighted by the number of patients per study, revealed the following mean scores (in rounded percents) on sexual dysfunctioning for the entire patient population (outcomes of prospective studies in parentheses): – loss of desire: 20% (11%) – male erectile disorder: 11.5% (14%) – orgasmic dysfunction: 20% (9%) – ejaculation disorder: 44% (51%) – decrease in sexual activity: 24% (13%) – sexual dissatisfaction: 19% (18%) The mean age was 35 (30.3) years and the mean follow-up period 6.9 (2.0) years. The mean response rate was 77% (88%). For more detailed results, that is, exact
P1: FZN Archives of Sexual Behavior [asb]
58
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops Table I. Overview of Meta-Analytic Outcomes of 36 Reviewed Studies Number of studies
Total patients n = 2,775 (100%)
Range
Weighted meana
SD
retrospect prospect
29 7
2,437 (88) 338 (12)
16–264 29–76
83.4b 53.5b
57.6 19.7
retrospect prospect Follow-up retrospect prospect Response retrospect prospect Desire retrospect prospect Erection retrospect prospect Orgasm retrospect prospect Ejaculation retrospect prospect Sexual Activity retrospect prospect Sexual retrospect Dissatisfaction prospect
24 5 24 7 25 5 15 4 20 6 13 2 19 5 10 1 16 2
2138 (88) 248 (73) 1988 (82) 338 (100) 2101 (86) 248 (73) 1521 (62) 147 (43) 1792 (74) 239 (77) 1251 (51) 71 (21) 1836 (75) 239 (71) 990 (41) 31 (9) 1400 (57) 93 (28)
20–77 years 17–51 years 0.25–25.5 years 0.25–3 years 43–100% 60–100% 2–69% 10–13% 0–35.2% 0–29% 0–53% 9%–? 17–100% 30–81% 13–40% 13%–? 4–38% 18%–?
34.7 years 30.3 years∗ 6.9 years 2.0 years∗ 76.6% 87.9%∗ 19.6% 11.2%∗ 11.5% 13.8% 19.8% 9.0%∗ 44.2% 51.3%∗ 24.2% 13%∗ 19.1% 18.0%∗
4.1 1.7 4.2 1.1 15.8 18.4 16.5 1.5 10.7 11.5 13 — 24.5 19.4 6.8 — 10.3 —
Age
Indicated are the number of studies in which the concerning variable was reported and the number of patients included in these studies. a Weighted mean: mean score of total of studies, weighted by sample-sizes of the studies involved. b Mean number of patients not weighted by number of patients. ∗ Using t-test to compare means of retro- and pro-spective studies; all means, except concerning erectile dysfunction, were significantly different, p < .001.
percentages, ranges, and standard deviations (SDs), see Table I; note that SD values of the reported sexual functions are broad, and that ranges vary widely between studies. Outcomes of Specific Treatment Modalities The study of outcomes of specific treatment modalities is important because it may highlight differences in sexual morbidity. In part of the studies, outcomes specified per treatment modality were reported. This concerned about half of the patients included in retrospective studies (n = 1,311 out of a total n = 2,437; Table II and Figs. 1–5). Only three out of seven prospective studies reported outcomes specified according to treatment modality; because of this low number the outcomes of these studies cannot be compared. Despite wide ranges and standard deviations (SD) in reported data concerning sexual dysfunction, meta-analysis revealed significant differences between treatments with respect to all sexual variables. The following mean scores (in rounded percentages) were found per specific
a RT:
radiotherapy, PCT: polychemotherapy, RPLND: retroperitoneal lymphnode dissection.
One-way Anova P: Scheff´e-test (group-differences with p < .05)
21.4 (13.8): 0–54.5 n = 846 0.0000 5—Rest of groups
50.9 (28.1): 0–100 n = 1108 0.0000 All groups different
15.9 (11.9): 7–44 n = 108 39.9 (14): 0–60 n = 273 28.4 (16.5): 0–64 n = 150 62.2 (21.5): 40.5–95 n = 358 80.5 (27.5): 38–100 n = 193 60 (0) n = 26
Ejaculatory Problems
27 (10.8): 0–40 n = 431 + ? 0.0000 All groups different, except 2 & 4
10.5 (0) n = 59 28.5 (11): 0–39 n = 85 34.3 (10.2): 8–40 n = 103 28.5 (3.9): 26–40 n = 178 0 (0) n=6 n=?
Reduced Activity
16.0 (9.2): 0–33 n = 583 + ? 0.0000 1—2 & 4
n=?
7.5 (1.4): 7–11 n = 75 15.8 (11.8): 7.5–33 n = 126 14.5 (6.2): 0–19 n = 137 19.9 (7.8): 15–33 n = 203 n=?
Sexual Dissatisfaction
19:29
13.52 (10.1): 0–48 n = 1013 0.0000 2—1,3,4,5
23.8 (14.3): 12–42.5 n = 101 22.5 (8.1): 14.5–38 n = 236 28.3 (6): 20–40 n = 67 21.5 (10): 9–39.5 n = 242 10.6 (16.3): 0–54 n = 174 54.5 (0) n = 26
Reduced Orgasm
October 19, 2000
22.85 (18.3): 2–69 n = 778 0.0000 All groups different, except 2 & 4
7.4 (10.1): 3.5–33 n = 75 24.8 (18.8): 0–48 n = 175 11.1 (5.8): 0–20 n = 150 11.3 (9.6): 0–31 n = 407 9.7 (8.7): 0–20 n = 180 23.5 (0) n = 26
Loss of Erection
PL186-228372
Total mean treatments number 1–6:
24.8 (16.8): 12–48.5 n = 108 14.1 (8.9): 2–22 n = 131 24.9 (3.6): 21–28.5 n = 137 13.4 (7.1): 2–21 n = 313 65.7 (1.6): 65–69 n = 89 n=?
Loss of Desire
Archives of Sexual Behavior [asb]
1. Surveillance (patients from 4 studies) n = 108 (8.2%) 2. RTa (patients from 9 studies) n = 417 (32%) 3. PCT (patients from 6 studies) n = 160 (12%) 4. PCT + surgery (patients from 9 studies) n = 404 (31%) 5. RPLND (patients from 6 studies) n = 193 (15%) 6. PCT + RPLND + RT (patients from 1 study) n = 26 (2%)
Total n = 1311 (100%)
Mean % (SD): range available n
Table II. Overview of Outcomes of Sexual Functioning Per Treatment-Modality (Means Weighted by Number of Patients Per Subgroup)
P1: FZN Style file version Nov. 19th, 1999
Sexuality and Testicular Cancer: Literature Review 59
P1: FZN Archives of Sexual Behavior [asb]
60
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
Fig. 1. Surveillance (4 studies, n = 108).
Fig. 2. Irradiation (9 studies, n = 417).
treatment modality (for more detailed results, i.e., exact percentages, SDs, ranges, and number of observations, see Table II). Surveillance (Concerning Four Studies, n = 108) – loss of desire: 25% – male erectile disorder: 7% – orgasmic dysfunction: 24% – ejaculation disorder: 16% – decrease in sexual activity: 11% – sexual dissatisfaction: 8%
P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Sexuality and Testicular Cancer: Literature Review
61
Fig. 3. PCT (6 studies, n = 160).
Fig. 4. PCT + surgery (9 studies, n = 404).
Compared to the entire patient population, relatively high percentages of loss of sexual desire and orgasmic disorders were reported, especially if we take into account that, medically, orchidectomy followed by surveillance is the least invasive treatment modality. As expected, relatively little (but still some) ejaculatory dysfunction was reported. Radiotherapy (RT) (Concerning Nine Studies, n = 417) – loss of desire: 14% – male erectile disorder: 25% – orgasmic dysfunction: 23% – ejaculation disorder: 40%
P1: FZN Archives of Sexual Behavior [asb]
62
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
Fig. 5. Surgery (6 studies, n = 193).
– decrease in sexual activity: 29% – sexual dissatisfaction: 16% Results revealed that irradiated patients reported the highest rate of erectile disorders and the lowest rate of loss of desire, compared to other treatment groups. Chemotherapy (PCT) (Concerning Six Studies, n = 160) – loss of desire: 25% – male erectile disorder: 11% – orgasmic dysfunction: 28% – ejaculation disorder: 28% – decrease in sexual activity: 34% – sexual dissatisfaction: 15% Treatment with PCT resulted in a rather “average” pattern of sexual disorders. The outcome of ejaculatory dysfunctioning was low compared to patients treated by RT, whereas the outcome of decrease in sexual activity was relatively high compared to the mean score for the entire population. PCT + Surgery (Retroperitoneal Lymph Nodes, RPLND, or Residual Tumor Mass, RRRTM) (Concerning Nine Studies, n = 404) – loss of desire: 13% – male erectile disorder: 11% – orgasmic dysfunction: 22%
P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Sexuality and Testicular Cancer: Literature Review
63
– ejaculation disorder: 62% – decrease in sexual activity: 29% – sexual dissatisfaction: 20% Like PCT alone, PCT + surgery also resulted in a rather average pattern of reported sexual dysfunctioning. As expected, patients treated by surgery in the abdominal area reported a much higher rate of ejaculatory dysfunctioning compared to patients treated by PCT alone. With respect to these studies it must be noted that surgical therapeutic principles have changed since the introduction of cisplatin in 1977, and that the extent of surgery has evolved from “very radical” to “more concise.” The effect is that in older studies concerning PCT + surgery, patients reported more ejaculatory dysfunction than in the more recent studies. However, the most striking result in this group of patients can be seen in the reported loss of sexual desire: the combination of two invasive treatment modalities lead to less reported loss of sexual desire (13%) than either PCT (25%) or abdominal surgery alone (66%). Retroperitoneal Lymph Node Dissection (RPLND) (Concerning Six Studies, n = 193) – loss of desire: 66% – male erectile disorder: 10% – orgasmic dysfunction: 11% – ejaculation disorder: 81% – decrease in sexual activity: 0% – sexual dissatisfaction: not reported As the table shows, studies about sexual outcome after RPLND-alone reported a very high percentage of ejaculation disorder, probably due to the very radical surgical procedures used in the period that RPLND-alone was the common intervention. Especially, bilateral RPLND implicated the risk for retrograde ejaculation (e.g, Bracken, 1976; Nijman et al., 1987). The high outcome of reported loss of sexual desire in this subgroup of RPLND-treated patients (6%) needs to be interpreted with caution, as this outcome could be based on only two studies (one of them used very small subgroups, Gritz et al., 1989, and the other used rather vague assessment methods, Nijman et al., 1987). PCT + RPLND + RT (Concerning One Study, n = 26) Fossa et al. (1988) offered specified data concerning this combined treatment. Results are depicted here only to provide a picture “as complete as possible,” but
P1: FZN Archives of Sexual Behavior [asb]
64
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops Table III. Correlations Between Outcomes of Variables of 36 Studiesa Desire
Desire Erection Orgasm Ejaculation Activity Dissatisfaction Age Follow-up a Spearson’s
Erection
Orgasm Ejaculate Activity Dissatisfaction Age Follow-up
1
.74∗ .18 .13 .67 .72∗∗ .19 −.06
1
.77∗∗ .03 .59∗ .60∗ −.020 .10
1 .07 .54 .24 .54∗ −.15
1 .07 −.12 .33 .16
1 .48 −.32 −.02
.02 −.18
1 .11
1
Rho Significant if ∗ p < .01, ∗∗ p < .05.
will not be taken into account in the discussion. – loss of desire: not reported – male erectile disorder: 24% – orgasmic dysfunction: 55% – ejaculation disorder: 60% – decrease in sexual activity: not reported – sexual dissatisfaction: not reported The total means across the specified treatment modalities in Table II were 2–7% higher compared to the general means presented in Table I (29 retrospective studies, irrespective of treatment modality). Between treatments, there appeared to be significant differences in reported sexual functioning (Table III, lowest row); it must be noted that the number of patients included per sexual variable is not fixed (due to the fact that the studies vary in their report of sexual variables). Taking into account this variability the following image emerges: – loss of desire appeared to be relatively high in patients treated by Surveillance and PCT-alone (both groups, 25%) – loss of erection was generally low, but highest in patients treated with RT (25%) – reduced orgasm was relatively low in patients treated with RPLND-alone (11%) – ejaculatory problems were high (62–81%) in patients treated with PCT ± surgery, but were also reported by 40% of patients from studies concerning RT – reduced sexual activity was relatively low, especially in patients treated with Surveillance (but still 10.5%) – sexual dissatisfaction generally was reported as being less frequent than was sexual dysfunctioning (<20%), and as the least by patients treated with Surveillance (7.5%)
P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
Sexuality and Testicular Cancer: Literature Review
19:29
Style file version Nov. 19th, 1999
65
Interrelations Interrelations between outcomes of sexual functioning across studies were moderately high (Table III), especially between desire and erection (Rho = 0.74, p = .001), and between sexual satisfaction and desire as well as, to some lesser degree, erectile dysfunctioning (resp (response rate) Rho = 0.72, p = .009 and .60, p = .039). But there was also a moderately strong relationship between sexual activity and desire, erection (resp Rho = 0.67, p = ns, and Rho = 0.59, p = .097), and orgasm (Rho = 0.54, p = ns). However, in the presence of high interrelations, erectile dysfunction was reported much less frequently as compared to other variables. Ejaculatory functioning, although the most prevalent sexual dysfunction, was hardly at all related to subjective reports of other functions (Rho’s between 0.03 and 0.13, p = ns). Interrelations, with ejaculation excluded, revealed an a-value of 0.79 across the studies. In general, reported sexual desire and sexual activity contributed most to the a-value across studies, and reported orgasmic failure least. Age of the respondents was minimally related to reported sexual functioning, except for orgasm (Rho = 0.54, p = 0.08), and to a lesser degree to ejaculation (Rho = 0.33, p = ns). Follow-up period also seemed not related to reported sexual functioning. Interestingly, interrelations with publication year all except one were positive, which means that respondents tended to report more problems in more recent studies, except where it concerned ejaculatory problems: those were reported less in more recent studies (Rho − 0.43). DISCUSSION The aim of this study was to review literature concerning sexual functioning after treatment for testicular cancer. Thirty-six studies (29 retrospective and 7 prospective) could be found, and these were analysed. This concerned over 20 studies more than those quoted by Heidenreich (Heidenreich and Hofmann, 1999), who suggested that concerning testicular cancer “there is only a limited number of research data available with regard to sexual and marital satisfaction of the patients.” Besides aspects of the sexual response cycle in terms of disorders as described in DSM-IV (APA, 1994), absence of ejaculation, reduced sexual activity, and sexual dissatisfaction were taken into account in screening and describing outcomes of the reviewed studies. In general, the reviewed studies varied widely in variables and treatments included, and also in reported sexual morbidity. Furthermore, comparison of outcomes was hindered because different research methods were used, and only a limited number of studies used standardized questionnaires, or healthy individual/patient comparison groups (see Appendix). Therefore we performed a meta-analysis in which the number of patients per study, as well as the type(s) of treatment was taken into account.
P1: FZN Archives of Sexual Behavior [asb]
66
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
Erectile dysfunction was reported least frequently (mean 11.5% in available retrospective studies and 14% in prospective studies), and ejaculatory dysfunction most frequently (mean 44% in retrospective and 51% in prospective studies). With respect to specific treatment modalities, it appeared that erectile dysfunction, although not frequently reported, was related to irradiation therapy. Ejaculatory dysfunction was straightforwardly connected with surgical techniques concerning retroperitoneal lymph node dissection, disrupting important nerve fibres (i.e., retrograde ejaculation). In view of this high mean rate it may be promising that in more recent studies, in which more focal surgical techniques are used with cisplatin-based chemotherapy (resection of residual retroperitoneal tumor mass, RRRTM + PCT), less ejaculatory dysfunction is reported (Gels et al., 1997; Tekgul et al., 1994; Wood et al., 1992). There was a relative independence of reported sexual functioning and age of respondents. Furthermore there is no clear relationship between follow-up periods and sexual function. Although prospective studies offered insufficient data for statistical comparison, retrospective studies generally showed higher rates of sexual morbidity than did prospective studies. This suggests the presence of a response bias: retrospective questioning triggers another type of response compared to prospective follow-up research (Fichten et al., 1991). At first glance, these contradictory findings, as well as the wide range of outcomes, seem to preclude definite conclusions concerning sexual morbidity after treatment for testicular cancer. However, if we make a distinction between a physiological and a psychological perspective, a comprehensible pattern can be detected. Looking at the sexual responses that are perceived as (at least partially) physiological phenomena (erection and ejaculation) we see, as could be expected, that these dysfunctions are related to treatment modalities that directly affect the nerve systems or innervation or both (RT and RPLND/RRRTM), whereby erectile dysfunction generally is the least-reported problem. On the other hand, the medically and physiologically least-invasive treatment (Surveillance) leads to the lowest rate of these two problems. This means that the physiological domain shows a high level of consistency. But if we look at the sexual responses that are perceived as predominantly psychological and behavioral phenomena (sexual desire, orgasmic joy, sexual activity, and satisfaction) another pattern can be detected. All treatment modalities reported a decrease of sexual desire, orgasmic intensity, sexual activity, and sexual satisfaction, whereby patients treated by the medical, relatively less-invasive treatment reported higher sexual morbidity compared to more invasive treatments, for example, data of patients treated by “Wait and See” (orchidectomy-alone), or PCT-alone compared to PCT + surgery. This indicates that changes in sexual functioning after testicular cancer treatment on a psychological level are relatively independent from physiological changes, caused by factors such as the stage of disease and influences of treatment-type. Interrelations also underscored the distinction between physical and psychological effects of cancer
P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
Sexuality and Testicular Cancer: Literature Review
19:29
Style file version Nov. 19th, 1999
67
treatment: reported sexual functions were strongly interrelated, except for ejaculation. Also interesting is the recurrent result that reported sexual dissatisfaction is much lower than is reported sexual dysfunction. Possibly men change their sexual satisfaction-values after having experienced a life-threatening genital cancer (Jonker-Pool et al., 1997). Aspects of sexual functioning that are predominantly mediated by cognition, perception, and emotion (subjective sexual experiencing and sexual motivation) may be affected by the psychotraumatic experience of having cancer, and not by physiological factors per se (Jonker-Pool et al., 1997; Van Basten et al., 1997; Van Basten et al., 1999). This result replicates findings in a female population who were treated for gynecological cancer (Weijmar Schultz et al., 1993). Outcomes of this study reveal that future research should, on the one hand, take into account effects of specific treatments, to address the risk of physiological sexual morbidity. On the other hand future medical studies should not focus only on biological– medical causes in phenomena that are bio-psychosocially regulated by their very nature (Bancroft, 1989). Fortunately there is a trend to a more comprehensive research attitude. When we take into account the publication year of the studies it appeared that older studies tended to stress more biological-organic sequelae of testicular cancer, whereas more recent studies also paid attention to psychosocial issues related to sexuality, such as marital relationship and subjective sexual distress (Fossa et al., 1988; Hannah et al., 1992; Schover and von Eschenbach, 1985). When the trends found in this meta-analytic study appear to be correct, this includes important suggestions for the coaching of patients. Patients can be accurately informed about the physiological-sexual risks to be expected after specific treatment, as well as about the psychological-sexual vulnerability that may evolve due to the intrinsic actual and symbolic danger where it concerns a genital tumor at a relatively young age. Adequate information and support may prevent, or reduce, unnecessary sexual and relational anxiety and suffering.
Bisset (1990) Blackmore (1988) Bloom (1993) Bracken (1976) Brenner (1985) Caffo (1999) Cassileth (1987) Couzijn (1982)
2
3b
5
6
9c
39
89 s
29 s
37 s
42 s
20
3
44
15
PCT
30 bil 6 uni ns
1
RPLND
14 bil ns
RPLND + RT
41 (?)
15
RT + PCT
61 bil
44 ns
14
19
PCT + RPLND
3 bil orch
Other/Unclear
19:29
8a
16
9
RT
October 19, 2000
7
48 s 37 ns (79%) 8s 66 ns (44%) 16 (80%) 39 s 49 ns (77%) 29 s 50 ns (51%) 67 ns (95%) 89 s (69%) 39 s (58%) 20 cpl
Surv
PL186-228372
4a
Arai (1997)
1b
n (resp %)
68
Author (Publication year)
Archives of Sexual Behavior [asb]
Sample Sizes and (Combinations of ) Treatments Involved in 29 Retrospective and 7 Prospective Studies Describing Sexual Functioning After Testicular Cancer
APPENDIX
P1: FZN Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
Hannah (1992) Hartman (1999) Johansson (1992) Jonker-Pool (1997)
13a
14b
15
Kaasa (1991) Levison (1986) Moynihan (1987)
18
19
4s
15 s
15 s
32
58
2
42 ns
39
32 ns
3 ns
3 ns
2
32 uni
13 ns
8 ns
8 ns
4
4
1s
1s
3
2
2
46
122 ns
42 ns
6 ns
6 ns
69
(Continued )
32 RT + PCT ± RPLND
19 all treatment 49 PCT or RPLND or both
19:29
12
44
39
59 ns 41 s
7s
1s
1s
37 ns
11
October 19, 2000
17
34 cpl 17 s 17 ns (83%) 34 cpl 17 s 17 ns (?) 20 s 78 ns (78%) 39 (87%) 41 s 223 ns (85%) 46 s 103 ns (93%) 53 34 s (?) ns (88%) 102 (84%)
39 s 49 ns (?)
109 ns
PL186-228372
16a
Gritz (1989)
Douchez (1993) Gritz (1988)
Archives of Sexual Behavior [asb]
12b
11b
10a
P1: FZN Style file version Nov. 19th, 1999
Sexuality and Testicular Cancer: Literature Review 69
Rieker (1989)
Schover (1985)
Schover (1986) Stoter (1989) Stuart (1990)
Tinkler (1992) Tross (1984) abstract Aass (1993) prosp
23a,b
24a,b
25
28a,b
30
41 s 35 ns (100%)
36
137
28
48
13
47/121
38
63 bil
51
RPLND
2
8/121
11
4
RPLND + RT
4
3
RT + PCT
23
30
38/121
74
37
27
PCT + RPLND
21 PCT/ RPLND + 10 RT 20 RT + PCT/ RPLND 26/121 RPLND + RT + PCT 2/121: (?)
Other/Unclear
19:29
29a
18
34
79
20
PCT
October 19, 2000
27
84 s (51%) 48 ns (84%) 35 s 27 ns (63–78%) 155 (56–62%) 30 ns (?)
71
6
RT
PL186-228372
26
22
55 ns (?) 101 ns (100%) 9s 65 ns (80%) 40 s 61 ns (81%) 52 ns (43%)
Surv
Archives of Sexual Behavior [asb]
21
Narayan (1982) Nijman (1987) Rieker (1985)
n (resp %)
70
20
Author (Publication year)
APPENDIX (Continued )
P1: FZN Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
Johnstone (1991) prosp Nijman (1988) prosp Tamburini (1989) prosp Trump (1985) prosp/abstract Van Basten (1999) prosp
32c
17 ns
9
(?)
(?)
5
39
8
(?)
13
4
10
(?)
6
5
15 prosp 29 ret
(?)
(?)
(?)
7
42 part 8 compl
17 prosp 43 ret ± RT
(?)
26 ret PCT + RT ± RPLND
October 19, 2000
Note. resp = response rate; Surv = surveillance; RT = radiotherapy; PCT = poly chemotherapy; RPLND = retroperitoneal lymph node dissection; n = responding number of patients; s = seminoma, ns = non-seminoma; orch = orchiectomy; bil = bilateral RPLND; uni = unilateral RPLND; part = partial RPLND; compl = complete RPLND; cpl = couples; prosp = prospective study; ret = retrospective. a Comparing to controls or other patient comparison-groups. b Comparing different treatment modalities within the study . c Using validated questionnaires.
36b,c
35c
5s 26 ns (100%) 29 (?)
16
32 prosp 24 ret
PL186-228372
34b
40 s 30 ns (60%) 54 ns (100%)
64 prosp 122 ret (?)
Archives of Sexual Behavior [asb]
33b
Fossa (1988) prosp?
31
P1: FZN 19:29 Style file version Nov. 19th, 1999
Sexuality and Testicular Cancer: Literature Review 71
P1: FZN Archives of Sexual Behavior [asb]
72
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
ACKNOWLEDGMENT This study was supported by a grant from the Dutch Cancer Society, RUG 94-873. REFERENCES Aass, N., Grunfeld, B., Kaalhus, O., and Fossa, S. D. (1993). Pre- and post-treatment sexual life in testicular cancer patients: A descriptive investigation. Br. J. Cancer 67: 1113–1117. Adami, H. O., Bergstrom, R., Mohner, M., Zatonski, W., Storm, H., Ekbom, A., Tretli, S., Teppo, L., Ziegler, H., and Rahu, M. (1994). Testicular cancer in nine northern European countries. Int. J. Cancer 59: 33–38. American Psychiatric Association (1994). DSM-IV. Diagnostic and Statistic Manual of Mental Disorders, American Psychiatric Association, Washington, DC. Arai, Y., Kawakita, M., Okada, Y., and Yoshida, O. (1997). Sexuality and fertility in long-term survivors of testicular cancer. J. Clin. Oncol. 15: 1444–1448. Bancroft, J. (1989). The biological basis of human sexuality. In: Bancroft, J., Human sexuality and its problems, Churcill Livingstone, Edinburg, London, Melbourne, and New York, pp. 12–145. Bisset, D., Kunkeler, L., Zwanenburg, L., Paul, J., Gray, C., Swan, I. R. C., Kerr, D. J., and Kaye, S. B. (1990). Long-term sequelae of treatment for testicular germ cell tumors. Br. J. Cancer 62: 655–659. Blackmore, C. (1988). The impact of orchidectomy upon the sexuality of the man with testicular cancer. Cancer Nursing 11: 33–40. Bloom, J. R., Fobair, P., Gritz, E., Wellisch, D., Spiegel, D., Varghese, A., and Hoppe, R. (1993). Psychosocial outcomes of cancer: A comparative analysis of Hodgkin’s disease and testicular cancer. J. Clin. Oncol. 11: 979–988. Bracken, R. B. (1976). Sexual function and fecundity after treatment for testicular tumors. Urology 1: 35–38. Brenner, J., Vugrin, D., and Whitmore, W. F. Jr. (1985). Effect of treatment on fertility and sexual function in males with metastatic nonseminomatous germ cell tumors of testis. Am. J. Clin. Oncol. 8: 178–182. Caffo, O., and Amichetti, M. (1999). Evaluation of sexual life after orchidectomy followed by radiotherapy for early-stage seminoma of the testis. BJU International 83: 462–468. Cassileth, B. R., and Steinfeld, A. D. (1987). Psychological preparation of the patient and family. Cancer 60: 547–552. Couzijn, A. L., van Dam, F. S., and Hanewald, G. J. (1982). Chemotherapie van het gemetastaseerde testicarcinoom; ervaringen van patienten en hun partners. [Chemotherapy of metastasized carcinoma of the testis; experiences of patients and their partners] Ned. T. Geneesk. 126: 1854–1857. Douchez, J., Droz, J. P., Desclaux, B., Allain, Y., Fargeot, P., Caty, A., and Charrot, P. (1993). Quality of life in long-term survivors of nonseminomatous germ cell testicular tumors. J. Urol. 149: 498–501. Fichten, S., Libman, E., Amsel, R., Creti, L., Weinstein, N., Rothenberg, P., Liederman, G., and Brender, W. (1991). Evaluation of the sexual consequences of surgery: Retrospective and prospective strategies. J. Behav. Med. 14: 267–285. Fossa, S. D., Aass, N., and Kaalhus, O. (1988). Testicular cancer in young Norwegians. J. Surg. Oncol. 39: 43–63. Fung, C. Y., and Garnick, M. B. (1988). Clinical stage I carcinoma of the testis: A review. J. Clin. Oncol. 6: 734–750. Gels, M. E., Hoekstra, H. J., Sleijfer, D. Th., de Bruijn, H. W., Molenaar, W. M., Freling, N. J., Droste, J. H., and Schraffordt Koops, H. (1995). Detection of recurrence in patients with clinical stage I nonseminomatous testicual germ cell tumors and consequences for further follow-up: A single-centre 10 year experience. J. Clin. Oncol. 13: 1188–1194. Gels, M. E., Nijboer, A. P., Hoekstra, H. J., Heuvel, F., Molenaar, W. M., Plukker, J. T., Droste, J. H., and Schraffordt Koops, H. (1997). Complications of the post-chemotherapy resection of
P1: FZN Archives of Sexual Behavior [asb]
PL186-228372
October 19, 2000
Sexuality and Testicular Cancer: Literature Review
19:29
Style file version Nov. 19th, 1999
73
retroperitoneal residual tumor mass in patients with nonseminomatous testicular germ cell tumors. Br. J. Urol. 79: 263–268. Gritz, E., Wellisch, D., and Landsverk, J. A. (1988). Psychosocial sequelae in long-term survivors of testicular cancer. J. Psychosoc. Oncol. 6: 41–63. Gritz, E. R., Wellisch, D. K., Wang, H. J., Siau, J., Landsverk, J. A., and Cosgrove, M. D. (1989). Longterm effect of testicular cancer on sexual functioning in married couples. Cancer 64: 1560–1567. Hadu, I. (1979). Pathology of germ cell tumors of the testis. Sem. Oncol. 6: 14–25. Hannah, M. T., Gritz, E., Wellisch, D., Fobair, P., Hoppe, R. T., Bloom, J. R., Sun, G.-W., Varghese, A., Cosgrove, M. D., and Spiegel, D. (1992). Changes in marital and sexual functioning in longterm survivors and their spouses: Testicular cancer versus Hodgkin’s disease. Psycho-Oncology 1: 89–103. Harding, M., Hole, D., and Gillis, C. (1995). The epidemiology of nonseminomatous germ-cell tumors in the west of Scotland 1975–1989. Br. J. Cancer 72: 1559–1562. Hartmann, J. T., Albrecht, C., Schmoll, H.-J., Kuczyk, M. A., Kollmannsberger, C., and Bokemeyer, C. (1999). Long-term effects on sexual function and fertility after treatment for testicular cancer. Br. J. Cancer 80(5/6): 801–807. Heidenreich, A., and Hofmann, R. (1999). Quality-of-life issues in the treatment of testicular cancer. World J. Urol. 17: 230–238. Hoff Wanderas, E., Tretli, S., and Fossa, S. D. (1995). Trends in the incidence of testicular cancer in Norway 1955–1992. Eur. J. Cancer 31A: 2044–2048. Johansson, S., Steineck, G., Hursti, T., Fredrikson, M., Furst, C. J., and Peterson, C. (1992). Aspects of patient care. Interviews with relapse-free testicular cancer patients in Stockholm. Cancer Nursing 15: 54–60. Johnstone, B. G. M., Silberfeld, M., Chapman, J. A., Phoenix, C., Sturgeon, J. F. G., Till, J. E., and Sutcliffe, S. B. (1991). Heterogeneity in responses to cancer. Part II: Sexual responses. Can. J. Psychiat. 36: 182–185. Jonker-Pool, G., van Basten, J. P., Hoekstra, H. J., van Driel, M. F., Heuvel, F., Schraffordt Koops, H., and van de Wiel, H. B. M. (1997). Sexuality after testicular cancer treatment—Comparison of treatment modalities. Cancer 80: 454–464. Kaasa, S., Aass, N., Mastekaasa, A., Lund, E., and Fossa, S. D. (1991). Psychosocial well-being in testicular cancer patients. Eur. J. Cancer 27: 1091–1095. Kaplan, H. S. (1979). Disorders of Sexual Desire, Brunner/Mazel, New York. Levison, V. (1986). The effect on fertility, libido and sexual function of post-operative radiotherapy and chemotherapy for cancer of the testicle. Clin. Radiol. 37: 161–164. Masters, W. H., and Johnson, V. E. (1966). Human Sexual Response. Little, Brown, Boston. Moynihan, C. (1987). Testicular cancer: The psychosocial problems of patients and their relatives. Cancer Surv. 6: 477–510. Narayan, P., Lange, P. H., and Fraley, E. E. (1982). Ejaculation and fertility after extended retroperitoneal lymph node dissection for testicular cancer. J. Urol. 127: 685–688. Nijman, J. M., Schraffordt Koops, H., Kremer, J., and Heuvel, F. (1987). Gonadal function after surgery and chemotherapy in men with stage II and III nonseminomatous testicular tumors. J. Clin. Oncol. 5: 651–656. Nijman, J. M., Schraffordt Koops, H., Oldhoff, J., Kremer, J., and Heuvel, F. (1988). Sexual function after surgery and combination chemotherapy in men with disseminated nonseminomatous testicular cancer. J. Surg. Oncol. 38: 182–186. Peckham, M. J., Barret, A., Horwich, A., and Hendry, W. F. (1983). Orchiectomy alone for stage I testicular nonseminoma. A progress report on the Royal Marsden Hospital Study. Br. J. Urol. 55: 754–759. Raina, V., Shukla, N. K., Gupta, N. P., Deo, S., and Rath, G. K. (1995). Germ cell tumors in uncorrected cryptorchid testis at Institute Rotary Cancer Hospital, New Delhi. Br. J. Cancer 71: 380–382. Rieker, P. P., Edbril, S. D., and Garnick, M. B. (1985). Curative testis cancer therapy: Psychosocial sequelae. J. Clin. Oncol. 3: 1117–1126. Schover, L. R., Gonzalez-Mariscal, G., and von Eschenbach, A. C. (1986). Sexual and marital relationships after radiotherapy for seminoma. Urology 27: 117–123. Schover, L. R. and von Eschenbach, A. C. (1985). Sexual and marital relationships after treatment for nonseminomatous testicular cancer. Urology 25: 251–255.
P1: FZN Archives of Sexual Behavior [asb]
74
PL186-228372
October 19, 2000
19:29
Style file version Nov. 19th, 1999
Jonker-Pool, Van de Wiel, Hoekstra, Sleijfer, Van Driel, Van Basten, and Koops
Stoter, G., Koopman, A., Vendrik, C. P., Struyvenberg, A., Heuvel, F., Willemse, P. H., Schraffordt Koops, H., van Oosterm, A. T., and Pinedo, H. M. (1989). Ten-year survival and late sequelae in testicular cancer patients treated with cisplatin, vinblastine, and bleomycin. J. Clin. Oncol. 7: 1099–1104. Stuart, N. S., Grundy, R., Woodroffe, C. M., and Cullen, M. H. (1990). Quality of life after treatment for testicular cancer—The patient’s view. Eur. J. Cancer 26: 291–294. Tamburini, M., Filiberti, A., Barbieri, A., Zanoni, F., Pizzocaro, G., Barletta, L., and Ventafridda, V. (1989). Psychological aspects of testis cancer therapy: A prospective study. J. Urol. 142: 1487– 1490. Tekgul, S., Ozem, H. A., Celebi, I., Ergen, A., and Demircin, B. (1994). Postchemotherapeutic surgery for metastatic germ cell tumors: Results of extended primary chemotherapy and limited surgery. Urology 43: 349–354. Tinkler, S. D., Howard, G. C., and Kerr, G. R. (1992). Sexual morbidity following radiotherapy for germ cell tumors of the testis. Radiother. Oncol. 25: 207–212. Tross, S. and J. C. Holland (1984). A controlled study of psychosocial sequelae in cured survivors of testicular neoplasms (Abstract). Proc. Am. Soc. Clin. Oncol. 3: 74. Trump, D. L., Romsaas, E. P., Cummings, K. C., and Malec, J. F. (1985). Assessment of psychologic and sexual dysfunction in patients following treatment of testis cancer: A prospective study (Abstract). Proc. Am. Soc. Clin. Oncol. 4: 250. Van Basten, J. P., Jonker-Pool, G., van Driel, M. F., Droste, J. H. J., van de Wiel, H. B. M., Schraffordt Koops, H., Molenaar, W. M., and Hoekstra, H. J. (1997). Sexual functioning after multimodality treatment for disseminated nonseminomatous testicular germ cell tumor. J. Urol. 158: 1411–1416. Van Basten, J. P., van Driel, M. F., Hoekstra, H. J., Sleijfer, D. T., van de Wiel, H. B. M., Droste, J. H. J., Schraffordt Koops, H., and Mensink, H. J. A. (1999). Objective and subjective effects of testicular cancer treatment on sexual function. Br. J. Urol. (Abstract) Visser, O., Coebergh, J. W. W., and Schouten, L. J. (1996). Incidence of Cancer in The Netherlands 1993, The Netherlands Cancer Registry, Utrecht. Weijmar Schultz, W. C. M., van de Wiel, H. B. M., Van de Haan, D. E. E., and van Driel, M. F. (1993). Sexuality and cancer in women. Ann. Rev. Sex Res. 3: 151–200. Wingo, P. A., Tong, T., and Bolder, S. (1995). Cancer Statistics. CA Cancer J. Clin. 45: 8–30. Wood, D. P., Herr, H. W., Heller, G., Vlamis, V., Sogani, P. C., and Motzer, R. J. (1992). Distribution of retroperitoneal metastases after chemotherapy in patients with nonseminomatous germ cell tumors. J. Urol. 148: 1812–1815. Zimmerman, R. R., and Kung’u, A. (1978). Testicular neoplasms in Kenyan Africans. Cancer 41: 2452–2455.
