cigarette smoking associated with premature facial wrinkling: image analysis of facial skin replicas
TRANSCRIPT
© 2002
The International Society of Dermatology International Journal of Dermatology
2002,
41
, 21–27
21
Abstract
Background
Despite the obvious relation between smoking and facial wrinkling, grossly
undetectable wrinkling and the consequences of smoking on the face have been poorly studied.
Objective
To assess the risk factor of cigarette smoking on the development of premature facial
wrinkling.
Methods
One hundred and twenty-three nonsmokers, 160 current smokers, and 67 past
smokers, aged 20–69 years, were studied. Cigarette smoking status, weight changes, average
sun exposure time (recreational and occupational) in 1 month, and past medical and facial
cosmetic surgery were quantified by self-questionnaire. Computerized image analysis of
silicone skin replicas was used in addition to clinical visual measurement, and a severity score
based on predetermined criteria was assigned to each patient.
Results
Current smokers have a higher degree of facial wrinkling than nonsmokers and past
smokers. Past smokers who smoked heavily at a younger age show less facial wrinkling than
current smokers. In the analysis, which was adjusted for age group, the relative risk of moderate
to severe wrinkling for current smokers compared with nonsmokers was 2.72 (confidence
interval, CI: 1.32–3.21,
P
< 0.05). In current smokers, the relative risks associated with more
than 19 pack-years and 11–19 pack-years of smoking compared with nonsmokers were 2.93
(CI: 1.14–4.1,
P
< 0.05) and 1.75 (CI: 1.54–3.67,
P
< 0.05), respectively. On image analysis of
facial skin replicas, the mean values of Ra (arithmetic average roughness), Rz (average
roughness), and Rt (distance between the highest and lowest values) of current smokers were
higher than those of nonsmokers and past smokers in all age groups. This indicates a strong
correlation between cigarette smoking and skin wrinkling. In addition, microscopic superficial
wrinkling (Ra and Rt) was noted in current smokers in the younger age group (20–39 years).
Conclusions
This study suggests that attention should be paid to smoking-associated facial
wrinkling (not evident from a visual assessment) in young people and added to the list of
disorders seemingly caused by smoking.
Blackwell Science Ltd
Report
Cigarette smoking and premature facial wrinkling
Cigarette smoking associated with premature facial wrinkling: image analysis of facial skin replicas
Jae Sook Koh,
P
h
D
, Hoon Kang,
MD
, Sung Woo Choi,
MD
, and Hyung Ok Kim,
MD
From the Department of Dermatology, College of Medicine, The Catholic University of Korea, Seoul, South Korea
Correspondence
Hyung Ok Kim,
MD
Department of Dermatology Kangnam St. Mary’s Hospital The Catholic University of Korea 505, Banpo-dong, Seocho-ku Seoul, 137-040 South Korea E-mail: [email protected]
Introduction
Facial skin aging takes place gradually with little clinicalevidence. It is recognized by the emergence of wrinkles,together with a loss of skin tone. Wrinkling has been the sub-ject of considerable interest for many years, and a number ofinvestigations have been carried out on wrinkling of the face.
In 1856, Solly proposed several adverse effects of smokingon the skin, including a pale sallow skin color, increasedwrinkling, and a gaunt facial appearance.
1
Since then, severalreports have demonstrated the effects of cigarette smoking onskin quality, such as wrinkling, color, and tone.
2–5
Despite theobvious relationship between smoking and facial wrinkling,grossly undetectable wrinkling and the consequences of smokingon the face have been poorly studied. Cursory examination
of the skin with the naked eye can reveal deep facial wrinklesthat are the result of a decrease in the quality of collagen andelastic fibers in the reticular dermis. This study is an attemptto measure directly the fine wrinkles on the face, which maybe caused by cigarette smoking, and to provide smokers withan effective motivation to stop smoking, especially those whomay be concerned about their appearance.
Subjects and methods
Subjects and basic data collection
Subjects were recruited from the dermatologic clinics at Kangnam
St. Mary’s Hospital, Our Lady of Mercy Hospital and the National
Medical Center in South Korea between September 1, 1997 and
June 30, 1999. In order to avoid selection bias, we enrolled
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Cigarette smoking and premature facial wrinkling
Koh
et al.
subjects who volunteered during the study period and randomly
selected from them. All participating subjects were arranged by
age in five 10-year age groups between 20 and 69 years.
They were asked to complete a self-questionnaire, which
contained information on their cigarette smoking status, weight
changes, average sun exposure time in 1 month, both recreational
and occupational, and past medical and facial cosmetic surgery.
To determine the quantity of exposure to cigarette smoke, each
subject was asked how many packs of cigarettes per day they had
smoked since taking up smoking. The number of packs per day
and the number of years of smoking were used to generate an
exposure value to smoke. This value is called a pack-year. If a
patient smokes one pack per day for one year, this is equivalent to
“1 pack-year.” The average sun exposure time for 1 month was
calculated by multiplying the duration of exposure by the number
per month of exposure since the age of 20 years; only subjects
whose outdoor exposure time was less than 30 h were selected.
To exclude the medical or artificial factors affecting facial wrinkling,
we chose subjects who had never undergone facial cosmetic
surgery and had never used antiwrinkling agents.
Classification of smoking groups
According to a previous report by Model,
6
all subjects were
arranged by smoking status into three groups: nonsmokers,
current smokers, and past smokers. Nonsmokers were defined as
those who smoked fewer than 10 cigarettes a week or had smoked
for less than 10 years, or both. Current smokers were defined as
those who, within the past year, had smoked 10 or more cigarettes
a week and had smoked for 10 years or more. Past smokers were
those who had not smoked within the past year, but had smoked
10 or more cigarettes a week for 10 years or more prior to that.
Visual examination of crow’s feet wrinkling
Before examination, all participants were asked to wash their faces
and to avoid wearing makeup, and were then allowed to relax on
a comfortable diagnostic bed in a well air-conditioned room. Four
well-trained dermatologists closely examined their right crow’s feet
area, which extends radially from 0.5 cm medial to the lateral
canthus of the right eye to the hairline. To determine the degree of
wrinkling, a modified Daniell’s skin wrinkle grading method
2
was
used, as shown in Table 1. We defined a grade III wrinkle as
moderate and a grade IV or V wrinkle as severe.
Skin replicas and image analysis
The silicone rubber used for skin replication was Silflo® resin
(Flexico Development Ltd, Potters Bar, UK). The replicas were
taken from the crow’s feet area to quantify the fine variations in skin
wrinkles. An adhesive paper ring (diameter, 11 mm) was attached
to the objective site of the crow’s feet area. Care was taken to
preserve the orientation of the replica with respect to the lateral
canthus of the right eye to allow for accurate interpretation. A layer
of silicone mixture (thickness, 2 mm) was spread over the
restricted area of the adhesive paper and left to dry for 5 min. After
the silicone mixture had dried sufficiently, the specimen was
identified by subject number, initials and date and was stored in a
tracing paper envelope until removed for analysis.
The skin replicas were analyzed using the SKIN-VISIOMETER
SV 500® (Courage-Khazaka Electronic GmbH, Germany). The
silicone skin replica was placed in a special holding device and then
inserted into a rotator system graduated in degrees. A floodlight,
oriented with an incidence angle of 26
°
to generate shadows behind
the crests, illuminated the replica. The shadows from the crests
were detected and analyzed by a video-sensor charge coupled
device (CCD) camera (752
×
582 pixel) located on the opposite
side of the specimen. Under these conditions, we rotated the skin
replica in 90
°
increments from 0
°
to 360
°
. Visualization was performed
by a video digitalization unit and a PC equipped with a graphics
card. The device was connected to the digitalization unit by coaxial
cord. On the PC screen, the contours of the picture were displayed
in a corresponding classification in 256 gray values (0, black; 256,
white), and were calculated in micrometers by the software.
The analysis of the data yielded several parameters proportional
to the degree of wrinkling, roughness, and other surface markings,
including Ra, Rz, and Rt, which were found to be especially useful.
Ra represents the arithmetic average roughness, i.e. the area
surrounded by the profile and the middle line divided by the middle
line. Rz is the average roughness, i.e. the arithmetic average of the
different segment roughnesses calculated from five succeeding
measurement segments of the same length. Rt is the distance
between the highest and lowest values. To ensure consistency of
computer settings, lighting, and other technical variables, the
same operator performed image analysis on all replicas at the
conclusion of the study. The analyses were carried out with no
knowledge of the previous smoking history or other clinical data.
Statistical analysis
Statistical analyses were performed using SPSS for Windows. To
calculate odds ratios of visual wrinkle grade, logistic regression
modeling was used with the presence of moderate or severe
wrinkling as the outcome. Multiple linear regressions and multiple
analyses of variance for repeated measures (
ANOVA
) were used to
model bivariate relationships. Confidence intervals for the
Table 1 Facial skin wrinkle grading
Grade Skin appearance
I Essentially unwrinkled; minimal shallow wrinkles may be present
II Uniform shallow wrinkles with or without 1–3 wrinkles of moderate depth
III Uniform moderate wrinkles present throughout the temple area
IV Development of up to four large deep wrinkles superimposed on a moderately wrinkled background
V Numerous large deep wrinkles present or a complex cross-hatched pattern of wrinkles
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2002,
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, 21–27
23
Koh
et al. Cigarette smoking and premature facial wrinkling
Report
correlations were calculated to evaluate the accuracy of the
regressions, and image analysis data were assessed using the
nonparametric Mann–Whitney
U
-test. All values were expressed
as the mean
±
standard deviation (SD).
Results
Study population
Of the 432 subjects enrolled in this study, 350 were eligiblefor statistical analyses. Of the 82 subjects who were not suit-able for our study, 14 failed to complete the questionnaire, 43were deemed invalid for our protocol due to their monthlysun exposure time, and 25 showed an unacceptable replica-tion pattern on analysis. The distribution of subjects by age
group and smoking status is shown in Table 2. As describedpreviously, the subjects were arranged into three groupsaccording to their smoking status: 123 (34.8%) nonsmokers,160 (46.0%) current smokers, and 67 (19.2%) past smokers.In the group of current smokers, the number of pack-yearsof cigarette smoking ranged from 2 to 84 and revealed anincreasing trend with increasing age.
Visible wrinkling according to cigarette smoking
We examined the effect of cigarette smoking on facial wrin-kling according to age group. The distribution of the subjectpopulation, classified according to the modified gradingmethod of Daniell, is shown in Table 3. The percentage ofsubjects who presented with high wrinkle grades increased
Age group (years) Smoking status Total
Non (column %) Past (column %) Current (column %)
20–29 69 (56.1) 22 (32.8) 70 (43.8) 1616.8 ± 2.9*
30–39 23 (18.7) 21 (31.3) 53 (33.0) 9710.8 ± 5.8*
40–49 16 (13.0) 4 (6.0) 18 (11.3) 3825.3 ± 11.4*
50–59 12 (9.8) 5 (7.5) 7 (4.4) 2445.7 ± 14.8*
60–69 3 (2.4) 15 (22.4) 12 (7.5) 3056.6 ± 19.6*
Total 123 67 160 35015.6 ± 16.8*
*Pack-years (mean ± SD).
Table 2 Number of subjects by age group and smoking status
Smoking group Age group (years) Wrinkle grade (% of each age group) Total
Mild Moderate Severe
Non 20–29 69 (100.0%) 6930–39 19 (82.6%) 4 (17.4%) 2340–49 11 (68.8%) 4 (25.0%) 1 (6.3%) 1650–59 4 (33.3%) 8 (66.7%) 1260–69 3 (100.0%) 3
Current 20–29 69 (98.6%) 1 (1.4%) 7030–39 47 (88.7%) 4 (7.5%) 2 (3.8%) 5340–49 6 (33.3%) 6 (33.3%) 6 (33.3%) 1850–59 2 (28.6%) 5 (71.4%) 760–69 12 (100.0%) 12
Past 20–29 20 (99.1%) 2 (0.9%) 2230–39 15 (71.4%) 6 (28.6%) 2140–49 2 (50.0%) 2 (50.0%) 450–59 2 (40.0%) 3 (60.0%) 560–69 4 (26.7%) 11 (73.3%) 15
Total 256 41 53 350
Table 3 Distribution of wrinkle grade by age and smoking status
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Cigarette smoking and premature facial wrinkling
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with age in all groups. Current smokers had a higher wrinklegrade than nonsmokers and past smokers. Past smokers whosmoked heavily at a younger age showed less facial wrinklingthan current smokers.
To investigate the effect of cigarette smoking duration onmoderate to severe facial wrinkle formation, current smokerswere classified by pack-years: < 10, 11–19, and > 19. Duringdata analysis, it was found that all subjects in the 20–29-yearage group had few moderate to severe facial wrinkles. It wasdecided not to enroll this age group in the analysis of pack-years of smoking (Table 4). In the analysis adjusted for agegroup, the relative risk (RR) of moderate to severe wrinklingfor current smokers compared to nonsmokers was 2.72 (con-fidence interval, CI: 1.32–3.21,
P
< 0.05). In current smokers,the RRs associated with more than 19 pack-years and 11–19pack-years of smoking compared with nonsmokers were 2.93(CI: 1.14–4.1,
P
< 0.05) and 1.75 (CI: 1.54–3.67,
P
< 0.05),respectively. In past smokers, only the group with more than19 pack-years of smoking showed significantly elevated RRcompared with nonsmokers (RR = 1.67, CI: 1.33–2.99).
Although subjects with more than 19 pack-years of ciga-rette smoking presented with a higher percentage of moderateor severe wrinkles than the low pack-years group, there wasno consistent dose–response gradient between pack-years andwrinkle category (Fig. 1).
Image analysis of crow’s feet replicas
Replicas taken from the crow’s feet area were measured byimage analyzer with no intervening changes in instrumentalset-up. The representative data for each age group by smokingstatus are presented as Ra, Rz, and Rt. As shown in Fig. 2, the
means of all the parameters of current smokers were higherthan those of nonsmokers and past smokers in all age groups.These findings indicate that a possible relationship existsbetween cigarette smoking and wrinkling. In the 20–29-yearage group, the means
±
SD of Ra and Rz of current smokers(Ra: 4.31
×
10
–2
±
7.9
×
10
–3
; Rz: (0.21
±
2.10)
×
10
–2
) werestatistically significantly higher (
P
< 0.05) than the meansof nonsmokers (Ra: 2.60
×
10
–2
±
5.12
×
10
–3
; Rz: (0.13
±
Table 4 Distribution of wrinkle grade by age group and pack-years of cigarette smoking in current smokers
Age group (years) Pack-years of smoking Wrinkle grade (% of pack-years of smoking) Total
Mild Moderate Severe
21–29 < 10 61 (98.4%) 1 (1.6%) 6210–20 8 (100.0%) 8Total 69 (98.6%) 1 (1.4%) 70
30–39 < 10 18 (86.7%) 2 (6.7%) 2010–20 26 (90.0%) 2 (10.0%) 2 (6.7%) 30> 21 2 (66.7%) 1 (33.3%) 3Total 46 (86.8%) 5 (9.4%) 2 (3.8%) 53
40–49 10–20 4 (44.4%) 4 (44.4%) 1 (11.1%) 9> 21 2 (22.2%) 2 (22.2%) 5 (55.6%) 9Total 6 (33.3%) 6 (33.3%) 6 (33.3%) 18
50–59 10–20 1 (100.0%) 1> 21 1 (16.7%) 5 (83.3%) 6Total 2 (28.6%) 5 (71.4%) 7
60–69 > 21 12 (100.0%) 12Total 12 (100.0%) 12
Figure 1 Percentage of subjects with moderate to severe crow’s feet wrinkling by age group and pack-years of cigarette smoking
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, 21–27
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Koh
et al. Cigarette smoking and premature facial wrinkling
Report
3.12)
×
10
–2
) and past smokers (Ra: 2.70
×
10
–2
±
5.91
×
10
–3
;Rz: (0.14
±
1.02)
×
10
–2
). In the 30–39-year age group, as inthe 20–29-year age group, all three parameters of currentsmokers (Ra: 4.75
×
10
–2
±
6.79
×
10
–3
; Rz: (0.22
±
3.21)
×
10
–2
) showed significantly higher values (
P
< 0.05) than thoseof nonsmokers (Ra: 2.64
×
10
–2
±
7.80
×
10
–3
; Rz: (0.12
±
2.12)
×
10
–2
) and past smokers (Ra: 2.83
×
10
–2
±
8.82
×
10
–3
;Rz: (0.13
±
5.19)
×
10
–2
). The mean values of Ra and Rzobtained from past smokers were, however, not significantlydifferent from those obtained from nonsmokers in the 20–29-year and 30–39-year age groups. In contrast to the youngerage groups (between 20 and 39 years), there were no statisticallysignificant differences in the older age groups (age between 40and 69 years).
Rt demonstrated reverse results compared to Ra and Rz.In the age groups 50–59 and 60–69 years, the Rt values ofcurrent smokers (50–59 years: (0.58
±
5.03)
×
10
–2
; 60–69 years: (0.64
±
6.12)
×
10
–2
) were significantly higher(
P
< 0.05) than those of nonsmokers (50–59 years: (0.43
±
4.22)
×
10
–2
; 60–69 years: (0.48
±
5.14)
×
10
–2
) and pastsmokers (50–59 years: (0.46
±
5.17)
×
10
–2
; 60–69 years:(0.50
±
8.10)
×
10
–2
).A similar analysis was performed to examine the effect of
the number of pack-years of cigarette smoking on wrinklingfor subjects aged 30–69 years in the current smoking group.Ra and Rz were significantly higher (
P
< 0.05) in the > 19pack-years group than in the 10–19 and < 10 pack-yearsgroups. No differences were found, however, between the10–19 pack-years group and the < 10 pack-years group. Inaddition, no association was evident between Rt and thenumber of pack-years of smoking in current smokers (Fig. 3).
Discussion
The aging process is an unavoidable, dynamic phenomenonthat induces progressive functional reduction in all systems in
Figure 2 Results of Ra, Rz and Rt measurements on crow’s feet for all age groups by smoking status. *Statistically significant compared to nonsmokers and past smokers
Figure 3 Results of Ra, Rz and Rt measurements on crow’s feet in current smokers by pack-years. *Statistically significant compared to 10–19 and < 10 pack-years
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the body and increased susceptibility to disorders. The degreeof aging depends on genetic factors, life span, various dis-orders, drugs, and environmental factors.
7
Concerning the skin,most of the commonly observed aging processes result fromrepetitive environmental stimulations in combination withchronological factors. Of these environmental factors, a closecorrelation between cigarette smoking and skin changes hasbeen suggested by several investigators.
2,4–6,8
Effects of ciga-rette smoking on skin quality criteria, such as color, turgor,facial complexion, and facial wrinkling, have been observed.
On visual assessment, we found that current cigarettesmokers have more facial wrinkles than nonsmokers and pastsmokers. Furthermore, among current smokers, the RR ofmoderate to severe wrinkling appears to increase after 11pack-years of smoking compared with that of nonsmokersand past smokers. These findings are in agreement with otherstudies,
2,9
except for the 20–29-year age group. In general,wrinkling occurs with aging whether or not clothing protectsthe skin. Wrinkles are precocious in sun-exposed areas, andslow to appear in protected skin areas. Skin changes broughtabout by UV damage and by aging do not differ in quality,only in quantity.
10
In this regard, it is very difficult to detectwith the naked eye some wrinkles occurring in young persons.In the study of Ernster
et al.
,
9
it was suggested that the effectsof smoking on facial wrinkling do not appear until middle age.By contrast, the initiation of cigarette-associated wrinkling inour study occurred earlier than that suggested by previousinvestigators. This discrepancy could be partly the result ofthe use of computer-generated skin replica measurements toevaluate wrinkling.
Most of the previous studies on smoking-associatedwrinkling have been carried out by visual assessment only.Although perceptible changes in the skin observed using thevisual grading system more or less correspond to clinicalfeatures, the method is subjective and prone to interobserverbias.
11
The use of skin image analysis in the study of wrinklingis becoming increasingly more widespread in the dermatologicfield. The skin replica technique provides a number of advan-tages, such as ease of operation, stability, and simple storage.
11
Nevertheless, in the case of crow’s foot wrinkles, as the numberof significant events is relatively small, studies of wrinkles inthis area must be based on strictly identical areas of analysis.In addition, it is best to use approaches that analyze as largean area as possible, and a large number of samples.
Although the results of this study were obtained from anobjective method of evaluation, we cannot entirely rule outthe possibility of bias in several confounding factors. Thesefactors include socioeconomic status, skin type, sun protec-tion products, occupation-related sun exposure, geographicarea, and the small number of subjects. We minimizedseveral biases by excluding subjects who were exposed tosunlight for over 30 h per month, had undergone cosmeticsurgery, and had used antiwrinkling agents. Our questionnaire
was designed to check for confounding factors, and subjectswho did not comply with the protocol of this study wereexcluded.
Although the pathomechanisms of wrinkling by cigarettesmoking remain unclear, some investigations have shown aclose relationship between the toxic components of cigarettesand skin changes. Cigarette smoke has been shown to increaseplasma neutrophil elastase activity
12
and the inactivationof
α
-1-proteinase inhibitor, which may also contribute toabnormal elastin.
13
These effects resemble those of actinicelastosis, except that they occur in the mid- and reticulardermis while the papillary dermis remains unaffected.Smoking-induced peripheral vasoconstriction may inducelocal dermal ischemia,
4,14 and this may play a role in decreasedcollagen synthesis and elastic fiber changes.15 Smoking mayalso contribute to facial wrinkling by decreasing vitamin Alevels and facial stratum corneum moisture, which areinvolved in premature wrinkling.16,17 In addition, continuousclose contact with or exposure to cigarette heat causes pre-mature skin wrinkling in smokers.18
This study suggests that attention should now be paid tosmoking-associated facial wrinkling in young people, althoughit is not evident by unaided visual assessment. Becausesmoking-associated wrinkling is not readily apparent in theearly stages, compared to photoaging, many young personsunderestimate the harmful cumulative effects of smoking onthe skin. Nonetheless, the computer-generated data obtainedin this study – showing greater changes in Ra and Rz ofcrow’s feet replicas than in Rt – support the presence ofsuperficial fine wrinkling after smoking. Age-associatedfacial wrinkling is a naturally occurring result of aging. Thedetrimental effects of smoking are likely to be additivewith those induced by aging and sun exposure. Therefore,microscopic premature wrinkling in young people shouldnow be added to the list of disorders that seem to be causedby smoking, although further studies will be necessary toestablish a causal relationship. Smokers need to be madeaware of the increased risks of premature skin aging as aresult of their smoking habit, which hopefully may lead to thedecision to stop smoking.
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