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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2006-1705
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The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 1 186-189
Copyright © 2007 by The Endocrine Society

Atherogenic Lipoprotein Phenotype and Low-Density Lipoproteins Size and Subclasses in Women with Polycystic Ovary Syndrome

Kaspar Berneis, Manfredi Rizzo, Veronica Lazzaroni, Franca Fruzzetti and Enrico Carmina

Clinic of Endocrinology, Diabetes, and Clinical Nutrition (K.B.), University Hospital, 8091 Zurich, Switzerland; Department of Clinical Medicine and Emerging Diseases (M.R., E.C.), University of Palermo, 90139 Palermo, Italy; and Department of Obstetrics and Gynecology (V.L., F.F.), University of Pisa, 56100 Pisa, Italy

Address all correspondence and requests for reprints to: Prof. Enrico Carmina, M.D., Department of Clinical Medicine and Emerging Diseases, University of Palermo, Via delle Croci 47, 90139 Palermo, Italy. E-mail: enricocarmina{at}libero.it.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Context: An altered lipid profile is common in polycystic ovary syndrome (PCOS) and is usually characterized by increased triglycerides and low high-density lipoprotein (HDL)-cholesterol levels. In the general population, these alterations are often associated with the increase of small low-density lipoproteins (LDLs) in the so-called "atherogenic lipoprotein phenotype" (ALP) that determines a further increase of cardiovascular risk. In this study, we evaluated the presence of ALP in the plasma of women with PCOS.

Setting: Measurements and analysis of LDL size were performed at the Clinic of Endocrinology, Diabetes, and Clinical Nutrition, University Hospital, Zurich. PCOS patients were recruited at the Department of Clinical Medicine, University of Palermo, and the Department of Obstetrics and Gynecology, University of Pisa.

Patients: Thirty patients with PCOS (hyperandrogenism and chronic anovulation) and 24 matched controls were studied. Anthropometric data, blood glucose, serum insulin lipid profile, and LDL size and subclasses were evaluated.

Results: Compared with controls, patients with PCOS had higher plasma concentrations of insulin and triglycerides and lower HDL-cholesterol concentrations but no differences in LDL-cholesterol and total cholesterol. Patients with PCOS had smaller LDL size due to a reduction in LDL subclass I, with a concomitant increase in LDL subclasses III and IV. Fourteen PCOS patients had an increase of smaller LDL particles, and it represented the second most common lipid alteration after decrease in HDL-cholesterol. However, because in this PCOS population hypertriglyceridemia was only present in two patients, complete ALP was relatively uncommon.

Conclusions: Increase of type III or type IV LDL subclasses is a common finding in PCOS and represents the second most common lipid alteration after HDL-cholesterol decrease. However, in our PCOS patients, because of relatively low triglyceride levels, complete ALP is uncommon.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
POLYCYSTIC OVARY SYNDROME (PCOS) probably constitutes the most frequently encountered endocrinopathy in women, affecting 6–7% of women in reproductive age (1, 2). Although for many years it has been known that PCOS is associated with reproductive morbidity and increased risk for endometrial cancer, more recently a large number of studies have shown that women with PCOS also bear an increased cardiovascular (CV) risk (3, 4, 5, 6, 7, 8).

Although most markers of CV risk may be increased in women with PCOS (3, 4, 5, 6, 7, 8), altered lipid profile is particularly common and is usually characterized by increased triglycerides and reduced high-density lipoprotein (HDL) cholesterol levels. Increased low-density lipoprotein (LDL) and total cholesterol have also been found but with a lower prevalence (2, 7).

In the general population, the alteration of circulating triglycerides and HDL-cholesterol is often associated with increased levels of small, dense LDL in the so-called lipid triad or "atherogenic lipoprotein phenotype" (ALP) that determines an important increase of CV risk (9, 10). In fact, LDLs comprise multiple distinct subclasses that differ in size, density, physicochemical composition, metabolic behavior, and atherogenicity, with at least four major subspecies: large LDL-I, medium LDL-II, small LDL-III, and very small LDL-IV (11), and the predominance of small and very small LDL has been accepted as an emerging CV risk factor by the National Cholesterol Education Program Adult Treatment Panel III (12).

In PCOS, a few studies have shown that LDL size is decreased because of an increase of small LDL (13, 14, 15, 16), but the presence of ALP has not been determined. Therefore, it is unclear whether in women with PCOS this lipid alteration is linked or not to the other lipid abnormalities. In addition, the new subclasses of LDL have not been determined, and it limits the utility of the information we have on atherogenic risk in PCOS.

In this study, we evaluated the complete lipid profile in 30 women with PCOS. Contemporary to the usual lipid study, a careful evaluation of LDL size and subclasses was conducted. In particular, seven different LDL subclasses were determined, and the prevalence of ALP in PCOS was determined.


   Patients and Methods
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 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Patients and control subjects

Thirty consecutive women of reproductive age with PCOS, all referred because of androgen excess to our Endocrine Units, were included in the present study. The diagnosis of PCOS was based on the presence of clinical or biological hyperandrogenism and chronic anovulation (17). Therefore, these patients presented the classic, more severe form of PCOS (7).

The project design included a medical examination and biochemical analyses. The adopted procedures were in agreement with the Helsinki Declaration of 1975 as revised in 1983, and the study was approved by the local Ethics Council. All subjects gave their informed consent to participate to the study. At admission, all subjects underwent a medical examination and also answered a questionnaire on personal and medical items, including age, past medical history, and use of medications. Exclusion criteria included the presence of renal or hepatic diseases able to modify plasma lipoproteins and the use of hypolipidemic drugs. No patient had type II diabetes or was taking medications from at least 3 months before the study.

As controls, we selected a group of 24 healthy female subjects, matched for age and body weight with the same exclusion criteria described above. They were recruited from family members of hospital co-workers. Controls were women with regular menses, no clinical or biological hyperandrogenism (normal testosterone and SHBG in blood), and normal (>7 ng/ml in d 22 of the cycle) serum progesterone levels.

Height, weight, and waist circumference were recorded, and body mass index (BMI) was calculated as kilograms per square meter.

Biochemistry

A blood sample was collected in a sodium-EDTA tube from each subject after a 12- to 14-h overnight fast. Total cholesterol, triglycerides, and HDL-cholesterol were quantified by standard enzymatic-colorimetric methods (18, 19, 20). LDL-cholesterol was calculated by the Friedewald formula: total cholesterol – (triglycerides/5) – HDL-cholesterol. To assess the prevalence of each individual component of ALP in both groups of subjects, we considered low HDL-cholesterol levels as those less than 50 mg/dl and elevated triglyceride concentrations as those greater than 150 mg/dl (12). Higher levels of small, dense LDL were considered as those greater than mean + 2 SD of the values of controls.

Nondenaturing polyacrylamide gradient gel electrophoresis

Nondenaturing polyacrylamide gradient gel electrophoresis of plasma was performed in Switzerland in the laboratory of K.B. at 10–14 C in 2–16% polyacrylamide gradient gels. Gels were subjected to electrophoresis for 24 h at 125 V in Tris borate buffer (pH 8.3) as described elsewhere (21, 22). Gels were fixed and stained for lipids in a solution containing oil red O in 60% ethanol at 55 C. Gels were placed on a light source and photographed with a Canon G3 digital camera (Canon, Inc., Tokyo, Japan). Migration distance for each absorbance peak was determined, and the molecular diameter corresponding to each peak was calculated from a calibration curve generated from the migration distance of size standards of known diameter, which includes carboxylated latex beads (Duke Scientific, Palo Alto, CA), thyroglobulin, and apoferritin (HMW Std., Pharmacia, Piscataway, NJ) having molecular diameter of 380, 170, and 122 Å, respectively, and lipoprotein calibrators of previously determined particle size. LDL subclass distribution (LDL I, IIA, IIB, IIIA, IIIB, IVA, and IVB) as percentage of total LDL was calculated as previously described (23).

Statistical analysis

Statistical analyses were performed using StatView 4.5 (Abacus Concepts Inc., Berkeley, CA) and SPSS 9.0 for PC (SPSS Inc., Chicago, IL). Univariate analyses were performed using Student’s unpaired t test for the numeric variables, whereas the differences in the prevalence for the nominal variables were analyzed by {chi}2 test. Analysis of covariance was performed to assess whether the difference in LDL size between PCOS and controls was independent of the other lipid and nonlipid biochemical variables. Correlation analyses were performed using the Spearman rank correlation method. All data are expressed as mean ± SD.


   Results
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 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
As shown in Table 1Go, patients with PCOS and matched controls had similar age, BMI, and waist circumference, whereas serum insulin was higher (P < 0.01) in PCOS than in controls. Patients with PCOS showed increased levels of triglycerides (P < 0.01) and decreased HDL-cholesterol concentrations (P < 0.01), whereas no significant differences were found in total cholesterol and LDL-cholesterol plasma levels (Table 1Go).


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  		TABLE 1. Clinical data, serum insulin, and plasma lipids in patients with PCOS and in age- and weight-matched controls (mean ± SD)

 
Patients with PCOS had significantly smaller LDL peak particle size (Table 2Go), and LDL subclass analysis revealed that this was due to a strong reduction in the largest LDL particles, LDL-I (P < 0.0001), with a concomitant increase in medium-sized LDL-IIB (P = 0.0013), -IIIA (P = 0.0029), and -IIIB (P = 0.0062), as well as in the smallest, most dense LDL-IVA (P = 0.0042) and -IVB (P < 0.0001). In Fig. 1Go, the differences in levels of four major classes (I, II, III, and IV) of LDL are shown.


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  		TABLE 2. LDL size and subclasses in patients with PCOS and controls (mean ± SD)

 

Figure 1
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  		FIG. 1. LDL classes in PCOS patients and weight-matched controls.

 
Spearman correlation analysis (Table 3Go) was performed in all subjects to assess the potential linear correlations between LDL size and subclasses and all other numeric variables. Triglyceride levels were significantly inversely correlated with LDL size (r = –0.62; P < 0.0001) and LDL-I (r = –0.38; P < 0.05), whereas positively with LDL-IIB (r = –0.38; P < 0.05) and -IIIA (r = –0.46; P < 0.005). By contrast, HDL-cholesterol concentrations were significantly positively correlated with LDL size (r = –0.44; P < 0.005) and LDL-I (r = –0.39; P < 0.05), whereas inversely with LDL-IIB (r = –0.36; P < 0.05), -IIIA (r = –0.35; P < 0.05), and -IVB (r = –0.37; P < 0.05). In addition, insulin levels were significantly inversely correlated with LDL size (r = –0.32; P < 0.05) and positively with LDL-IIIB (r = 0.34; P < 0.05) and -IVB (r = 0.39; P < 0.05).


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  		TABLE 3. Spearman correlations between LDL size and subclasses and age, BMI, plasma lipids, and insulin levels in all subjects

 
Analyzing individual PCOS lipid values, it was found that total cholesterol was normal in all patients, whereas HDL-cholesterol was low (<50 mg/dl) in 16 patients and represented the most common lipid alteration in PCOS. Triglycerides were increased in only two patients, and in a similar proportion of patients LDL-cholesterol was also increased.

An increase of small size LDL classes [LDL III (A+B) or LDL IV (A+B)] was found in 14 PCOS patients and represented the second most common lipid alteration. However, because of low prevalence of hypertriglyceridemia, only two women with PCOS had ALP.

In controls, altered lipid concentrations were uncommon (low HDL-cholesterol in two subjects, increased LDL-cholesterol and triglycerides in one subject). Increased LDL type III or IV was found in only one subject, and no control had ALP.


   Discussion
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 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
In PCOS, the alteration of lipid pattern represents the most common marker of increased CV risk. In a recent study, we have observed that 36% of patients with classic PCOS (hyperandrogenism and chronic anovulation) present an altered lipid pattern (7), and this phenomenon is more prevalent in other populations, as in the U.S. population (24, 25), where, probably because of higher body weight and different diet (26), dyslipidemia may be present in up to 70–90% of women with PCOS. Generally, dyslipidemia of PCOS is characterized by increased triglycerides and low HDL-cholesterol (24, 25), but in our population, although low HDL-cholesterol is common, hypertriglyceridemia is relatively uncommon (27). To the contrary, the most classic lipid alteration determining CV risk, increase of LDL-cholesterol, is relatively uncommon in all populations with PCOS (7, 24, 25).

Beyond total LDL-cholesterol concentrations, the quality of LDL may exert a direct influence on the CV risk (11). Several reasons have been suggested for the atherogenicity of small dense LDL. In relation to larger, more buoyant LDL, small dense LDL are taken up more easily by arterial tissue, have decreased sialic acid content and receptor-mediated uptake, as well as increased oxidative susceptibility and reduced antioxidant concentrations (11, 28).

The predominance of small, dense LDL has been associated with an approximately 3-fold increased risk for coronary artery disease (29), and it has been accepted as an emerging CV risk factor by the National Cholesterol Education Program Adult Treatment Panel III (12). In particular, the association of increased small LDL with hypertriglyceridemia and low HDL-cholesterol, the so-called ALP, seems to determine a particularly elevated CV risk (9, 10, 29).

In the past, some studies have already shown that patients with PCOS may have reduced LDL size (13, 14, 15, 16) but the prevalence of this phenomenon, its possible association with other lipid alterations, and the finding of ALP in PCOS has not been determined.

In our group of Mediterranean patients with classic PCOS, LDL subclass analysis revealed a strong reduction in the largest fraction, with a concomitant increase in both medium-sized and smallest, most dense particles. Because no clear normal limits for LDL subtypes have been defined, we considered elevated levels greater than mean + 2 SD of the values of weight and age-matched controls. By this way, the prevalence of increased small (type III or IV) LDL subtypes was 47%, and in our PCOS population, this lipid alteration represented the second most common lipid alteration (after low HDL-cholesterol values). Because the number of studied patients was relatively small, our data are not sufficient to establish the exact prevalence of LDL abnormalities in our PCOS population. However, it was interesting to observe that LDL abnormalities were common, although in the same patients, serum triglycerides were generally normal. In fact, only two studied patients presented plasma triglycerides higher than 150 mg/dl. It is not surprising because we have already reported that in our PCOS population (and in our general population) serum triglycerides are lower than in other PCOS populations (26, 30).

Despite this, we found significant correlations between LDL size and triglycerides (inverse) and HDL-cholesterol (positive) in our patients with PCOS. LDL subclass analysis revealed that triglycerides significantly inversely correlated with largest particles (type I) and positively with medium-sized LDL (type IIB) and small-sized LDL (type IIIA); by contrast, HDL-cholesterol positively correlated with largest particles (type I) and inversely with medium-sized and smallest, most dense LDL (types IIB, IIIA, and IVB). Interestingly, these correlations were lost when the values were corrected for insulin levels, indicating that in PCOS most lipid alterations are not genetically determined but are linked to insulin resistance.

It has been suggested that changes in the quality of LDL particles may be genetically transmitted but also depend on insulin levels (23). In fact, insulin resistance and diabetes are associated with the predominance of small, dense LDL (23); consistent with the hypothesis that hyperinsulinemia plays a pivotal role in determining increased CV risk in PCOS (31), we found that insulin levels were inversely correlated with LDL size and positively with LDL particles types III and IV. It is probable that in PCOS, increased insulin levels modify the quality of circulating LDL increasing the more atherogenic types III and IV.

Because of relatively low triglyceride levels, complete ALP was relatively uncommon in our PCOS women but was more common than in matched controls where no ALP was found. It is probable that ALP is much more common in the U.S. PCOS population where circulating triglycerides are higher but, to date, no data on prevalence of LDL abnormalities or of ALP in the U.S. PCOS population have been reported.

In conclusion, we found in the present study, using high-quality methodology, that young Mediterranean women with PCOS show reduced LDL size, in comparison to age- and BMI-matched controls, due to peculiar changes in their LDL particle distribution, with a strong reduction in type I particles and a concomitant increase in type III and IV LDL subclasses. We also found in such patients that individual features of ALP may be common, but, because of relatively low triglyceride levels, complete ALP is relatively uncommon.


   Acknowledgments
 
The authors gratefully acknowledge the excellent technical assistance of S. Vosmeer.


   Footnotes
 
K.B. was supported by the Swiss National Foundation Grant 3200B105258.

Disclosure Summary: K.B., M.R., V.L., F.F., and E.C. have nothing to declare.

First Published Online October 24, 2006

Abbreviations: ALP, Atherogenic lipoprotein phenotype; BMI, body mass index; CV, cardiovascular; HDL, high-density lipoprotein; LDL, low-density lipoprotein; PCOS, polycystic ovary syndrome.

Received August 9, 2006.

Accepted October 18, 2006.


   References
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 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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