Email updates

Keep up to date with the latest news and content from BMC Public Health and BioMed Central.

Open Access Research article

Childhood meat eating and inflammatory markers: The Guangzhou Biobank Cohort Study

CM Schooling14, CQ Jiang2, TH Lam1*, WS Zhang2, KK Cheng3 and GM Leung1

Author Affiliations

1 School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China

2 Guangzhou Occupational Diseases Prevention and Treatment Centre, Guangzhou Number 12 Hospital, Guangzhou, China

3 Department of Public Health and Epidemiology, University of Birmingham, UK

4 School of Public Health, CUNY, New York, USA

For all author emails, please log on.

BMC Public Health 2011, 11:345  doi:10.1186/1471-2458-11-345

The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1471-2458/11/345


Received:12 October 2010
Accepted:19 May 2011
Published:19 May 2011

© 2011 Schooling et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

We hypothesized that socio-economic development could, via nutritionally driven levels of pubertal sex-steroids, promote a pro-inflammatory state among men but not women in developing countries. We tested this hypothesis, using recalled childhood meat eating as a proxy for childhood nutrition, in southern China.

Methods

We used multivariable linear regression in the Guangzhou Biobank Cohort Study phase 3 (2006-8) to examine the adjusted associations of recalled childhood meat eating, <1/week (n = 5,023), about once per week (n = 3,592) and almost daily (n = 1,252), with white blood cell count and its differentials among older (≥50 years) men (n = 2,498) and women (n = 7,369).

Results

Adjusted for age, childhood socio-economic position, education and smoking, childhood meat eating had sex-specific associations with white blood cell count and lymphocyte count, but not granulocyte count. Men with childhood meat eating almost daily compared to <1/week had higher white blood cell count (0.33 109/L, 95% confidence interval (CI) 0.10 to 0.56) and higher lymphocyte count (0.16 109/L, 95% CI 0.07 to 0.25). Adjustment for obesity slightly attenuated these associations.

Conclusion

If confirmed, this hypothesis implies that economic development and the associated improvements in nutrition at puberty may be less beneficial among men than women; consistent with the widening sex differentials in life expectancy with economic development.

Keywords:
Cardiovascular disease; inflammation; sex; China; developing country; white blood cell count; childhood nutrition

Background

In long term industrialized western populations poor childhood conditions are associated with cardiovascular disease [1], although the underlying biological pathway is unclear. Cardiovascular disease may have an inflammatory component [2,3]. Poor childhood conditions are also usually associated with a pro-inflammatory state [4-9]. It is increasingly clear that the social patterning of cardiovascular disease or its risk factors, both traditional and non-traditional, is not universal but epidemiologic stage specific [9-14]. There is often a more marked and longer lasting reversal of the usual social patterning among men than women [9-11] for reasons which have tended to be interpreted mainly in terms of contemporaneous risk factors that differ by sex [11].

A factor that countered the generally protective effect of social advantage among men at the early stages of economic development would explain the observed patterns. Inter-generationally and nutritionally driven increases in the amount, tempo and intensity of pubertal development with macro-economic improvement provide a potential explanation [10,15], because pubertal sex-steroids may have long-term sex-specific effects on fat patterning [16], some lipids [17,18] and immune responsiveness [19-21], which are detrimental among men but sometimes protective among women [16-22]. There is increasing evidence from populations with a recent history of economic development, that growing up in more affluent conditions is positively associated among men, but not women, with central obesity [10], ischemic heart disease [23-26] and inflammation [9]. However, the positive association with inflammation among men may be due to obesity [9]. In a large sample from the developing country setting of southern China, we examined whether a marker of childhood nutrition, positively associated with cognition [27], but sex-specifically associated with central obesity and some lipids [28], also had sex-specific associations with inflammatory markers.

Methods

Sources of data

The Guangzhou Biobank Cohort Study is a collaboration between the Guangzhou No. 12 Hospital, the Universities of Hong Kong and Birmingham, and has been described in detail [29]. Recruitment of participants draws from "The Guangzhou Health and Happiness Association for the Respectable Elders", a community social and welfare association unofficially aligned with the municipal government where membership is open to anyone aged 50 years or older for a monthly, nominal fee of 4 Yuan (50 US cents). Recruitment for phase 3 took place from September 2006 to January 2008. About 7% of permanent Guangzhou residents aged 50 years and over are members of "The Guangzhou Health and Happiness Association for the Respectable Elders", of whom 11% enrolled for phase 3 recruitment, and were included if they were capable of consenting, ambulatory, and not receiving treatment modalities which if omitted may result in immediate life threatening risk, such as chemotherapy or radiotherapy for cancer, or dialysis for renal failure. Participants underwent a half-day detailed medical interview, including disease history, and physical examination. The Guangzhou Medical Ethics Committee of the Chinese Medical Association approved the study and all participants gave written, informed consent before participation.

The detailed methods of measurement have been reported [29]. In brief, standing height was measured without shoes to the nearest 0.1 centimeter. Sitting height was measured with the participants sitting on a standard stool; leg length was calculated as the difference between height and sitting height. Weight was measured in light clothing to the nearest 0.1 kilogram. Hip circumference was measured at the greatest circumference round the buttocks below the iliac crest. Waist circumference was measured horizontally around the smallest circumference between the ribs and iliac crest, or at the level of the navel for obese participants. Quantitative haematological analysis was performed using a SYSMEX KX-21 haematology analyzer, from which white blood cell counts, lymphocyte and granulocyte counts were available.

Exposure assessment

In developing countries long running cohort studies that could provide life long measures are not available, potentially precluding valuable evidence from such settings in the foreseeable future. Instead, in this study childhood nutrition was assessed from a simple question about a notable aspect of childhood nutrition, i.e., meat eating, because this cohort grew up in era and setting where meat consumption was relatively low, highly valued and not constrained by religious beliefs. Recalled childhood meat eating was ascertained by asking participants whether they ate meat as a child with answers in Chinese which translate as "never", "about once a year", "about once a month", "about once a week" or "almost daily". Few (<1%) reported "never" eating meat in childhood, and both "about once a year" and "about once a month" represent occasional meat eating, so we created a 3 point scale: "</1 week", "about once a week" and "almost daily". We cannot validate recalled childhood meat eating against actual childhood intake or maternal recall given the age of our participants. However, we have previously shown that recalled childhood meat eating does have the expected negative association with age of menarche and positive associations with height and childhood socio-economic position [27,28]. Moreover, in other contexts, recalled dietary intake from adolescence has been shown to have some reproducibility and validity [30].

Outcome measure

White blood cell count was considered, as in other studies, as a marker of a pro-inflammatory state [4], and less well functioning immune system. As we do not have a detailed breakdown of different white blood cell types, such as macrophages, we also considered granulocyte and lymphocyte counts as outcomes because these immune cell sub-populations largely relate to innate and adaptive immunity respectively. They have previously been used as markers of inflammation [31,32]. Sex-steroids may also have differential effects on immune cell sub-populations [20,33].

Statistical analysis

Multivariable regression was used to assess the adjusted association of recalled childhood meat eating with total white blood cell count and its differentials. We examined whether the outcomes had different associations with recalled childhood meat eating by sex or age from the heterogeneity across strata and model fit assessed from the Akaike Information Criterion for models with and without the relevant interaction term. We also included in the model all other interactions of sex or age, as appropriate, with other confounders that contributed to model fit.

Potential confounders considered were age (5 year age-groups), sex (if appropriate), socio economic position at three life stages (based on parental possession of three relevant items (watch, bicycle and sewing machine) in childhood [10], education and longest held occupation), measures of early life living conditions (leg length and seated height (both continuous)) and lifestyle habits (smoking, alcohol use and physical activity). These were selected for inclusion in the final model on a change in estimate criteria for white blood cell count, on which basis longest held occupation, leg length, seated height, alcohol use and physical activity were dropped. The final model (model 1) included age, childhood socio-economic position (from parental possessions), education and smoking status. Model 2 additionally adjusted for body mass index and waist-hip ratio.

Results

Of the 10,088 participants, 9,867 (99%) had complete data on inflammatory markers, as well as age, body mass index and waist-hip ratio and were included. There were more women (7,369) than men (2,498), and the women were younger (mean age 59.2 (standard deviation 7.6)) than the men (mean age 63.2 (standard deviation 7.6)). Age ranged from 50 to 96 years, but few participants were older than 75 years.

Table 1 shows that recalled childhood meat eating was positively associated with height and socio-economic position. Table 2 shows that the associations of childhood meat eating with total white blood cell count or its differentials did not differ with age, but did differ by sex for total white blood cell count and lymphocyte count.

Table 1. Participant Characteristics by Recalled Childhood Meat Eating in 9,867 Older Chinese Men (2,498) and Women (7,369) in Phase 3 Of The Guangzhou Biobank Cohort Study (2006-8).

Table 2. Akaike Information Criterion values‡ for Models with and without Interactions by Sex and Age in 9,867 Older Chinese Men (2,498) and Women (7,369) in Phase 3 of the Guangzhou Biobank Cohort Study (2006-8).

Table 3 shows that among men, childhood meat eating was positively associated with total white blood cell count and lymphocyte count in model 1. The associations were attenuated slightly by additional adjustment for body mass index and waist-hip ratio in model 2. In contrast, among women childhood meat eating was not clearly associated with total white blood cell count, lymphocyte count or granulocyte count.

Table 3. Adjusted Associations of Recalled Childhood Meat Eating with Inflammatory Markers in 9,867 Older Chinese Men (2,498) and Women (7,369) in Phase 3 of the Guangzhou Biobank Cohort Study (2006-8).

Discussion

In a large study from an understudied non-western developing population, we found that a marker of early life conditions, i.e., recalled childhood meat eating, had sex-specific associations with some inflammatory markers. More frequent childhood meat eating, adjusted for childhood socio-economic position, was positively associated with white blood cell count and lymphocyte count among men but not women.

Despite using a large study, there are caveats. First, we used self-report of childhood meat eating as a proxy for childhood nutrition, which is undoubtedly subject to measurement error. Random misclassification most likely makes the results conservative, for which our large sample size compensates. Recall bias is also possible, although the participants were unlikely to have been aware of their inflammatory status, nor is it obvious why such status should affect their recall of childhood events. As would be expected, recalled childhood meat eating was strongly positively associated with childhood socio-economic position, education and height. Second, our participants were not a randomly selected, population representative sample; however that should not affect internal associations, unless we missed people with specific combinations of childhood meat eating and inflammatory markers. Third, survivor bias is possible, in which case we would have expected differences in associations by age, of which there was no evidence. Fourth, a single measurement of total white blood cell count and its differentials might not reflect long-term immune function. However, white blood cell count is used as a marker of immune status in clinical settings. Within the normal range, white blood cell count is associated with cardiovascular mortality [3]. Fifth, white blood cell count or its differentials could be affected by acute infection or trauma, however people in such a condition would have been unlikely to participate in our study. Finally, we did not adjust for potential confounding by diet, because of the difficulty of obtaining reliable and accurate dietary data in large-scale studies of free-living participants, particularly amongst the Chinese who share several dishes during a meal making individual intake difficult to gauge.

Childhood conditions, in long-term developed countries, are usually consistently negatively associated with markers of a pro-inflammatory state [4-8]. However, a study from a similarly middle income country [9] also found that childhood living conditions had sex-specific associations with an inflammatory marker that were less favourable among men. In the United States, early life socio-economic position has been observed to have a negative association with infectious pathogens among women but not men [34]. Our findings, of childhood meat eating positively associated with some potential markers of a pro-inflammatory state among men but mot women, has some commonality with these later two studies [9,34]. Our study went further by specifically examining a measure of childhood nutrition, recalled childhood meat eating, adjusted for childhood socio-economic position.

There are several possible explanations for our observations. Childhood meat eating could be a marker of a generally unhealthy childhood diet, including fast food, trans fats and a low fruit and vegetable intake, with corresponding consequences. However, our participants spent their lives in China. Their childhood in China spanned the mid-20th century when living standards were low, and diet was very limited with no fast food and little trans fat [35,36]. More frequent meat eating in our population almost certainly represents a less limited diet, which is consistent with the taller height and earlier age of menarche amongst those with more frequent recalled childhood meat eating [27,28].

Alternatively, we could place these observations within a theoretical hypothesis driven framework [15,37]. Specifically, pubertal sex-steroids are nutritionally driven [38-40], either by meat eating or some other aspect of a less limited diet, with potentially long-term effects. Testosterone suppresses immune responsiveness, while estrogen may promote it [19-21]. Higher sex-steroids might be expected to result in a more pro-inflammatory state among men but not women. Whether a greater impact would be expected on lymphocytes than granulocytes remains to be determined, as do any other possible consequences for immunity or auto-immunity. As such, this hypothesis potentially provides an explanation for several previous observations [9,34] as well as ours; nevertheless it remains speculative because pubertal testosterone is not available in this study. Moreover, our study cannot establish causality; merely provide evidence consistent with a hypothesis.

Conclusions

Protective effects of better childhood conditions may be less evident among men than women at the early stages of economic development, perhaps due to the biological consequences of up-regulation of the gonadotropic axis. Fully delineating the intergenerational and life long biological effects of changes in nutrition with economic development could be key to developing effective interventions and ensuring that men benefit as much as women from economic development.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

THL, CQJ and KKC initiated and oversee the Guangzhou Biobank Cohort Study, WSZ and GML assisted in the planning and co-ordination of the study. CMS designed this analysis. GML contributed to the interpretation of this analysis. CMS drafted the manuscript. All authors critically reviewed the manuscript for intellectual content. All authors read and approved the final manuscript.

Acknowledgements

The Guangzhou Biobank Cohort Study investigators include: Guangzhou No. 12 Hospital: WS Zhang, M Cao, T Zhu, B Liu, CQ Jiang (Co-PI); The University of Hong Kong: CM Schooling, SM McGhee, GM Leung, R Fielding, TH Lam (Co-PI); The University of Birmingham: P Adab, GN Thomas, KK Cheng (Co-PI). This work was supported by the University of Hong Kong Foundation for Development and Research, Hong Kong; The University of Hong Kong University Research Committee Strategic Research Theme Public Health, Hong Kong; Guangzhou Public Health Bureau, and Guangzhou Science and Technology Committee, Guangzhou, China; and The University of Birmingham, Birmingham, UK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  1. Galobardes B, Smith GD, Lynch JW: Systematic review of the influence of childhood socioeconomic circumstances on risk for cardiovascular disease in adulthood.

    Ann Epidemiol 2006, 16:91-104. PubMed Abstract | Publisher Full Text OpenURL

  2. Ross R: Atherosclerosis--an inflammatory disease.

    N Engl J Med 1999, 340:115-126. PubMed Abstract | Publisher Full Text OpenURL

  3. Jee SH, Park JY, Kim HS, Lee TY, Samet JM: White blood cell count and risk for all-cause, cardiovascular, and cancer mortality in a cohort of Koreans.

    Am J Epidemiol 2005, 162:1062-1069. PubMed Abstract | Publisher Full Text OpenURL

  4. Pollitt RA, Kaufman JS, Rose KM, ez-Roux AV, Zeng D, Heiss G: Early-life and adult socioeconomic status and inflammatory risk markers in adulthood.

    Eur J Epidemiol 2007, 22:55-66. PubMed Abstract | Publisher Full Text OpenURL

  5. Jousilahti P, Salomaa V, Rasi V, Vahtera E, Palosuo T: Association of markers of systemic inflammation, C reactive protein, serum amyloid A, and fibrinogen, with socioeconomic status.

    J Epidemiol Community Health 2003, 57:730-733. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  6. Tabassum F, Kumari M, Rumley A, Lowe G, Power C, Strachan DP: Effects of socioeconomic position on inflammatory and hemostatic markers: a life-course analysis in the 1958 British birth cohort.

    Am J Epidemiol 2008, 167:1332-1341. PubMed Abstract | Publisher Full Text OpenURL

  7. Gimeno D, Ferrie JE, Elovainio M, Pulkki-Raback L, Keltikangas-Jarvinen L, Eklund C, Hurme M, Lehtimaki T, Marniemi J, Viikari JS, Raitakari OT, Kivimaki M: When do social inequalities in C-reactive protein start? A life course perspective from conception to adulthood in the Cardiovascular Risk in Young Finns Study.

    Int J Epidemiol 2008, 37:290-298. PubMed Abstract | Publisher Full Text OpenURL

  8. Loucks EB, Pilote L, Lynch JW, Richard H, Almedia N, Emelia JB: Life Course Socioeconomic Position Is Associated With Inflammatory Markers: The Framingham Offspring Study.

    Soc Sci Med 2010, 71:187-95. PubMed Abstract | Publisher Full Text OpenURL

  9. Nazmi A, Oliveira IO, Horta BL, Gigante DP, Victora CG: Lifecourse socioeconomic trajectories and C-reactive protein levels in young adults: findings from a Brazilian birth cohort.

    Soc Sci Med 2010, 70:1229-1236. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  10. Schooling CM, Jiang CQ, Lam TH, Zhang W, Cheng KK, Leung GM: Life-Course Origins of Social Inequalities in Metabolic risk in the Population of a Developing Country.

    Am J Epidemiol 2008, 167:419-428. PubMed Abstract | Publisher Full Text OpenURL

  11. McLaren L: Socioeconomic status and obesity.

    Epidemiol Rev 2007, 29:29-48. PubMed Abstract | Publisher Full Text OpenURL

  12. Colhoun HM, Hemingway H, Poulter NR: Socio-economic status and blood pressure: an overview analysis.

    J Hum Hypertens 1998, 12:91-110. PubMed Abstract | Publisher Full Text OpenURL

  13. Ezeamama AE, Viali S, Tuitele J, McGarvey ST: The influence of socioeconomic factors on cardiovascular disease risk factors in the context of economic development in the Samoan archipelago.

    Soc Sci Med 2006, 63:2533-2545. PubMed Abstract | Publisher Full Text OpenURL

  14. Kim MH, Kim MK, Choi BY, Shin YJ: Educational disparities in the metabolic syndrome in a rapidly changing society--the case of South Korea.

    Int J Epidemiol 2005, 34:1266-1273. PubMed Abstract | Publisher Full Text OpenURL

  15. Schooling CM, Leung GM: A socio-biological explanation for social disparities in non-communicable chronic diseases - the product of history?

    J Epidemiol Community Health 2010, 64:941-9. PubMed Abstract | Publisher Full Text OpenURL

  16. Roemmich JN, Rogol AD: Hormonal changes during puberty and their relationship to fat distribution.

    Am J Human Biol 1999, 11:209-224. Publisher Full Text OpenURL

  17. Berenson GS, Srinivasan SR, Cresanta JL, Foster TA, Webber LS: Dynamic changes of serum lipoproteins in children during adolescence and sexual maturation.

    Am J Epidemiol 1981, 113:157-170. PubMed Abstract OpenURL

  18. Kirkland RT, Keenan BS, Probstfield JL, Patsch W, Lin TL, Clayton GW, Insull W Jr: Decrease in plasma high-density lipoprotein cholesterol levels at puberty in boys with delayed adolescence. Correlation with plasma testosterone levels.

    JAMA 1987, 257:502-507. PubMed Abstract | Publisher Full Text OpenURL

  19. Grossman CJ: Interactions between the gonadal steroids and the immune system.

    Science 1985, 227:257-261. PubMed Abstract | Publisher Full Text OpenURL

  20. Tanriverdi F, Silveira LF, MacColl GS, Bouloux PM: The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity.

    J Endocrinol 2003, 176:293-304. PubMed Abstract | Publisher Full Text OpenURL

  21. Shames RS: Gender differences in the development and function of the immune system.

    J Adolesc Health 2002, 30:59-70. PubMed Abstract | Publisher Full Text OpenURL

  22. Orchard TJ, Rodgers M, Hedley AJ, Mitchell JR: Changes in blood lipids and blood pressure during adolescence.

    Br Med J 1980, 280:1563-1567. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  23. Yano K, Blackwelder WC, Kagan A, Rhoads GG, Cohen JB, Marmot MG: Childhood cultural experience and the incidence of coronary heart disease in Hawaii Japanese men.

    Am J Epidemiol 1979, 109:440-450. PubMed Abstract OpenURL

  24. Marmot MG, Syme SL: Acculturation and coronary heart disease in Japanese-Americans.

    Am J Epidemiol 1976, 104:225-247. PubMed Abstract OpenURL

  25. Schooling CM, Lam TH, Ho SY, Mak KH, Leung GM: Does economic development contribute to sex differences in ischaemic heart disease mortality? Hong Kong as a natural experiment using a case-control study.

    BMC Public Health 2008., 8 OpenURL

  26. Chung RY, Schooling CM, Cowling BJ, Leung GM: How does socioeconomic development affect risk of mortality? An age-period-cohort analysis from a recently transitioned population in China.

    Am J Epidemiol 2010, 171:345-356. PubMed Abstract | Publisher Full Text OpenURL

  27. Heys M, Jiang C, Schooling CM, Zhang W, Cheng KK, Lam TH, Leung GM: Is childhood meat eating associated with better later adulthood cognition in a developing population?

    Eur J Epidemiol 2010, 25:507-516. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  28. Heys M, Jiang C, Cheng KK, Zhang W, Lam TH, Leung GM, Schooling CM: Does childhood meat eating contribute to sex differences in risk factors for ischaemic heart disease in a developing population?

    J Epidemiol Community Health 2010. OpenURL

  29. Jiang C, Thomas GN, Lam TH, Schooling CM, Zhang W, Lao X, Adab P, Liu B, Leung GM, Cheng KK: Cohort profile: The Guangzhou Biobank Cohort Study, a Guangzhou-Hong Kong-Birmingham collaboration.

    Int J Epidemiol 2006, 35:844-852. PubMed Abstract | Publisher Full Text OpenURL

  30. Maruti SS, Feskanich D, Colditz GA, Frazier AL, Sampson LA, Michels KB, Hunter DJ, Spiegelman D, Willett WC: Adult recall of adolescent diet: reproducibility and comparison with maternal reporting.

    Am J Epidemiol 2005, 161:89-97. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  31. Taylor B, Tofler G, Morel-Kopp MC, Carey H, Carter T, Elliott M, Dailey C, Villata L, Ward C, Woodward M, Schenck K: The effect of initial treatment of periodontitis on systemic markers of inflammation and cardiovascular risk: a randomized controlled trial.

    Eur J Oral Sci 2010, 118:350-356. PubMed Abstract | Publisher Full Text OpenURL

  32. Dawczynski C, Schubert R, Hein G, Muller A, Eidner T, Vogelsang H, Basu S, Jahreis G: Long-term moderate intervention with n-3 long-chain PUFA-supplemented dairy products: effects on pathophysiological biomarkers in patients with rheumatoid arthritis.

    Br J Nutr 2009, 101:1517-1526. PubMed Abstract | Publisher Full Text OpenURL

  33. McMurray RW, Suwannaroj S, Ndebele K, Jenkins JK: Differential effects of sex steroids on T and B cells: modulation of cell cycle phase distribution, apoptosis and bcl-2 protein levels.

    Pathobiology 2001, 69:44-58. PubMed Abstract | Publisher Full Text OpenURL

  34. Dowd JB, Aiello AE: Socioeconomic differentials in immune response.

    Epidemiology 2009, 20:902-908. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  35. Du S, Lu B, Zhai F, Popkin BM: A new stage of the nutrition transition in China.

    Public Health Nutr 2002, 5:169-174. PubMed Abstract | Publisher Full Text OpenURL

  36. Geissler C: China: the soyabean-pork dilemma.

    Proc Nutr Soc 1999, 58:345-353. PubMed Abstract | Publisher Full Text OpenURL

  37. Schooling CM, Hui LL, Ho LM, Lam TH, Leung GM: Cohort Profile: 'Children of 1997': a Hong Kong Chinese birth cohort.

    Int J Epidemiol 2011. OpenURL

  38. Dorgan JF, Hunsberger SA, McMahon RP, Kwiterovich PO Jr, Lauer RM, Van Horn L, Lasser NL, Stevens VJ, Friedman LA, Yanovski JA, Greenhut SF, Chandler DW, Franklin FA, Barton BA, Buckman DW, Snetselaar LG, Patterson BH, Schatzkin A, Taylor PR: Diet and sex hormones in girls: findings from a randomized controlled clinical trial.

    J Natl Cancer Inst 2003, 95:132-141. PubMed Abstract | Publisher Full Text OpenURL

  39. Dorgan JF, McMahon RP, Friedman LA, Van Horn L, Snetselaar LG, Kwiterovich PO Jr, Lauer RM, Lasser NL, Stevens VJ, Robson A, Cooper SF, Chandler DW, Franklin FA, Barton BA, Patterson BH, Taylor PR, Schatzkin A: Diet and sex hormones in boys: findings from the dietary intervention study in children.

    J Clin Endocrinol Metab 2006, 91:3992-3996. PubMed Abstract | Publisher Full Text OpenURL

  40. Slob AK, Vreeburg JT, Van der Werff ten Bosch JJ: Body growth, puberty and undernutrition in the male guinea-pig.

    Br J Nutr 1979, 41:231-237. PubMed Abstract | Publisher Full Text OpenURL

Pre-publication history

The pre-publication history for this paper can be accessed here:

http://www.biomedcentral.com/1471-2458/11/345/prepub