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Keywords:
cardiovascular disease, carotid intima–media thickness, female androgenetic alopecia,
lipid parameters
Copyright © Egyptian Women’s Dermatologic Society. Unauthorized reproduction of this article is prohibited.
70 Journal of the Egyptian Women’s Dermatologic Society
Medicine, Ain Shams University. or greater than 0.8 mm were considered as having
increased IMT, indicating subclinical atherosclerosis [25].
Diagnosis of AGA was based on a detailed history of
onset, course and duration of hair loss, and clinical
findings of the pattern of hair loss. The degree of AGA Statistical analyses
was determined by application of the Ludwig scales (I, II, Statistical analyses were performed using statistical
and III) [22]. Clinical manifestations suggestive of any package for social science (SPSS 15.0.1 for windows;
systemic or endocrinal disease were assessed. Demo- SPSS Inc., Chicago, Illinois, USA; 2001). Numerical
graphic and clinical data of the patients were recorded. data were expressed as mean ± SD and range, whereas
Detailed family histories of AGA, hyperlipidemia, and non-numerical data were expressed as frequency and
CVD were obtained from patients and controls. Data percentage. The Student’s t-test was used to assess the
were also collated on age, body weight (kg) and height statistical significance of the difference between the
(m), and BMI (kg/m2). mean values of the two study groups. Correlation analysis
(using Pearson’s method) was used to assess the strength
Female patients with other causes of diffuse hair loss such of the association between two quantitative variables.
as telogen effluvium; those with any precipitating or The correlation coefficient denoted symbolically as ‘r’
aggravating factors such as trauma, infection, or drug use; defines the strength and direction of the linear relation-
those who had physiological causes of diffuse hair loss ship between two variables. The w2-test was used to
such as pregnancy or lactation; those having other types examine the relationship between two qualitative vari-
of alopecia; those with a known cause of hyperandrogen- ables. Fisher’s exact test was used to examine the
ism such as polycystic ovary syndrome; smokers; those relationship between two qualitative variables when the
with a BMI of 30 or more; and those with a history of expected count is less than 5 in more than 20% of cells.
diabetes, hypertension, cardiovascular, or cerebrovascular A P-value of 0.05 or less was considered significant.
disease were excluded from the study. Patients who had
received any systemic, topical, or intralesional treatment
for AGA during the previous 6 months; those who had
received hormonal replacement therapy with contra- Results
ceptives or chronic corticoid therapy; and those on The age of the patient group ranged from 20 to 60 years,
lipid-lowering therapy, antihypertensive drugs, systemic with a mean of 32.52 ± 7.62 years, whereas that of the
retinoids, antiplatelet aggregation drugs, or oral antidia- control group ranged from 22 to 60 years, with a mean of
betics were also excluded. 31.74 ± 7.44 years. Among the patient group, 13 (26%)
belonged to stage I, 31 (62%) belonged to stage II, and six
After a 12-h fasting period, 5 ml of venous blood samples patients (12%) belonged to stage III AGA on the Ludwig
were withdrawn from every patient for analyzing: serum scale [23] (Fig. 1). The duration of AGA varied from 2 to
levels of total cholesterol (TC; normal: < 200 mg/dl, 20 years, with a mean of 7 ± 4.5 years. The patient group
borderline: 200–239 mg/dl, high: Z240 mg/dl), triglycer- included four (8%) menopausal women out of 50
ides (TG; normal: 35–135 mg/dl), high-density lipopro- compared with three (6%) out of 50 in the control group.
tein cholesterol (HDL-C; normal: 30–85 mg/dl), and low- There was no significant difference as regards the BMI
density lipoprotein cholesterol (LDL-C; normal: between the patient and control groups (range from 19.5
< 130 mg/dl, borderline high: 130–159 mg/dl, high: to 47.9 kg/m2, with a mean of 29.3 ± 6.9 kg/m2 and from
160–189 mg/dl, very high: Z190 mg/dl). These measure- 19.4 to 49.9 kg/m2, with a mean of 28 ± 5.9 kg/m2,
ments were performed through quantitative enzymatic respectively) (P40.05). There was a significant differ-
colorimetric determination using a kit (Quimica Clinica ence as regards the presence of a positive family history of
S.A Company, Tarragona, Spain). The TC : HDL-C and AGA and CVD between patients and controls (84 vs. 4%;
LDL-C : HDL-C ratios were calculated [23]. P = 0.001 and 30 vs. 6%; P = 0.002, respectively).
The IMT of the right and left common carotid arteries for There was a highly significant difference in all serum
all patients were measured using a high-resolution lipid parameters on comparing AGA patients with
B-mode ultrasound with a linear array transducer of controls. Women with AGA, compared with controls,
7.5 MHz (Hitachi model EUB-525; Hitachi Medical showed statistically significantly higher levels of TC
Corp., Tokyo, Japan). The ultrasound was performed at (244.9 ± 32.31 vs. 182.6 6 ± 29.22 mg/dl, respectively;
the unit of Ultrasonography at the Department of P = 0.0001), TG (139.6 ± 28.15 vs. 116.98 ± 55.05 mg/dl,
Copyright © Egyptian Women’s Dermatologic Society. Unauthorized reproduction of this article is prohibited.
Female androgenetic alopecia and dyslipidemia Youssef et al. 71
Figure 1.
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Different stages of female AGA according to the Ludwig scale: (a) stage I, (b) stage II, (c) stage III. AGA, androgenetic alopecia.
respectively; P = 0.002), and LDL-C (179.9 ± 27.98 vs. difference may be due to differences in the ethnicity,
115.18 ± 38.98 mg/dl, respectively; P = 0.0001) and high- habits, and/or lifestyles of both studied populations.
er ratios of TC : HDL-C (6.67 ± 1.35 vs. 4.53 ± 1.53 mg/
Second, as regards the lipid parameters, female patients
dl, respectively; P = 0.0001) and LDL-C : HDL-C (4.92 ±
with AGA showed unmistakable dyslipidemia, as they had
1.21 vs. 2.99 ± 1.48 mg/dl, respectively; P = 0.0001). The
significantly higher mean levels of TC, TG, LDL-C,
HDL-C was significantly lower in patients compared with
TC : HDL-C, and LDL-C : HDL-C when compared with
controls (37.6 ± 6.04 vs. 44.5 ± 14.2 mg/dl, respectively;
healthy controls. The mean levels of HDL-C were found
P = 0.002).
to be significantly lower than those in healthy controls,
The IMT of the common carotid arteries of the patient despite being within the normal range in both groups.
group ranged from 0.3 to 1.6 mm, with a mean of Furthermore, the CVD risk ratios (TC : HDL-C and
0.7 ± 0.31 mm and was significantly increased in compar- LDL-C : HDL-C) were significantly higher than those in
ison with the control group, in which it ranged from 0.4 to controls. Increased LDL-C : HDL-C [27] and TC : HDL-
1.0 mm, with a mean of 0.5 ± 0.1 mm (P = 0.001). The C [28] ratios are considered sensitive predictors of CVD
main demographic, clinical, laboratory, and imaging risk. Elevated levels of TG and low levels of HDL-C are
features of the studied patients are presented in Table 1. well known to be associated with the development of
atherosclerosis and the transition from atheroma to
On using the Pearson correlation coefficient test, no
atherothrombosis [29].
correlation was detected between the mean levels of TC,
TGs, HDL-C, LDL-C and each of the age of the female It is important to specify that female patients in the
patients, their BMI, or the duration and stage of AGA present study were not diabetic or hypertensive and had
(P40.05). However, the same variables (age, BMI, and no previous history of CVD, which are all known risk
duration and stage of female AGA) showed a highly factors of hyperlipidemia. Therefore, this state of
statistically significant correlation with the mean values increased lipid parameters in women with AGA leads us
of IMT (Po0.01) (Table 2 and Fig. 2). to assume that AGA is a risk factor of future CVD, even in
absence of other risk factors of cardiac disease.
The results of the present study support those of
Discussion previous studies [20,26,30] that reported that women
The results of the present study support the theory that with AGA have higher significant mean levels compared
women with AGA are at higher risk for developing cardiac with nonalopecic women in terms of TG, LDL-C, TC,
diseases. This conclusion has been drawn on the basis of TC : HDL-C, and LDL-C : HDL-C and lower significant
the following findings: First, a highly statistically sig- HDL-C levels when compared with healthy controls.
nificant positive family history of CVD was found in There was no correlation between increased lipid
women with AGA when compared with age-matched and parameters and both the Ludwig stage of AGA and BMI
BMI-matched controls. This indicates that both AGA and in patients of the present study, which is concordant with
CVD may be linked together either through a common the results of another study by Arias-Santiago et al. [30].
genetic predisposition or a casual relationship. However, It is apparent that the degree of expression of AGA is
such an association was not detected when Arias-Santiago dependent primarily on genetic factors. In contrast,
et al. [26] carried out a study on 150 male and female women with AGA in a study by Matilainen et al. [31]
Spanish patients with AGA and compared them with age- did not show significant differences in their lipid profiles
matched and sex-matched controls; This remarkable or BMI when compared with women without AGA,
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72 Journal of the Egyptian Women’s Dermatologic Society
Table 1. Comparison between women with androgenetic alopecia and controls as regards various demographic data and clinical,
laboratory, and radiological findings
Groups [mean ± SD or n (%)]
Table 2. Correlation between the mean of carotid intima–media despite of presence of greater central obesity in AGA
thickness and different variables women compared with those with normal or minimal hair
Parameters IMT (mm) loss. The absence of differences in lipid parameters
between AGA patients and controls may be because the
Age (years)
r 0.483 authors of the previous study did not exclude patients
P 0.0001a who were receiving lipid-lowering drugs.
BMI (kg/m2)
r 0.444 Third, as regards the measurement of common carotid
P 0.001a
Duration of AGA (years) artery IMT, our study showed that women with AGA had
r 0.587 higher values of common carotid IMT compared with
P 0.0001a controls. This reinforces the finding of Arias-Santiago
Stage of AGA
r 0.516 et al. [18] who confirmed the association between early-
P 0.0001a onset AGA and higher cardiovascular risk in both male
AGA, androgenetic alopecia; IMT, intima–media thickness. and female groups and found a higher prevalence of
a
Significant. carotid atheromatosis in patients with AGA compared
with healthy patients. The relationship between the
vertex pattern AGA in men and carotid atherosclerosis
and the hypothesis that AGA could be considered as an
Figure 2. additional increased risk for premature atherosclerosis
have previously been proved in men [12].
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Female androgenetic alopecia and dyslipidemia Youssef et al. 73
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74 Journal of the Egyptian Women’s Dermatologic Society
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