• Users Online: 250
  • Print this page
  • Email this page


 
 Table of Contents  
ORIGINAL ARTICLES
Year : 2021  |  Volume : 12  |  Issue : 5  |  Page : 73-78

Postpartum abnormal glucose tolerance and predictive factors among women with gestational diabetes mellitus in Gampaha District, Sri Lanka


1 Directorate of Environmental Health, Occupational Health and Food Safety, Sri Sangaraja Mawatha, Colombo 08, Sri Lanka
2 University of Colombo, Colombo 08, Sri Lanka
3 Epidemiological Unit, No. 231, De Saram Place, Colombo 01, Sri Lanka

Date of Submission23-Jan-2021
Date of Decision26-Apr-2021
Date of Acceptance03-May-2021
Date of Web Publication20-Jul-2021

Correspondence Address:
Dr. Buddhika Hemali Sudasinghe
No. 94, Kalugashinna, Pattiyagama, Pugoda.
Sri Lanka
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jod.jod_9_21

Rights and Permissions
  Abstract 

Context: Gestational diabetes mellitus (GDM) is a recognized risk for abnormal glucose tolerance (AGT) long-term. Aims: The aim of this study is to determine the prevalence of postpartum diabetes and AGT and predictive factors among Sri Lankan women with GDM. Settings and Design: The follow-up study was conducted in Gampaha District, Sri Lanka. Materials and Methods: Pregnant women with GDM were identified by a community-based longitudinal study (n = 1200) by WHO 1999 criteria and followed up till 1 year postpartum. Study instruments were interviewer-administered questionnaire, anthropometric measurements, and fasting 75 gOGTT. Statistical Analysis Used: χ2 tests with P-values and odds ratios (ORs) with 95% confidence interval (CI) were used to assess the statistical significance and strength of the associations. Predictive factors of postpartum AGT were identified by the multivariate analysis. Results: Of those identified with GDM (194), 169 participated in postpartum follow-up at 2 months (87.1%). Of the 169, 59 participated at 1 year. At 2 months, 17/169 (10.1%) had diabetes and 55/169 (32.5%) had AGT (diabetes=17, impaired glucose tolerance= 36, impaired fasting glucose=2). At 1 year, 11/59 (18.6%) had diabetes and 28/59 (47.5%) had AGT. Predictive factors of postpartum AGT at 2 months were 2-h postprandial blood sugar (2-h PPBS) before 12 weeks ≥97.5 mg/dL (adjusted OR (aOR)=2.8; 95% CI=1.3–6.0), GDM diagnosis before 16 weeks (aOR=7.7; 95% CI=1.5–39.7), and 1-h oral glucose tolerance test (OGTT) ≥179 mg/dL (aOR=3.1; 95% CI=1.5–6.4). Predictive factors of postpartum AGT at 1 year were 2-h PPBS before 12 weeks ≥97.5 mg/dL (aOR=8.4; 95% CI=2.3–30.3) and physical activity (aOR= 0.2; 95% CI=0.1–0.8). Conclusion: Postpartum AGT following GDM is high among Sri Lankan women. Long-term follow-up is recommended.

Keywords: 75 gOGTT, GDM, gestational diabetes mellitus, postpartum abnormal glucose tolerance, predictive factors


How to cite this article:
Sudasinghe BH, Wijeyaratne CN, Ginige SP. Postpartum abnormal glucose tolerance and predictive factors among women with gestational diabetes mellitus in Gampaha District, Sri Lanka. J Diabetol 2021;12, Suppl S1:73-8

How to cite this URL:
Sudasinghe BH, Wijeyaratne CN, Ginige SP. Postpartum abnormal glucose tolerance and predictive factors among women with gestational diabetes mellitus in Gampaha District, Sri Lanka. J Diabetol [serial online] 2021 [cited 2021 Jul 30];12, Suppl S1:73-8. Available from: https://www.journalofdiabetology.org/text.asp?2021/12/5/73/321826




  Key Messages: Top


Postpartum follow-up of women with GDM is important.


  Introduction Top


Gestational diabetes mellitus (GDM) is defined as any degree of glucose intolerance with onset or first recognition during pregnancy.[1] GDM predisposes women to an increased risk of postpartum abnormal glucose tolerance (AGT) (impaired glucose tolerance (IGT), impaired fasting glucose (IFG), and type 2 diabetes). Risk factors for the development of postpartum AGT following GDM have been identified; nevertheless, the reported data are not conclusive due to different methodologies and diverse diagnostic criteria for GDM. Therefore, this study was conducted to assess the prevalence of postpartum AGT and its predictive factors among a cohort of women with GDM in Sri Lanka.


  Subjects and Methods Top


Study design

This was a descriptive follow-up study of women with GDM.

Study setting

The study was conducted in Gampaha District, Sri Lanka.

Study population

A cohort of women with GDM were identified by a community-based universal screening approach by a longitudinal study conducted in Gampaha District, Sri Lanka.

Ethical clearance for the study was granted by Ethics Review Committee (ERC) Medical Research Institute, Colombo (project 48/2012, date May 29, 2013). Permission was obtained from the Regional Director of Health Services of Gampaha District prior to data collection, with data collected by research assistants under the supervision of the principal investigator (PI).

Data collection procedure

Sri Lanka is divided into 25 districts and about 11% (2,304,833) of the Sri Lankan population lives within Gampaha District. Gampaha District consists of 16 Medical Officer of Health (MOH) areas, of them, two MOH areas were selected randomly and 15% of the population of Gampaha District lives in these MOH areas.[2] Each MOH area is supervised by an MOH. The MOH and his team are responsible for provision of preventive health care within the defined area. Public Health Midwife (PHM), a member of MOH team, is a grassroot health worker in the Sri Lankan health system, and the main responsibility of the PHM is to provide maternal and child health care at the domiciliary level for a population of about 3000.

At the initiation of the study, a population survey was conducted by the PI to assess the completeness of registration of pregnant women by PHM in these selected MOH areas, and the survey revealed that pregnant women registration by PHM in these two MOH areas were more than 98%. Whenever a woman in her area becomes pregnant, PHM enters her details in a register called “pregnant mother’s register” and advises to come to the field-based antenatal clinic at the earliest.

Therefore, from January 2014 to March 2015, a longitudinal study was conducted among pregnant women (n = 1200) attending field-based antenatal clinics in the randomly selected MOH areas in Gampaha District to identify women with GDM. Pregnant women with period of amenorrhea (POA) less than 12 weeks were recruited. Those diagnosed as having DM before pregnancy, on prescribed diabetogenic drugs such as steroids, anti-epileptics, and anti-psychotics, and having severe co-morbidities or mental subnormality were excluded. Informed written consent was obtained from all the study participants. GDM was diagnosed by fasting 75 gOGTT and WHO 1999 criteria (fasting plasma glucose (FPG) value ≥ 126 mg/dL or 2-h plasma glucose value of ≥140 mg/dL). All pregnant women diagnosed as having GDM were invited for the follow-up study.

They were advised to come to child welfare clinics at 2 months postpartum. Reminders to attend the postpartum clinic were sent via the PHM by home visits and in parallel with personalized telephone calls from the PI in order to optimize compliance. Since nearly all mothers bring their babies for immunization at 2 months postpartum, their routine activities were not interfered with. Mothers were instructed to come following an overnight 8-h fast in order to perform oral glucose tolerance test (OGTT) and total cholesterol. Venous blood was taken for FPG and total cholesterol, while recording their sociodemographic details; 75 g glucose dissolved in 250 mL of water was swallowed and the 2-h blood sample obtained while ensuring non-consumption of food or water in the interim period, when an interviewer-administered questionnaire was completed by the research assistants. Maternal blood pressure, weight, hip and waist circumference were measured using standard calibrated instruments as per guidelines. Diabetes, IGT, and IFG were identified by WHO 2006 criteria.[3] Test reports were made available for the next clinic. If test reports were abnormal, the PI informed each woman over the phone and provided appropriate medical advice and referral. The study participants were made aware of the importance of this research to themselves and to the country’s health services. They were all advised on the importance of their next follow-up visit at 1 year postpartum.

At 1-year postpartum, the mothers again were expected to come to the child welfare clinics for immunization of their babies. The procedures described at 2 months were repeated at 1-year postpartum. Data were recorded at follow-up, with variables such as demographic, socio-economic, family history of diabetes, and pregnancy-related and co-morbid factors for postpartum AGT. International Physical Activity Questionnaire Short Version (IPAQ) was applied to ascertain their activity level. A 3-day diet record was used to obtain information on nutritional intake.

Data analysis

Data analysis was conducted using SPSS 18 Software. χ2 tests with P-values were used to assess the statistical significance of the observed associations. Odds ratios (ORs) with 95% confidence interval (CI) were used to assess the strength of the associations. Next, univariate analysis, followed by multivariate analysis, was carried out to identify predictive factors of postpartum AGT. All variables with P-value <0.15 in the univariate analysis were entered into logistic regression model as directions of the variables could have got changed due to confounders and the variables retained in the final model were identified as predictive factors and strength of association was given by adjusted OR (aOR).

The three-day diet record was analyzed using a computerized food composition database containing Sri Lankan food items and mixed dishes.[4] Mean scores for each nutrient were calculated and compared between women with and without AGT by t-test and P-values.


  Results Top


One hundred and ninety-four pregnant women with GDM were identified in the longitudinal study. Of them, 169 mothers with GDM participated in the follow-up study (response rate: 87.1%) at 2 months postpartum. Of 169 mothers who participated at 2 months, only 59 participated at 1-year postpartum (response rate: 30.4%). [Table 1] describes the study population at 2 months and 1-year postpartum. At 2 months, 27.3% women were above 35 years and this was raised to 39.3% in 1 year. About one-third of women showed maternal history of diabetes at 2 months and half of women at 1 year but paternal history of diabetes was fairly similar at 2 months and 1 year. At 2 months, 43.6% were overweight or obese and this was increased to 53.6% in 1 year.
Table 1: Description of the study population at 2 months and 1-year postpartum

Click here to view


AGT at 2 months and 1-year postpartum among women diagnosed as having GDM

At 2 months postpartum, of the 169 women with GDM, 10.1% (17/169) had DM, 21.3% (36/169) had IGT, and 1.2% (2/169) had IFG. The total rate for AGT was 32.5% (55/169).

At 1-year postpartum, out of the 169 women with GDM, only 59 participated and of them, 18.6% (11/59) had diabetes, 28.8% (17/59) had IGT, and none had IFG. The total rate for AGT was 47.5% (28/59).

Predictors of AGT at 2 months postpartum among women with GDM

Significant predictive factors of AGT at 2 months postpartum identified by the bivariate analysis were shown in [Table 2].
Table 2: Significant findings in the bivariate analysis at 2 months postpartum

Click here to view


Following the multivariate analysis, the 2-h postprandial blood sugar (2-h PPBS) of ≥ 97.5 mg/dL detected at ≤ 12 weeks POA (aOR=2.8; 95% CI= 1.3–6.0), GDM diagnosis at POA ≤16 weeks (aOR=7.7; 95% CI= 1.5–39.7), and 1-h value of OGTT ≥179 mg/dL (aOR=3.1; 95% CI= 1.5–6.4) were identified as predictive factors for AGT at 2 months postpartum.

Predictors of AGT at 1-year postpartum among women with GDM

Significant predictive factors of AGT at 1-year postpartum identified by the bivariate analysis were shown in [Table 3].
Table 3: Significant findings in the bivariate analysis at 1-year postpartum

Click here to view


Following the multivariate analysis, the 2-h PPBS ≥ 97.5 mg/dL at ≤ 12 weeks POA (aOR=8.4; 95% CI = 2.3–30.3) and physical activity (moderate and vigorous activity vs. low activity) (aOR=0.2; 95% CI 0.1–0.8) were identified as predictive factors of AGT at 1-year postpartum.


  Discussion Top


To the best of our knowledge, this is the first report of a community-based long-term follow-up of a cohort of women with GDM in Sri Lanka. It is noteworthy that the affected semi-urban-based women had a cumulative prevalence of 32.5% for AGT at 2 months postpartum with a response rate of 87%. Of them, 10% were frankly diabetic and 21.3% had IGT with 1.2% having IFG. At 1-year postpartum, the cumulative proportion with AGT had increased to 47.5% with the proportions with diabetes rising to 18.6% and IGT to 28.8%, albeit with a lower response rate of 30%.

Our findings are mirrored by other reports from Asia and beyond. Several studies have reported that nearly one-third of women with GDM would have AGT at 6 weeks postpartum which is similar to our findings.[5],[6],[7],[8]

A retrospective study conducted at a center in Omura, Japan, between 2007 and 2011, analyzed data of 169 women with GDM who had undergone OGTT 6–8 weeks postpartum. Women with DM or IGT were categorized as postpartum AGT, and the study revealed 34.3% prevalence of AGT.[5] In another retrospective study, electronic medical files of all women (n = 231) with a recent history of GDM (diagnosed by Carpenter and Coustan criteria) at the University Hospital UZ Leuven in Belgium from 2010 to 2013 were analyzed. The postpartum OGTT was performed at a median of 12 weeks (8–13) with a minimum of 6 weeks. Of the 231 women with GDM, only 169 participated in follow-up OGTT and of them 5.3% (n = 9) had diabetes and 39.1% (n = 66) had glucose intolerance. Among glucose-intolerant women, 21.2% (14/66) had IFG, 66.7% (44/66) had IGT, and 12.1% (8/66) had IFG/IGT combined [American Diabetic Association (ADA) criteria].[6] A longitudinal study was conducted by Jindal et al.[7] among Asian-Indian women aged ≥18 years with GDM (diagnosed by ADA criteria) (n = 62), at a tertiary care center, Delhi, and 2-h 75 gOGTT was carried out at 6 weeks postpartum. One-third (33.8%) of them were identified as having postpartum AGT: 14.5% had IFG, 4.8% had IGT, 8% had both IFG and IGT, and 6.4% had overt type 2 diabetes. Another prospective study (1993–1997) was performed among Korean women with GDM [diagnosed by the National Diabetic Data Group (NDDG) criteria] to determine the prevalence of glucose intolerance between 6 and 8 weeks postpartum by applying fasting 75 gOGTT, and postpartum glucose intolerance was diagnosed by the WHO criteria. Of the total 392 women detected with GDM, 311 women participated. Of the 311 participants, 119 (38.3%) women had persistent glucose intolerance; 47 (15.1%) had diabetes and 72 (23.2%) had IGT.[8]

Several systematic reviews had also shown an increased risk for developing DM among women with GDM when compared with women without GDM.[9],[10]

Recently conducted Indian WINGS MOC program revealed a stepwise rise in the occurrence of DM and prediabetes between 6 weeks and 1 year postpartum, but the reported postpartum glucose intolerance was relatively less than that of the current study. Of the 161 women diagnosed with GDM [International Association of Diabetes and Pregnancy Study Group (IADPSG criteria)] and tested at 6–12 weeks postpartum by OGTT, 1.2% had DM, with the cumulative prevalence of AGT being 15.5%. Screening 26% of the women of the original sample between 6 weeks and 1-year postpartum revealed 11.9% DM, 23.8% isolated IFG, and 2.4% combined IFG/IGT (AGT 38.1%). The multivariate analysis showed that body mass index (BMI) ≥25 kg/m2 was significantly associated with postpartum AGT (OR= 4.47; 95% CI= 1.8–11.2).[11] Different diagnostic criteria for GDM might explain the differences noted with postpartum AGT rates between our study (WHO 1999) and Indian study (IADPSG). It is noteworthy that WHO 1999 criteria were developed considering risk of postpartum diabetes but IADPSG criteria were developed considering short-term maternal and offspring outcome. Though the Indian study identified BMI ≥25 kg/m2 as a predictor of postpartum AGT, our study failed to identify BMI as a significant predictor.

A study conducted by Kim et al.[12] in Korea reported 18.5% occurrence of AGT (IGT: 9.0% and DM: 9.5%) at 6 weeks postpartum among 211 women with GDM. Independent predictors for both postpartum DM and IGT were the glucose area under the curve of the antepartum 100 g OGTT, family history of DM, and the gestational age at diagnosis of GDM. The most important independent predictor for persistent postpartum glucose intolerance was the degree of severity in glucose intolerance during pregnancy. The lower incidence of postpartum AGT reported by Kim et al. may be explained by differing diagnostic criteria for GDM (O’Sullivan and Mahan’s vs. WHO 1999). Although we did not find a significant association with family history of diabetes in the Sri Lankan women, we found a similarly significant association with GDM diagnosis made early in pregnancy.

McElnay and Elnour[13] conducted 75 gOGTT within 6–12 weeks postpartum among all women diagnosed with GDM (n = 165) in a single hospital to identify predictors of postpartum diabetes. Family history of DM (OR=5.51), severe antenatal hyperglycemia (OR= 4.62), gestational age at GDM diagnosis <16 weeks (OR= 3.96), and gravida >5 (OR= 3.23) were the significant predictors. We also identified GDM diagnosis ≤16 weeks and hyperglycemia as predictors but not family history of DM and multiparity. It is noteworthy that we failed to identify a positive family history of DM to be a predictor, unlike several others, which may be explained by the insufficient screening of populations to elucidate a negative family history with certainty.[14],[15],[16]

Early diagnosis of GDM, raised fasting glucose, and use of insulin were identified as risk factors for diabetes in Rayanagoudar et al.[16] in a systematic review and are in keeping with our findings. They also identified multiparity, hypertensive disorders in pregnancy, and preterm delivery as risk factors for future diabetes that were not evident in our study. Increased physical activity level was found to be a significant protective factor for postpartum AGT, in parallel with the previous findings that increased maternal physical activity reduced the incidence of diabetes.[17],[18]

Our follow-up study clearly demonstrates how GDM has an adverse impact on long-term maternal metabolic health that extends well beyond the pregnancy. Identification of predictive factors for postpartum AGT is important to implement pragmatic preventive programmes to delay the progression of postpartum AGT. Several intervention studies have shown that lifestyle intervention among subjects with IGT delays progression to diabetes.[17],[18] Hence, health systems in South Asia could utilize these data to formulate policies and incorporate these aspects to national guideline development in the postpartum screening of women with GDM.

Strengths of the study

This was a community-based study, and detailed characteristics of all the study participants were available.

All the study participants underwent universal screening, and the diagnosis of GDM was confirmed by the gold standard fasting 75 gOGTT, analyzed in a single accredited laboratory.

All pregnant women identified as GDM were included as study population for the follow-up study. Therefore, selection bias was not observed.

Limitation of the study: The present study was carried out in two MOH areas in Gampaha District.

High dropout rate was observed at 1-year postpartum.


  Conclusions and Recommendations Top


One in 10 women with GDM had diabetes and a third had AGT at 2 months postpartum among semi-urban women in Sri Lanka. Despite a substantial dropout rate, an approximate one-fifth had diabetes and one half had AGT at 1-year postpartum. Significant predictors for developing postpartum glucose intolerance are early diagnosis of GDM prior to the currently applied standard timing of screening by the OGTT. We have also determined that first trimester 2-h PPBS exceeding 97.5 mg/dL and blood glucose exceeding 179 mg/dL in the first hour value of the OGTT are predictors for postpartum metabolic derangement, while high maternal physical activity is protective.

We recommend that further study of the feasibility in applying a risk predictor model be studied at the field level in the South Asian settings. We recommend these data to be utilized in formulation of policies and development of national guidelines in the postpartum screening of women with GDM.

Acknowledgements

We thank Medical Officer Maternal and Child Health Gampaha, Staff of Medical Officer of Health Gampaha and Dompe, and all the participants for their valuable support for the success of the study.

Financial support and sponsorship

Medical Research Institute (MRI 48/2012) and Nirogi Maatha project supported by World Diabetic Foundation (WDF 12–683).

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2004;27(Suppl 1):5-10.  Back to cited text no. 1
    
2.
Department of Census and Statistics. Districts final reports-Gampaha. 2014. Available from www.statistics.gov.lk. [Accessed January 6, 2015].  Back to cited text no. 2
    
3.
World Health Organization. Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia: Report of a WHO/IDF consultation. Geneva: 2006.  Back to cited text no. 3
    
4.
Thamilini J, Silva KDRR, Krishnapriya K. Development of food composition database for nutrient composition of mixed dishes for Sri Lanka by recipe calculation. Paper presented at the Wayamba university International Conference, August 29–30, 2014.  Back to cited text no. 4
    
5.
Kugishima Y, Yasuhi I, Yamashita H, Fukuda M, Kuzume A, Sugimi S, et al. Risk factors associated with abnormal glucose tolerance in the early postpartum period among Japanese women with gestational diabetes. Int J Gynaecol Obstet 2015;129:42-5.  Back to cited text no. 5
    
6.
Benhalima K, Leuridan L, Calewaert P, Devlieger R, Verhaeghe J, Mathieu C. Glucose intolerance after a recent history of gestational diabetes. Int J Endocrinol 2014;2014:727652.  Back to cited text no. 6
    
7.
Jindal R, Siddiqui MA, Gupta N, Wangnoo SK. Prevalence of glucose intolerance at 6 weeks postpartum in Indian women with gestational diabetes mellitus. Diabetes Metab Syndr 2015;9:143-6.  Back to cited text no. 7
    
8.
Jang HC, Yim CH, Han KO, Yoon HK, Han IK, Kim MY, et al. Gestational diabetes mellitus in Korea: Prevalence and prediction of glucose intolerance at early postpartum. Diabetes Res Clin Pract 2003;61:117-24.  Back to cited text no. 8
    
9.
Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes mellitus after gestational diabetes: A systematic review and meta-analysis. Lancet 2009;373:1773-9.  Back to cited text no. 9
    
10.
Hopmans TE, van Houten C, Kasius A, Kouznetsova OI, Nguyen LA, Rooijmans SV, et al. [Increased risk of type II diabetes mellitus and cardiovascular disease after gestational diabetes mellitus: A systematic review]. Ned Tijdschr Geneeskd 2015;159:A8043.  Back to cited text no. 10
    
11.
Bhavadharini B, Anjana RM, Mahalakshmi MM, Maheswari K, Kayal A, Unnikrishnan R, et al. Glucose tolerance status of Asian Indian women with gestational diabetes at 6weeks to 1year postpartum (WINGS-7). Diabetes Res Clin Pract 2016;117:22-7.  Back to cited text no. 11
    
12.
Kim YL, Cho YW, Park SW, Lee SK, Ahn IS, Na BW, et al. Antepartum characteristics predicting persistent postpartum glucose intolerance in the patients with gestational diabetes mellitus (GDM). J Korean Diabetes 2000;24:46-59.  Back to cited text no. 12
    
13.
McElnay JC, Elnour AA. Risk factor model for developing postpartum diabetes mellitus in patients with gestational diabetes mellitus (GDM). Int J Med2006. Available from: http://www.priory.com/med.htm. ISSN 1360-0168. Accessed July 1, 2018.  Back to cited text no. 13
    
14.
Alves JM, Stollmeier A, Leite IG, Pilger CG, Detsch JC, Radominski RB, et al. Postpartum reclassification of glycemic status in women with gestational diabetes mellitus and associated risk factors. Rev Bras Ginecol Obstet 2016;38:381-90.  Back to cited text no. 14
    
15.
Krishnaveni GV, Hill JC, Veena SR, Geetha S, Jayakumar MN, Karat CL, et al. Gestational diabetes and the incidence of diabetes in the 5 years following the index pregnancy in South Indian women. Diabetes Res Clin Pract 2007;78:398-404.  Back to cited text no. 15
    
16.
Rayanagoudar G, Hashi AA, Zamora J, Khan KS, Hitman GA, Thangaratinam S. Quantification of the type 2 diabetes risk in women with gestational diabetes: A systematic review and meta-analysis of 95,750 women. Diabetologia 2016;59:1403-11.  Back to cited text no. 16
    
17.
Diabetes Prevention Program Research Group. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002;346:393-403.  Back to cited text no. 17
    
18.
Ramachandran A, Snehalatha C, Mary S, Mukesh B, Bhaskar AD, Vijay V; Indian Diabetes Prevention Programme (IDPP). The Indian Diabetes Prevention programme shows that lifestyle modification and metformin prevent type 2 diabetes in Asian Indian subjects with impaired glucose tolerance (IDPP-1). Diabetologia 2006;49:289-97.  Back to cited text no. 18
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Key Messages:
Introduction
Subjects and Methods
Results
Discussion
Conclusions and ...
References
Article Tables

 Article Access Statistics
    Viewed100    
    Printed2    
    Emailed0    
    PDF Downloaded8    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]