IJE Advance Access originally published online on June 17, 2005
International Journal of Epidemiology 2005 34(4):742-749; doi:10.1093/ije/dyi124
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Cohort Profiles |
Cohort Profile: The Boyd Orr cohort—an historical cohort study based on the 65 year follow-up of the Carnegie Survey of Diet and Health (1937–39)
1 Department of Social Medicine, University of Bristol, Canynge Hall, Whiteladies Road, Bristol BS8 2PR, UK
2 Iona, Cannon Fields, Hathersage, Sheffield, UK
* Corresponding author. E-mail: richard.martin{at}bristol.ac.uk
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How did the study come about? |
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Top
How did the study...
What does it cover,...The Boyd Orr cohort is an historical cohort study based on the long term follow-up of 4999 children who were surveyed in the Carnegie United Kingdom Trust's study of Family Diet and Health in Pre-War Britain (1937–39).1 With funding from the British Heart Foundation, the cohort was established in 1988 by Professors George Davey Smith and Stephen Frankel who retrieved the original research records of the pre-war survey from the Rowett Research Institute, Aberdeen, Scotland.
The Carnegie Survey was the brainchild of Sir (later Lord) John Boyd Orr, director of the Rowett Research Institute from 1914 to 1945. The original research was funded by a grant of £15 000 from the trustees of the Carnegie United Kingdom Trust. Key members of the original survey team were David Lubbock (research administrator), Isabella Leitch (study design), John Pemberton and Angus Thomson (medical examinations), and Isabel Dods (supervision of the diet survey team).1 The historical background to the study has previously been described in detail.2 Its aim was to investigate ‘the connection between economic factors and physical welfare’.2
Subsequent work on the cohort has been funded by grants from the Medical Research Council (UK), the World Cancer Research Fund, Research into Ageing, UK Survivors, the Economic and Social Research Council, the Wellcome Trust, and the British Heart Foundation. The core team consists of Professors George Davey Smith, Stephen Frankel and David Gunnell, and Dr Richard Martin.
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What does it cover, and how has this changed? |
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The aim of the original cross sectional survey upon which the Boyd Orr cohort is based was to study the diet of a large number of families from around England and Scotland and relate the quality of the measured diet both to the family income and to the health of the children living in the households. In addition, the effects of subsequently providing nutritional supplements to some of the children on their health and growth were studied. Around 500 children aged 2–14 received supplements and a similar number of non-supplemented children acted as controls.1,3
The initial aim of establishing the Boyd Orr cohort was to investigate the long-term impact of environmental factors in early life on adult coronary heart disease mortality. Whilst the possible impact of poor childhood nutrition on adult health had been the subject of research and policy interest for many years,4–7 specific interest in the influence of early life exposures on adult cardiovascular disease was re-awakened by a series of studies that began in the 1980s by Professor David Barker and colleagues at the University of Southampton.8,9 These studies demonstrated inverse associations of markers of foetal growth with cardiovascular risk factors and mortality. An important strength of the material collected in the Carnegie Survey/Boyd Orr cohort was the availability of detailed measures of childhood diet; most of the research in this field uses proxy measures of pre-natal and childhood nutrition (e.g. birth weight, height).10
Studies on the cohort to date have investigated a range of disease endpoints, particularly coronary heart disease and cancer in relation to infant and childhood diet, the socio-economic conditions experienced by the children, and markers of childhood nutritional status (body mass index, leg length, and height).
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Who is in the sample? |
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The reconstruction of the original survey material, tracing of survey members, and the representativeness of those who were traced and flagged have been described in detail previously.11 A total of 4999 children from 1343 families living in 16 urban and rural districts in Britain were surveyed during 1937–39. Districts were chosen to be generally representative of urban and rural areas and of particular industrial and social conditions (Figure 1). Only families with children were selected for the survey. In each district the aim was to survey all the families whose children were attending certain schools, chosen on the advice of the Medical Officer of Health. Families were usually identified from the more deprived localities through contacts made by local health workers, and two-thirds consented to participation. As a consequence of the method of identifying the participants, middle and upper class families were under-represented (Table 1). A total of 3762 of the 4999 children aged 0–19 years from all but two of the districts (Edinburgh and Kintore) also underwent detailed physical examination.
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The names, ages (in months and years), and addresses at the time of the survey of the children in the study obtained from the archived material have been used to trace those individuals who took part in the original survey using the National Health Service Central Register (NHSCR) at Southport and its equivalent in Edinburgh. Of the 4999 original participants, 4397 (88%) have been traced and flagged.
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How often have they been followed up? |
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There have been three main phases of follow-up so far. Firstly, for those who have been successfully identified, the NHSCR notifies the Boyd Orr study team of the occurrence of death, cancer registration, emigration, and area of current residence. This follow-up is ongoing; deaths, cancer registrations, and emigrations have been entered up to the end of February 2005 and the database is updated with these event details approximately every 2 years.
Secondly, between 1997 and 1998 a follow-up questionnaire survey re-established contact with subjects from the original sample of families who were traced, alive, and living in Britain (n = 3182). These subjects were sent a detailed health and lifestyle questionnaire and 1648 (52%) responded (Table 2).12
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Thirdly, follow-up to obtain physiological measurements and blood assays was undertaken in 2002–03 (Table 2), based on a target population of all the 1295 surviving subjects who in 1997–98 had consented to further follow-up. There were two components to the 2002–03 follow-up. Firstly, detailed clinical examinations were undertaken on those who lived in or around four of the original survey centres—London, Wisbech, Aberdeen, and Dundee. Measurements included anthropometry, biophysical cardiovascular risk factors, and ultrasound scanning of their carotid and femoral arteries. Participants also provided a blood specimen and completed a detailed health, lifestyle, and dietary questionnaire. Secondly, for those surviving study members who did not attend the clinic or did not live in the vicinity of the clinics, blood samples and basic clinical measurements were taken by their general practitioner, and posted back to the research team in Bristol in approved Post Office packaging along with a health, lifestyle, and dietary questionnaire (‘bloods-by-post’ follow-up). A separate follow-up of a sub-sample of around 300 cohort members is described in an accompanying paper.13
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What has been measured? |
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Baseline data from the original survey
In the original Carnegie survey, dietary, social, and economic data were recorded in a specially designed Dietary Study booklet and the physical examination findings were recorded on a medical examination sheet. Repeat dietary data were collected on over 300 families. The data items are summarized in Table 3.
A strength of the cohort is the detailed exposure data in childhood, in particular the family dietary data and the measures of growth that were undertaken on the participants when they were children. Their measurement is thus described in more detail. Dietary data in the original Carnegie survey were obtained using a 7-day household inventory method. A weighed inventory of all foods in the household was recorded in a diary at the beginning of the survey period. A weighed record of all subsequent foods brought into the home was made, and a second inventory was carried out at the end of the survey week. Data from the diaries were transcribed onto separate summary sheets for each household. To include nutrients not measured in the original study and to utilize the advances in analytical techniques, the household diet diaries have been re-coded using DIDO (diet in data out) and re-analysed using a combination of 1930s and modern day food tables to obtain the childhood nutrient intake.
The techniques used to measure standing height, leg length, and body weight have been described previously.1 Standing height was measured to the nearest millimetre with a portable measuring stand. Leg length was measured with a steel tape measure and recorded as the distance from the ground to the summit of the iliac crest (cristal height). Trunk-length was calculated by subtracting leg length from the overall height. Weight was measured using a W&T Avery standard model calibrated level balance (now known as Avery Berkel, Smethick, UK) and recorded to the nearest ounce (28.4 g). Internally age- and sex-standardized Z-scores for height, leg length, trunk length, and body mass index have previously been computed using polynomial regression models based on the complete dataset.
Measured birth weights in pounds and ounces have recently been successfully retrieved for 10% (500) of the cohort members living in 7 of the 16 survey centres.14 Data were collected through searches of original maternity records held in hospitals, and Health and Local Authority archives mainly in Aberdeen, Dundee, Edinburgh, and London.
Questionnaire follow-up 1997–98
A self completed postal questionnaire was administered between 1997 and 1998. The main areas covered in this are summarized in Table 3. The questionnaire included a 113-item modified version of the food frequency questionnaire (FFQ) developed for use in the Cambridge arm of the European Prospective study Into Cancer and nutrition (EPIC). Other questions included the personal medical history, Rose angina questionnaire, lifestyle, anthropometry (adult height, leg length, and weight), family history of illness (cause of death), occupation and socioeconomic indices, and current medication (see Table 3). Social class in adulthood is based on the subject's (for men and unmarried women) or spouse's (women) main employment, classified using the 1966 Classification of Occupations.
Clinic and bloods by post follow-up 2002–03
Clinic measurements were made by a specially trained team of one nurse and one doctor on a selected group of survivors during 2002–03. Repeat measurements were obtained on a sub-sample of 39 participants providing measures of reliability. Measurements made on the clinic sample are summarized in Table 3.
The following measurements were also made on the ‘bloods-by-post’ sample: GP measured height, weight, and blood pressure; non-fasting blood samples for HbA1c, insulin-like growth factors (IGF)-I and II; IGF binding proteins (BP) 2 and 3, frozen whole blood for DNA extraction, sera and plasma.
An identical questionnaire was self-completed by both the clinic and bloods by post participants, giving details of major diseases, chest pain, current medications, smoking and alcohol intake, diet, exercise, family history of major diseases, 12-item GHQ (mental health) scores, indices of pain and disability, and memory questions.
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What is attrition like? |
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The numbers of participants involved at each of these stages of follow-up is summarized in Table 2. Of the 4999 survey participants a total of 4379 (88%) subjects were traced, and were alive and resident in Britain as on January 1, 1948, the year the NHS was established (Figure 2). The trace rate has increased slightly since the earlier publications as a result of further searches of archived records, contacts with surviving study members, and additional notifications from the NHSCR. A small number of previously traced subjects (n = 121) are not currently registered with a Health Authority doctor and their status is not known (though this may be re-established, for example, on receipt of a death certificate or cancer registration).
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These subjects are not currently on the NHS Central Register as registered with a Health Authority doctor. This happens, for example, if they have been removed from a doctor's list by the Health Authority and their current whereabouts or status is unknown. These subjects are censored on the date they were classified as not currently registered with a Health Authority doctor on the Central RegisterBetween 1997 and 1998 all the 3182 surviving members traced at the NHSCR were sent health and lifestyle questionnaires. Of the 1648 (52%) responses, 1378 (84%) subjects consented to further follow-up. The characteristics of questionnaire responders compared with non-responders have previously been documented. They were more likely to come from more affluent childhood social backgrounds and to have been taller as children.
In February 2002, 1295 (94%) of the 1378 subjects who consented to further follow-up were known to be still alive and contactable. These subjects were contacted to collect a blood sample and to complete a diet and health questionnaire either by clinic or ‘bloods-by-post’ follow-up. A total of 799 (62%) responded to the questionnaire and 728 (56%) provided a blood sample. DNA extraction on these blood samples is complete (Professor Ian Day) (see below for details). A total of 405 (55%) out of 732 subjects living near clinics in Bristol, London, Wisbech, Aberdeen, and Dundee underwent a detailed clinical examination and 339 (46%) returned for an arterial ultrasound scan.
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DNA bank (n = 728) |
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DNA was extracted from 4 ml K-EDTA venous blood and quantitated by the picoGreen assay.15,16 Long-term stock DNA aliquots were laid down, and working 96-well plates of DNA dilutions to 10 ng/ml were prepared. These dilutions are suitable for direct usage, for preparation of long PCR sub-banks of specific gene regions, and for genomewide pre-amplifications to conserve stock DNA.17–19
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What has it found? Key findings and key publications |
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Diet in childhood, cancer, and cardiovascular disease risk
A unique feature of the Boyd Orr cohort is the detailed record of family diet in childhood on all cohort members. Analysis of these records has shown, for the first time in humans, that high levels of energy intake are associated with increased cancer risk in later life.20 Furthermore, children whose family diets were rich in fruits have a reduced cancer risk.21 There are no strong associations of family diet with adult cardiovascular disease.22 The main limitation of the findings in relation to diet is that family diet, rather than individual diet, was measured. Whilst the household diet of family members in the 1930s was likely to be more similar than today, the aggregate family diet measures are not ideal for studying diet–disease associations.
Leg length
Another key group of findings relate to the anthropometric measures recorded on study members. Leg length has been found to be a sensitive indicator of pre-pubertal growth patterns23 and the component of stature that underlies the beneficial effects of breast feeding24 and diet supplements3 on childhood growth. Furthermore, studies of the Boyd Orr cohort have shown that not only is leg length the component of stature most strongly associated with adult coronary heart disease mortality and cancer25,26 but also is no more strongly related to birth weight than the trunk length.27 This suggests that associations of childhood growth with adult chronic diseases may be independent of the association of foetal growth with such diseases. The leg length of the girls in the study who later became mothers was associated with their own children's birth weights,28 suggesting that early nutrition and growth may have effects on health that span generations.
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Breastfeeding |
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A series of studies examining the relationship between infant nutrition, growth, and health in adulthood is underway. Breastfeeding was associated with being taller in childhood and adulthood; the component of height associated with breastfeeding was leg length but not trunk length.24 These findings suggest that breastfeeding may be a biologically relevant exposure underlying previous findings that taller people (in particular those with longer legs) have less heart disease. We have found little evidence, however, that breastfeeding was associated with all-cause, cardiovascular, or ischaemic heart disease mortality, compared with bottle-feeding.29 Nevertheless, based on analyses of the clinic follow-up study, we showed that breastfeeding was associated with reductions in common carotid intima media thickness (IMT), bifurcation IMT, and carotid and femoral plaques, compared with bottle-feeding.30
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What are the main strengths and weaknesses? |
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The Carnegie Survey provides a uniquely detailed record of the diet and health of families living in pre-war Britain. For its time (the 1930s) it was a landmark study using the best techniques then available. Whilst the diet data are not ideal by today's standards (for instance no biomarker data were collected and the records are based on households rather than individuals), we are aware of no other cohorts of this age that have such data. The repeat diet data collected on over 300 families allows us to assess the possible impact of measurement error of diet–disease associations.
Whilst there are clear limitations with using household diet data as a proxy for individual intake, family diet in the 1930s is likely to be a considerably better proxy for individual diet than in the 1990s. Few of the types of food eaten by the Boyd Orr families are specifically aimed at children. The majority of the Boyd Orr families came from poor backgrounds and research suggests that the poorer a family is the more similar is the diet of individuals within that family.31
The Carnegie Survey took place in the 1930s, before the importance of random sampling and assessment of non-response bias was widely recognized. The 16 survey centres were selected so as to give a mixture of rural and urban areas. Many of the districts surveyed in Scotland were chosen because of their proximity to the Rowett Research Institute. Crude information on response rates and sampling has been obtained from interviews with former researchers involved with the survey. Furthermore, the diet supplementation study was non-randomized,3 so it is possible that differences between supplemented and control children are due to baseline differences in the intervention and control groups. Whilst it is possible to control for measured baseline differences between the two groups, residual confounding remains a possibility.
We have relatively limited birth weight and ante-natal data on study subjects. This is because the parents of most study subjects had died before contact was re-established in the 1990s and relatively few maternity/birth records have survived since the 1920s/30s.14
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Can I get hold of the data? Where can I find out more? |
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The Boyd Orr cohort offers a unique opportunity to link detailed measures of diet, health, and social circumstances in childhood with a range of outcomes in adulthood. The study includes an intensively phenotyped sub-sample of 728 participants who have their DNA extracted and available for future genetic studies. Proposals for collaboration are welcome, and enquiries or requests for further information should be made to Richard Martin. Further information about the study, including questionnaires, data collection documents and a bibliography, are available on the website http://www.epi.bris.ac.uk/boydorr/.
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A complete list of publications |
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Leitch I. Growth and Health. Br J Nutr 5:142–51, 1951.[CrossRef][Web of Science][Medline]
Baines AHJ, Hollingsworth DF, Leitch I. Diets of working-class families with children before and after the second world war. With a section on height and weight of children. Nutr Abstr Rev 1963;33:653–69.[Medline]
Rowett Research Institute. Family diet and health in pre-war Britain. Dunfermline: Carnegie United Kingdom Trust, 1955.
Gunnell D, Frankel S, Nanchahal K, Bradden F, Davey Smith G. Lifecourse exposure and later disease: a follow-up study based on a survey of family diet and health in pre-war Britain (1937–9). Public Health 1996;110:85–94.[CrossRef][Web of Science][Medline]
Kemp M, Gunnell D, Davey Smith G, Frankel S. Finding and using inter-war maternity records. Soc Hist Med 1997; 10:305–29.[Abstract]
Gunnell D, Davey Smith G, Frankel S et al. Childhood leg length and adult mortality: follow up of the Carnegie (Boyd Orr) Survey of Diet and Health in Pre-War Britain. J Epidemiol Community Health 1998;52:142–152.[Abstract]
Gunnell D, Davey Smith G, Frankel S, Kemp M, Peters TJ. Socio-economic and dietary influences on leg length and trunk length in childhood: a re-analysis of the Carnegie survey of diet and health in pre-war Britain (1937–9). Paediatr Perinat Epidemiol 1998;12(suppl 1):96–113.
Gunnell DJ, Davey Smith G, Holly JMP, Frankel S. Leg length and risk of cancer in the Boyd Orr cohort. BMJ 1998;317:1350–51.
Frankel S, Gunnell DJ, Peters T, Maynard M, Davey Smith G. Childhood energy intake and adult mortality from cancer: the Boyd Orr cohort. BMJ 1998;316:499–504.
Gunnell DJ, Frankel S, Nanchahal K, Peters T, Davey Smith G. Childhood Obesity and adult cardiovascular mortality. Am J Clin Nutr 1998;67:1111–18.[Abstract]
Frankel S, Davey Smith G, Gunnell D. Childhood socioeconomic position and adult cardiovascular mortality: the Boyd Orr cohort. Am J Epidemiol 1999;150:1081–84.
Gunnell DJ, Davey Smith G, McConnachie A, Greenwood R, Upton M, Frankel S. Separating in-utero and postnatal influences on later disease. Lancet 1999;354:1526–27.[Web of Science][Medline]
Blane D, Berney L, Davey Smith G, Gunnell DJ, Holland P. Reconstructing the life course: health during early old age in a follow-up study based on the Boyd Orr cohort. Public Health 1999;113:117–24.[CrossRef][Web of Science][Medline]
Kemp M, Gunnell D, Maynard M, Davey Smith G, Frankel S. How accurate is self-reported birth weight amongst the elderly? J Epidemiol Community Health 2000;54:639–40.
Gunnell DJ, Berney L, Holland P et al. How accurately are height, weight and leg length reported by the elderly and how closely are they related to measurements recorded in childhood. Int J Epidemiol 2000;29:456–64.
Gunnell D, Davey Smith G, Ness AR, Frankel S. The effects of dietary supplementation on growth and adult mortality: a re-analysis and follow-up of a pre-war study. Public Health 2000;114:109–16.[CrossRef][Web of Science][Medline]
Gunnell D. Epidemiological follow up of the Carnegie Survey of Diet and Health in Pre-War Britain. In: Fenton A (ed). Order and Disorder: the health implications of eating and drinking in the nineteenth and twentieth centuries. Edinburgh: Pub Tuckwell Press, 2000, pp. 30–44.
Dedman DJ, Gunnell D, Davey Smith G, Frankel S. Childhood housing conditions and later mortality in the Boyd Orr cohort. J Epidemiol Community Health 2001;55:10–15.
Martin R, Davey Smith G, Mangtani P, Frankel S, Gunnell D. Association between breastfeeding and growth: the Boyd Orr cohort study. Arch Dis Child Fetal Neonatal Ed 2002;87:F193–F201.
Maynard M, Gunnell D, Emmett PM, Frankel S, Davey Smith G. Fruit, vegetables, and antioxidants in childhood and risk of adult cancer: the Boyd Orr cohort. J Epidemiol Community Health 2003;57:218–25.
Martin R, Davey Smith G, Frankel S, Gunnell D. Parents growth in childhood and the birthweight of their offspring. Epidemiology 2004;15:308–16.[CrossRef][Web of Science][Medline]
Martin R, Davey Smith G, Frankel S, Tilling K, Gunnell D. Breastfeeding and Cardiovascular mortality: the Boyd Orr cohort and a systematic review with meta-analysis. Eur Heart J 2004;25:778–86.
Jeffreys M, Davey Smith G, Martin RM, Frankel S, Gunnell D. Childhood body mass index and later cancer risk: a 50 year follow up of the Boyd Orr study. Int J Cancer 2004;112:348–451.[CrossRef][Web of Science][Medline]
Maynard M, Ness A, Abraham L, Blane D, Bates C, Gunnell D. Selecting a healthy diet score: experience from a study of diet and health in early old age (Boyd Orr cohort). Public Health Nutr 2005;8:321–26.[CrossRef][Web of Science][Medline]
Ness A, Maynard M, Frankel S et al. Diet in childhood and adult cardiovascular and all-cause mortality: the Boyd Orr cohort. Heart 2005 (in press).
Martin RM, Ebrahim S, Griffin M et al. Breastfeeding and coronary atherosclerosis: intima-media thickness and plaques at 65 year follow up of the Boyd Orr Cohort. Arterioscler Thromb Vasc Biol 2005 (in press).
Martin RM, Mittleton N, Gunnell D, Owen CG, Davey Smith G. Breastfeeding and cancer: the Boyd Orr cohort and a systematic review with meta-analysis. J Natl Cancer Inst 2005 (in press).
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Acknowledgments |
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We are very grateful to the cohort members who participated so willingly in the follow-up study. We also wish to acknowledge all the research workers who participated in the original survey in 1937–39. We thank Professor Peter Morgan, director of The Rowett Research Institute, for the use of the archive and in particular Walter Duncan, honorary archivist to the Rowett, and the staff at the NHS Central Register at Southport and Edinburgh. Susie Potts is thanked for all her hard work in providing secretarial and administrative support to the study. Simone Watson was the research nurse during the 2002–03 follow-up. Nicos Mittleton currently maintains the Boyd Orr cohort database.
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References |
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1 Rowett RI. Family diet and health in pre-war Britain. Dunfermline: Carnegie United Kingdom Trust, 1955.
2 Smith D. The Carnegie Survey: background and intended impact. In: Fenton A (ed). Order and Disorder: the health implications of eating and drinking in the nineteenth and twentieth centuries. East Linton: Tuckwell Press Ltd, 2000, pp. 64–80.
3 Gunnell D, Davey Smith G, Ness AR, Frankel S. The effects of dietary supplementation on growth and adult mortality: a re-analysis and follow-up of a pre-war study. Public Health 2000;114:109–16.[CrossRef][Web of Science][Medline]
4 Kuh D, Davey Smith G. When is mortality risk determined? Historical insights into a current debate. Soc Hist Med 1993;6:101–23.
5 Leitch I. Growth and Health. Br J Nutr 1951;5:142–51.[CrossRef][Web of Science][Medline]
6 Baines AHJ, Hollingsworth DF, Leitch I. Diets of working-class families with children before and after the second world war. With a section on height and weight of children. Nutr Abstr Rev 1963;33:653–69.[Medline]
7 Forsdahl A. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prev Soc Med 1977;31:91–95.[Web of Science][Medline]
8 Barker DJP, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986;1:1077–81.[Web of Science][Medline]
9 Barker DJP, Martyn CN. The maternal and fetal origins of cardiovascular disease. J Epidemiol Community Health 1992;46:8–11.
10 Gunnell D. Commentary: Can adult anthropometry be used as a ‘biomarker’ for prenatal and childhood exposures? Int J Epidemiol 2002;31:390–94.
11 Gunnell DJ, Frankel S, Nanchahal K, Braddon FEM, Davey S. Lifecourse exposure and later disease: a follow-up study based on a survey of family diet and health in pre-war Britain (1937–39). Public Health 1996;110:85–94.[CrossRef][Web of Science][Medline]
12 Gunnell D, Berney L, Holland P et al. How accurately are height, weight and leg length reported by the elderly, and how closely are they related to measurements recorded in childhood? Int J Epidemiol 2000; 29:456–64.
13 Blane D. Cohort Profile: The Boyd Orr lifegrid sub-sample—medical sociology study of life course influences on early old age. Int J Epidemiol 2005;34:750–54.
14 Kemp M, Gunnell D, Davey Smith G, Frankel S. Finding and Using Inter-war Maternity Records. Soc Hist Med 1997;10:305–29.[Abstract]
15 Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988;16:1215.
16 Ahn SJ, Costa J, Emanuel JR. PicoGreen quantitation of DNA: effective evaluation of samples pre- or post-PCR. Nucleic Acids Res 1996;24:2623–25.
17 Gu DF, Hinks LJ, Morton NE, Day IN. The use of long PCR to confirm three common alleles at the CYP2A6 locus and the relationship between genotype and smoking habit. Ann Hum Genet 2000;64:383–90.[CrossRef][Web of Science][Medline]
18 Cheung VG, Nelson SF. Whole genome amplification using a degenerate oligonucleotide primer allows hundreds of genotypes to be performed on less than one nanogram of genomic DNA. Proc Natl Acad Sci USA 1996;93:14676–79.
19 Dean FB, Nelson JR, Giesler TL, Lasken RS. Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 2001;11:1095–99.
20 Frankel S, Gunnell DJ, Peters TJ, Maynard M, Davey Smith G. Childhood energy intake and adult cancer—The Boyd Orr cohort study. BMJ 1998;316:499–504.
21 Maynard M, Gunnell D, Emmett PM, Frankel S, Davey Smith G. Fruit, vegetables and antioxidants in childhood and risk of adult cancer: the Boyd Orr cohort. J Epidemiol Community Health 2003; 57:218–25.
22 Ness A, Maynard M, Frankel S et al. Diet in childhood and adult cardiovascular and all-cause mortality: the Boyd Orr cohort. Heart 2005 (in press).
23 Gunnell DJ, Davey Smith G, Frankel SJ, Kemp M, Peters TJ. Socio-economic and dietary influences on leg length and trunk length in childhood: a reanalysis of the Carnegie (Boyd Orr) survey of diet and health in prewar Britain (1937–39). Paediatr Perinat Epidemiol 1998;12:96–113.
24 Martin R, Davey Smith G, Mangtani P, Frankel S, Gunnell D. Association between breastfeeding and growth: the Boyd Orr cohort study. Arch Dis Child Fetal Neonatal Ed 2002;87:F193–F201.
25 Gunnell DJ, Davey Smith G, Holly JMP, Frankel SJ. Leg length and risk of cancer in the Boyd Orr cohort. BMJ 1998;317:1350–51.
26 Gunnell DJ, Davey Smith G, Frankel SJ, Nanchahal K, Braddon FEM, Peters TJ. Childhood leg length and adult mortality: follow up of the Carnegie (Boyd Orr) survey of diet and health in pre-war Britain. J Epidemiol Community Health 1998;52:142–52.[Abstract]
27 Gunnell D, Davey-Smith G, McConnachie A, Greenwood R, Upton M, Frankel S. Separating in-utero and postnatal influences on later disease. Lancet 1999;354:1526–27.[Web of Science][Medline]
28 Martin RM, Davey Smith G, Frankel S, Gunnell D. Parents' growth in childhood and the birth weight of their offspring. Epidemiology 2004;15:308–16.[CrossRef][Web of Science][Medline]
29 Martin RM, Davey Smith G, Tilling K, Frankel S, Gunnell D. Breastfeeding and cardiovascular mortality: the Boyd Orr cohort and a systematic review with meta-analysis. Eur Heart J 2004; 25:778–86.
30 Martin RM, Ebrahim S, Griffin M et al. Breastfeeding and coronary atherosclerosis : intima-media thickness and plaques at 65 year follow up of the Boyd Orr Cohort. Arterioscler Thromb Vasc Biol 2005 (in press).
31 Dowler E and Calvert C. Nutrition and diet in lone parent families in London. London: Family Policy Studies Centre, 1995.
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 R. M. Martin, J. M. P. Holly, G. Davey Smith, and D. Gunnell Associations of Adiposity from Childhood into Adulthood with Insulin Resistance and the Insulin-Like Growth Factor System: 65-Year Follow-Up of the Boyd Orr Cohort J. Clin. Endocrinol. Metab., September 1, 2006; 91(9): 3287 - 3295. [Abstract] [Full Text] [PDF]
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I. Bray, D. Gunnell, J. M. P. Holly, N. Middleton, G. D. Smith, and R. M. Martin Associations of Childhood and Adulthood Height and the Components of Height with Insulin-Like Growth Factor Levels in Adulthood: A 65-Year Follow-Up of the Boyd Orr Cohort J. Clin. Endocrinol. Metab., April 1, 2006; 91(4): 1382 - 1389. [Abstract] [Full Text] [PDF]
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 R. M. Martin, N. Middleton, D. Gunnell, C. G. Owen, and G. D. Smith Breast-Feeding and Cancer: The Boyd Orr Cohort and a Systematic Review With Meta-Analysis J Natl Cancer Inst, October 5, 2005; 97(19): 1446 - 1457. [Abstract] [Full Text] [PDF]
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 D. Blane Cohort Profile: The Boyd Orr lifegrid sub-sample--medical sociology study of life course influences on early old age Int. J. Epidemiol., August 1, 2005; 34(4): 750 - 754. [Full Text] [PDF]
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