Original Article

International Journal of Impotence Research (2010) 22, 127–133; doi:10.1038/ijir.2009.57; published online 26 November 2009

There is a Retraction (1 July 2012) associated with this article.

Effects of exposure to a mobile phone on sexual behavior in adult male rabbit: an observational study

N Salama1,2, T Kishimoto1, H-o Kanayama1 and S Kagawa1

  1. 1Departments of Urology, Tokushima School of Medicine, Tokushima City, Japan
  2. 2Department of Urology, Alexandria Faculty of Medicine, Alexandria, Egypt

Correspondence: Professor N Salama, Department of Urology, Alexandria Faculty of Medicine, Alexandria 11111, Egypt. E-mail: nadersalama58@yahoo.com

Received 20 September 2009; Revised 21 October 2009; Accepted 22 October 2009; Published online 26 November 2009.

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Abstract

The accumulating effects of exposure to electromagnetic radiation emitted by a conventional mobile phone (MP) on male sexual behaviour have not yet been analyzed. Therefore, we studied these effects in 18 male rabbits that were randomly divided into phone and control groups. Six female teasers were taken successively to the male's cage and the copulatory behavior was recorded. Serum total testosterone, dopamine and cortisol were evaluated. The animals of the phone group were exposed to MPs (800MHz) in a standby position for 8h daily for 12 weeks. At the end of the study, the copulatory behavior and hormonal assays were re-evaluated. Mounts without ejaculation were the main mounts in the phone group and its duration and frequency increased significantly compared with the controls, whereas the reverse was observed in its mounts with ejaculation. Ejaculation frequency dropped significantly, biting/grasping against teasers increased notably and mounting latency in accumulated means from the first to the fourth teasers were noted in the phone group. The hormonal assays did not show any significant differences between the study groups. Therefore, the pulsed radiofrequency emitted by a conventional MP, which was kept on a standby position, could affect the sexual behavior in the rabbit.

Keywords:

mobile phone; sexual behavior; rabbit; radiofrequency

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Introduction

During recent years, the mobile phone (MP) has encountered a wide and rapidly growing use in daily life. This rapid expansion of mobile communication urges research efforts to focus on possible health risks of MPs on different body systems and, in particular, the brain. Currently, MP users are exposed to MP-emitted electromagnetic waves (EMWs). Owing to the close proximity of the MP device to the head, the brain is exposed to relatively high specific absorption rates compared with the rest of the body. Various non-thermal effects of MP-emitted EMW on the central nervous system, including permeability of the blood–brain barrier, neuronal electrical activity, neurotransmitter balance, cognitive function and sleep, have recently been reviewed.1, 2

Sexual behavior is a continuum of separate but linked processes: libido, erection, ejaculation, orgasm, detumescence and refractory period.3 Sexual behavior in the male is a good example of the mutual collaboration between the brain and the male genital system. The human brain is complexly involved in the production and enjoyment of sexual behavior. The thoughts, emotions and physiological responses involved in sexual behavior are mediated by the brain.4 Disorders of the brain structure or function are mostly associated with disturbances in male sexual behavior.5, 6

Recent studies showed the negative effect of MPs on the male genital system, both in animals7, 8 and in human subjects.9 All these studies dealt only with the influence of MPs on testicular structure and function7, 9, 10, 11 and male accessory genital organs.8 However, no studies to date have analyzed the potential effect of exposure to EMWs emitted from MPs on male sexual behavior. Therefore, an experimental study, using the adult male rabbit as a model, was undertaken to examine this effect.

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Materials and methods

Animals

A total of 18 adult male White New Zealand rabbits (Nihon SLC, Hamamatsu, Japan), 20 weeks of age and weighing 3.15–3.25kg, were used in this study. The rabbits were individually caged and kept in a temperature-controlled environment (22–24°C) under a 12h light/dark cycle (light on at 0700h). Animals were provided standard rabbit chow and water ad libitum, and left for acclimatization for 3 weeks.

The protocol for this experimental study was approved by the ethics committee of experimentation on animals at the University of Tokushima.

Copulatory behavior testing

After acclimatization, animals were given a period of 3 weeks for mating to establish their copulatory pattern, and to confirm that they were sexually active.12 Testing was performed once a week for 3 weeks to determine each rabbit's individual profile.

On the day of mating, males were given access to six estrous females for a period of 3min each. The female was considered in estrous if the vulva was red and tumefactive. The first female was placed in the male's cage for 3min. If the male could not mount until the end of this time, or if it mounted and ejaculated at any time within it, the procedure was ended and the observation was considered as completed. Just then, the female was immediately replaced by another estrous female, and another 3min of exposure to the male was reinitiated. This procedure continued for the remaining females.

Sexual performance was recorded by observing mount latency, time from introduction of the female until the first mount, ejaculation latency (EL), and time from introduction of the female until ejaculation. The frequency (MF), duration (MD) and types of mounts with or without ejaculation were noted. The frequency of ejaculations (EF) was also recorded. Presence of biting, grasping and kicking inside the cage were also registered and these observations were considered an expression of sexual aggressiveness.13

Exposure to the mobile phone (MP)

Animals were randomly and equally divided into three groups. The first group was the MP group whose members were placed individually in specially designed cages (50 × 25 × 35cm) as they represented the same material used by some previous studies.7, 8 These cages could accept placing plastic partitions according to the animal dimensions (averaged 30 × 16 × 18cm), to restrict movements. Therefore, the animals rested throughout the period of the daily phone exposure with their genitalia opposing the antennas of the MPs that were fixed to the cage bottoms. The MPs were conventional GSM (global system for mobile communications) handsets (800MHz) that were turned to the standby position in which they emit a low amount of intermittent EMW pulses to signal the network that they are still connected. The average strength of the electric field was 2.92Vm−1 estimated at 0.5cm away from the phone and 0.487Vm−1 at the most distant region inside the cage. The whole-body average specific absorption rate was 0.43Wkg−1 as defined in the MP handbook. Phones were applied for 8h (0900 to 1700h) daily for 12 weeks. After this daily phone exposure, the animals were returned to their individual standard cages (90 × 60 × 40cm).

Owing to the restriction of animal movements and the possibility of stress-related outcome, we added two control groups, as the relationship between stress and disruption in sexual behavior in restraint animal models has been shown in several studies.14, 15 Therefore, the animals in the first control group were the stress controls. They were placed in identical cages daily for 8h; however, the phone was switched off. The animals in the second group represented the ordinary controls whose members were left throughout the duration of the study in the standard cages. In both control groups, the cages were positioned 7m away from the phone group; the average strength of the electric field detected was equivalent to background radiation (0.18Vm−1).

After a 12-week exposure to MPs, the rabbits were mated thrice a week for a period of 2 weeks. Their sexual behavior was recorded again. Hence, six experiments were performed. As each experiment included 36 observations, we had a total of 216 observations per study group.

Rectal temperature assessment

This was carried out for all animals in this study twice a week. The measurement was made both before and after phone exposure.

Hormonal assays

Blood samples were collected, at the start and end of this research study, from the ear vein of each buck at a constant time of the day (1000h) for testosterone, cortisol and dopamine assays. This was to avoid the influence of time of the day on these hormonal levels as the three hormones are characterized by circadian cycles.16 The plasma total testosterone and cortisol concentrations were determined using radioimmunoassays, whereas dopamine was measured using radioenzymatic assay (SRL, Osaka, Japan). Both intra- and inter-assay coefficients of variation were 8.5% for testosterone and 4.1% for dopamine. The intra- and inter-assay coefficients of variation were 5.1 and 15.9% for cortisol.

Statistics

Data were expressed as mean±s.d. on a single experiment basis. Statistical analysis was carried out using SPSS statistical software (SPSS for Windows, Chicago, IL, USA). Mann–Whitney and Fisher's exact tests were performed to examine both the difference between each of the two groups and the longitudinal change within each group. A P-value of <0.05 was considered significant.

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Results

General features and hormonal assay

The mean rectal temperature (37.6±0.3°C) did not alter after exposure to MPs (37.5±0.27°C) and total body weights were not significantly different in the different groups (Table 1). Serum total testosterone, cortisol and dopamine levels did not show any significant differences among the different study groups at the start or the end of the study (Table 1).


Basic events of sexual behavior of the study animals

These appeared with no difference between the three study groups. The averages of these events included mount latency (130.7±25.3s), ejaculation latency (154.9±28.8s), EF (4.9±0.7), MF without ejaculation (2.8±1.5), MD without ejaculation (28.8±15.2s), MF with ejaculation (6.6±1.1), MD with ejaculation (93.4±15.5s) and biting/grasping (0.37±0.45).

Sexual behavior and mating ability on a per experiment basis

At the end of the study, mounts were mainly (56%) without ejaculation in the MP group compared with stress (26%) or ordinary control (27%) groups (Figure 1). Table 2 shows that MF and MD with ejaculation and EF were significantly lower, whereas MF and MD without ejaculation and biting/grasping were significantly higher in the MP group. Both mount latency and ejaculation latency did not show any significant differences among the different study groups.

Figure 1.
Figure 1 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Types of mounts (in relation to ejaculation) in the three study groups at the end of the study (data were obtained after recording 216 matings).

Full figure and legend (63K)


Lack of sexual interest of the animals

There were 11 animals in the three study groups that lacked sexual interest during the last six experiments, when presented with a female teaser (Table 3). The MP group animals had more frequent but nonsignificant (P=0.315) occasions with this defect. Any observation with lack of sexual interest was followed in all animals by a good reaction in the subsequent observation except in the phone group in which two animals showed two or three repeated non-reactive observations (MP2 in experiments 4, 5 and 6, and MP3 in experiments 3 and 5).


Sexual behavior and mating ability on a per teaser order

Mount latency in accumulated means from the first to the third teasers was noted in the control groups, but this appeared from the first to the fourth teasers with the exception of the second teasers in the MP group (Figure 2). The MP animals also showed a decreasing EF from the first to the fifth teasers (Figure 3), but this tendency in ejaculation appeared only until the third teasers in the control groups.

Figure 2.
Figure 2 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Mounting latency in relation to the order of female teasers at the end of the study (data were obtained after recording 216 matings; each data marker is the resulting sum of 36 observations).

Full figure and legend (91K)

Figure 3.
Figure 3 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Distribution pattern of animal ejaculations in relation to the order of female teasers at the end of the study (data were obtained after recording 216 matings; each bar is the resulting sum of 36 observations).

Full figure and legend (78K)

The longitudinal change in sexual behavior of mobile phone (MP) animals

Most parameters of sexual behavior of these animals revealed significant differences before and after this study research. These included P-values for EF (0.037), MF without ejaculation (0.009), MD without ejaculation (0.037), MF with ejaculation (0.045), MD with ejaculation (0.025) and biting/grasping (0.013).

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Discussion

This work is an observational study that evaluated the negative effects of MPs, which were kept in the standby position, on sexual behavior in adult rabbits. A literature review did not yield any studies analyzing this possible effect of MPs on male sexual behavior. In this work, we examined this possibility by applying a copulatory behavior testing approach. The main idea of this approach was to let the animals go into a state of sexual exhaustion. This exhaustion in rabbits is usually related with the ‘Coolidge effect,’ which was first proposed by Wilson et al.17 It describes the reinitiation of sexual behavior in a sexually satiated animal in response to a novel receptive mate.

The copulatory behavior of the sexually active male rabbit is characterized by a series of alternate mounts and intromissions that culminated in ejaculation. Adult rabbits mounted and ejaculated 6–8 times before refusing to copulate with a novel female, and before being considered to be sexually exhausted.18 This study, therefore, applied the Coolidge effect phenomenon showing that the MP animals got sexually exhausted earlier, as indicated by the decreasing order of their EF from the first to the fifth teasers. Adding a stress control group beside the ordinary controls was intended to avoid the possibility of getting stress-related outcome. This study, however, did not show any significant findings in these stress controls with cage restriction. This may be related to adaptation of animals to the restraint inside the cages during the period of the study, as indicated by the normal cortisol levels in all animals inside restrained cages.19 Therefore, we think that it was only the MPs that produced these evident changes in the sexual behavior of the phone group animals in spite of the different radiofrequency-exposure protocol applied in this study. This protocol did not simulate as closely as possible the radiofrequency exposure during the usual mobile communication. Many researchers20, 21 have applied special rockets to restrain their animals, giving the chance to put the phone antenna opposite the animal heads all the time in what is called the head-only exposure system. The exposure condition in our study, or what is called whole-body exposure system, was similarly used by other researchers who did not apply the MPs directly to the animal heads.22 We did not apply this head-only exposure in this study as this model has obviously some intrinsic limitations. First, owing to the much smaller body size of the rabbit, the ratio of the head to the whole-body specific absorption rate is very different in rabbits compared with humans. Second, owing to the small size of the external ear of the rabbit, it is not possible to have a restricted exposure exactly mimicking the one present in humans. These limitations tend to overestimate the effects of a head-only exposure rather than underestimate it. In addition, we used the MPs while on standby mode. In spite of these obvious differences in the exposure protocol, a negative effect of MPs was shown in our current study and that of the researchers who applied a quite similar protocol.22

A large body of evidence has implicated the testosterone and dopamine in the control of male sexual behavior in rabbits and other vertebrate species.23, 24 Testosterone has a key role in initiating and maintaining the sexual behavior in males. It is necessary for libido, spontaneous erections and ejaculation. Dopamine influences both sexual motivation and copulatory performance through the enhancement of sensorimotor function achieved by the removal of the inhibition of tonic outputs from the medial preoptic area to the mesencephalic periaqueductal gray. In this study, the testosterone and dopamine levels did not change in the MP animals. This may explain the absence of changes in the sexual motivation of the animals and their mount latency time, which is under hormonal control. This motivation even increased and pushed the phone animals to have significantly frequent mounts with longer durations compared with controls to ejaculate.25 The animals sometimes succeeded in ejaculating, but mostly they failed to achieve it, which made the mounts without ejaculation significantly frequent and longer in the MP animals.

In this study, the EF and mount duration and frequency ending with ejaculation decreased significantly in the MP animals. This may be attributed to failure of the animals to attain an erection or accomplish ejaculation as they were kept in a prolonged refractory period, in which most animals that failed to ejaculate at one session with a teaser were able to ejaculate in the next session with the following teaser. Lack of hormonal changes could not explain these observations in sexual behavior of the MP animals. However, we may attribute such changes in sexual behavior to oxidative stress occurring in the brain tissue, including supraspinal areas, which are well known to control, beside hormonal factors, male sexual function including erection and ejaculation.26 This oxidative stress might affect the numerous neurotransmitters coming out of the brain tissue, including oxytocin, which has been reported to be able to decrease the latency to the first ejaculation and to retard the sexual exhaustion of male rabbits paired with receptive females.27 In support of our explanation, three lines of evidence were present. First, aggressive behavioral changes, such as grasping and biting, were observed in the MP animals. Previous studies have related oxidative stress in the brain to the development of such aggressive changes.28 Second, the MPs used in this study had a carrier frequency of 800MHz and the animal model used was the rabbit. A large number of studies have reported the occurrence of oxidative stress in brain tissues with the use of MPs with a similar carrier frequency and the same animal model29 or other close rodents such as rats.22 Third, the same group of MP animals represented the subjects of another two studies. Both indicated the negative influence of MPs on testicular function and structure7 and semen fructose.8 Interestingly, these retrieved findings were related to the oxidative stress occurring in the testes and accessory genital organs of the animals.

There are various antioxidant mechanisms in the brain that neutralize the harmful effects of reactive oxygen species. However, with EMW exposure and the suggested occurrence of oxidative stress, the efficiency of these antioxidant mechanisms will be lost. This will result in an increase in reactive oxygen species production,30, 31 which may lead to cellular damage.32 A limitation of this study is that we did not determine the level of oxidative stress in the brains of our animals. Further studies, therefore, may reveal the precise effects of MP-associated EMWs on brain tissues, and define safeguards against oxidative damage.

In conclusion, the results of this observational study might have some practical implications, given the ubiquity of MPs. As there were no other similar studies in the literature, we could not compare our data with others. However, we could show for the first time that exposure to the pulsed radiofrequency emitted by a conventional MP, which was kept on a standby position, could affect the sexual behavior in the rabbit. Results from this preliminary study should be corroborated in larger studies to have a detailed clue about the effect of MPs on male sexual behavior.

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Conflict of interest

The authors declare no conflict of interest.

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