Functional and morphological studies of photodamaged skin on the hands of middle-aged Japanese golfers

ARTICLE

Both intrinsic and actinic aging contribute to the development of the elderly appearance of the skin. The study of photoaging should be performed by comparison between anatomically similar portions of the body of the same individuals. However, many of the studies conducted in the past have utilized different skin regions of the same individuals for such comparison, e.g., between the upper ventral arm and dorsal forearm [1] or between the dorsal surface of the hand and that of the foot [2], or to use the same locations of different people with various ages [3]. There are a few studies [4, 5] that examined the skin of sun-exposed and adjacent unexposed sites. As far as we know, however, there has been no study performed on anatomically symmetrical sites of the same subjects for the evaluation of photodamage. We have noticed that the dorsal skin of the right and left hands of the people who frequently play golf show a different clinical appearance. These golfers usually wear a glove on only one of their hands. Therefore, one of their hands is exposed, whereas the other one is protected by the glove from the outer environment, especially from sunlight. In the present study, we examined the dorsal surfaces of the hands of the same middle-aged golf players to determine the effects of photodamage by using non-invasive measurements.

Materials and methods

Study I: biophysical study of the skin

Subjects

Twelve middle-aged healthy Japanese male subjects who had frequently played golf from the morning to early afternoon approximately 5 to 6 hrs a day at least twice or 3 times a month for the past 4 to 25 years participated in the study after submitting informed consent (Table I). All of them were right-handed and played golf with a glove on only the left hand. One of them had used sunscreen on the right hand while he played golf for the past 15 years. All of them were indoor workers and have not been engaged in any other outdoor activities which would expose their skin to sunlight. None of the subjects used moisturizer prior to the study on the hands.

Non-invasive biophysical measurements

From November 1997 to March 1998, non-invasive bioengineering measurements were performed on the skin of the dorsum of the hands. High frequency conductance [6] to assess hydration state of the stratum corneum (SC) was measured with Skicon^®-200 (IBS, Hamamatsu, Japan). Transepidermal water loss (TEWL) [7], a parameter for the water barrier function of the SC, was measured with Evaporimeter^® EP-1 (SevoMed, Stockholm, Sweden) according to the guideline [8]. Skin color was determined with a Minolta CR-300 (Minolta, Osaka, Japan) chromameter according to a 3-dimentional L* a* b* system, where L* is an attribute on the luminance scale, a* on the red-vs-green attribute and b* on the yellow-vs-blue attribute. All measurements were conducted in an air-conditioned room with a room temperature of 16-22° C and relative humidity of 21-50% after 15-min acclimation. The values obtained were compared between the right and left hands (exposed and protected hands during the play, respectively).

Study II: Morphological study of the skin surface

Subjects

A separate study on the skin surface contour was conducted from November to December 1997 with 12 male Japanese golfers who had frequently played golf from morning to early afternoon approximately 5 to 6 hrs a day at least twice or 3 times a month for the past 4 to 25 years (Table I). All were right handed and had a glove on only the left hand during play. Two of them had used sunscreen on the exposed hand during play for the past 15 and 20 years.

Replica analysis

Silicon rubber dental replicas (Shiseido, Japan) of the skin surface were obtained from the dorsal surface of the hands to study the skin surface microrelief. Replicas were obtained in a relaxed position with the palms placed flat on the desk and other ones were taken when the subjects' dorsal hands were in a slightly stretched position by gently holding a golf ball placed on the desk.

The replicas obtained were processed using a skin surface replica image analyzer [9, 10] (Shiseido, Japan). An image of 4 x 4 mm² skin replica was obtained by illuminating it and feeding it into the computer to calculate the various parameters. Among those parameters, KSD, depth of the skin furrows, was compared between the right and left hands.

The replicas taken in the relaxed position were further analyzed by scanning the surface approximately 1 cm perpendicularly to the direction of the large wrinkles by laser profilometry. Roughness parameters, Ra and Rz, were compared between the right and left hands. Ra represents the area above and below an average line drawn at the central portion of the profile. Rz is the average difference between the maximum heights and nadirs in five equally spaced sections of the profile (Fig. 1).

Statistical analysis

The biophysical parameters obtained by non-invasive measurements and those from the replica image analyzer were analyzed between the exposed and protected skin by using Wilcoxon signed ranks test.

Results

Clinical appearance

The typical clinical feature of the dorsum of the hands of a 47-year-old golfer with a 25-year playing history is shown in Figure 2. Although not so striking as that found on the photodamaged skin of fair skined elderly people, there were more freckles on the skin of the right hand, which was an exposed site during play. Moreover, the right hand had a darker and coarser skin surface accompanied by wrinkles compared to the left hand, which was always protected by a glove during play. More or less similar differences in appearance were noticed in all the golfers studied.

Biophysical non-invasive measurements of the skin

Summary data are shown in Table II. High frequency conductance values were significantly lower on the exposed hand as compared to those on the left hand protected with a glove (Fig. 3a). These differences seemed to be dependent on the length of the past golf playing history (data not shown). In contrast, there was no statistically significant difference in TEWL values between the exposed right and protected left hand. In the golfers, L* value was significantly lower on the exposed skin than the protected one with such differences being dependent on the length of the past golf playing history (data not shown). Although a* and b* values were significantly higher on the exposed skin than the protected hands, the differences in them were not dependent on the length of the past golf playing history.

Morphological study of the skin surface

Computerized image analysis revealed that KSD values, means of the depth of the fine furrows, on the exposed hand was significantly lower than those on the protected hand (Table II), although these changes were not dependent on the length of the past golf playing history. Laser profilometry showed that R_z and R_a values on the exposed hand were significantly higher than those on the protected hand (Table II). The differences were found to be larger in those with a lower handicap (Fig. 4).

Discussion

Concerning intrinsic aging, some researchers reported a decrease in skin surface hydration state [2, 11] whereas others pointed out that this decrease was not always the case with every anatomical site [12]. In contrast, there is no agreement as to the changes in the hydration state of the skin surface with photoaging, although sun-exposed skin has been expected to be drier on the basis of the clinical aspect. Histologically, the SC of photodamaged skin shows variations. Some individuals have a typical basket weave appearance, whereas others display compact or a mixture of basket weave and compact appearance [13]. At any rate, the SC observed under an ordinary microscope does not seem to be appreciably altered morphologically by chronological aging [14].

Long time golf players display a distinct clinical difference between the right and left hands, because one of them has been constantly protected from the environment by a glove during play. In the present study, utilizing this unique situation of the golfers' hands, we measured high frequency conductance, which reflects the hydration state of the SC, to find that it was significantly lower on the sun-exposed hand than on the hand protected by a glove.

The results of the present study performed in middle-aged Japanese golfers definitely indicate that chronic exposure to the outdoor environment induces disorders in the keratinization process that contributes to the lower hydration state in the SC of the exposed skin. We suspect that the dry skin surface of the exposed hand in the golfers was produced mostly due to the chronic sun exposure. However, the effects of other environmental factors such as the exposure to dry air or wind should also be taken into account. The occlusive effect caused by constantly wearing a glove during the play might have also contributed to the hydrated state of the protected skin. Moreover, the right hand was a more sun-exposed side since most of them had driven a car with right-hand drive in Japan for a long time. Not only the environmental influence but also their life style may affect the skin conditions, since the exposed hands are also their dominant hands. However, because we could not find such a difference between the right and left hands of middle-aged Japanese indoor workers (data not shown), the influence of these factors seems to be relatively small.

Although a decrease in TEWL, a parameter for the SC water barrier function, with intrinsic aging has been reported by many investigators [2, 11, 12], there has been no agreement on changes as to the TEWL induced by photoaging. Our present results show that there is no difference in TEWL between the sun-exposed skin and relatively protected skin, at least during the golf play, of the same anatomical portion of the same individuals. Thus, the skin barrier function does not seem to be impaired by the chronic exposure at least until middle age.

One of the most distinct clinical changes of the hands was their color difference between the right and left. The L*a*b* system is most frequently used as biophysical parameters to quantify changes in skin color, in which L* reflects luminance of the color, whereas a* and b* are on the red-green and blue-yellow color scales, respectively. Photoaged skin is generally described as yellowish with erythematous areas, also being associated with telangiectasia and heterogeneity of skin pigmentation. Richard et al. [5] found that standard errors of the mean values in L*a*b* were larger in the exposed skin than those of the adjacent protected skin. Their results seem to be consistent with such color heterogeneity in the photoaged skin. Some authors reported that L* decreased, while a* increased with photoaging [3, 5]. In contrast, others found no change in L*a*b* [15]. Those who reported that L* and b* were decreased and that a* was increased in the aged as compared to the young individuals conducted their measurements on the ventral forearm [16], which is considered to be a relatively photo-protected area. Taken together, a decrease in L* observed in our study seems to occur in cutaneous aging both from the intrinsic aging process and from the chronic UV light exposure.

To analyze skin surface contour, several methods are available including computerized image analysis, mechanical and optical (laser) profilometry [17, 18]. Our study of the skin surface contour with computerized image analysis of microrelief showed that fine furrows became shallower on the sun-exposed hand than the protected one. These results are consistent with those of the study that showed less dense and less deep furrows on the V zone of the neck than on the protected subclavicular zone situated at a very adjacent area [5]. In regard to the reason why the difference in the skin microrelief was not dependent on the length of the past golf play history, we think that the skin phototype of the individuals influenced the degree of dermal skin change. We found that, when the skin was relaxed, large wrinkles or sags became more prominent on the exposed hand in golfers. We showed that roughness parameters increased on the exposed skin as compared to those of protected skin by laser profilometry. Moreover, the differences became larger in those with a lower handicap and longer golf history. We suspect that elastogenesis in the dermis of the photodamaged skin [15] is related to this change. This tendency was also noted in the hands of the middle-aged non-golfers although the difference was not statistically significant (data not shown). We think that this change was mainly caused by the sunlight exposure while driving, because most people drive on the right side of the car in Japan.

We propose that our method of study utilizing the comparison between the exposed and protected hand in the middle-aged golf players is a suitable model to investigate skin aging (damage) influenced by our outer environment, especially by sunlight, because these two sites are anatomically symmetrical, showing the same intrinsic aging process. Such a study performed in more fair-skinned Caucasian golf-players will provide much more clear out characteristics of photodamaged skin.

Article accepted on 21/3/00

CONCLUSION

The present study was supported by a grant from the Cosmetology Research Foundation, Japan. Also the authors give the special thanks to Miss Yuko Nagahamaya for her technical assistance.

REFERENCES

1. Lavker RM. Structural alterations in exposed and unexposed aged skin. J Invest Dermatol 1979; 73: 59-66.

2. Saijo S, Hashimoto-Kumasaka K, Takahashi M, et al. Functional changes of the stratum corneum associated with aging and photoaging. J Soc Cosmet Chem 1991; 42: 379-83.

3. Adhoute H, de Rigal J, Marchand JP et al. Influence of age and sun exposure on the biophysical properties of the human skin: an in vivo study. Photodermatol Photoimmunol Photomed 1992; 9: 99-103.

4. Lévêque JL, Porte G, de Rigal J, et al. Influence of chronic sun exposure on some biophysical parameters of the human skin: an in vivo study. J Cutan Aging Cosmet Dermatol 1988; 1: 123-7.

5. Richard S, de Rigal J, de Lacharriere O, et al. Non-invasive measurement of the effect of lifetime exposure to the sun on the aged skin. Photodermatol Photoimmunol Photomed 1994; 10: 164-9.

6. Tagami H, Ohi M, Iwatsuki K, et al. Evaluation of the skin surface hydration in vivo by electrical measurement. J Invest Dermatol 1980; 75: 500-7.

7. Nilsson GE. Measurement of water exchange through skin. Med Biol Engl 1977; 15: 209-18.

8. Pinnagoda J, Tupker RA, Agner T, et al. Guidelines for transepidermal water loss (TEWL) measurement. Contact Dermatitis 1989; 22: 164-78.

9. Nakayama Y, Kawasaki K, Kumagai H, et al. Application of image analysis to the study of skin Surface microtopography in relation to aging. Cosmetic Dermatology, vol. 1. Rome: International Ediemme, 1986: 187-96.

10. Takahashi M. Image analysis of skin surface contour. Acta Derm Venereol (Stockh) 1994; 185 (suppl.): 9-14.

11. Berardesca E, Farinelli N, Rabbiosi G, et al. Skin bioengineering in the noninvasive assessment of cutaneous aging. Dermatologica 1991; 182: 1-6.

12. Wilhelm KP, Cua AB, Maibach HI. Akin aging. Arch Dermatol 1991; 127: 1806-9.

13. Bhawan J, Oh CH, Lew R, et al. Histopathologic differences in the photoaging process in facial versus arm skin. Am J Dermatopathol 1992; 14: 224-30.

14. Lavker RM. Cutaneous aging: chronologic versus photoaging. In: Photodamage. Gilchrest BA, ed. Cambridge, MA: Blackwell Science. 1995: 123-35.

15. Warren R, Gartstein V, Kligman AM, et al. Age, sunlight, and facial skin: a histologic and quantitative study. J Am Acad Dermatol 1991; 25: 751-60.

16. Pauly G, Gillon V, Le Joliff JC, et al. Fundamental study of skin color in women. Variation with age and cutaneous area. In: Preprints of the 16th IFSCC International Congress 1990: 336-68.

17. Caputo R, Monti M, Motta S, et al. The treatment of visible signs of senescence: the Italian experience. Br J Dermatol 1990; 122 (suppl.) 35: 97-103.

18. Grove GL, Grove MJ, Layde JJ, et al. Skin replica analysis of photodamaged skin after therapy with tretinoin emollient cream. J Am Acad Dermatol 1991; 25: 231-7.