International Congress Series 1297 (2007) 310 – 318

Is vegetable protein more beneficial to bone than animal protein?
S.A. Lanham-New a,⁎, W.T.K. Lee a , D.J. Torgerson b , D.J. Millward a
a b

Centre for Nutrition and Food Safety , School of Biomedical and Molecular Sciences, University of Surrey, Guildford, Surrey GU2 7XH, UK York Trials Unit, Area 4, Seebohm Rowntree Building, Department of Health Sciences, University of York, York YO10 5DD, UK

Abstract. The aim of this presentation was to assess the impact of a ‘vegetarian diet’ on indices of skeletal integrity. Analyses of existing literature were assessed in relation to bone health for: lactoovo-vegetarian and vegan diets vs. omnivorous; predominantly meat diets; consumption of animal vs. vegetable protein; fruit and vegetable consumption. The key findings include: (i) no differences in bone health indices between lacto-ovo-vegetarians and omnivores; (ii) conflicting data for protein effects on bone, with high and low protein intake being detrimental to the skeleton; (iii) growing support for a beneficial effect of fruit and vegetable intake on bone, with mechanisms of action currently remaining unclarified. © 2007 Elsevier B.V. All rights reserved.
Keywords: Vegetarianism; Osteoporosis; Protein; Calcium; Bone metabolism; Dietary acidity; Vegans; Fruit and vegetables; Bone mass; Vitamin K; Phytoestrogens; Herbs; Omnivores

1. Introduction 1.1. General Public health strategies aimed to target, on a population-wide basis, the prevention of poor bone health throughout the lifecycle are urgently required given the certainty of prediction that hip fractures will rise dramatically over the next decade and beyond. Clearly, nutrition (as an exogenous factor) has a crucial role to play in the optimization and
⁎ Corresponding author. Tel.: +44 1483 876476; fax: +44 1483 576978. E-mail address: (S.A. Lanham-New). 0531-5131/ © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2006.11.003

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maintenance of skeletal integrity. It is essential that specific dietary lifestyles, such as the particular inclusion or exclusion of particular foods/food groups within the overall diet, are carefully monitored to ensure that any such regime does not place the individual/population group at an increased risk of osteoporosis or its associated risk factors. 1.2. Defining vegetarianism The term ‘vegetarian’ is non-specific. It can often be used to describe a whole range of diets, practiced with varying degrees of restriction. Vegetarians may be referred to as ‘semi/ demi’-vegetarian, if they merely exclude meat [1]. Other categories include: lacto-ovovegetarian, if they exclude meat, fish and poultry but eat eggs and milk products; lactovegetarian, if they exclude all animal foods except milk and milk products; and vegan, if they exclude all foods of animal origin. Vegetarianism has become particularly popular in recent years. In the UK, approximately 4.3% of the population (equivalent to roughly 1:20 people) state that they follow a vegetarian diet, with young women being particularly represented; approximately one in four women aged 16–24 years avoiding red meat [2]. Since adolescence is a critical time with respect to bone health, individuals need to ensure that there are sufficient intakes of energy, calcium, iron and vitamins B12 and D given the required extra nutritional demand [3]. However, a well-planned varied vegetarian diet has been shown to be consistent with good health and there is data to suggest that following such a regime can potentially reduce the risk of chronic disease. 2. Historical aspect: fundamental theories linking vegetarianism to the skeleton 2.1. General concepts There is evidence to show that vegetarianism is associated with several factors which are likely to have a detrimental impact on bone including lower circulating levels of oestrogen and a lower average body mass index [4]. Additionally, with the recognition of the potential criticality of acid–base balance to skeletal integrity, it was considered that long-term ingestion of ‘vegetable-based’ diets may have a beneficial effect on bone mineral density (BMD) [5]. 2.2. Criticality of acid–base homeostasis to health Acid–base homeostasis is critical to health. Diet and the ageing process have been shown to affect systemic acidity; firstly, adult humans on a normal Western diet generate ∼ 1 mEq of acid/kg per day and the more acid precursors a diet contains, the greater the degree of systemic acidity; secondly, as people age, the overall renal function declines, including the ability to excrete acid [6], and thus with increasing age, humans become slightly but significantly more acidic [7]. 2.3. Mechanisms of action for a skeletal role in maintaining acid–base balance Theoretical considerations of the role alkaline bone mineral may play in the defense against acidosis date back as far as the late 19th Century. The pioneering work of Lemann


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and Barzel over three decades ago showed extensively the effects of ‘acid’ from the diet on bone mineral in both man and animal [8,9]. More recently, Arnett and Dempster [10] have demonstrated a direct enhancement of osteoclastic activity following a reduction in extracellular pH, an effect that has been shown to be independent of parathyroid hormone. Osteoclasts and osteoblasts appear to respond independently to small changes in pH in culture media [11] and there is evidence that a small drop in pH, close to the physiological range, causes a tremendous burst in bone resorption [12,13]. Furthermore, metabolic acidosis has been shown to stimulate resorption by activating mature osteoclasts already present in calvarial bone as opposed to the inducement of new osteoclast formation [14]. There are also data showing that excess hydrogen ions directly induce a physiochemical calcium release from bone [15]. It is very important to note, however, that a number of key questions remain unanswered in this area; specifically, work is urgently required to determine whether metabolically generated acid, hence a lowering of blood pH, exerts influence on osteoclasts ‘in vivo’. 2.4. Potential for a link between ‘vegetable-based foods’ and osteoporosis Considerations of the potential criticality of acid–base balance to skeletal integrity led to the development in the 1960s of a hypothesis linking the daily diet to the development of osteoporosis. It was noted specifically that ‘the increased incidence of osteoporosis with age, may represent, at least in part, the results of a lifelong utilisation of the buffering capacity of the basic salts of bone for the constant assault against pH homeostasis’ [16]. The extent of loss, over a given period of time, need not be of astronomical proportions: if 2 mEq/kg per day of calcium is required to buffer approximately 1 mEq/kg per day of fixed acid, over a decade this would account for a 15% loss of inorganic bone mass assuming a total body calcium of approximately 1 kg. Thus, it was proposed that long-term ingestion of ‘vegetable-based’ diets may have a beneficial effect on bone mineral mass. 3. The evidence: vegetarian diets and their impact on bone health indices 3.1. Studies in Eskimo populations Little data is available on bone health in populations consuming a diet highly dependent on animal foods, particularly that of meat. Mazess and Mather [17] examined forearm bone mineral content (BMC) in a sample of 217 children, 89 adults and 107 elderly Eskimo natives of the north coast of Alaska. Eskimo children were found to have a 5–10% lower BMC than US white children, a finding which was consistent with smaller body and bone size. In the young Eskimo adult population (age range 20–39 years), BMD was similar to the white population. However, after the age of 40 years, the Eskimos of both sexes were found to have a deficit of bone mineral in the order of magnitude between 10% and 15% relative to white standards. The authors note that aging bone loss, which occurs in many populations, was found to have an earlier onset and greater intensity in the Eskimo population. Similar results (showing an even greater bone loss) have also been found in Canadian Eskimos [18]. Clearly these findings of are of considerable interest to the interaction between diet and bone in the regulation of systemic acid–base balance. Whilst the issue of ‘dietary change’

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amongst the Eskimo population has been extensively discussed [19,20], these studies remain one of the few available examining indices of bone health in a population consuming a predominantly ‘animal-based’ diet. However, it is important to note that the studies on the Eskimo populations have a number of limitations; there is a lack of an internal comparison group as well as sufficient statistical control for major confounders. For example, the Eskimo population consume a diet that is extremely low in calcium (approximately 200 mg/day) which is likely to impact on the effect of protein in the diet on indices of bone health. 3.2. Earlier studies in vegetarian populations A number of population-based cross-sectional studies were undertaken investigating the effect of lacto-ovo-vegetarian diets on bone mineral mass. These earlier studies found BMD to be higher in the vegetarian group compared to those individuals consuming an omnivorous dietary lifestyle [21–27]. However, it is important to note that in the paper by Ellis et al. [21], there was a fundamental error in the interpretation of the photographic density measurements. Additionally, subjects studied in several of the published data were Seventh Day Adventists (SDA) who had a significantly different lifestyle to that of the omnivorous group. For example, the SDA group refrained from smoking and caffeine intake and their physical levels were higher). This is likely to have been an important confounding influence, which may have, at least in part, biased some of the study findings. 3.3. Later studies (post-1984) in vegetarian populations Cross-sectional and longitudinal population-based studies published in the last two decades suggest no differences in BMD between vegetarians and omnivores [28–32]. Lloyd et al. [28] found no differences in lumbar spine BMD between omnivorous and vegetarian premenopausal women and in the study by Tesar et al. [29], differences in nutrient intake and trabecular/cortical bone density were examined in postmenopausal Caucasian vegetarian and omnivorous women. Whilst the vegetarian group were found to consume greater quantities of carbohydrate, fibre, magnesium, ascorbic acid, copper and energy as percent carbohydrate, and lower amounts of protein, niacin, alcohol, vitamin B12, cholesterol and energy as percent protein, neither cortical or trabecular bone mass was affected by a lacto-ovo-vegetarian diet. In a 5-year prospective study of changes in radial bone density of elderly white American women (mean age of 81 years) living in residential communities, no differences were seen in bone loss rates between the lacto-ovo-vegetarians and the omnivorous group [30]. In the most recently published studies, bone mass was found to be significantly lower in the vegetable-based dietary groups. 4. Concept of dietary ‘acidity’: potential renal acid load (PRAL) The potentially deleterious effect of specific foods on the skeleton has been a topic of recent debate [33,34]. If the acid : base/skeletal link is to be believed, a possible explanation for there being no difference in indices of bone health between vegetarian vs. omnivorous populations, is that vegetable-based proteins generate a large amount of acid in the urine.


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Work by Remer and Manz [35] on the potential renal acid load (PRAL) of foods has shown that many grain products and some cheeses have a high PRAL level. These types of products are likely to be found in abundance in a lacto-ovo-vegetarian diet. 4.1. Dietary ‘acidity’ and ‘alkalinity’ in vegetarian populations As shown in Table 1, a comparison of dietary intakes of protein, calcium and potassium between omnivores and vegetarian/vegan groups show, in general, that protein intakes are generally lower in the vegetarian/vegan groups but there are few statistically significant differences in intakes of either calcium or potassium. Few studies have reported either a comparison of fruit and vegetable intakes between the groups or the level of intake of dietary alkali. In the study by Marsh et al. [25], the acid–base excess was found to be different between the groups: the omnivorous group had a mean value of 9.8 mmol excess HCl whereas the lacto-ovo-vegetarian group had a mean value of 26.1 mmol excess NaOH. Whilst the method used to determine the dietary acid and base excesses (i.e. the reaction of food expressed as the number of milliliters of 1 mol NaOH/L or 1 mol HCl/L (acid) to which it is equivalent) was rather imprecise, it does at least give acceptable indications that there were differences between the groups. Interestingly, the bone health results of this particular study showed that those who had followed a lacto-ovo-vegetarian diet for at least 20 years had only 18% less bone mineral by age 80 years whereas closely paired omnivores had 35% less bone mineral. 5. Animal vs. vegetable protein intake: impact on bone Ecological studies have shown that world-wide per capita consumption of animal protein has been associated with a higher risk of hip fracture in women aged N 50 years [36]. More recently, the correlation has been shown to be stronger with the ratio of animal protein
Table 1 Dietary ‘acidity’ and ‘alkalinity’ in omnivores, vegetarians and vegan population groups Omnivores Protein (g) Marsh et al. [25] Hunt et al. [27] Tesar et al. [29] Janelle and Barr [51] Lau et al. [32] a Ca (mg) K (mg) Lacto-ovo-vegetarians Protein Ca (g) (mg) K (mg) Vegans Protein Ca (g) (mg) – – – – – – K (mg) – – 3587 ± 908 – 3460 ± 1240

68 712 63 ± 19 ⁎ 772 ± 390 76 ± 20⁎ 863 ± 199 77 ± 20 60 ± 21⁎ 950 ± 437 344 ± 261

2177 56 898 2238 – 52 ± 20 748 ± 351 – 2687 ± 626 63 ± 24 821 ± 351 3012 ± 701 3042 ± 833 57 ± 11 875 ± 255 2884 ± 742 – 35 ± 16 385 ± 216 – – –

Larsson and 80 ± 18⁎ Johansson [52]

1328 ± 372⁎ 3160 ± 921 –

52 ± 12 578 ± 184 39 ± 20 359 ± 126 55 ± 17 538 ± 350

Reproduced with permission from New [53]. a Urinary K/Cr ratio significantly higher in the vegetarian vs. omnivorous group (7.8 ± 4.4 vs. 4.3 ± 4.5). ⁎ P b 0.05.

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to vegetable protein, a study which has adjusted for important cultural differences [37]. It is important to note, however, that in these correlational studies, the unit of measurement is country and not individual and as such, these types of studies have a number of limitations which must be considered in the interpretation of such data. The effect of a high dietary ratio of animal protein to vegetable protein on bone loss and risk of fracture has been investigated in a prospective cohort of 1035 women who participated in the Study of Osteoporotic Fractures (SOF) [38]. Women with a higher ratio of animal to vegetable protein intake had a higher rate of bone loss at the femoral neck than did those with a low ratio as well as a greater risk of hip fracture. Other published studies that present data specifically examining animal vs. vegetable protein effects on bone include both the IOWA Women's Health Study and the Framingham Study. Munger et al. [39] report that higher intakes of animal sources of protein were associated with a 70% reduction in hip fracture [39] and Hannan et al. [40] found that the lowest quartile of animal protein consumption was significantly related to hip and spine bone loss in men and women aged between 67 and 93 years [40]. Both population groups had adequate calcium intakes. 5.1. Protein and bone health: importance of dietary calcium and/or dietary alkalinity? Of interest to the protein controversy is the growing recognition that dietary calcium may play a crucial role; that is, dietary protein is not detrimental to bone health provided that dietary calcium is in adequate supply [41]. Whilst there are a number of studies which provide direct support for this [42,43], there remains plausible mechanisms by which alkali salts also have a critical role to play [44–46]. 6. Fruit and vegetable link to bone: other potential mechanisms of action? There are growing data, both observational and experimental which show a positive link between fruit and vegetable consumption and bone health [47,48]. However, more intervention studies are required before a causal link can be claimed. Furthermore, it remains to be determined the exact mechanisms behind a fruit and vegetable link to the skeleton since these foods provide not only a source of dietary alkali but also a wide variety of micronutrients, many of which have plausible workings for an effect on bone. The exciting work by Muhlbauer et al. suggest that vegetables, salads and herbs affect bone by a mechanism independent of their base excess [49]. Furthermore, the potential for a role of bone in the buffering of ‘acid’ remains a topic of debate and challenge [50]. 7. Discussion There is a clear and urgent need for public health strategies to target prevention of poor bone health on a population-wide basis and, similarly, it is critical that particular dietary habits resulting in the exclusion of specific foods are carefully monitored to ensure that population groups are not placing themselves at an increased risk of osteoporosis or its associated risk factors. Existing and available data indicate that consumption of a lacto-ovo-vegetarian does not have an over-riding negative or positive effect on skeletal integrity. The effect of dietary


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protein consumption per se (as well as the intake of animal vs. vegetable) on bone remains a controversial issue: data are conflicting and it is an area for further research. Both high protein consumption (particularly without supporting calcium/alkali intakes) and low protein intakes (particularly in vegan diets) have been shown to be detrimental to the skeleton. There is growing support from a combination of clinical, observational and intervention studies for a beneficial effect of fruit and vegetable intake on bone health. The mechanisms behind this ‘fruit and veg’ link remains to be fully determined: these foods provide not only a source of dietary alkali (for which there is growing data to suggest a critical role for the skeleton in acid : base homeostasis) but also a wide variety of micronutrients, many of which have plausible workings for an effect on bone. 8. Conclusion The impact of a ‘vegetarian’ diet on bone health is a hugely complex area for the following reasons: 1) components of the diet (such as calcium, protein, alkali, vitamin K, phytoestrogens) may be varied; 2) key lifestyle factors which are important to bone (such as physical activity) may be different; 3) the tools available for assessing consumption of food are relatively weak. However, from data available and given the limitations stipulated above, ‘vegetarians’ do certainly appear to have ‘normal’ bone mass. What remains to be the challenge is to determine what components of a ‘vegetarian’ diet are of particular benefit to bone, at what levels and under which mechanisms. References
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