The Prevalence of Gestational Diabetes Mellitus and Glucose

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The Prevalence of Gestational Diabetes Mellitus
and Glucose Abnormalities in Pregnant Women
With Hepatitis C Virus Infection in British Columbia
Michelle C. Buresi, MD, PhD,1 Julie Lee, MD, FRCPC,2 Sabrina Gill, MD, MPH, FRCPC,2
Jason M. Kong, MD, FRCPC,2 Deborah M. Money, MD, FRCSC,3,4 Eric M. Yoshida, MD, MHSc, FRCPC1;
on behalf of the Hepatitis C Vertical Transmission Study Group*
Division of Gastroenterology, University of British Columbia, Vancouver BC
Division of Endocrinology, University of British Columbia, Vancouver BC
Department of Obstetrics and Gynaecology, University of British Columbia, Vancouver BC
Women’s Health Research Institute, Vancouver BC
*See Appendix for list of members.

Abstract                                                                   Résumé
    Objective: There is evidence to support an association between           Objectif : Certaines données soutiennent l’existence d’une association
      diabetes mellitus (DM) and hepatitis C virus (HCV) infection. The        entre le diabète sucré (DS) et l’infection au virus de l’hépatite C (VHC).
      insulin resistant state of pregnancy suggests a predisposition to        L’insulinorésistance de la grossesse semble indiquer une
      developing gestational diabetes mellitus (GDM) in women infected         prédisposition à l’apparition d’un diabète sucré gestationnel (DSG)
      with HCV. The aim of this study was to compare the prevalence of         chez les femmes infectées au VHC. Cette étude avait pour but de
      GDM and impaired glucose tolerance (IGT) of pregnancy between            comparer la prévalence du DSG et de la diminution de la tolérance
      women infected with HCV and the general population of British            au glucose (DTG) de la grossesse chez les femmes infectées au
      Columbia screened for GDM.                                               VHC et chez la population générale de la Colombie-Britannique
                                                                               soumises à un dépistage visant le DSG.
    Methods: The HCV cohort was drawn from a population-based
      prospective cohort of 148 pregnant women infected with HCV in          Méthodes : La cohorte VHC a été issue d’une cohorte prospective
      British Columbia. GDM screening tests were completed in 84 women.        en population générale de 148 femmes enceintes infectées au
      The prevalence of GDM and IGT of pregnancy in the general                VHC en Colombie-Britannique. Des tests de dépistage du DSG
      population of British Columbia was estimated by acquiring 24 321         ont été menés chez 84 femmes. La prévalence du DSG et
      GDM screening tests performed by the two major laboratories in           de la DTG de la grossesse au sein de la population générale
      the province.                                                            de la Colombie-Britannique a été estimée en se prévalant des
    Results: Non-compliance was the primary reason for incomplete              résultats de 24 321 tests de dépistage du DSG menés par les deux
      screening. The prevalence of GDM was 9.5% in the HCV cohort              principaux laboratoires de la province.
      and 6.8% in the screened general population (c test P = 0.33).         Résultats : La non-observance constituait la principale raison expliquant
      Similarly, there was no difference in IGT of pregnancy between the
                                                                               un dépistage incomplet. La prévalence du DSG était de 9,5 % au
      two cohorts (2.4% vs. 3.5%; c2 test P = 0.57).                           sein de la cohorte VHC et de 6,8 % au sein de la population générale
    Conclusion: A difference in the prevalence of either GDM or IGT of         dépistée (test c P = 0,33). De façon semblable, nous n’avons
      pregnancy was not detected between HCV-infected patients who             constaté aucune différence en matière de DTG de la grossesse entre
      were screened for GDM and those screened in the general                  les deux cohortes (2,4 %, par comp. avec 3,5 %; test c2 P = 0,57).
      population. Further studies are required to assess whether HCV
      infection is an independent risk factor for GDM.                       Conclusion : Aucune différence en matière de prévalence du DSG
                                                                               ou de la DTG de la grossesse n’a été détectée entre les patientes
                                                                               infectées au VHC qui s’étaient soumises à un dépistage du DSG
                                                                               et les femmes de la population générale s’étant soumises à un tel
                                                                               dépistage. La tenue d’autres études s’avèrent requise pour évaluer
                                                                               si l’infection au VHC.
                                                                           J Obstet Gynaecol Can 2010;32(10):935–941
    Key Words: Gestational diabetes, impaired glucose tolerance of
    pregnancy, hepatitis C, British Columbia
    Competing Interests: None declared.
    Received on May 30, 2010
    Accepted on June 23, 2010

                                                                                                         OCTOBER JOGC OCTOBRE 2010 l                 935

INTRODUCTION                                                      information to indicate that HCV infection is an independent
   n Canada, it is estimated that 247 200 people are              risk factor for GDM. Therefore, we sought to determine
I  chronically infected with hepatitis C.1 Hepatitis C virus
                                                                  whether HCV infection predisposes a woman to develop
                                                                  GDM during the progressive insulin resistant state of preg-
infection primarily affects the liver to cause cirrhosis and
                                                                  nancy. Such a demonstration would represent compelling
hepatocellular carcinoma, although a number of extrahepatic       evidence for mandatory glucose tolerance screening in pregnant
manifestations have been described and occur in approxi-          women with hepatitis C in order to improve diagnosis and
mately 38% of infected patients at some point during their        minimize the maternal and fetal complications of GDM.
illness. Conditions that have a well-documented association
with chronic HCV infection include glomerulonephritis,            METHODS
cryoglobulinemia, porphyria cutanea tarda, lymphoma, and
Sjögren syndrome.2 Over recent years there has been increas-      We conducted a retrospective review of a population-based
ing evidence of an association between HCV infection and          cohort of women with HCV infection in pregnancy.
diabetes mellitus, to the extent that DM is now considered        The HCV cohort was drawn from an existing database of
an extrahepatic manifestation of hepatitis C. Studies have        148 pregnant women infected with HCV in British Columbia,
suggested that the prevalence of type 2 DM is more than           who were prospectively enrolled in the Hepatitis C Vertical
three times higher among persons with chronic HCV infection       Transmission study conducted between 2000 and 2003.
                                                                  This study was a collaboration between the BC Centre for
than in those without HCV.3–6 Further, it is suggested that
                                                                  Disease Control, Canadian Blood Services, and the Chil-
the association is specific to HCV infection, rather than
                                                                  dren’s and Women’s Health Centre of British Columbia.
other forms of liver disease.4,7,8                                Ten women were excluded because they were enrolled
During pregnancy, maternal insulin resistance results from        twice or later declined enrolment. Screening for GDM was
increased placental secretion of diabetogenic hormones.           carried out according to criteria developed at the Fourth
Gestational diabetes mellitus occurs when a woman’s pan-          International Workshop-Conference on Gestational Diabetes
creatic function is insufficient to overcome the insulin resis-   Mellitus (Figure).19 Briefly, 79 women completed GDM
tance, and its prevalence varies with established risk factors    screening tests that measured blood glucose one hour after
including advanced maternal age, elevated BMI, African-           a 50 g oral glucose load. GDM was diagnosed in women
American, Latino, Native American, or Asian ethnicity,            with blood glucose levels ³ 10.3 mmol/L. If an intermediate
family history of diabetes, and previous delivery of a baby       value (7.8 to 10.2 mmol/L) was obtained after the 50 g
weighing more than 4 kg.9–13 In Canada, the prevalence of         GTT, blood glucose levels were measured in the fasting
GDM is estimated at 3.7% in non-Aboriginals, but may be           state and at one, two, and three hours after ingestion of
as high as 18% in Aboriginal populations.14                       100 g glucose. GDM was diagnosed if two or more abnor-
Several adverse fetal and maternal outcomes have been             mal values were obtained, and impaired glucose tolerance of
associated with glucose intolerance during pregnancy. The         pregnancy was diagnosed if one value was abnormal. Three
diagnosis and treatment of GDM are thus important in pre-         women underwent the 100 g GTT without first being
venting perinatal complications such as preeclampsia, fetal       screened with the 50 g test, and two women who had not
macrosomia, and perinatal mortality.15,16                         undergone any screening were found later in pregnancy to
In pregnant women, the prevalence of HCV infection is             require insulin to maintain blood glucose levels in the normal
estimated to range between 1% and 2%.17,18 It is unclear          range. These two women had histories of GDM during
whether HCV infection adversely affects glucose metabolism        multiple previous pregnancies and were not tested for that
during pregnancy, and there is currently insufficient             reason. A total of 84 patients were tested for GDM.

                                                                  The prevalence of GDM and IGT of pregnancy in the general
                                                                  population of British Columbia was estimated by acquiring
 ABBREVIATIONS                                                    24 321 GDM screening tests performed by the two major
 ALT         alanine aminotransferase                             commercial laboratories in British Columbia. These tests
 ARV         antiretroviral therapy                               represent all of the GDM screening tests done by the labo-
 DM          diabetes mellitus                                    ratories between July 1, 2003, and June 30, 2004, and
 GDM         gestational diabetes mellitus                        account for almost half of all GDM testing performed in
 GTT         glucose tolerance test                               the province of British Columbia during that time period.
 HAART       highly active antiretroviral therapy                 Each laboratory submitted 50 g and 100 g oral GTT results
 HCV         hepatitis C virus                                    with patients identified only by age and anonymous patient
                                                                  identification number.

                        The Prevalence of Gestational Diabetes Mellitus and Glucose Abnormalities in Pregnant Women With Hepatitis C

             Screening for and diagnosis of GDM, according to criteria developed by the Fourth International
             Workshop-Conference on Gestational Diabetes Mellitus.19

              1hPG: 1-hour plasma glucose; 2hPG: 2-hour plasma glucose; 3hPG: 3-hour plasma glucose; FPG: fasting plasma glucose;
              OGTT: oral glucose tolerance test.

Demographic and clinical characteristics describing the                       incomplete screening. The average age of women in the
HCV cohort were obtained. Information regarding poten-                        HCV infection cohort who were screened for GDM was
tial confounding risk factors for GDM, such as age, ethnic-                   30.3 years. This was not significantly different from the
ity, BMI, hypertension, previous GDM, history of delivery                     average age of the general population (30.4 years). Weight
of a baby with a birth weight of greater than 4 kg, HIV status                and height were not known for the majority of
and antiretroviral therapy, corticosteroid therapy, and pre-                  HCV-infected women, but of the 21 subjects for whom
vious diagnosis of GDM, were obtained when available.                         BMI could be calculated, nine (42.9%) were within the nor-
The degree of liver disease was estimated by alanine amino-                   mal weight range and 11 (52.3%) were either overweight or
transferase levels, number of years since diagnosis of HCV                    obese (BMI > 25). In the screened HCV infection cohort,
infection, and hepatitis B co-infection status. Unpaired                      61.9% were Caucasian and 22.6% were Aboriginal (First
t tests were used to compare age, BMI, and liver dysfunc-                     Nations). A previous history of GDM was present in 4.8%,
tion in women who completed GDM screening with those                          and 3.6% had either pregnancy-related hypertension or
variables in women who did not. A raw rate comparison of                      essential hypertension. Of the screened HCV cohort, 9.5%
the prevalence of GDM in the general population of preg-                      had co-infection with HIV and 8.3% were treated with
nant women in British Columbia and in the HCV infection                       antiretroviral therapy. Twenty-one women from the HCV
cohort was performed with a chi-square test.                                  cohort had documented birth weights from previous deliv-
This substudy was approved by the University of British                       eries. Four mothers in this group had a history of delivering
Columbia Clinical Research Ethics Board. There was no                         a large baby; two of these had IGT and one had an abnor-
contact between the subjects and the HCV/GDM study                            mal screening test but did not go on to have the 100 g test
research staff. Relevant data were collected from the exist-                  (Table 1).
ing Hepatitis C Vertical Transmission study database, with
all personal identifiers removed.                                             With respect to the degree of liver disease, 65.5% of the
                                                                              women had a diagnosis of HCV infection for less than
RESULTS                                                                       five years; 40.5% had ALT levels in the normal range
Unpaired t tests showed no significant differences in age or                  (³ 35 IU/L), 35.7% had ALT levels between 36 and
BMI between women in the HCV infection cohort who                             100 IU/L, and 16.7% had levels above 100 IU/L. Hepatitis
completed screening and those who did not (data not                           B co-infection was present in 4.8% (Table 1). Unpaired
shown). Non-compliance was the primary reason for                             t tests showed no significant differences in liver dysfunction

                                                                                                          OCTOBER JOGC OCTOBRE 2010 l   937

                                                                   between women who completed screening and those who
 Table 1. Maternal characteristics of HCV cohort (subset
 having undergone GDM testing)                                     did not (data not shown).
                                                                   The prevalence of GDM among screened persons was
 Demographics                                  HCV cohort, n (%)
                                                                   9.5% in the HCV infection cohort and 6.8% in the general
 Age                                                               population (Table 2). These values were not significantly
      Age > 25 years                               67 (79.8)       different (P = 0.33). Similarly, there was no difference in the
      Age £ 25 years                               17 (20.2 )
      Average age*                                   30.3
                                                                   prevalence of IGT of pregnancy between the two cohorts
 Ethnicity                                                         (2.4% vs. 3.5%; c2 test P = 0.57).
      Caucasian                                    52 (61.9)
      African Canadian                              1 (1.2)
      South African                                 2 (2.4)        In the present study, we found no significant difference
      Asian                                         1 (1.2)        between the rates of GDM in HCV infected women and
      First Nations                                19 (22.6)       women in the general population (9.5% vs. 6.8%). Similarly,
      Hispanic                                         0           there was no difference between the two cohorts in the
      Other ethnicity                               3 (3.6)        prevalence of IGT of pregnancy. In Canada, the prevalence
      Unspecified                                   6 (7.1)        of GDM is estimated at 3.7%,14 and the higher prevalence
 BMI, kg/m2                                                        rates obtained in our study are likely an overestimation
      Total available                                 21
                                                                   because patients who were not screened for GDM were not
      Underweight < 18.5                            1 (4.8)
                                                                   included in either cohort.
      Normal weight 18.5–24.9                      9 (42.9)        The results of our study are in contrast with what has
      Overweight 25–29.9                           7 (33.3)        previously been reported. In general, there have been few
      Obesity ³ 30                                 4 (19.0)        studies on the effect of chronic hepatitis C infection on
                                                                   pregnancy, or on maternal and neonatal health outcomes.
 Comorbid conditions                                 n (%)
                                                                   Indeed, only one study examining the impact of HCV infec-
 Previous GDM                                       4 (4.8)        tion specifically on GDM has been previously published.20
 Hypertension                                                      This population-based study by Pergam et al.20 found an
      Pregnancy related                             2 (2.4)        increased risk of GDM in 497 HCV infected women. How-
      Essential                                     1 (1.2)        ever, in that study the association between HCV infection
 Previous high birth weight                                        and GDM was observed in women who had excess weight
      Total available                                 21           gain during pregnancy, but it was absent in women with
      birth weight > 4 kg                           4 (19)         adequate or insufficient weight gain.20 Other studies have
 HIV positive                                                      reported similar findings outside the context of pregnancy,
      Total                                         8 (9.5)        with abnormal glucose tolerance being increased in obese
      ARV therapy during                            7 (8.3)        individuals with hepatitis C, but not in non-obese partici-
      pregnancy                                                    pants.21 In the present study, BMI values were available in
      No ARV therapy during                         1 (1.2)        only 21 women of the HCV cohort, and 10 of these were
      pregnancy                                                    either normal weight or underweight. When weight gain
 Duration HCV infection, years                                     was not taken into account in the study by Pergam et al., the
      £5                                           55 (65.5)       prevalence of GDM in the HCV infection cohort was
      6–10                                         17 (20.2)       found to be 7%, similar to our rate of 9.5%.
      11–19                                        10 (11.9)
                                                                   The discrepancy between the two studies may also be
      ³ 20                                             0
                                                                   explained by underestimation of glucose abnormalities in
      not specified                                 2 (2.4)
                                                                   HCV-infected patients in our study, given that 40% of the
 Hepatitis B positive                               4 (4.8)        original cohort either was not screened or was incompletely
 ALT                                                               evaluated. For instance, two women with abnormal results
      £ 35 (normal)                                34 (40.5)       in the 50 g GTT, thus having a high likelihood of altered
      36–100                                       30 (35.7)       glucose metabolism, did not undergo the 100 g test. These
      > 101                                        14 (16.7)       women were therefore considered not to have IGT or GDM.
      unknown                                       6 (7.1)        Given this lack of screening in a significant proportion of
                                                                   the HCV-infected cohort, it may be difficult to draw the
*Average of the general population is 30.4 years
                                                                   definitive conclusion that this population is not at increased

                         The Prevalence of Gestational Diabetes Mellitus and Glucose Abnormalities in Pregnant Women With Hepatitis C

 Table 2. Prevalence of abnormal glucose tolerance in                infection on glucose metabolism among adults with HIV
 a sample of pregnant women infected with HCV and                    infection, and found that the prevalence of insulin resis-
 in the general population of pregnant women of                      tance was increased among HCV positive individuals (com-
 British Columbia                                                    pared to seronegative patients) even after adjustment for
                                       HCV       General             BMI, ethnicity, age, sedentary behaviour, ARV therapy, and
                                     patients   population           protease inhibitor use. Interestingly, ARV and protease
                                      n = 84    n = 20 726    P      inhibitor use were not associated with insulin resistance or
 Gestational diabetes mellitus, %      9.5         6.8       0.33    abnormal glucose tolerance.21 However, another study
 Impaired glucose tolerance of         2.4         3.5       0.57
                                                                     found that HIV/HCV co-infection was associated with a
 pregnancy, %                                                        significantly higher risk of diabetes in the HAART era, but
                                                                     not in the pre-HAART era.25
                                                                     Examining the effect of HCV infection on glucose metabo-
risk of GDM. We calculate that to definitively exclude the           lism, and DM in general, has been difficult due both to the
possibility of a beta error would require a minimal sample           frequent presence of confounding variables that predispose
size of 966 in each group, which was beyond the resources            to diabetes and to the lack of matched control groups. Our
available to us.                                                     study had similar limitations that, unfortunately, are inevitable
Non-compliance was the primary reason for incomplete                 with retrospective chart review/database studies. We were
screening, although inconsistent clinical practice may also          unable to obtain complete data on established or potential
have been a factor. The Canadian Diabetes Association                risk factors for GDM in either the HCV infection or the
2008 clinical practice guidelines recommend universal                reference cohort. Such information was not obtained
screening for GDM in all pregnant women between 24 and               because of lack of patient compliance, inconsistent clinical
28 weeks’ gestation.14 Despite this, oral GTTs are not con-          practice, or concerns that patient anonymity would be
sistently performed in current clinical practice.                    threatened. In addition, the prevalence of hepatitis C in the
                                                                     control group was not known. Although HCV infection in
The absence of severe liver dysfunction in our HCV infec-
                                                                     the control population represents a confounding variable, it
tion cohort may also have contributed to the lack of
                                                                     is unlikely to have had a significant impact on results given
increased incidence of GDM. More than 75% of women
                                                                     the likely relatively low prevalence of hepatitis C in the over-
had ALT values that were in the normal range or only mildly
                                                                     all general population of British Columbian women of
elevated. Although the prevalence of DM is increased in
                                                                     reproductive age.
HCV-infected persons even without significant hepatic
dysfunction, the association appears to be strongest among           Although several small studies did not find an increased risk
persons with end-stage liver disease.6,22,23 The effect of           of obstetrical complications in women with HCV infec-
HCV infection as an independent risk factor may also be              tion,26–28 Pergam et al.20 demonstrated an increased risk of
mitigated in otherwise healthy non-obese young women                 premature rupture of membranes, as well as low birth
who do not have other risk factors for DM, compared to               weight, small size for gestational age, and increased require-
the stereotypical male, older HCV-infected patient with a            ment for neonatal intensive care unit admission and assisted
high BMI and some degree of liver dysfunction.                       ventilation in babies born to mothers infected with HCV.20
Age above 25 years is a well-established risk factor for
development of GDM. Despite our HCV infection cohort’s
average age of 30 years, young age may also explain the lack         Reports to date suggest that pregnant women with HCV
of increased prevalence of glucose abnormalities in our              infection should be considered at higher medical risk in
HCV infection cohort. In previous studies, the association           general, and that mandatory glucose tolerance screening
between hepatitis C and DM was seen predominantly in                 would be a reasonable “good practice” in order to improve
older individuals. Indeed, among persons older than                  diagnosis and minimize the maternal and fetal complications
40 years, those with HCV infection were more than three              of GDM. With regard to the specific question of whether
times as likely to have type 2 DM as those without HCV               HCV infection is an independent risk factor for GDM,
infection.3                                                          further prospective studies are required.
HIV infection is also associated with an increased preva-
lence of disorders of insulin metabolism and DM, and the
cause of this is likely multifactorial, related both to the tox-     The Vertical Transmission of Hepatitis C parent study was
icity of antiretroviral therapies and to the effects of the virus    funded by Health Canada, and this work was supported by a
itself.24 Howard et al.21 investigated the effect of HCV             grant from the St. Paul’s Hospital Research Foundation.

                                                                                             OCTOBER JOGC OCTOBRE 2010 l          939

This work was presented as a poster at the Canadian Digestive                             prevention and management of diabetes in Canada. Canadian Journal
                                                                                          of Diabetes 2008;32(Suppl 1):S168–S180.
Diseases Week, March 2010, in Toronto ON.
                                                                                       15. Crowther CA, Hiller JE, Moss JR, McPhee AJ, Jeffries WS, Robinson JS;
                                                                                           Australian Carbohydrate Intolerance Study in Pregnant Women (ACHOIS)
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                   The Prevalence of Gestational Diabetes Mellitus and Glucose Abnormalities in Pregnant Women With Hepatitis C

HCV Vertical Transmission Study Group Investigators
Deborah Money, MD, FRCSC (Department of Obstetrics and Gynaecology, University of British Columbia),
Simon Dobson, MD, MBBS, MRC, FRCPC (Department of Pediatric Infectious Diseases, British Columbia
Children’s Hospital), Lesley Cole, BSN, RN (British Columbia Women’s Hospital), Emily Wagner, MSc
(Women’s Health Research Institute), Eric M. Yoshida, MD, MHSc, FRCPC (Division of Gastroenterology,
University of British Columbia), and the HCV Perinatal Study group*
*Mark Bingham, MD, FRCPC, MHSc (Canadian Blood Services BC and Yukon), Patrick Doyle, MD, FRCPC, MHSc
(Department of Pathology and Laboratory Medicine, University of British Columbia), Mel Krajden, MD, FRCPC
(British Columbia Centre for Disease Control), Fiona Liston, MD (Faculty of Medicine, Queen’s University),
David Patrick, MD, FRCPC, MHSc (British Columbia Centre for Disease Control), Vesna Popovska, MD
(BC Children’s Hospital), Rick Schreiber, MD, FRCPC, DAAP (Department of Pediatrics, University of British Colum-
bia), Chris Sherlock, MB, BSc, FRSM, LMCC (Department of Laboratory Medicine, University of British Columbia).

                                                                                       OCTOBER JOGC OCTOBRE 2010 l         941

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