Using the Androgen ExcessPCOS Society Criteria to Diagnose Polycystic

Ovary Syndrome and the Risk of Metabolic Syndrome in Adolescents

Andrea Hsu Roe, MD1, Erica Prochaska, BS1, Matthew Smith, BS1, Mary Sammel, ScD2, and Anuja Dokras, MD, PhD1

Objectives To use the Androgen ExcessPCOS Society (AE-PCOS) criteria in adolescents to diagnose polycystic
ovary syndrome (PCOS) and identify the prevalence of metabolic risk factors.
Study design Retrospective chart review of adolescents (>2 years postmenarche) presenting at a specialty clinic
from 2008 through 2010 with complete evaluation for PCOS and metabolic risk were reviewed. Metabolic risk in
adolescents with PCOS was compared with those with #1 AE-PCOS criteria.
Results Of the 205 adolescents evaluated, 66% were found to have PCOS based on the AE-PCOS criteria. The
most common presenting symptom was menstrual irregularity, followed by acne, hirsutism, and weight gain.
Adolescents with PCOS had a significantly higher prevalence of obesity, hypertension, and low level of high-
density lipoprotein cholesterol. Subjects with PCOS had $1 metabolic risk factor compared with the subjects with-
out PCOS (63.6% vs 33.3%, P = .002). More adolescents with PCOS had $2 abnormal metabolic risk factors
excluding body mass index compared with those without PCOS (P < .02). The prevalence of metabolic syndrome
($3 risk factors) was 10.8% in adolescents with PCOS compared with 1.7% in those without PCOS (P < .04).
Conclusions Adolescents diagnosed with PCOS based on the AE-PCOS criteria are at a significantly increased
risk of $1 metabolic abnormality. Our data underscore the need to accurately diagnose PCOS in the adolescent
population instead of delaying the diagnosis to adulthood. Further, using similar criteria for the diagnosis of
PCOS in adolescents (>2 years postmenarche) and adults will be more convenient for the clinician. (J Pediatr
2013;162:937-41).

W
ith increasing awareness and clarity in diagnostic criteria for polycystic ovary syndrome (PCOS), a number of adult
women are evaluated for this condition. There are currently 3 diagnostic sets of criteria used for adults: the National
Institutes of Health (NIH), Rotterdam, and Androgen ExcessPCOS Society (AE-PCOS) criteria. The NIH criteria
define PCOS as the presence of oligomenorrhea/anovulation and clinical or biochemical hyperandrogenism. The Rotterdam
criteria include women with any 2 of the following 3 criteria: oligomenorrhea/anovulation, clinical or biochemical hyperan-
drogenism, and polycystic ovaries on ultrasound. The AE-PCOS criteria include women with oligomenorrhea/oligoovulation
or polycystic ovaries on ultrasound and clinical or biochemical hyperandrogenism. In all cases, other conditions such as
hypothyroidism, hyperprolactinemia, and adrenal disorders that mimic the symptoms of PCOS need to be excluded. As ado-
lescents transition through puberty, they commonly have symptoms mimicking all of the diagnostic criteria for PCOS such as
oligomenorrhea/anovulation, signs of clinical hyperandrogenism, and the appearance of polycystic ovaries on ultrasound.
Irregular menses are commonly present during the first few years after menarche. By 2 years postmenarche, the majority of
adolescent menstrual cycles are normal according to adult standards.1 Based on these findings, it has been suggested that
the diagnosis of PCOS should be deferred during the first 2 years after menarche.2 Clinical hyperandrogenism is also difficult
to evaluate during adolescence as there is no standardized grading system targeted specifically to this age group for either acne
or hirsutism. Proposed risk factors for PCOS, including prenatal exposure to androgens, low birth weight, and premature
pubarche, are not well established.3 As a result of these limitations, some women diagnosed with PCOS in adolescence do
not meet the established criteria for PCOS on further evaluation as adults.
Given the challenges for diagnosis of PCOS in adolescents, some investigators have suggested use of different criteria specific
to the adolescent period. On the other hand, it has been argued that accurate diagnosis of PCOS may not be essential during the
transitional adolescent period, because clinical management of the patient is usually unaltered.

AE-PCOS Androgen ExcessPCOS Society From the 1Division of Reproductive Endocrinology and
Infertility, and 2Center for Clinical Epidemiology and
BMI Body mass index Biostatistics, University of Pennsylvania,
BP Blood pressure Philadelphia, PA
FG FerrimanGallwey The authors declare no conflicts of interest.
HDL-C High-density lipoprotein cholesterol Portions of the study were presented at the annual
NIH National Institutes of Health meeting of the American Society of Reproductive
Medicine, Orlando, FL, October 17-19, 2011.
PCOS Polycystic ovary syndrome
TG Triglycerides 0022-3476/$ - see front matter. Copyright 2013 Mosby Inc.
All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2012.11.019

937
THE JOURNAL OF PEDIATRICS  www.jpeds.com Vol. 162, No. 5

The AE-PCOS guidelines consider hyperandrogenism as cholesterol (HDL-C) #40 mg/dL, blood pressure (BP)
the core abnormality in PCOS and define the syndrome by $90th percentile for age (http://www.nhlbi.nih.gov/
the presence of clinical or biochemical hyperandrogenism guidelines/hypertension/child_tbl.pdf) or taking antihyper-
and irregular menses/anovulation or polycystic appearing tensive medication, and fasting blood glucose $100 mg/dL
ovaries on ultrasound.4 The aims of our study were to deter- or the presence of type 2 diabetes mellitus.6
mine the usefulness of the adult AE-PCOS criteria in the
diagnosis of adolescent subjects referred to a specialty prac- Statistical Analyses
tice. Second, we wanted to determine the metabolic risk in Pearson c2 test was performed to compare differences with
adolescents with AE-PCOSdefined PCOS compared with categorical variables. The 2-sample t tests were used to com-
those adolescents who were referred to our practice but did pare differences between means of the biochemical variables.
not meet these criteria. The differences in the overall metabolic risk (1-4) criteria was
analyzed using the Wilcoxon rank sum test. Logistic regres-
Methods sion analysis was used to control for variables such as age
and race. ORs along with 95% CIs measure the association
A retrospective chart review was performed of medical between PCOS diagnosis and each metabolic risk factor
records of all adolescents (#20 years) presenting to a spe- and metabolic syndrome.
cialty gynecology clinic from 2008 through 2010 for evalu-
ation of PCOS. Medical records were reviewed for Results
demographic information, clinical history, and laboratory
data. This study was approved by the Institutional Review Of the 205 subjects who met the inclusion criteria of our study,
Board at the University of Pennsylvania. Diagnosis of 34.6% did not meet the AE-PCOS criteria for PCOS. Table I
PCOS was confirmed by the AE-PCOS criteria4 as follows: shows the demographic information for the 148 adolescents
hyperandrogenism was defined as biochemical (total testos- with PCOS with both AE-PCOS criteria and 57 subjects
terone $55 ng/mL) or clinical (FerrimanGallwey [FG] without PCOS (#1 AE-PCOS criteria). The majority of the
score $8), irregular menses were defined as menses #9 adolescents with PCOS in our study (140/148) also met the
times per year, and polycystic appearing ovaries were de- NIH criteria. The mean age at presentation at our center was
fined as either ovary having a volume of $10 cm3 on ab- similar for the 2 groups. The majority of the subjects were
dominal or transvaginal ultrasound.5 Only volume criteria white. A higher proportion of adolescents with PCOS had
were used for ultrasound measurements, recognizing that a family history of PCOS, diabetes, hypertension, coronary
antral follicle counts are not a reliable finding for PCOS artery disease, and hyperlipidemia. All subjects were screened
in adolescents.2 We obtained an ultrasound when the diag- for other endocrine conditions that mimic the features of
nosis of PCOS could not be clearly established based on PCOS, such as hypothyroidism, hyperprolactinemia, and
menstrual frequency history and hyperandrogenism. All adrenal conditions (Table II). Six adolescents with PCOS
subjects with only hyperandrogenism or only menstrual ir-
regularity had ultrasound results. All oligomenorrheic sub-
jects were at least 2 years postmenarche. If a subject was Table I. Demographic information for adolescents with
taking combined oral contraceptives, she was asked to and without PCOS based on the AE-PCOS criteria
stop for 8 weeks before testosterone measurements. The Demographics PCOS (2 criteria) No PCOS (1 criteria)
turbulent-flow liquid chromatographymass spectrometry No. 148 57
method was used to measure total testosterone levels Age at presentation, y 16.9  1.9 16.6  2.5
Age range, y 13-20 14-20
(ARUP Laboratories, University of Utah Research Park, Age at menarche, y 12.2  1.6 12.4  1.4
Salt Lake City, Utah). Additional laboratory tests abstracted Race, %
from the medical records to establish the diagnosis of PCOS White 73.7 83.0
Black 14.5 5.7
included thyroid-stimulating hormone, prolactin, dehy- Asian 4.6 1.9
droepiandrosterone sulphate, and 17-hydroxyprogesterone Unknown 0.7 0.0
levels. Other 6.6 9.4
Ethnicity, %
Adolescents who presented to our center and did not meet Hispanic 3.3 1.9
the earlier AE-PCOS criteria (who had none or only 1 crite- Non-Hispanic 89.5 98.1
rion) were compared with the PCOS group. Of 400 charts Unknown 7.2 0.0
reviewed, 205 adolescents had adequate data to be accurately Maternal Paternal Maternal Paternal
classified according to the AE-PCOS criteria and had labora- Family history, %
tory testing to define metabolic risk and the presence or PCOS 9 0 0 0
absence of metabolic syndrome. Subjects were classified as Diabetes mellitus 26* 16* 1 0
Hypertension 21* 18* 1 0
having metabolic syndrome if they met 3 of the following Coronary artery disease 10* 10* 0 0
5 criteria based on the modified Cook criteria: body mass Hyperlipidemia 14* 12* 0 0
index (BMI) >90th percentile, serum triglycerides (TG) Values for age are mean  SD.
level $150 mg/dL, serum high-density lipoprotein *P < .01.

938 Roe et al
May 2013 ORIGINAL ARTICLES

Table II. Endocrine profile in adolescents evaluated for Table III. Metabolic risk factors in adolescents with and
the diagnosis of PCOS without PCOS
PCOS No PCOS PCOS No PCOS
(2 criteria) (1 criteria) (2 criteria) (1 criteria)
Thyroid-stimulating hormone, mIU/mL 2.2  1.5 1.8  0.9 Systolic BP, mm Hg 117.3  13.3 111.4  11.6
Prolactin, ng/mL 11.6  6.4 8.9  3.6* Diastolic BP, mm Hg 70.1  8.8 70.8  6.7
17-OH progesterone, ng/dL 80.2  62.2 66.7  86.7 Fasting glucose, mg/dL 81.1  13.8 80.8  10.2
Dihydroepiandrosterone sulphate, ng/mL 266  141 241.4  126.2 Total cholesterol, mg/dL 178  38.8 179.25  43.9
HDL-C, mg/dL 52.8  15.7 57.8  13.8*
Values are mean  SD. Low-density lipoprotein 105  35.9 101  33.1
*P < .05. cholesterol, mg/dL
TG, mg/dL 108.4  85 94.8  56.2
were receiving treatment for hypothyroidism compared with BMI, kg/m2 28.5  7.4 24.7  7.1
<25 38% 77%
3 adolescents without PCOS. 25-30 21% 9%
The most common presenting symptom in the adolescents >30 38% 9%
diagnosed with PCOS was menstrual irregularities (98%),
Values are mean  SD.
followed by acne, hirsutism, and weight gain. Of the subjects *P < .05.
with PCOS and menstrual irregularities, 68.3% had oligome- P < .01.

norrhea, 27.7% presented with secondary amenorrhea (no

menses during the preceding 6 months), and 4% presented A higher percentage of adolescents with PCOS (63.6%)
with primary amenorrhea (no menses up to the age of 16). had $1 metabolic risk factor as defined by the Cook criteria
Of the subjects with PCOS and clinical hyperandrogenism, for metabolic syndrome compared with the subjects without
37% complained of acne only, 40% had hirsutism only, and PCOS (33.3%, P = .002). Also, the distribution of 1-4 risk fac-
23% had both acne and hirsutism. About one-half of the ad- tors was significantly higher in the PCOS group (P < .02). No
olescents with acne had seen a dermatologist and used pre- adolescent subject had all 5 metabolic risk factors.
scription medications. In addition, 34% of adolescents The prevalence of metabolic syndrome ($3 risk factors)
diagnosed with PCOS complained of recent weight gain as was 10.8% in adolescents with PCOS compared with 1.7%
one of their presenting symptoms. Of the adolescents in those without PCOS (P < .04). The unadjusted OR for
who did not have PCOS, 48% had only irregular menses, metabolic syndrome in adolescents with PCOS was
28% had only biochemical hyperandrogenemia, 4% had 6.7 (95% CI 0.9-52.4, P < .06). The adjusted OR (age and
only polycystic appearing ovaries based on volume criteria, race) was 5.8 (95% CI 0.73-46.6, P < .09). BMI is one of
and the remaining met neither criterion after applying the the variables used to calculate the risk of metabolic syn-
AE-PCOS definition. Fifty percent of the adolescents without drome; it was not included in the logistic regression model.
PCOS had acne and 15% of these girls were using medications Only one subject with PCOS and normal BMI (n = 71) had
for the treatment of acne. Compared with the adolescents metabolic syndrome and no subjects without PCOS and nor-
with PCOS, fewer adolescents without PCOS complained of mal BMI (n = 44) had metabolic syndrome. Of the subjects
hirsutism (13%, P < .01) and weight gain (11.3%, P < .01). with BMI >95th percentile for age, 20% of adolescents with
Of the adolescents diagnosed with PCOS, 55% had an ul- PCOS and 7% of adolescents without PCOS had metabolic
trasound compared with 80% of the adolescents without syndrome (P = .2). Because the groups with only obese or
PCOS. The mean ovarian volume was 9.62  5.3 cm3 in only lean subjects were small, we also analyzed the risk of
the PCOS subjects compared with 6.25  2.8 cm3 in the ad- metabolic abnormalities excluding BMI. Adolescents with
olescents without PCOS (P < .01). PCOS had a significantly higher number of the remaining
The biomarkers measured for assessing the metabolic risk metabolic risk factors (than the adolescents without PCOS
profile in the 2 groups are shown in Table III. Adolescents
with PCOS had a significantly higher BMI compared with
Table IV. Prevalence of metabolic syndrome and its
the adolescents without PCOS (P < .01), and a larger
individual components in adolescents with and without
proportion of adolescents with PCOS were overweight
PCOS
and obese (based on adult definitions). The mean systolic
PCOS No PCOS OR
BP was significantly higher in the adolescents with PCOS (2 criteria) (1 criteria) (95% CI)
(P < .01), and 1 subject with PCOS was receiving
BMI $90th percentile 50.3% 22.8% 3.6 (1.8-7.1)
antihypertensive medications. The mean HDL-C levels were BP $90th percentile 27.7% 14% 2.3 (1.03-5.2)
significantly lower in adolescents with PCOS (P < .05). TG $150 mg/dL 16.2% 7% 2.6 (0.9-7.1)
Four adolescents with PCOS and 1 without PCOS had an TG $110 mg/dL 28.3% 17.5% 1.8 (0.9-3.8)
(Ford criteria)
impaired fasting glucose level (>100 mg/dL). No subjects Glucose $100 mg/dL 2.7% 1.7% 1.5 (0.6-7.79)
were diagnosed with diabetes in this cohort. Table IV HDL #40 mg/dL 17.4% 5.5% 3.14 (1-10.2)
shows the prevalence of each metabolic risk factor in the Metabolic syndrome 10.8% 1.7% 6.7 (0.9-52.7)
(Cook criteria)
2 groups. The OR for abnormal BMI and BP were 14.8% 7.02% 2.3 (0.8-6.7)
significantly higher in the PCOS group.
Using the Androgen ExcessPCOS Society Criteria to Diagnose Polycystic Ovary Syndrome and the Risk of Metabolic 939
Syndrome in Adolescents
THE JOURNAL OF PEDIATRICS  www.jpeds.com
(P < .01). More adolescents with PCOS had $2 abnormal
metabolic risk factors not including BMI compared with
those without PCOS (P < .02)).
The majority of the adolescents with PCOS in our study
(140/148) met the NIH criteria. Of the 8 subjects with
PCOS who did not meet the NIH criteria (high androgen
levels and polycystic ovaries), 6 had an elevated BMI, 2 had
elevated BP, 1 had low HDL-C, and 1 had high TG based
on the Cook criteria. One subject met the Cook criteria of
metabolic syndrome.
Discussion
Most gynecologists treat irregular menses in adolescents with
hormonal regulation or observation for a few years. Similarly,
acne is commonly treated with topical medications and com-
bination contraceptive pills. It has therefore been proposed
that the diagnosis of PCOS should perhaps be delayed to
the postadolescent years. On the contrary, our findings un-
derscore the need to accurately diagnose PCOS at an early
age and thereby allow for timely metabolic risk evaluation
and early intervention for prevention of cardiovascular dis-
ease. We also evaluated the unique group of adolescents
who mimic features of PCOS but do meet both AE-PCOS cri-
teria and found a low metabolic risk profile in this group.
Milder PCOS phenotypes may be more difficult to identify
in the adolescent transition, and waiting to confirm the diag-
nosis would be prudent given their metabolic findings.
Irregular menses is a common presentation in the adoles-
cent girl. Because persistent oligomenorrhea (for >2 years
postmenarche) is a stronger predictor of continued irregular
menses,7 it has been suggested to defer the diagnosis of
PCOS during this time period.2 In our study, all subjects
were post spontaneous menarche for >2 years except for 4 sub-
jects who presented with primary amenorrhea. A large propor-
tion of subjects had no menses for >6 months at the time of
presentation. It has been reported that hirsutism is not a com-
mon presentation in adolescents with PCOS.8,9 In our cohort,
hirsutism was one of the presenting symptoms in 65% of ado-
lescents diagnosed with PCOS, but the FG score was elevated in
only 37%. Most adolescents in our study described hirsutism
as excessive facial hair but minimal hair on other androgen-
sensitive areas of the body. Generalized hirsutism may take
longer to develop and our data suggest that an evaluation of
serum androgens, in the absence of an abnormal FG score, is
essential in this population. In the adult population, one study
describes the endocrine evaluation of oligomenorrheic women
with minimal hirsutism (FG score <5).10 Interestingly, 50%
(94/188) of these women were diagnosed with PCOS and the
authors concluded that routine endocrine workup should be
performed in all women with minimal unwanted hair.
Acne is common in the adolescent age group; however, its
validity as a surrogate clinical marker for hyperandrogenism
in this population is not established. Several subjects with
PCOS in our study were using topical medications and had
consulted with a dermatologist regarding the treatment of se-
vere acne. Not surprisingly, nearly one-half of the adolescents
940
Vol. 162, No. 5
who did not have PCOS also presented with acne, confirming
that acne is a common complaint during the adolescent pe-
riod. Further studies are needed to evaluate incorporation
of an acne scoring scale into diagnostic PCOS criteria, espe-
cially in the adolescent group.11
Given the technical and diagnostic limitations of ultra-
sound evaluation of polycystic ovaries in the adolescent2
and the ongoing debate regarding the criteria for polycystic
ovaries in adults,4 we found that this criterion is better
used for confirming the absence of PCOS. For example, for
adolescents with hyperandrogenism where the menstrual his-
tory did not satisfy the AE-PCOS criteria, we obtained an
ultrasound. As a result, 80% of subjects without PCOS
had an ultrasound to evaluate their ovaries.
Our study has some limitations. We used BMI as a surro-
gate for waist circumference in the definition of metabolic
syndrome. A high correlation between waist circumference
and BMI has been reported in the adolescent population6
(r = 0.94). In this study, the 95th percentile for BMI was
used as the threshold criterion for obesity, and we used the
same cut-off in our study. Also, we did not include a geo-
graphically matched control group. Other studies have com-
pared adolescents with PCOS to controls and evaluated the
risk of metabolic syndrome. The aim of our study was to iden-
tify differences between adolescents with PCOS and those
who may have some features that mimic PCOS. Of the con-
trols, 48% had only irregular menses and 28% had only bio-
chemical hyperandrogenemia. The remaining adolescents
presented with some irregularity of menses or severe acne
but did not meet either AE-PCOS criteria by strict definitions.
A few studies have examined the prevalence of metabolic
risk in adolescents with PCOS. The risk of metabolic syn-
drome was reported to be increased in adolescents with
PCOS in studies from the US (N = 4912 and N = 3613), India
(N = 51),14 and China (N = 128).15 Other studies reported no
difference in risk in adolescents with and without PCOS from
the US (N = 43)16 and Italy (N = 71).17 The disparity in the
prevalence of metabolic syndrome in adolescents is likely due
to application of differing diagnostic criteria for both PCOS
and metabolic syndrome. In community-based study of ado-
lescent Australian girls with PCOS,9 there was an increased
clustering of recognized metabolic risk factors 35.3% in
PCOS by NIH criteria and 26.2% in PCOS by Rotterdam cri-
teria compared with 15.4% in adolescents who did not meet
either definition of PCOS. In another study, it has been re-
ported that adolescents with different Rotterdam phenotypes
may not have a similar metabolic risk.18 Our study includes
one of the largest groups of adolescents with PCOS and we
report a significantly increased metabolic risk profile. The
use of metabolic risk cluster compared with the established
metabolic syndrome criteria recognizes that the sequence of
events leading to metabolic syndrome begins with obesity
and/or insulin resistance and then continues by varying path-
ways to manifest as clinical disease. In the longitudinal Boga-
lusa Heart Study, an increase in the number of cardiovascular
risk factors in childhood predicted the severity of asymptom-
atic coronary and aortic atherosclerosis in young people.19
Roe et al
May 2013
There are different definitions used to diagnose metabolic
syndrome in adolescents involving the same 5 criteria but dif-
fering cut-offs. This has resulted in variation in the range of
metabolic syndrome prevalence to vary between 2% and
10%. It has been proposed that metabolic syndrome can be
used as a marker for intervention in overweight and obese
youth. Longitudinal studies of adolescent girls have shown
persistence of multiple cardiovascular risk markers from
childhood to adulthood.20 In another longitudinal cohort,
childhood metabolic syndrome and abnormal metabolic
risk factors predict adult type 2 diabetes.20,21 Based on these
findings, it seems prudent to screen all adolescents with
PCOS for diabetes and lipid abnormalities and provide
them with treatment options. In our study, a large propor-
tion of adolescents with PCOS were overweight and obese.
The American Heart Association recommends treatment
options for childhood obesity based on the presence or
absence of comorbidities.21 There are very few studies exam-
ining the effects of weight loss on cardiovascular end points
in adolescents with PCOS.22,23 We found a higher proportion
of metabolic abnormalities in subjects with PCOS compared
with adolescents without PCOS even after excluding BMI.
These findings indicate screening of all adolescents with
PCOS for metabolic risk.
Using broad definitions and accommodating different
phenotypes of PCOS may be problematic in the adolescent.2
These data underscore the importance of accurate identifi-
cation of PCOS in the adolescent population. Using similar
criteria in the adolescent ($2 years postmenarche) and
adult for the diagnosis of PCOS will be more convenient
for the clinician. n
Submitted for publication Jun 19, 2012; last revision received Oct 11, 2012;
accepted Nov 2, 2012.
Reprint requests: Anuja Dokras, MD, PhD, Division of Reproductive
Endocrinology and Infertility, University of Pennsylvania, 3710 Market St,
Philadelphia, PA 19104. E-mail: adokras@obgyn.upenn.edu
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