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The Journal of Clinical Endocrinology & Metabolism Vol. 91, No. 12 4862-4865
Copyright © 2006 by The Endocrine Society

Mild Gestational Diabetes as a Risk Factor for Congenital Cryptorchidism

Helena E. Virtanen, Anna E. Tapanainen, Marko M. Kaleva, Anne-Maarit Suomi, Katharina M. Main, Niels E. Skakkebaek and Jorma Toppari

Departments of Physiology and Paediatrics (H.E.V., A.E.T., M.M.K., A.-M.S., J.T.), University of Turku, 20520 Turku, Finland; and University Department of Growth and Reproduction (K.M.M., N.E.S.), Rigshospitalet, DK-2100 Copenhagen, Denmark

Address all correspondence and requests for reprints to: Helena Virtanen, University of Turku, Department of Physiology, Kiinamyllynkatu 10, 20520 Turku, Finland. E-mail: helena.virtanen{at}utu.fi.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Cryptorchidism is the most common malformation in newborn boys. Maternal diabetes has previously been suggested to be a risk factor for this disorder in one epidemiological study.

Objective: Evaluation of the prevalence of maternal glucose metabolism disorders during pregnancy in newborn boys having normal testicular descent or congenital cryptorchidism.

Design: Postnatal analysis of maternal history concerning glucose metabolism abnormalities during pregnancy among cryptorchid and healthy Finnish boys.

Setting and Participants: The material of this case-control study comprises 1163 boys with normal testicular descent at birth and 125 boys with congenital cryptorchidism. All these singleton Finnish boys were born in Turku University Central Hospital (1997–2001) and were examined at birth and/or at the expected date of delivery.

Main Outcome Measures: Information about maternal diabetes diagnosis and abnormality of the result of a 2-h 75-g oral glucose tolerance test during pregnancy were obtained from the hospital records after delivery.

Results: After adjustment for possible confounding factors, i.e. maternal smoking during pregnancy, maternal age at delivery, and risk factors of cryptorchidism, e.g. prematurity and weight for gestational age, abnormal maternal glucose metabolism was significantly more common in the group of cryptorchid boys [diet-treated gestational diabetes, P = 0.0001; odds ratio, 3.98 (95% confidence interval, 1.97–8.05); diet-treated gestational diabetes or only an abnormal result in oral glucose tolerance test, P = 0.0016; odds ratio, 2.44 (95% confidence interval, 1.40–4.25)] when compared with boys with normal testicular descent.

Conclusions: Mildly abnormal glucose metabolism during pregnancy was associated with an increased risk for congenital cryptorchidism. The mechanism remains to be elucidated.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
IN ADDITION TO prepregnancy diabetes mellitus, gestational diabetes with fasting hyperglycemia has also been linked to an increased risk for congenital malformations in the newborn (1). Abnormal testicular descent, i.e. cryptorchidism, is a common urogenital malformation in newborn boys. In Finland, the birth prevalence rate was 2.4% in our prospective study (2). Maternal diabetes has been associated with an increased risk for cryptorchidism (3). However, only 30% of cases in that study had a diagnosis of cryptorchidism already in the newborn period. Thus, the material may include also cases with acquired, i.e. noncongenital, cryptorchidism. Furthermore, the type of diabetes was not analyzed. In another study evaluating the association between maternal diabetes and congenital cryptorchidism, the increase in risk was not statistically significant (4). However, cases were classified into two groups on the basis of spontaneous testicular descent by the age of 1 yr, and the groups were analyzed separately.

The aim of the present study was to evaluate postnatally the prevalence of disorders of maternal glucose metabolism during pregnancy among newborn boys having normal testicular descent or congenital cryptorchidism.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
The study material comprises 1163 boys with normal testicular descent at birth (controls) and 125 boys with congenital cryptorchidism (cases). All these singleton Finnish boys were born in Turku University Central Hospital, and they had participated either in a prospective cohort study on urogenital malformations in 1997–1999 (boys with normal testicular descent) or a case-control study on cryptorchidism in 1997–2001 (cryptorchid boys), and their mothers’ pregnancy records were available for this retrospective analysis. The research group examined all boys at birth and/or at the expected date of delivery (premature cases). Examination technique and the clinical classification of testicular position were previously described in detail (2). A total of 122 boys with congenital cryptorchidism (98%) were reexamined at 3 months or at the corrected age of 3 months (preterm cryptorchid boys). At this 3-month examination, 70 cases (57% of examined) were still cryptorchid. A total of 1098 control boys (94%) were also examined at the age of 3 months, and they all had scrotal testes at that age.

Of all mothers attending the study, information about the diabetes diagnosis and any abnormality of the result of a 2-h 75-g oral glucose tolerance test (OGTT) during pregnancy (abnormal/normal) were obtained from hospital records after delivery. In Finland, OGTT is performed during pregnancy if a mother has a risk factor for gestational diabetes [glucose in a morning urine sample, body mass index (BMI) > 25 kg/m2, previous delivery of a baby with a birth weight over 4.5 kg, mother’s age over 39 yr, fetal macrosomia (estimated fetal weight over two SD values above the mean fetal weight or > 90th weight percentile), or diabetes in a previous pregnancy]. In the test, plasma glucose level is measured after fasting and 1 and 2 h after giving 75 g glucose orally.

In this study, information on gestational age, boy’s birth weight, and preeclampsia was obtained from the hospital records. Information on mother’s smoking during pregnancy, height, and weight before pregnancy was obtained either from the hospital records or from the questionnaire of the cryptorchidism study. The study was done according to the Helsinki II declaration and was approved by the local ethics committee. Written informed consent was given by the mothers.

Pearson’s {chi}2 test, Fisher’s exact test, and simple and multiple logistic regression analysis were used for statistical analyses, which were performed using SAS for Windows, release 9.1.3. Odds ratios (OR) were used for evaluating the effects of categorized variables. P < 0.05 was defined as statistically significant. Multivariate models originally included all variables described in Table 2Go, but nonsignificant variables (maternal BMI, preeclampsia, OGTT performed during pregnancy) were excluded from the final model one at a time.


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  		TABLE 2. Prevalence of maternal risk factors for gestational diabetes (high maternal BMI, high maternal age, and smoking during pregnancy), percentage of mothers having OGTT performed during pregnancy, and prevalence of risk factors of cryptorchidism (preeclampsia, low birth weight for gestational age, and prematurity) in groups of boys with congenital cryptorchidism or normal testicular descent

 

   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
In the group of boys having normal testicular descent at birth, 1062 mothers (91.3%) had neither a diagnosis of diabetes nor an abnormal result in the OGTT (if performed), and these mothers were classified as having normal glucose metabolism during pregnancy. Forty-seven mothers (4.0%) had a diabetes diagnosis: two mothers had prepregnancy diabetes, two mothers had insulin-treated gestational diabetes, and 43 mothers had diet-treated gestational diabetes. In addition, 54 mothers (4.6%) had an abnormal result in the OGTT during pregnancy without a diagnosis of diet-treated gestational diabetes (Table 1Go).


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  		TABLE 1. Distribution of boys with congenital cryptorchidism or normal testicular descent into different maternal glucose metabolism classes during pregnancy

 
Correspondingly, in the group of cryptorchid boys, 105 mothers (84.0%) were classified as having normal glucose metabolism during pregnancy. Thirteen mothers (10.4%) had a diabetes diagnosis, and they all had a diet-treated gestational diabetes. Additionally, seven mothers (5.6%) had an abnormal result in the OGTT without a diagnosis of diet-treated gestational diabetes (Table 1Go).

Maternal diabetes was significantly more common among the cryptorchid boys compared with the boys with normal testicular descent at birth (P = 0.0013). In the group of cryptorchid boys, none of the mothers had any type of diabetes diagnosed other than a diet-treated gestational diabetes. Thus, in further analyses, only mothers having either a diet-treated gestational diabetes or only an abnormal result in the OGTT during pregnancy or normal glucose metabolism were compared.

Table 2Go describes the occurrence of risk factors for gestational diabetes (high maternal BMI, high maternal age, and maternal smoking), the frequency of performed OGTT, and the occurrence of previously described risk factors of cryptorchidism [preeclampsia (3), low birth weight for gestational age, and prematurity] among cryptorchid and healthy boys included in further analyses. Maternal age greater than 39 yr at delivery was significantly more common in the group of cryptorchid boys than in the group of boys with normal testicular descent. Maternal smoking during pregnancy, which has been suggested to be linked to an increased risk for gestational diabetes (5), was, however, significantly more common in the group of boys with normal testicular descent at birth. The frequency of performed OGTT was higher among the mothers of cryptorchid boys compared with mothers of boys with normal testicular descent at birth. Prematurity (length of gestation < 37 wk) and low birth weight for gestational age, i.e. being born as small for gestational age [SGA, i.e. gestational age-adjusted birth weight < –2 SD for a gender-differentiated reference group (6)], were significantly more common among cryptorchid boys compared with healthy boys.

Mothers of cryptorchid boys significantly more often had a diet-treated gestational diabetes diagnosis compared with mothers of boys with normal testicular location at birth (Table 1Go). Also the combined class of abnormal maternal glucose metabolism during pregnancy (including both maternal diet-treated gestational diabetes diagnosis and only an abnormal result in the OGTT during pregnancy) was significantly more common in the group of cryptorchid boys. When maternal age at delivery (≤39 vs. >39), and maternal smoking during pregnancy (yes vs. no), length of gestation (<37 wk vs. ≥37 wk), and weight for gestational age (small vs. appropriate for gestational age, large vs. appropriate for gestational age) were taken into the multivariate model as confounders, both maternal diet-treated gestational diabetes and the combined class of abnormal maternal glucose metabolism during pregnancy were still significantly more common in the group of cryptorchid boys (Table 1Go).

Among boys with normal testicular descent, maternal glucose metabolism abnormality during pregnancy was associated with a significantly increased odds for being born as large for gestational age (LGA) instead of appropriate for gestational age (AGA) (P < 0.0001; OR, 7.11; 95% confidence interval, 3.02–16.72). Such significant association was not observed among cryptorchid boys (P = 0.98 and P = 0.19 when comparing cryptorchid boys with normal and abnormal maternal glucose metabolism, respectively, to controls with normal maternal glucose metabolism).

In an additional subanalysis, only boys with congenital cryptorchidism were included. This analysis showed that the proportion of mothers belonging to the above-mentioned combined class was similar in the groups of boys with cryptorchidism prevailing still at the age of 3 months and of boys with spontaneous testicular descent by the age of 3 months (P = 0.80) (Table 3Go). In addition, the proportion of mothers belonging to the combined class was not different among cases with unilateral and bilateral cryptorchidism at birth (P = 0.09) (Table 3Go).


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  		TABLE 3. Distribution of boys with congenital cryptorchidism into different maternal glucose metabolism classes during pregnancy based on laterality of cryptorchidism and possible recovery by the age of 3 months

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Our study indicates that mild gestational diabetes is associated with an increased risk for congenital cryptorchidism. This risk is also increased when all mothers with only an abnormal result in the OGTT during pregnancy are included in the group of diabetic mothers. Thus, even if the used diagnostic criteria of gestational diabetes were not reevaluated in this analysis, the latter finding strengthens our result of increased risk for congenital cryptorchidism in pregnancies with mild gestational diabetes. The risk remains increased also after adjustment for known confounders, i.e. high maternal age and maternal smoking, and previously described risk factors of cryptorchidism, e.g. prematurity and low birth weight for gestational age.

This is to our knowledge a novel finding, well in line with previous reports showing that pregnancies with only one abnormal value in OGTT are associated with an increased risk for fetal morbidity (e.g. fetal macrosomia, hyperinsulinism, and postpartum hypoglycemia) (7, 8). There appears to be a continuum of the effects of increasing maternal glucose intolerance on fetal morbidity (8). Considering our results, the increasing prevalence of gestational diabetes (9) may have considerable effect on male reproductive health. Furthermore, because cryptorchidism is the best known risk factor for testicular cancer and it is also associated with impaired semen quality (10), it would be interesting to analyze whether abnormal maternal glucose metabolism during pregnancy is associated with these testicular disorders as well.

Gestational diabetes and milder pregnancy hyperglycemia have been suggested to be risk factors for preterm delivery (11, 12). Prematurity, in turn, has been linked to an increased risk for cryptorchidism (13). Similarly, low birth weight compared with the duration of pregnancy, i.e. being born SGA, has been linked to an increased risk for cryptorchidism in several studies (14, 15). Also in our material, prematurity and being born SGA were significantly more common in the group of cryptorchid boys. However, both diet-treated gestational diabetes and the combined class of abnormal maternal glucose metabolism were associated with an increased risk for cryptorchidism also when preterm delivery and low birth weight for gestational age were taken into account.

Among boys with normal testicular descent, the combined class of abnormal maternal glucose metabolism was associated with increased weight for gestational age. The absence of such significant association among cryptorchid boys may be due to the low number of boys born after pregnancy with glucose metabolism abnormality.

It remains to be elucidated how mildly abnormal glucose metabolism during pregnancy increases the risk for congenital cryptorchidism. However, previous studies have shown that women with gestational diabetes have lower SHBG levels than nondiabetic pregnant women already in the first trimester of pregnancy (16, 17, 18), which could theoretically expose their fetuses to increased levels of non-SHBG-bound estrogen. Furthermore, both impaired glucose tolerance and gestational diabetes have been associated with higher than normal levels of insulin in umbilical cord blood, indicating fetal hyperinsulinemia (19, 20). Although no difference in sex hormone concentrations in cord blood samples from pregnancies of diabetic vs. control mothers has been found, a negative correlation between SHBG levels and insulin levels has been observed to exist already at birth (21). Thus, fetal SHBG levels may be decreased also in pregnancies with mildly abnormal glucose metabolism. In adult men, decrease in SHBG level is associated with an increase in the ratio of non-SHBG-bound levels of estradiol and testosterone (22). Therefore, if mildly abnormal maternal glucose metabolism during pregnancy is associated with an imbalance between fetal estrogen and androgen action, this could potentially interfere with the descent of the testis because testicular descent is influenced by the effect of both androgens and estrogens (10, 23). Androgens are important in the second (i.e. inguinoscrotal) phase of testicular descent (24), whereas estrogens have been shown to affect the first (i.e. transabdominal) phase of testicular descent in animals by down-regulating the expression of Insl3 gene (25). INSL3 regulates the growth of gubernaculum, i.e. the structure that guides the transabdominal descent of testis (26, 27, 28).

In conclusion, mild abnormal maternal glucose metabolism during pregnancy (diet-treated gestational diabetes only or in combination with abnormal result in OGTT without a diabetes diagnosis) was associated with an increased risk for congenital cryptorchidism. The mechanism for the increased risk remains to be elucidated.


   Acknowledgments
 
We thank biostatistician Heikki Hiekkanen for his kind help with the statistical analyses. We also thank Mrs. Leena Karlsson for technical help in the data collection.


   Footnotes
 
This work was supported by The Turku University Central Hospital, the Academy of Finland, the Sigrid Jusélius Foundation, and the European Commission (contracts BMH4-CT96-0314, QLK4-CT1999-01422, QLK4–2000-00684, QLK4–2001-00269, and QLRT-2001-00603).

Disclosure statement: The authors have nothing to disclose.

First Published Online October 10, 2006

Abbreviations: AGA, Appropriate for gestational age; BMI, body mass index; LGA, large for gestational age; OGTT, oral glucose tolerance test; OR, odds ratio; SGA, small for gestational age.

Received July 3, 2006.

Accepted September 28, 2006.


   References
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 Introduction
 Subjects and Methods
 Results
 Discussion
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