Original Study

Utility of the Oral Glucose Tolerance Test to Assess Glucose

Abnormalities in Adolescents with Polycystic Ovary Syndrome
Nicole Coles MD 1, Kimberly Bremer MD 2, Sari Kives MD 2, Xiuyan Zhao MD 1, Jill Hamilton MD 1,*
1
Division of Endocrinology, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada
2
Division of Pediatric Adolescent Gynecology, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada

a b s t r a c t
Study Objective: The aim of this study was to examine the prevalence of and risk factors for abnormal glucose metabolism in a large
population of adolescents with polycystic ovary syndrome (PCOS).
Design, Setting, Participants, Interventions, and Main Outcome Measures: A retrospective chart review was performed of 360 patients who
presented to the pediatric gynecology outpatient clinic for evaluation of PCOS between January 2004 and May 2012.
Results: A total of 163 patients fullled criteria for a diagnosis of PCOS and had adequate clinical and laboratory data. Twenty-six ado-
lescents (16.0%) had impaired glucose tolerance and 2 patients (1.2%) met criteria for a provisional diagnosis of type 2 diabetes. All 28
subjects with abnormal glucose metabolism were identied using the 2-hour plasma glucose of the oral glucose tolerance test. Conversely,
the fasting glucose values only successfully detected 2 patients with hyperglycemia, both of whom also had abnormal 2-hour glucose
levels. Adolescents with abnormal glucose metabolism were more likely to have reported a positive family history (P 5 .02) and had higher
body mass index z scores (2.8  1.1 vs 1.8  1.2; P ! .01). When patients were classied into normal weight (n 5 29) and obese/overweight
groups (n 5 117), all of the patients with abnormal glucose metabolism were overweight or obese.
Conclusion: In the largest series to date, we describe a prevalence of abnormal glucose metabolism in adolescent patients with PCOS of
17.2%. Abnormal glucose metabolism is associated with many of the known risk factors for metabolic syndrome. Our results support that
the oral glucose tolerance test is a superior diagnostic test to assess abnormal glucose levels in overweight and obese adolescents but that
this test might have limited utility in normal weight adolescents with PCOS.
Key Words: Polycystic ovary syndrome, Adolescents, Glucose intolerance, Diabetes mellitus

Introduction Additionally, there is debate about the optimal screening

Polycystic ovary syndrome (PCOS) is one of the most
common endocrine disorders among women and is now
recognized to affect 4%-6% of young women.1e5 PCOS is
characterized by chronic oligo-ovulation or anovulation,
hyperandrogenism, and the appearance of polycystic
ovaries on ultrasound imaging.6 In addition to these char-
acteristics, insulin resistance is also known to play an in-
tegral role in the etiology of the disease. Accordingly, PCOS
patients are at increased risk of impaired glucose tolerance,
impaired fasting glucose, and diabetes mellitus. Insulin
resistance and pancreatic beta cell dysfunction are thought
to be the main mechanisms that account for the predispo-
sition to diabetes, however, the precise nature of their
relationship remains unclear.1,7e9
The rates of glucose abnormalities in the adult PCOS
population are estimated to be approximately 30%-40%.10
However, there is a more limited body of literature that
describes the prevalence of abnormal glucose levels in
adolescent PCOS patients and variation in their estimates.
Jill Hamilton is supported by the Mead Johnson Chair in Nutritional Science. The
other authors have no relevant conicts to disclose.
* Address correspondence to: Jill Hamilton, MD, Division of Endocrinology, The
Hospital for Sick Children, University of Toronto, 555 University Ave, Toronto,
Ontario M5G 1X8, Canada; Phone: (416) 813-5115
E-mail address: jill.hamilton@sickkids.ca (J. Hamilton).
1083-3188/$ - see front matter 2016 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc.
http://dx.doi.org/10.1016/j.jpag.2015.06.004
test for the presence of altered glucose metabolism in this
age group. Several smaller studies have documented
glucose abnormalities in 27-66 adolescents with PCOS,
estimating rates at 9%-33.3% (3/33, 9/27).11e15 A recent
study in 66 adolescents with PCOS reported abnormal
glucose levels in 18.2% (12/66) of PCOS adolescents with
impaired glucose tolerance that occurred among obese
and nonobese individuals.12
Despite this limited body of literature, an oral glucose
tolerance test (OGTT) is recommended to screen for
diabetes every 2-5 years in obese and nonobese adoles-
cents with PCOS.6,16 In contrast, guidelines for diabetes
screening from the American Diabetes Association rec-
ommends the use of fasting plasma glucose for only obese
adolescents with additional risk factors including condi-
tions such as PCOS.17 This creates potential confusion for
the health care provider who manages adolescents with
PCOS. Further understanding of the exact prevalence and
nature of glucose abnormalities in this population is
warranted to support the use of OGTT for screening in this
population because of the increased cost and difculty
of performing this test. The primary aim of this study was
to examine the prevalence of abnormal glucose meta-
bolism in a large population of adolescents with PCOS.
Second, we sought to determine specic clinical and
biochemical risk factors associated with an increased
 N. Coles et al. / J Pediatr Adolesc Gynecol 29 (2016) 48e52
risk of glucose abnormalities to help inform screening
practices.
Materials and Methods
A retrospective chart review was performed of 360 pa-
tients who presented to the pediatric gynecology outpatient
clinic at the Hospital for Sick Children for evaluation of PCOS.
Charts between January 2004 and May 2012 were reviewed.
Patients were included if they were 18 years of age or
younger at the time of their visit and met diagnostic criteria
for PCOS. The diagnosis of PCOS was made on the basis of
evidence of clinical or biochemical hyperandrogenism (ie,
hirsutism or increased serum androgen levels) and persis-
tent oligomenhorrhea.6 All patients were biochemically
euthyroid with normal prolactin levels and no evidence of
congenital adrenal hyperplasia, which was screened using
17-hydroxyprogesterone. Patients were excluded if they did
not meet criteria for diagnosis or if they were receiving
confounding medications at the time of initial evaluation.
Medical charts were reviewed and relevant de-
mographic, clinical, and laboratory data were extracted.
This information included age, age of menarche, current
medications, ethnicity, family history of features of the
metabolic syndrome (hypertension, dyslipidemia, obesity),
coronary artery disease, diabetes and PCOS, weight, height,
blood pressure, and presence of clinical hyperandrogenism.
Collected laboratory values included glucose (fasting and
2-hour plasma glucose according to the OGTT), insulin,
hemoglobin A1c, total and free testosterone, dihy-
droepiandrosterone, androstenedione, luteinizing hor-
mone, follicle-stimulating hormone, and fasting lipid
prole. OGTTs were conducted (1.75 g/kg to a maximum of
75 g). Body mass index (BMI; calculated as the weight in
kilograms divided by the height in meters squared) and BMI
z scores were calculated for each patient. Overweight was
dened as a BMI between the 85th to 97th percentile
(z score $1 and !2) and obesity was dened as a BMI
greater than the 97th percentile for age and sex (z score $2)
according to the World Health Organization.18 Impaired
glucose tolerance, impaired fasting glucose, and diabetes
were dened based on the Canadian Diabetes Association
2013 Clinical Practice Guidelines criteria.19 Glucose abnor-
malities were dened as any of impaired glucose tolerance
(2-hour plasma glucose in 1.75 g/kg up to 75 g OGTT of 7.8-
11.0 mmol/L [140-198 mg/dL]), impaired fasting glucose
(fasting plasma glucose 6.1-6.9 mmol/L [110-124 mg/dL]) or
presumptive type 2 diabetes mellitus (2-hour plasma
glucose in 1.75 g/kg up to 75 g OGTT of $11.1 mmol/L
[200 mg/dL] or fasting plasma glucose $7.0 mmol/L
[126 mg/dL]). The study was approved by the Research
Ethics Board at the Hospital for Sick Children.
Statistical Analyses
The characteristics of patients were analyzed using
descriptive statistics. Continuous variables were described
as mean and SD. Discrete variables were described as fre-
quency and cross tabulates. BMI values were standardized
as z scores using the World Health Organization Child
49
Growth Standards.20 Blood pressure values were stan-
dardized as z scores using the National Health and Nutrition
Exercise Survey database.21 O2, Fisher exact tests, and
t tests were used to compare variables between cohorts of
patients. Comparisons of clinical and biochemical features
with 2-hour plasma glucose were performed using univar-
iate linear and logistic regression analysis. Clinically sig-
nicant variables with P values less than 0.15 were selected
to create a multivariate linear regression with 2-hour OGTT
value as the outcome. All statistical analyses were per-
formed using Statistical Analysis System software, version
9.3 (SAS Institute, Cary, NC).
Results
A total of 300 patients reviewed fullled criteria for a
diagnosis of PCOS. Of these, 219 subjects had adequate
clinical and laboratory data including a fasting glucose level
and 163 patients had completed an OGTT (Fig. 1). The mean
age of the subjects at presentation was 15.4  1.5 years and
age at menarche was 11.7  1.4 years. Ethnicity was
documented in 143 of the 219 patients (65.3%). Of those
recorded, there was a diverse mixture of Caucasian, Medi-
terranean, African or Caribbean, East or Southeast Asian,
Hispanic, and Middle Eastern patients. Because data were
widely distributed and incomplete, further analysis of
ethnicity was not conducted. Similarly, statistical analysis of
hemoglobin A1c was not conducted because there were
inadequate data available. Seventy-one adolescents (32.4%)
reported having a family member with at least 1 feature of
metabolic syndrome (hypertension, hyperlipidemia, coro-
nary artery disease, or obesity) and 96 adolescents (43.8%)
reported a family history of type 2 diabetes mellitus. Most
patients in our population were overweight or obese, with
mean BMI of 30.4  12.1.
As part of the assessment for PCOS, 163 of the 219 pa-
tients underwent an OGTT, and the other 56 patients
(25.6%) completed only fasting glucose studies. Sixty-one
patients (27.9%) received a pelvic ultrasound in the course
of their diagnostic evaluation. These were not included in
our analysis because diagnostic guidelines for PCOS in
Fig. 1. Flowchart of the study design with prevalence of glucose abnormalities. DM,
diabetes mellitus; IGT, impaired glucose tolerance; PCOS, polycystic ovary syndrome.
50 N. Coles et al. / J Pediatr Adolesc Gynecol 29 (2016) 48e52

Table 1
Clinical and Biochemical Characteristics of Patients with Glucose Abnormalities Compared with Patients with Normal Glucose Tolerance

Characteristic Normal OGTT (Mean  SD) Abnormal OGTT (Mean  SD) P

Age, years) 15.4  1.4 (12.3-17.9) 14.8  1.6 (11.8-17.6) .0198

BMI z score 1.8  1.2 ( 1.5 to 6.2) 2.8  1.1 (1.3-6.2) .0006
Systolic BP z score 0.3  1.1 ( 2.3 to 5.2) 0.7  1.1 ( 1.1 to 3.5) .0999
Diastolic BP z score 0.5  0.9 ( 1.4 to 2.9) 0.8  0.8 ( 0.8 to 2.2) .1085
HDL, mmol/L 1.3  0.3 (0.7-2.5) 1.2  0.4 (0.7-2.1) .2336
Triglycerides, mmol/L 1.7  0.6 (0.4-4.7) 2.1  1.7 (0.7-5.7) !.0001
DHEA, mmol/L 5.8  3.1 (1-16.7) 6.0  2.7 (0.8-11.4) .8376
Androstendione, nmol/L 10.2  3.9 (1.2-23.5) 10.3  3.5 (5.5-16.2) .9895
Testosterone, nmol/L 2.8  1.8 (0.7-11.7) 2.7  1.1 (0.7-4.3) .7275
Free testosterone, pmol/L 6.7  4.9 (0.3-28.9) 7.7  5.4 (0.5-22.3) .3729

BMI, body mass index; BP, blood pressure; DHEA, dihydroepiandrosterone; HDL, high-density lipoprotein; OGTT, oral glucose tolerance test
Bolded values indicate a P value ! .001

adolescents do not recommend the use of radiologic nd-
ings.6 Clinical characteristics (age, BMI z score, and blood
pressure z scores) were compared between groups with and
without screening glycemic blood work and between the
groups with and without an OGTT. No statistically signi-
cant differences were observed (data not shown).
The subsequent analysis was restricted to include only
patients with available OGTT data. From this group of 163
patients, 26 adolescents (16.0%) had impaired glucose
tolerance. Two patients met criteria for a provisional
diagnosis of type 2 diabetes (1.2%) with 1 patient who met
criteria on the basis of fasting and 2-hour glucose values
(Fig. 1).
Screened adolescents with abnormal glucose levels were
more likely to have reported a positive family history,
dened as a family member with at least 1 of diabetes,
PCOS, hypertension, hyperlipidemia, or coronary artery
disease (P 5 .02; Table 1). Adolescents with abnormal
glucose levels had higher BMI z scores (2.8  1.1 vs 1.8  1.2;
P ! .01). Other variables were not signicantly different
between the groups. Univariate linear regression analysis
revealed that higher 2-hour plasma glucose levels on the
OGTT were associated with higher systolic and diastolic
blood pressure readings (parameter estimates 5 0.48 and
0.31; P ! .05 and P ! .01), higher BMI z scores (parameter
estimate 5 0.51; P ! .01), and a positive family history
(parameter estimate 5 0.72; P ! .05). Finally, in laboratory
evaluation, higher 2-hour plasma glucose levels on the
OGTT were associated with lower high-density lipoprotein
levels (parameter estimate 5 1.42; P ! .01) and higher
triglyceride levels (parameter estimate 5 1.1; P ! .01). In
multiple linear regression analysis, increased BMI z score
and triglyceride levels were independently associated with
increased 2-hour plasma glucose level values on the OGTT
(r2 5 0.24; P ! .001; Table 2).
Table 2
Results of Multivariate Linear Regression Analyses
Parameter Estimate t R2
BMI z score 0.31 2.66 0.13
Triglycerides 0.85 4.52 0.23
Overall 0.2429
BMI, body mass index
Variables entered into the model included those with a P ! .15 in univariate ana-
lyses: BMI Z score, systolic and diastolic blood pressure, positive family history,
luteinizing hormone, 17-hydroxyprogesterone, total cholesterol, triglycerides, and
high-density lipoprotein cholesterol.
Patients without complete anthropometric data were
excluded from the subsequent analysis. When patients with
PCOS were divided into obese (n 5 80) and nonobese
cohorts (n 5 66), there was a notable difference in the
prevalence of glucose abnormalities between the 2 groups.
Of the obese patients, 25.0% (20/80) had abnormal glucose
levels whereas only 9.0% (6/60) of nonobese patients had
laboratory evidence of abnormalities in glucose levels.
Furthermore, when patients were classied into normal
weight (n 5 29) and obese/overweight groups (n 5 117), all
of the patients with abnormal glucose levels were over-
weight or obese (Fig. 2).
Obese adolescents were younger than nonobese ado-
lescents (14.8  1.8 years vs 15.6  1.2 years; P ! .002). This
group also showed lower androstendione levels
(9.6  3.6 nmol/L vs 11.4  3.7 nmol/L; P 5 .018), higher
mean triglyceride levels (1.6  0.7 mmol/L vs
1.1  0.8 mmol/L; P ! .001) and lower high-density lipo-
protein levels (1.2  0.3 mmol/L vs 1.4  0.3 mmol/L;
P ! .001). Finally, the obese group was more likely to have
reported a positive family history of cardiometabolic
disease (P 5 .008).
Last, we sought to compare the differences between the
2 screening tests: isolated fasting plasma glucose and OGTT.
All 28 subjects with abnormal glucose metabolism were
identied using the 2-hour plasma glucose of the OGTT. The
fasting glucose values only successfully detected 2 patients
with hyperglycemia, both of whom also had abnormal
2-hour glucose levels.
Discussion
To our knowledge, this is the largest study to describe the
prevalence of abnormalities in glucose levels in adolescent
patients with PCOS in a clinical setting. Glucose abnormal-
ities occurred in 17.2% (28/163) with impaired glucose
tolerance being the most common abnormality. Glucose
intolerance is often asymptomatic but represents a signi-
P cant metabolic risk. Early detection is important because
!.01
the morbidity of associated conditions such as diabetes can
!.001 be reduced with early intervention.
!.001 Current recommendations regarding screening for ab-
normalities in glucose levels in patients with PCOS among
adolescents are contentious, and differ between guidelines.
The Canadian Diabetes Association advocates for screening
of type 2 diabetes with a fasting plasma glucose in pubertal
 N. Coles et al. / J Pediatr Adolesc Gynecol 29 (2016) 48e52
Fig. 2. Prevalence of glucose abnormalities among different BMI categories. (A) Obese vs nonobese cohorts; (B) normal BMI vs overweight/obese cohorts. BMI, body mass index;
OGTT, oral glucose tolerance test.
children with 2 or more risk factors including PCOS, obesity,
high-risk ethnic group, family history of type 2 diabetes,
and/or exposure to hyperglycemia in utero, and signs or
symptoms of insulin resistance (acanthosis nigricans, hy-
pertension, dyslipidemia, nonalcoholic fatty liver disease).19
Similarly, the American Diabetes Association recommends
screening in adolescents who are overweight with 2 addi-
tional risk factors. However, the Androgen Excess Society
proposes universal screening, every 2 years, for all adoles-
cents with PCOS using an OGTT, irrespective of BMI.16 This
can lead to confusion for clinicians and has implications for
health use.
Characterization of patients at greatest risk for glucose
abnormalities allows for targeted screening in select
individuals. More specically, identication of risk factors
helps stratify high-risk patients and eliminate the
need for potentially unjustied, universal screening. We
found that adolescents who were clinically overweight or
obese were more likely to merit screening with an
OGTT. These patients also frequently had derangements
in lipid metabolism, in particular, increased triglyceride
levels.
Existing literature suggests that fasting plasma glucose
might be unable to detect early biochemical changes in
glucose metabolism, highlighting the importance of an
oral glucose tolerance.14,22,23 A prospective study of 27
adolescent patients with PCOS by Palmert and colleagues
found that 8 of 27 (29.6%) had impaired glucose tolerance
on a 2-hour OGTT and 1 of 27 (3.7%) met criteria for type
2 diabetes.14 In our study, isolated fasting glucose iden-
tied only 2 of 28 patients with abnormal glucose levels.
The remainder of this group was detected only on results
of their 2-hour plasma glucose from the OGTT. One
consideration is that Canadian guidelines for detection of
impaired fasting glucose levels use a different lower limit
than American guidelines (6.1 mmol/L [110 mg/dL] vs
5.6 mmol/L [100 mg/dL]); however, reanalysis using this
American denition for impaired fasting glucose did not
add any additional cases.17,24,25 These results strongly
support the use of the OGTT as the optimal screening test
for abnormal glucose metabolism in this population. An
evolving but limited body of literature suggests that he-
moglobin A1c might offer signicant utility for diagnosis
51
in this population with comparable detection rates.26
However, studies that demonstrate its association with
long-term complications are still needed. Guidelines
from the Androgen Excess Society continue to support
the use of the OGTT as the gold standard for diagnosis of
dysglycemia in adults with PCOS.27
In adult populations of women with PCOS, abnormal
glucose tolerance occurs independently of BMI.9,22 How-
ever, our study identied abnormal glucose tolerance only
among obese and overweight adolescents with all dysgly-
cemic patients having a BMI at the 85th or greater
percentile. This appears contrary to other clinic reports
including the recent ndings from Flannery et al, who found
abnormal glucose tolerance among obese and nonobese
cohorts of adolescents with PCOS when obesity was dened
as a BMI at the 95th or greater percentile.12 However, this
analysis was not performed on normal weight compared
with overweight and obese adolescents. This might be an
important cutoff distinction for screening, which requires
further validation.
Our study had several limitations, many of which arise
from the retrospective nature of the design. The avail-
ability of clinical information was dependent on data
documented in the charts. Pertinent variables such as
ethnicity were not consistently reported and in those
reported were very diverse, therefore could not be used in
the analysis. Although there were no signicant differ-
ences in those who had undergone an OGTT vs those who
did not, these investigations were selected at the discre-
tion of the responsible physician and could be subject to
bias. Furthermore, the diagnosis of abnormal glucose
tolerance was based solely on a single value, with no
conrmatory testing, which is necessary for a diagnosis of
type 2 diabetes in an asymptomatic adolescent. Longitu-
dinal, prospective studies will be necessary to understand
the evolution of these glycemic changes and further
delineate the relative effect of obesity and PCOS on
abnormal glucose metabolism in this age group. Our
study supports the use of the OGTT as a superior diag-
nostic test to assess for abnormal glucose levels in over-
weight and obese adolescents, and results suggest that
this test might have a limited utility in normal weight
adolescents with PCOS.
52 N. Coles et al. / J Pediatr Adolesc Gynecol 29 (2016) 48e52
Acknowledgments
Jill Hamilton is supported by the Mead Johnson Chair in
Nutritional Science.
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