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MINISTÉRIO DA EDUCAÇÃO
UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE
CENTRO DE CIÊNCIAS DA SAÚDE
PROGRAMA DE PÓS-GRADUAÇÃO EM CIÊNCIAS DA SAÚDE
EFETIVIDADE DA SUPLEMENTAÇÃO DE ZINCO NA FORÇA,
RESISTÊNCIA E EQUILÍBRIO MUSCULAR EM IDOSAS: ensaio
clínico randomizado duplo cego
MARIA APARECIDA BEZERRA
NATAL/RN
2013
MARIA APARECIDA BEZERRA
EFETIVIDADE DA SUPLEMENTAÇÃO DE ZINCO NA FORÇA,
RESISTÊNCIA E EQUILÍBRIO MUSCULAR EM IDOSAS: ensaio
clínico randomizado duplo cego
Dissertação apresentada ao Programa de Pós-Graduação em Ciências da Saúde da Universidade Federal do Rio Grande do Norte, como requisito para obtenção do Título de Doutor em Ciências da Saúde. Orientador: Prof. Dr. José Brandão Neto Coordenadora: Profa. Dra. Ivonete Batista Araújo
NATAL/RN
2013
B574i Bezerra, Maria Aparecida. Influência do zinco no desempenho muscular em mulheres jovens e idosas / Maria Aparecida Bezerra. – Natal/RN, 2013. 57f.: il. Orientador: Prof. Dr. José Brandão Neto
Tese (Doutorado em Ciências da Saúde) – Programa de Pós-Graduação em Ciências da Saúde. Universidade Federal do Rio Grande do Norte. Centro de Ciências da Saúde.
1. Envelhecimento – Tese. 2. Nutrição – Zinco – Tese. 3. Força muscular – Tese. I. Brandão Neto, José. II. Título.
RN/UF/BSA01 CDU: 613.2-055.2
ii
MARIA APARECIDA BEZERRA
EFETIVIDADE DA SUPLEMENTAÇÃO DE ZINCO NA FORÇA,
RESISTÊNCIA E EQUILÍBRIO MUSCULAR EM IDOSAS: ensaio
clínico randomizado duplo cego
Aprovada em: ______/______/______
BANCA EXAMINADORA
______________________________________________________________ Prof. Dr. José Brandão Neto (Presidente – UFRN)
______________________________________________________________ Profa. Dra. Selma Sousa Bruno (Membro Interno – UFRN)
______________________________________________________________ Prof. Dr. Eryvaldo Sócrates Tabosa do Egito (Membro Interno – UFRN)
______________________________________________________________ Profa. Dra. Margareth de Fátima Formiga Melo Diniz (Membro Externo – UFPB)
_____________________________________________________________ Prof. Dr. Eduardo Sérgio Soares Sousa (Membro Externo – UFPB)
iii
A Deus, fonte de sabedoria, de amor e de inspiração criadora. A Ele dedico este trabalho. Aos meus pais, João (in memoriam) e Irene, pelo esforço que fizeram para que os filhos pudessem estudar. Aos meus amados filhos, Amanda e Tiago, pelas palavras e ações de incentivo quando eu retornava para casa cansada da jornada de trabalho. Às mulheres que fizeram parte dessa pesquisa, pelo compromisso assumido em todas as fases do trabalho e por tudo o que aprendi com elas. Aos Mestres do passado e do presente pelo árduo trabalho com a fonte do conhecimento que pode propiciar o desenvolvimento da humanidade.
iv
AGRADECIMENTOS
A Deus, fonte de vida e amor, que me amparou durante todas as etapas deste
trabalho.
Ao Prof. Dr. José Brandão Neto, minha profunda gratidão, pela precisa e
preciosa orientação ao longo desta importante fase de minha vida.
A Profa. Áurea Nogueira de Melo por sua dedicação voluntária à avaliação
neurológica das pacientes, em todas as fases da pesquisa.
Aos colegas: Naira Josele Neves de Brito, Érika Dantas de Medeiros Rocha,
Alfredo de Araújo Silva e Denise Dal'Ava Augusto pela ajuda nos procedimentos de
avaliação em suas respectivas áreas de atuação.
À FAPERN e CNPq pelo financiamento da pesquisa.
Ao PPGCSA e aos docentes a ele vinculados.
A UFPB, especialmente aos colegas do Departamento de Fisioterapia, pelo
incentivo nesta etapa acadêmica.
Às equipes do Programa de Saúde da Família dos Bancários, Timbó I e Timbó
II pelo acolhimento, compromisso e dedicação com que nos receberam e
acompanharam durante toda esta pesquisa.
Às voluntárias, cuja colaboração permitiu a realização deste trabalho.
A todos os que, direta ou indiretamente, contribuíram para a conclusão deste
trabalho, a minha gratidão.
v
RESUMO
Introdução: O decréscimo na função muscular durante o envelhecimento limita a
capacidade funcional e, consequentemente, a independência física. Objetivo:
Avaliar a efetividade do zinco na força, na resistência e no equilíbrio muscular em
mulheres idosas atendidas em área de abrangência da Unidade de Saúde da
Família do Sistema Único de Saúde. Metodologia: Ensaio clínico randomizado
duplo cego placebo controlado com 38 participantes aleatoriamente distribuídos em
4 grupos: grupo-controle composto por 18 mulheres jovens, com idade entre os 20 e
os 30 anos, assim subdivido: Jovem Placebo (n=9) ingeriu placebo (sorbitol 10%);
Jovem Zinco (n=9) ingeriu 25mg do elemento zinco. Grupo experimental composto
por 20 mulheres idosas, com idade entre os 60 e os 80 anos e subdividido: Idosa
Placebo: (n=10) ingeriu placebo; Idosa Zinco (n=10) ingeriu 25mg do elemento
zinco. O seguimento teve duração de 90 dias. A força, a resistência e o equilíbrio
muscular foram estimados pelo pico de torque isocinético normalizado pelo peso
corporal, do quadríceps (PT/kg QUA) e dos isquiotibiais (PT/kg IQS) nas velocidades
angulares de 60°/s e de 180°/s por dinamometria Isocinética. Resultados: Na
medida inicial PT/kg IQS 60°/s, não houve diferença significativa entre os grupos.
Após 90 dias ocorreu redução significativa da força apenas no grupo Idosa Placebo:
PT/kg IQS 60°/s =58,53±16,37 Nm em relação ao grupo Jovem Placebo: PT/kg IQS
60°/s = 84,15±27,60 Nm p=0,01. Quanto à resistência dos isquiotibiais (PT/kg IQS
180°/s), os dois grupos de idosas (Placebo e Zinco) eram significativamente
menores do que o grupo Jovem Placebo na medida inicial. Após 90 dias, apenas o
grupo Idosa Placebo tinha resistência significativa menor que o grupo Jovem
Placebo. Efeito dentro de cada grupo: ocorreu aumento significativo de força e
resistência dos isquiotibiais no grupo Idosa Zinco e diminuição significativa no grupo
Idosa Placebo. A diferença de médias (Δ) entre Idosa Zinco e Idosa Placebo (teste t
independente) dos isquiotibiais, após 90 dias, foi significativa tanto para força (PT/kg
IQS60°/s Δ=8,97 Nm, p= 0,02) como para resistência (PT/kg IQS 180°/s Δ=11,88
Nm p=0,01). Conclusões: A diferença significativa entre as médias do inicio e as de
seguimento, tanto de força como de resistência dos isquiotibiais entre Idosa Zinco e
Idosa Placebo, mostra a vulnerabilidade desse músculo durante o envelhecimento.
Essas perdas poderiam ser minimizadas com a suplementação de zinco. Isso indica
que a nutrição adequada de zinco pode prevenir perda de força e resistência
muscular em mulheres com mais de 60 anos.
Descritores: Envelhecimento. Zinco.Nutrição. Força muscular. Dinamômetro de
força muscular.
vi
LISTA DE ABREVIATURAS E SIGLAS
ERO Espécie reativa de oxigênio DMO Densidade mineral óssea Zn Zinco
Nm Newton metro
PT Pico de torque
vii
SUMÁRIO
1 INTRODUÇÃO ...................................................................................................... 08
2JUSTIFICATIVA .................................................................................................... 12
3 OBJETIVOS ......................................................................................................... 13
3.1 Objetivo geral .................................................................................................... 13
3.2 Objetivos específicos ........................................................................................ 13
4 MÉTODO .............................................................................................................. 14
5 ANEXAÇÃO DO ARTIGO1 .................................................................................. 15
6 ANEXAÇÃO DO ARTIGO 2 ................................................................................. 40
7 COMENTÁRIOS, CRÍTICAS E CONCLUSÕES. .................................................. 45
REFERÊNCIAS ....................................................................................................... 48
ANEXO ................................................................................................................... 51
APÊNDICE ............................................................................................................. 52
8
1 INTRODUÇÃO
O envelhecimento populacional é uma realidade em países desenvolvidos e
em desenvolvimento(1). A prevalência de múltiplas condições crônicas e
incapacidade funcional são mais elevadas na senescência. Variações nas condições
de saúde, no bem-estar, na capacidade funcional e nas necessidades de cuidado
distinguem diferentes grupos de idosos. Tais variações poderão culminar com a
Síndrome da Fragilidade caracterizada pela diminuição da massa corporal, fraqueza,
fadiga, inatividade, redução da ingestão alimentar, sarcopenia, osteopenia,
anormalidades no equilíbrio e na marcha(2). Essas características estão direta ou
indiretamente interligadas com fatores, como: características demográficas,
socioeconômicas e outros aspectos relacionados com a saúde(3).
Estilo de vida sedentário, característico dessa população, está associado com
osteoartrite, consequente da inatividade física, redução da função mitocondrial,
desajuste do estado redox celular, aumento de inflamação crônica sistêmica que
torna o ambiente intracelular do músculo propenso à toxicidade de espécies reativas
de oxigênio (ERO)(4). Esses fatores podem contribuir para a redução da massa
muscular esquelética. Tal redução tem inicio discreto na terceira década e
diminuição significativaa partir do final da quinta década em homens e mulheres(5).
A diminuição do músculo esquelético, tecido metabolicamente ativo, afeta a
sua capacidade metabólica, particularmente as capacidades glicolíticas e
respirátórias(6)
, potencializa aumento da gordura corporal, diminuição da aptidão
aeróbica, da massa magra e da densidade mineral óssea(7).
Estudo de nosso grupo de pesquisa mostrou que 20,2% da variabilidade da
densidade mineral óssea na coluna lombar estava relacionada com a massa magra
e tempo de menopausa; 22,3% de variabilidade da densidade mineral óssea do colo
do fémur estava relacionada com o peso corporal e idade; 18,9% da variabilidade da
densidade mineral óssea no triângulo de Ward estavam relacionadas com a idade e
gasto energético basal; e 39% da variabilidade da densidade mineral no trocanter
estavam relacionadas com o índice de massa corporal, idade e menarca(8).
Essas evidências mostram que o organismo humano reage de forma
específica aos diferentes tipos de estímulo, ao longo do desenvolvimento, revelado
9
no bidirecional processo epigenético: de genótipo para fenótipo e de fenótipo para
genótipo(9).
O músculo esquelético sintetiza esse contexto e responde, de acordo com a
tipologia de suas fibras, ao metabolismo aeróbico e anaeróbico. Fibras musculares
de contração lenta (tipo I) têm metabolismo oxidativo e são ricas em capilares e
mitocondrias. São requisitadas durante exercícios que aumentam a resistência
muscualar. As fibras musclares de contração rápida (tipo IIa) têm perfil metabólico
semelhante às fibras do tipo I. As fibras musculares glicolíticas de metabolismo
anaeróbico (tipo IId e IIb) têm pouca mitocondria e pouca vascularização capilar.
Estão envolvidas nos exercícios que visam aumentam a força muscular(10).
O grupos musclares isquitibias e quadricepes, que são objetos de nosso
estudo, apresentam um percentual elevado de fibras musculares de contração
rápida tipo II. Em estudo histoquimico, Garrett et al.(11) mostram que há uma
proporção maior dessas fibras nos isquitibiais em comparação com o quadriceps. No
bícepes femoral (cabeça longa), na área proximal, há um pencentual de 55,2% e na
área distal, 53,8%; na cabeça curta do bíceps, na área central, o percentual é de
59,2%; no semitedinoso, na área proximal, 54,6% e na área distal, 60,4%; no
semimembranoso, na área proximal, 51% e na área distal, de 50,5%. Para o
quadríceps, no mesmo estudo, os músculos foram analisados apenas na área
central. Mostra portanto, um percentual de fibras musculares tipo II no vasto lateral
de 54,5%, no vasto intermédio de 45,7%, no vasto medial de 49,4% e no reto
femoral de 57,7%(11).
Os músculos com elevado percentual de fibras do tipo II são recrutados em
exercício de alta intensidade e geram elevados níveis de tensão nos tendões
produzidos por força de estiramento os quais podem expor os músculos a danos em
períodos de atividade muscular intensa(11). No envelhecimento a tendência ao dano
muscular aumenta, principalmente em mulheres, em decorência do aumento da
tensão isotônica, da baixa cinética das pontes cruzadas de actina e miosina. Estes
danos musculares que têm como consequência maior rigidez muscular e baixa
produção de força(12). Isso pode ser agravado devido à característica das fibras
musculares glicolícas tipo II que são mais suscetíveis também ao dano provocado
por alto nível de estresse oxidativo(10).
10
Pessoas idosas com mais de 40% de fibras musculares tipo II apresentaram
níveis mais baixos de peroxidação lipídica e desencadeiaram com mais eficiência o
sistema contra ânio superóxido do que das pessoas que têm menos de 40% dessas
fibras musculares(13). Também é reportado que há redução significativa da força
muscular, da área de secção transversa muscular, diminuição de fibras tipo I e
decréscimo de capilares por área de fibra muscular (14).
Essas transformações biológicas causadas por estilo de vida sedentário e
fatores nutricionais podem mudar a capacidade mitocondrial e interferir no
metabolismo oxidativo energético, o que pode tornar o organismo vulnerável a
agentes agressores celulares, como os radicais livres, principalmente no
envelhecimento, os quais estão relacionados com a sarcopenia e doenças crônicas(4,
12).
O estilo de vida fisicamente ativo das pessoas idosas, está associado com a
compensação parcial da preservação da biogênese mitocondrial e com a
capacidade antioxidante no músculo esquelético que pode retardar o início da
sarcopenia(4).
A sarcopenia (redução da massa muscular) e a dinapenia (redução da força
muscular) estão associadas com o aumento do estresse oxidativo e podem ser
potencializadas devido à menor atividade das enzimas anaeróbicas e aeróbicas, do
conteúdo de proteínas, e não apenas devido à diminuição da atividade física(6).
Existem evidências de que a deficiência de zinco no organismo pode afetar a
função do músculo estriado (15) e pode induzir a apoptose de células musculares
lisas vasculares. O estresse oxidativo, na deficiência de zinco, contribuiria para a
apopitose dessas células(16).
Estudos sobre a ação do zinco na saúde humana mostram avanços nesses
ultimos 50 anos. Segundo Prasad(17), no início da década de 1960, eram
conhecidadas apenas três enzimas que necessitavam de zinco para suas atividades.
Atualmente, são conhecidas mais de trezentas enzimas e mais de mil fatores de
transcrição que precisam de zinco para realizarem suas atividades. O zinco mostrou
ser efetivo para tratar diarréia aguda em crianças e resfriados comuns; prevenir
cegueira de pessoas com degeneração macular e reduzir a incidências de infecções
no envelhecimento(17).
11
O zinco é um abundante elemento de transição no cérebro, tem importante
papel na estabilização da proteína básica de mielina e na formação da bainha de
mielina(18), está envolvido no desenvolvimento e preservação das funções dos
nervos periféricos(19), na preservação da quantidade de fibras musculares e no
metabolismo energético dessas fibras musculares(20). Já mostrou exercer influência
no trabalho total isocinético dos músculos extensores do ombro e do joelho em
homens jovens(21).
Durante prolongados períodos de restrição de atividade motora, parece que
são modificados mecanismos endógenos da homeostase do zinco. Zorbas et al.(22)
mostram que ratos mantidos em hipocinesia, mesmo estes recebendo
suplementação de zinco na dieta, esta não garantiu que o zinco penetrasse nos
tecidos onde são normalmente depositados, como ocorre nos ossos e nos músculos.
Foi obervado também aumento do zinco no plasma, na excreção fecal e urinária, o
que resultou em significante perda de zinco corporal(22).
Considerando a importância da nutrição de zinco associado com estilo de vida
ativo, a pesquisadora propôs essa pesquisa com a finalidade de estudar a influência
do zinco na força, na resistência e no equilíbrio muscular em mulheres idosas
sadias.
12
2 JUSTIFICATIVA
A redução do desempenho muscular em homens e mulheres está associada
com a sarcopenia, que é uma das principais causas da redução da força e do
desempenho muscular no envelhecimento(23) e que é caracterizada pela redução do
número, do tamanho e do nível da vascularização das fibras musculares(13). A
estimativa de sarcopenia aumenta à medida que as pessoas envelhecem. Em
pessoas com idade entre os 60 e os 70 anos, o percentual de sarcopenia fica entre
5% e 13%. Já em pessoas com mais de 80 anos, essa estimativa aumenta para os
percentuais de 11% a 50%(24).
A diminuição da força muscular relacionada com a idade foi denominada
dinapenia em 2008(25). Ela tem consequência significativa, durante o
envelhecimento, por aumentar o risco de limitações funcionais, de incapacidade e de
mortalidade(26). É reportado atualmente que a dinapenia do quadríceps e do punho e
não a sarcopenia, é preditor independentes de mortalidade(27).
O estudo da dinapenia em mulheres é um tema que tem relevância clínica,
por ser fator de risco para a maioria das doenças crônicas relacionadas com o
envelhecimento. Por outro lado, um aporte suplementar de zinco pode favorecer
aumento da força muscular devido sua ação como antioxidante, estimulante
imunológico e como agente inflamatório(16).
Considerando a realidade do decréscimo do desempenho muscular no
envelhecimento e sua associação com a nutrição adequada de zinco, o presente
estudo investigou a efetividade da suplementação de zinco (25 mg do elemento
Zn++) no aumento da força, da resistência e do equilíbrio entre os músculos
isquiotibiais e quadríceps em mulheres jovens e idosas. Portanto, este projeto
atendeu à finalidade primordial da Política Nacional de Saúde da Pessoa Idosa
(Portaria nº 2.528 de 19 de outubro de 2006)(28). Tal política visa a “recuperar,
manter e promover a autonomia e a independência dos indivíduos idosos” por estar
inserido o projeto na Atenção Básica de Saúde, em consonância com os princípios e
diretrizes do Sistema Único de Saúde.
13
3 OBJETIVOS
3.1 Objetivo geral
Avaliar a efetividade do zinco (25 mg do elemento Zn++) no desempenho dos
músculos isquiotibiais e dos quadríceps nas velocidades angulares de 60°/s e de
180°/s entre mulheres jovens e idosas.
3.2 Objetivos específicos
Verificar se a suplementação de zinco em mulheres idosas diminuiu a
diferença de força e resistência, em comparação com as mulheres jovens.
Observar se a suplementação de zinco aumentou a força, resistência e
equilíbrio muscular em mulheres idosas.
Constatar se houve diferença significativa entre as mulheres idosas que foram
suplementadas com zinco e aquelas que ingeriram placebo.
14
4 MÉTODO
Ensaio clínico randomizado duplo cego placebo controlado com um
seguimento de sessenta dias. Trinta e oito mulheres foram distribuídas,
aleatoriamente, em quatro grupos. O grupo-controle foi constituído por 18 mulheres
jovens com idade entre os 20 e os 30 anos e subdivido em dois grupos: Jovem
Placebo (n=9) ingeriu placebo (sorbitol 10%) e Jovem Zinco (n=9) ingeriu 25 mg do
elemento zinco. O grupo experimental foi composto de 20 mulheres idosas com
idade entre os 60 e os 80 anos, subdividido em dois grupos: Idosa Placebo (n=10)
ingeriu placebo e Idosa Zinco (n=10) ingeriu 25 mg do elemento zinco. A força, a
resistência e o equilíbrio muscular foram estimados pelo torque isocinético
normalizado pelo peso corporal do quadríceps e dos isquiotibiais nas velocidades
angulares de 60°/s e de 180°/s, antes e após os sessenta dias de tratamento.
15
5 ANEXAÇÃO DO ARTIGO 1
ARTIGO 1
Título: Efetividade da suplementação de zinco na força, na resistência e no
equilíbrio muscular em mulheres idosas: ensaio clínico randomizado duplo cego.
Periódico: Clinical Interventions in aging
ISSN: 1176-9092 (Print) Qualis: A2 (Medicina II – CAPES) Fator de impacto: 2.083 Status: a ser submetido
16
ORIGINAL RESEARCH
Clinical Interventions in aging
Effectiveness of zinc supplementation on strength, endurance, and muscle balance
in elderly women: a randomized double blind clinical trial.
Maria Aparecida Bezerra1
Simone Bezerra Alves1
Áurea Nogueira de Melo2
Érika Dantas de Medeiros Rocha3
Naira Neves de Brito3
José Brandão-Neto4
1 Departamento de Fisioterapia da Universidade Federal da Paraíba (João Pessoa,
Brasil);
2 Departamento de Pediatria da Universidade Federal do Rio Grande do Norte (Natal,
Brasil);
3 Pós-graduanda do Programa de Pós-graduação em Ciências da Saúde da
Universidade Federal do Rio Grande do Norte (Natal, Brasil);
4 Departamento de Medicina Clínica da Universidade Federal do Rio Grande do
Norte (Natal, Brasil).
Correspondente: José Brandão-Neto.
Av. Gal. Gustavo Cordeiro de Farias, s/n, Natal-RN, CEP 59012-570, Brazil.
Tel +55 84 3342 9748
Fax +55 84 3342 9776
17
ABSTRACT Introduction: The elderly generally show decreased muscle performance, accompanied by low consumption of dietary zinc. It is reported that zinc has positive effects on muscle performance. The aim of this study was to evaluate the influence of zinc on strength, muscular endurance, and balance in older women. Methodology: A randomized double-blind placebo-controlled clinical trial with 38 participants randomly subdivided into 4 groups: a control group comprised of 18 young women aged between 20 and 30 years, thus subdivided: Young Placebo (n = 9) ingested a placebo (sorbitol 10%), Young zinc (n = 9) ingested 25 mg of zinc. An experimental group of 20 elderly women, aged between 60 and 80 years and subdivided as: Elderly Placebo: (n = 10) ingested a placebo; Elderly Zinc (n = 10) ingested 25 mg of zinc. The follow-up lasted 90 days. The strength, endurance, and muscular balance (hamstring/quadriceps) were estimated by isokinetic peak torque, normalized by body weight, of the quadriceps, and hamstrings in the angular velocities of 60°/s (force), and 180°/s (resistance). Results: Compared with the strength of the Young placebo hamstring group, the Elderly Zinc showed a proportional increase in strength, and the Elderly Placebo group was significantly reduced. The same was seen for hamstrings resistance, only that the Elderly Placebo group showed a significant reduction compared to the Young Placebo group. Effect within each group: a significant increase in strength and endurance of the hamstrings in the Elderly Zinc group, and a significant decrease in the Elderly Placebo group. Mean difference(Δ) between Elderly Zinc and Elderly Placebo for hamstring strength was significant for (PT/kg IQS60°/s Δ = 8.97 Nm, p = 0.02) and for resistance (PT/kg IQS 180°/s Δ = 11.88 Nm p = 0.01). Conclusions: The study showed that zinc may be effective in increasing the strength and endurance of the hamstring, (a vulnerable muscle), and prevents disproportionate reduction of its strength relative to the quadriceps, atypical muscle imbalance that increases the risk of falls in older people. Keywords: Aging. Zinc, Nutrition, Muscle strength, Dynamometer, muscle strength.
18
Introduction
Population aging is a reality on all continents1, and results in the need for the
elderly to seek ways to address the related challenges; high prevalence of chronic
disease, and functional disability2. All this may predispose this population to develop
the Fragility Syndrome, compromising both their quality of life and interfering in their
autonomy. Additional commitments and financial input from their families and the
state are required to aid these people with their new needs in regard to personal
care3. These factors are also directly or indirectly linked to demographic and
socioeconomic factors, as well as to other aspects health2.
During aging, muscle performance is directly associated with decreased
functional capacity4. Sarcopenia, characterized by reduced number, size5, and
vascularization of the muscle fibers4, is directly related to accelerating muscle mass
loss,after 60 years of age6, and has a direct effect on muscle strength reductions in
the elderly 5.
Reduced muscle mass and strength are associated with increased oxidative
stress, which may be potentiated due to lower anaerobic and aerobic enzyme
activity, and protein losses, and not just due to decreased physical activity7.
There is evidence that zinc deficiency in the body can affect striate8 muscle
function, and can induce apoptosis of vascular smooth muscle cells. Oxidative stress
combined with zinc deficiencies, would contribute to this cellular apoptosis9.
Zinc is an abundant transition element in the brain, it plays an important role
in the stabilization of basic myelin proteins, and the formation of the myelin sheath10,
it is involved in the development and preservation of peripheral nervefunctions11, and
in preserving the amount of muscle fibers, and their energy metabolism12. Zinc was
also demonstrated to influence the total isokinetic work of the extensor muscles in the
shoulders and knees in young men13.
During prolonged restrictions of motor activity, it appears that endogenous
mechanisms of zinc homeostasis are modified. Zorbas et al.14 showed that rats kept
in hypokinesia, did not guarantee tissue zinc penetration (normally deposited in
bones and muscles) even when receiving dietary zinc supplements. Increased zinc in
plasma, fecal and urinary excretions was also observed, resulting in significant losses
of corporalzinc14.
19
In healthy aging, skeletal muscle shows a significant reduction in isokinetic
muscle strength (especially in women), increased stiffness of the muscle fiber,
reduced phosphorylation of the myosin light chains, and diminished actin and myosin
cross-bridge kinetics, which results in low rates of force production15. There are also
reductions in muscle cross-sectional area, type I fiber percentage, capillaritizedarea5
and a decline in mitochondrial oxidative capacity4.
Older people with an active lifestyle show partial compensation, preserving
mitochondrial oxidative capacity. An active lifestyle helps retain antioxidant capacity.
In contrast, in the sedentary elderly, mitochondrial function is compromised with
deregulation of the redox function. This anomaly may increase chronic inflammatory
processes, which make the intracellular spaces of skeletal muscle an environment
prone to toxicity, as mediated by reactive oxygen species (ROS)16.
Proper zinc nutrition is essential to preserve muscle function8. Its deficiency, a
characteristic of human aging, results in decreased immune response, and
development of chronic degenerative diseases 17, which may predispose the elderly
to long periods of restricted movement, and make them vulnerable to precipitate fecal
and urinary excretion of zinc, thus decreasing corporalzinc14.
Decreased muscle strength related to age, called dynapenia by Clark and
Maniniin 200818, has significant consequences for the aged, and increases the risks
of functional limitations, disabilities and mortality 19. Study shows that dynapenia of
the quadriceps and wrists are independent predictors of mortality20. Thus, we see the
clinical relevance of dynapenia studies.
During human aging there is usually a gradual change from an active to
sedentary lifestyle. The sedentary lifestyle is associated with chronic inflammatory
disease, sarcopenia16, and dynapenia20. Zinc, being recognized as an anti–
inflammatory21, could prevent the evolution of dynapenia, since the hand grip
strength is negatively associated with levels of urinary 8-hydroxy-20-deoxyguanosine
(8-OHdG)22. Based on the above, the present study aims to investigate the
effectiveness of zinc supplementation (25 mg Zn++/day) in preventing strength,
endurance, and quadricep/hamstring muscle balance losses in young and elderly
women.
20
Materials and methods
Patient and study design
The volunteers, 60 to 80 years old were selected from a population of healthy
elders3, as routed by the doctors of three family health clinics in the 3rd Sanitary
District of the city of João Pessoa (PB), and by active search of the medical records
of families enrolled at these health clinics. After selection, a home visit (with the agent
responsible for the covered area of the local Family Health Clinic) was made in order
to inform the volunteers about the research, and to invite their participation.
The study included women; who practiced physical activities twice a week (at
most), were residents in the areas covered by the study, which agreed to participate
freely, and were aged from 20 to 30, and from 60 to 80. Women with a history of
diseases such as diabetes mellitus, liver disease, thyroid disease, neurological
disease, and rheumatoid arthritis were excluded. Besides these were excluded; users
of medications that interfere with nerve function, and/or of pharmacological vitamin
and mineral supplements, or which had a history of recent surgery. Those who were
under hormone replacement therapy, or with mental illness, or had been bedridden
during the last two months for more than two weeks, or whom did not agree to
participate in the study were also excluded.
Initially, we pre-selected 56 women between 60 and 80 years of age. After
initial assessments, 20 women were excluded: two for not being able to leave home
during the evaluations, four were living in another neighborhood with their children,
eleven were self-medicating with anti-inflammatory, analgesic, and/or vitamin
supplements, three walked every day and practiced gym exercise three times a
week.
Thirty-six women were referred for specialist clinical assessment in
rheumatology, endocrinology, gastroenterology, cardiology, and neurology. At this
stage, four with knee osteoarthritis, one with gastritis, two with diabetes, three with
carbohydrate intolerance, and two with hypothyroidism were excluded.
After these assessments, 24 elderly participants were selected and were the
basis for selecting the pairs of young women to form the control group. The young
women aged between 20 and 30 years were selected from the same area covered by
21
the family health clinics of the older women, following all the procedures for
evaluating the elderly.
Ethics
After being informed about all stages of the research, the reading and signing
of the informed consent (as approved by the Ethics and Research Committee, Center
of Health Sciences, Federal University of Paraiba (Protocol. 0193) was completed.
Who agreed to be a volunteer then signed.
Experimental Design
Clinical randomized double blind controlled placebo. The professional
responsible for carrying and storing bottles containing the zinc supplement and
placebos was also responsible for group randomization, drawn randomly 1:1,
randomly distributed into 4 groups. The control group included 18 young women
between 20 and 30 years of age, and was subdivided into: Young Placebo: (n = 9)
ingesting (10% sorbitol); Young Zinc: (n = 9) ingesting 25mg of elemental zinc/day.
The experimental group comprised 20 elderly women aged between 60 and 80 years
old, and was subdivided into: Elderly Placebo: (n = 10)ingesting a placebo(10%
sorbitol); Elderly Zinc:(n = 10) ingesting 25 mg of zinc/day.
The women were supplemented with 25 mg of zinc daily in the form of hepta-
hydrated zinc sulfate (ZnSO47H2O, Merck, Darmstadt, Germany). The solutions of
zinc, and the placebo (10% sorbitol) were prepared at the Department of Pharmaco-
technics (UFRN, Brazil). Each volunteer was given a bottle of white matte plastic,
containing 30 ml. A drop contained 5 mg of the element Zn++, or placebo (10%
sorbitol). The volunteers were instructed to add 5 drops of the solution to a piece of
bread, juice, or milk daily for breakfast. The study lasted for seven months. Each
week 10 women were randomly selected to begin the experimental phase that lasted
90 days. The women drawn were referred by the professional responsible for
randomization. Assessments started for the first phase of the study. After the final
procedure of the assessment, they would receive a bottle containing a solution of
22
either zinc or placebo that they would use during the ninety days. In the end all of the
assessment procedures were performed for the initial stage.
Instruments and data collection procedures
Anthropometric assessment
The weights and heights of the participants were obtained on a manual
balance (Elmer) with a capacity of 150 kg, 100 g precision, and a metal scale of 200
cm with a precision of 1 cm, leveled and calibrated (Balmak; BK50F, Sao Paulo, SP,
Brazil). The body mass index (BMI) was obtained from the ratio weight/height 2.
Evaluation of alimentary consumption
The food intake assessment was performed using an estimated weekly food
intake based on three days, two days mid-week, and one day on the weekend. The
volunteers were instructed to properly perform the technique of food accounting,
noting the time of each meal, and all food consumed in their respective home
measures.
The calculation of energy, macronutrients, fiber, calcium, iron, and zinc
consumed (from the menus) was done through the Nut Win software version 1.5 a
Nutrition Support Program, provided by the Department of Health Informatics,
Federal University of São Paulo/UNIFESP. We also used the Brazilian Food
Composition Table (TACO), provided by the Center for Studies and Research in
Food (NEPA), State University of Campinas (UNICAMP)23.
Assessment of physical activity
The level of physical activity was measured using the Baecke physical activity
questionnaire (modified for elders), and used to characterize a homogeneous
physical activity group 24.
23
Evaluation of strength, endurance, and muscle balance
Peak isokinetic torque, normalized by body weight(PT/kg) to assess strength,
endurance, and muscle balance, 25 was measured at angular velocities of 60°/s, and
180°/s,on a Computerized Isokinetic Dynamometer (Biodex Multi-Joint System
3,Biodex System Biomedical Inc, New York, USA),at the Laboratory for Analysis of
Muscular Performance, Department of Physical Therapy, UFRN.
The dynamometer was calibrated before each session, as described in the
equipment manual. All tests were performed by the same physician in all phases of
the study. Women performing the tests initiated a brief warm-up for five minutes on a
stationary bicycle, adjusted to a resistance of 25 W at a speed of 20 km/h. They then
conducted quadriceps stretching for both limbs. The stretching was conducted with
the volunteers standing erect, the knee in complete flexion, and the hip extended to
the maximum tolerable amplitude. Each maneuver was maintained for 30 seconds
and repeated three times, at an interval of 30 seconds.
After stretching, each participant was positioned on the dynamometer chair
with the backrest reclined (with respect to the vertical position) by 5°. The
participant’s trunk (thorax) is stabilized by means of two cross straps, and a
transverse strap fixes the waist (pelvis). The support of the dynamometer lever arm
was positioned in the distal region of the leg, 5 cm above the lateral malleolus, so
that a complete arc of ankle dorsiflexionis allowed. The mechanical axis of rotation of
the dynamometer was aligned with the lateral epicondyle of the femur (the axis of
rotation of the knee joint). During all testing procedures, all women were told to hold
firmly to the lateral seat support so as to keep all body segments stabilized.
Adjustments to correct the effect of gravity on the torque were performed with
the knee at 60°, and calculated by the dynamometer software. After a brief period of
familiarization with the dynamometer, three sub maximal contractions were
performed. The volunteers were then instructed to relax completely for three minutes.
After this interval, they began is kinetic evaluation in the non-dominant limb. The
isokinetic dynamometer was set in isokinetic mode, with the angular velocities at
60°/s and 180º/s. Five repetitions with the angular velocity at 60°/s(rated power), and
fifteen repetitions with the angular velocity at 180°/s (rated resistance), and the
hamstrings/quadriceps ratio was used to assess relative muscularbalance25. The
24
three-minute rest period was maintained between sets to minimize the effects of
fatigue.
Collection of biological material
8 mL of blood were collected: 2 mL for zincexamination (BD Vacutainer, Trace
Element, Serum, BD Franklin Lakes, NJ,USA), 2 mL for hematologic tests
(VacuetteK3EK3EDTA, Greiner Bio -One, Monroe, North Carolina, USA), 2 mL for
biochemical tests, and 2 mL for hormonal dosage (Z Vacuetteserumclotactivator,
GreinerBio-One, Monroe, North Carolina, USA).The samples for zinc were
immediately kept at a temperature of 37oC in a stainless steel oven, suitable for
metals. Six hours later, the tubes were taken, and the sera collected with plastic
ferrules, and stored in plastic tubes with metal-free caps. Hemolyzed samples were
discarded because red blood cells are richer in zinc than is plasma. All procedures
related to the handling of zinc samples were followed according to international
standards. The serum samples were stored in a freezer at -20ºC until analysis.
Laboratory analyzes
Hormones (GH, IGF - 1, IGFBP3, E2, LH, FSH, TSH, T4) were measured by
chemiluminescence (Immulite 1000 systems), the blood count was performed by an
auto-analyzer(Horiba ABX Diagnostics, Micros 60, Montpellier, France), glucose,
total protein, albumin, alanine transaminase, aspartate transaminase, total bilirubin,
urea, creatinine and lipids were analyzed by auto analyzer (DadeBehring, Dimension
AR, Illinois, USA). Zinc was determined by atomic absorption spectrophotometry (AA
- 240FS, Varian, Victoria, Australia) according to the manufacturer's instructions.
Statistical Analysis
Data normality was assessed by the Shapiro-Wilk test. The data of the
descriptive statistics were presented in a table as the mean, standard deviation, and
mean difference (Δ). To detect the homogeneity between the groups, the parametric
test one- way ANOVA was used with post hoc Tukey. The difference in average peak
25
torque, normalized by body mass (PT/kg) for the quadriceps and hamstring muscles,
at the angular velocities of 60°/s and 180°/s, and the muscle equilibrium ratio
(between hamstrings/quadriceps) were analyzed. We compared between the control
group Young Placebo, and the experimental Elderly Placebo and Elderly Zinc
groups(one-way ANOVA) at the beginning and at the end of testing. The difference of
effects within each group was made by paired the Student's t test. The treatment
effect, comparing the Zinc Elderly with the Placebo Elderly group was made from the
difference between the averages of the initial and the final evaluations, by
independent t test.
RESULTS
The final sample consisted of 20 elderly women and 18 young women. In table
1 are summarized the characteristics of homogeneity between the groups. After
analyzing the data, the randomization layout of the groups was revealed. To compare
the effectiveness of zinc on force (PT/kg 60°/s), on resistance (PT/kg180°/s), and on
muscle balance (IQS/QUA) in aging, the control group of reference was the Young
Placebo group, which was not affected by zinc supplementation.
In Table 2, the differences in averages (Δ), and standard deviations between
the control group Young Placebo with the experimental groups Elderly Zinc and
Elderly Placebo are expressed. In the initial measures of muscle strength APT/kg
IQS 60°/s, the percentage difference between the groups Young Placebo and Elderly
Zinc was 9.24%, between Young Placebo and Elderly Placebo it was 18.33%, no
significant differences. Following 90 days of supplementation with 25 mg, the Elderly
Zinc group had peak torque increased PT/kg IQS 60°/s by 8:18 Nm, with no
significant difference in muscle strength continuing in the Young Placebo group.
However, the Elderly Placebo group in contrast observed a decrease in PT/kg IQS
60°/s of 1.50 Nm from their initial measurements(A) representing a significant
30,45% reduction in strength when compared to the Young Placebo group.
In the original measurement APT/kg QUA 60°/s, there was a significant
percentage of difference in strength between the Young Placebo and Elderly Zinc
groups of 28.24%,between the Young Placebo and Elderly Placebo groups, the
difference was 29%. In the follow-up DPT/kg QUA 60°/s measurements we observed
26
reductions in strength difference between the Young Placebo, and Elderly Zinc
groups at 22.83%, between the Young Placebo and Elderly Placebo groups it was
24%, the difference was not significant. As to muscle balance between the
hamstrings and quadriceps (AIQS/QUA 60°/s), it was observed that the Young
Placebo group showed lower muscular balance than the two elderly groups, which
could expose their knees to damage. The evaluation, after 90 days of
supplementation with 25 mg zinc revealed that the Elderly Zinc group maintained
muscle balance within limits, but were 7.74% above the Placebo Young control
group. However, in the Elderly Placebo group, there was a decreased muscle
balance (DIQS/QUA 60°/s Nm) of 18.69% compared to the Young Placebo group.
Concerning hamstring muscle strength, in the initial (APT/kg IQS
180°/s),measurements a significant difference between the Young Placebo group
and the Elderly Zinc group of 31.76%, and between the Young Placebo and Elderly
Placebo group of26.86%, was observed, which shows decreasing hamstring strength
with age. In the follow-up measurements, after 90 days of supplementation with zinc,
increased hamstring resistance in the Elderly Zinc group was observed. The increase
was enough to verify no significant differences between the Elderly Zinc and the
Young placebo groups. However, in the Elderly Placebo group we observed
decreased hamstring muscle strength, and a greater significant difference between
the Young Placebo and the Elderly Placebo groups.
When the effect of zinc supplementation was compared in the same group
between the initial measurement sand after 90 days, as seen in Table 3,the Elderly
Zinc group showed significant increases (10.93%) in the strength of the hamstrings
(PT/kg ISQ 60°/s), and significant increases (10.22%) in the quadriceps muscle
(PT/kg QUA 60°/s). This represented an increase of 1.28%in the strength balance
between the hamstrings and the quadriceps (ISQ/QUA 60°/s), approximating 60%.
However, in the Elderly Placebo group seen in Table 4, there was a decrease of
2.56% in the strength of the hamstrings (PT/kg ISQ 60°/s), and significant increase of
9.80% in quadriceps strength (PT/kg QUA 60°/s), which represented a significant
decrease of 12.78% in the balance of muscle strength (ISQ/QUA 60°/s).
Muscular endurance analyzed before and after 90 days in the Elderly Zinc
group showed a significant increase of 16.46%for the hamstring (PT/kg ISQ 180°/s),
and the mean increase was 9.21% for the quadriceps (PT/kg QUA 180°/s). This
27
represented an increase of 10.39% in the muscle strength balance (ISQ /QUA
180°/s). In contrast, it was found that for the Elderly Placebo group (in comparing the
initial assessments with the subsequent 90 days of experiment), there was a
decrease of 6.79% in the hamstring strength(PT/kg ISQ 180°/s), and 5.65% increase
in quadriceps strength, this represented a decrease of 15.28% in the muscle strength
balance (ISQ/QUA 180°/s).
The effect of zinc supplementation between the Elderly Zinc group, and the
Elderly Placebo, seen in Table 5, shows a significant increase in both strength and
endurance for the hamstring muscles and the quadriceps. It can be assumed that
zinc supplementation of 25 mg may be effective in the prevention of muscle strength
and endurance losses, while increasing muscle strength and endurance in healthy
women over 60 years of age.
DISCUSSION
The main results of this study show that supplementation of 25 mg daily for a
period of 90 days increased strength, endurance, and muscle balance in women
between 60 and 80 years of age. This may contribute to the prevention of strength,
endurance, and muscular balance losses common during aging.
It was found that daily zinc intake was below recommended levels in all three
groups, both for age and for sex26. However, serum zinc levels were within the
reference standard normal27. In this nutritional condition, and in the initial assessment
of hamstring strength measured by peak torque normalized by body weight at an
angular velocity of 60°/s, the Young Placebo control had 9.24% more power than the
Elderly Zinc group and 18.33% more than the Elderly Placebo group. No significant
differences. However, the follow-up measurement showed that the Young placebo
group had increased hamstrings strength (12.66%), and in the Elderly Zinc group,
increased strength was 10.81%.In contrast the Elderly Placebo group showed
reduced strength (2.56%). This decreased hamstring strength generated a significant
difference of 30.45% compared to the Young Placebo group. Serum zinc observed in
follow-up was seen ata significant reduction of 22.50% in the Young placebo group;
the Elderly Placebo group saw a significant reduction of 9.8%. However in the group
supplemented with 25 mg of zinc (Zinc Elderly), serum zinc reduction was
28
insignificant. This shows that in the Young Placebo group, who increased their
hamstring strengths by 12.66 that zinc may have been used in intramuscular
structures thus reducing its availability in the plasma by 22.50%, leaving the group at
the upper limit of zinc deficiency27. In the Elderly Placebo group, a significant
reduction in serum zinc represented a reduction of force of 2.56%. This shows the
importance of adequate amounts of zinc in the diet to preserve the strength of the
hamstrings, since the supplemented Elderly Zinc group at 25 mg of zinc for ninety
days, seems to have used the additional zinc, and secured increases in strength.
This muscle group is extremely important in muscular balance for older people25.
Zinc could also reduce or prevent hamstring injuries characteristic of aging 28.It is
reported that to preserve muscle function, zinc is essential for proper nutrition8. Its
deficiency is characteristic of human aging, and leads to immune response
decreases, and the development of chronic degenerativediseases17.
Of interest in this study was the quadriceps strength. In the initial evaluation,
strength of the quadriceps for the Young Placebo group was 28.24% higher than the
Elderly Zinc group and larger by 29%than the Elderly Placebo group, significant
differences. In the follow-up measure, the difference in strength between the groups
decreased as the Elderly Zinc group increased by 10.22%, the group Elderly Placebo
by 9.8%, and the Young Placebo group by only 3.46%. The proportionate gains of
force, both in the hamstring muscles as well as the quadriceps for the Elderly Zinc
group resulted in a better muscular balance. In contrast, in the Elderly Placebo group,
decreased strength of the hamstrings to 1.50 Nm, and increased strength in the
quadriceps of 12.53 Nm, led to a significant decrease in muscular balance from 51.59
± 7.74 to 45.74 ± 8.24. Accordingly, with muscle imbalance, an overload of the
quadriceps can occur, because the most requested of movements, from sitting to
standing position, spares the hip extensor 29.
During normal walking, balance between the flexor and extensor musculature
is necessary for perfect dynamism between the concentric and eccentric contractile
mechanisms. Because of aging, lesions of the quadriceps and hamstring muscle
groups can interfere with this mechanism, due to decreased potential for muscle
tissue regeneration 30. Elderly people with lower muscle strength have higher rates of
mortality 31. Muscular force reduction18is closely related to decreased muscle mass
with age5. Reductions in strength, and muscular endurance, as well as unbalanced
29
knee flexor and extensor muscles are inversely correlated with pain, stiffness, and
functionality25.
A Brazilian study of the elderly with mean ages of 69 ± 3.64 years, established
benchmarks for balance between the knee flexors and extensors (the hamstrings,
and quadriceps)at an angular velocity of 60°/s: 47.95 ± 10.99% and an angular
velocity of 180°/s: 59.59 ± 13, 40%32.In our study the approximate age of the women
was by groups Elderly Zinc: 66.40 ± 6.20, and Elderly Placebo: 65.30 ± 5.03.Our
study showed that at the angular velocity of 60°/s the muscular balance between
flexors and extensors (during the initial evaluation of Elderly Placebo group) was
51.59 ± 7.74%, close to the reference values above. In the follow-up measurements,
the balance between flexors and knee extensors of 45.74 ± 8.24% was lower, both in
terms of their initial measurements as with the elderly of reference 32. However, in the
Elderly Zinc group,(initial average of 58.09 ± 11.29% and final average of 58.84 ±
9.90), the average hamstring/quadriceps balance, the equilibrium force directed to
the knee joint, was maintained at 22.27%,above the average benchmark for this
parameter 32. These results indicate what zinc supplementation can do in addition to
other factors that improve the health of the elderly 26, 27, and it may also be effective
in increasing muscular strength, especially the hamstring muscles.
In the muscle balance measurements (ISQ/QUA180°/s), the Elderly Placebo
group showed an initial mean of 61.69 ± 11.95, and a final average of 53.51 ± 6.21,
the Elderly Zinc group showed an initial mean of 57, 98 ± 11.29, and final average of
64.70 ± 9.79. Therefore, the present study showed that the average strength of the
muscle balance of the knee joint 90 days after the first assessment of Elderly
Placebo group was 11.25% lower than the reference population. In contrast, the
Elderly Zinc group after the same time was 7.9% higher than the reference
population average 32. The increase in muscle balance in strength and resistance
seen in this study could make it easier to change from the sitting position to the
standing position, or the starting and maintaining walking speed for a longer time.
With reference to the comparison between the muscle balance averages
outlined in this study, and the reference population32, there is evidence that zinc
supplementation might be beneficial to prevent muscle imbalance for both strength
and endurance. This is because the final averages for the group of women which
were supplemented with zinc during 90 days at an angular velocity of 60°/s,
30
maintained close to 60%, and at the angular velocity of 180°/s they were close to
65%. This might help to focus future studies elucidating the role of zinc in muscle
strength and endurance.
During aging, the hamstrings are most vulnerable to injury because a one-year
increase in age increases the likelihood of tendon injury in this muscle group 1.3
times 33. Actions that develop increased muscle strength can be effective in
improving the daily life of elderly women, and contribute to the maintenance and
extension of their autonomy, of the functional capabilities of this population 34, 35.
The hamstrings are a muscle group, with a predominance of fast twitch type II
muscle fibers. In healthy aging, there is a reduction of skeletal muscle fiber type I, of
capillaritzed area4, of strength, and of cross-sectional area. In the hamstrings, the
femoral biceps are made up of mainly 2c fibers that can become fast fiber or slow,
depending on the demand for action requested 36.
Reduction of muscle mass and muscle strength is associated with increased
oxidative stress and may be increased due to lowered activity of anaerobic and
aerobic enzymes, and protein content, not just due to decreased physicalactivity7.
There is evidence that zinc deficiency in the body can adversely affect the
function of striated muscle 8,and can induce apoptosis of vascular smooth muscle
cells; oxidative stress with zinc deficiency could contribute to the apoptosis of these
cells 9. Acute depletion of zinc in the body; also changes the working capacity of
skeletal muscle 13. However, the effectiveness of zinc in the metabolism depends on
lifestyle, because in experimental conditions of restricted mobility in mice, zinc
supplementation was not effective in maintaining its metabolic balance 14.
To preserve muscle function, proper zinc nutrition is essential 8 because zinc
deficiency in human aging causes a decrease in the immune response, and the
development of chronic degenerativediseases17.
The significant difference between the initial and follow-up averages for both
strength and endurance of the hamstrings between the Elderly Zinc and Elderly
Placebo groups shows the vulnerability of this muscle during aging. The decrease in
strength, endurance, and balance was minimized with zinc supplementation, while
increasing strength, muscular endurance, and balance in the older zinc
supplemented women was observed. This indicates that adequate zinc nutrition can
prevent loss of strength and muscle endurance in women over 60 years. Accordingly,
31
Public Health Action could minimize the effects of dynapenia and neuromuscular
aging syndrome.
FINANCING AND CONFLICT OF INTEREST
This study was funded by FAPERN (Case Notice PPSUS 3 - in. 011/2009).
The authors have no conflicts of interest in publishing this article.
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33
22. Muzembo BA, Nagano Y, Eitoku M, Ngatu NR, Matsui T, Bhatti SA, et al. A cross-sectional assessment of oxidative DNA damage and muscle strength among elderly people living in the community. 1-9.Environ Health Prev Med. 2013;1-9. DOI 10.1007/s12199-013-0350-x
23. Universidade Estadual de Campinas (UNICAMP). Núcleo de Estudos e Pesquisas em Alimentação (NEPA). Tabela Brasileira de Composição de Alimentos (TACO). 2 ed. Campinas, São Paulo, 2006.
24. MazoGZ, Mota J, Benedetti TB, Barros MVGD. Validade concorrente e reprodutibilidade: teste-reteste do questionário de Baecke modificado para idosos. Ver Bras Ativ Fis Saúde. 2001;6(1):5-11.
25. Santos MLADS, Gomes WF, de Queiroz BZ, de Brito Rosa NM, Pereira DS, Dias JMD, et al. Desempenho muscular, dor, rigidez e funcionalidade de idosas com osteoartrite de joelho. Acta Ortop Bras. 2011;(4):193-7.
26. Suplementação com zinco no tratamento da anorexia nervosa. Revista da Associação Médica Brasileira. 2013;59(04):321-324.
27. Yanagisawa H. Zinc deficiency and clinical practice. Japan Med Assoc J.2004;47(8):359-364.
28. Gabbe BJ, Bennell KL, Finch CF. Why are older Australian football players at greater risk of hamstring injury?. J Sci Med Sport. 2006;9(4):327-333
29. Meijer K, WillemsPJ, SavelbergHH. Muscles limiting the sit-to-stand movement: an experimental simulation of muscle weakness.GaitPosture. 2009;30(1):110-114.
30. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science. 2003;302(5650):1575.
31. Rantanen T, Volpato S, Ferrucci L, Heikkinen E, Fried LP, Guralnik JM.
Handgrip Strength and Cause‐Specific and Total Mortality in Older Disabled Women: Exploring the Mechanism.J AmGeriatr Soc. 2003;51(5):636-41.
32. Dias JMD, Arantes P, Alencar M, Faria J, Machala C, Camargos F, et al. Relacao isquiotibiais/quadriceps em mulheres idosas utilizando o dinamometro isocinetico; Isokinetic hamstring/quadriceps ratio in elderly women. Rev bras fisioter. 2004;8(2):111-5
33. Verrall G, Slavotinek J, Barnes P, Fon G, Spriggins A. Clinical risk factors for hamstring muscle strain injury: a prospective study with correlation of injury by magnetic resonance imaging.Br J Sports Med. 2001;35(6):435-9.
34 Holloszy JO, Tseng BS, Marsh DR, Hamilton MT, Booth FW. Strength and aerobic training attenuate muscle wasting and improve resistance to the development of disability with aging.J Gerontol A BiolSci Med Sci. 1995;50(Spec):113-109.
34
35. Offord E A, Karagounis LG, Vidal K, Fielding R, Meydani S, Penninger JM. Nutrition and the biology of human ageing: Bone health & osteoporosis / sarcopenia / immune deficiency. J Nutr Health Aging. 2013;17(8):712-716.
36. Dahmane R, Djordjevič S, Smerdu V. Adaptive potential of human biceps femoris muscle demonstrated by histochemical, immunohistochemical and mechanomyographical methods. Med Biol Eng Comput. 2006;44(11):999-1006
35
Table 1. Bioanthropometrics and health characteristics between Young Placebo, Elderly Zinc, and Elderly Placebo Groups
Young Placebo (n=9) ElderlyZinc (n=10) ElderlyPlacebo(n=10)
Age 24.11±2.97 66.40±6.20* 65.30±5.03*
Monthly income 1732.40±1080 1544.60±1111 2210.30±1865
Body mass(kg) 62.45±15.44 62.45±15.44 64.26±10.67
Height(m) 1.61±0.04 1.50±0.08* 1.51±0.03*
BMI(kg/m²) 23.75±5.41 25.96±5.33 27.82±4.03
Physical Activity 4.94±3.19 6.98±2.57 6.56±2.83
RBC(million/mm3) 4.45±0.19 4.48±0.35 4.56±0.30
Diet zinc(mg/dia) 7.42±1.15 5.74±2.17 6.54±2.09
Zinc (μg/mL) 1.081±0.06 1.068±0.11 1.079±0.04
Note- * Statistical significance (p ≤ 0.05).
BMI= Body Mass Index; RBC= Red Blood Cell
36
Table 2. Peak torque; normalized by body mass of the quadriceps and hamstrings in the angular velocities of 60°/s and 180°/s, for Young Placebo, Elderly Placebo and Elderly Zinc Groups (one-way ANOVA).
Young
Placebo (n=9)
Elderly
Zinc (n=10) P Δ1
Elderly
Placebo
(n=10)
p Δ2
APT/kg IQS-60°/s,Nm 73.50±25.59 66.71±13.13 0.73 6.79 60.03±18.56 0.30 13.47
DPT/kg IQS-60°/s,Nm 84.15±27.60 74.89±14.46 0.57 9.26 58.53±16.37 0.02 25.62*
APT/kg QUA- 60°/s,Nm 162.44±43.69 116.58±24.64 0.01 45.86*
115.34±29.24 0.013 47.10*
DPT/kg QUA 60°/s,Nm 168.25±59.75 129.84±29.61 0.11 38.41 127.87±30.04 0.13 40.38
APTIQS/QUA 60°/s,Nm 45.00±8.97 58.09±11.23 0.01 -13.09* 51.59±7.74 0.29 -6.59
DIQS/QUA 60°/s,Nm 54.29±18.23 58.84±9.90 0.71 -4.54 45.74±8.09 0.31 8.55
APT/kg IQS 180°/s,Nm 65.75±18.10 44.87±15.49 0.01 20.88** 48.09±8.63 0.03 17.66
**
DPT/kg IQS 180°/s,Nm 68.06±21.74 53.71±9.18 0.10 14.35 45.03±11.34 0.006 23.03**
APT/kg QUA 180°/s,Nm 117.73±32.83 77.26±24.07 0.01 40.47** 79.33±15.55 0.006 38.40
**
DPt/kg QUA 180°/s,Nm 125.42±41.46 85.09±19.88 0.01 40.33 84.06±18.54 0.009 41.36*
A IQS/QUA 180°/sNm 56.73±8.90 57.98±11.87 0.96 -1.24 61.69±11.95 0.59 -4.95
DIQS/QUA 180°/s,Nm 57.56±18.29 64.70±9.79 0.42 -7.13 53.51±6.21 0.75 4.05
A Zinc (μg/mL) 1.0816±0.06039 1.0683±0.1167 0.93 0.0132 1.0796±0.0472 0.99 0.0020
D Zinc (μg/mL) 0.8383±0.0865 1.006±0.1387 0.005 -0.1679 0.9738±.0736 0.02 -0.1354
Note - * Statistical significance (p ≤ 0.05). Δ1= (difference of means between Young placebo and Elderly Zinc); Δ2= (difference of means between Young Placebo and Elderly Placebo. A = measured before supplementation, D = measurements after the 90 days of supplementation with zinc, PT = peak torque, Nm = Newton.meter; kg = body mass; QUA= quadriceps; ISQ = hamstring ISQ /QUA = hamstrings and quadriceps ratio
37
Table 3. Peak torque (normalized by body mass) of the quadriceps and hamstrings at angular velocities of 60°/s and 180°/s of the Elderly Zinc group (t test stopped).
Note - * Statistical significance (p ≤ 0.05).
PT = peak torque, Nm = Newton meter; kg = body mass; ISQ = hamstrings, QUA = quadriceps, and ISQ/QUA = hamstrings to quadriceps ratio: Δ = difference between averages before and after
Elderly Zinc 95% confidence interval
Before After P Δ
Lower
Limit
Upper
Limit
PT/kg IQS 60°/s Nm
66.71±13.13
74.89±14.46
0.02
-8.18*
-14.99 -1.36
PT/kg QUA 60°/s Nm
116.58±24.64
129.84±29.61
0.01
-13.26*
-23.12 -3.39
IQS/QUA 60°/s Nm
58.09±11.23
58.84±9.90
0.85
-0.74
-9.39 7.90
PT/kg IQS 180°/s Nm
44.87±15.49
53.71±9.18
0.01
-8.84*
-15.60 -2.07
PT/kg QUA 180°/s Nm
77.26±24.07
85.09±19.88
0.01
-7.83*
-13.57 -2.08
IQS/QUA 180°/s Nm
57.98±11.87
64.70±9.79
0.07
-6.72
-14.22 0.78
Zinc (μg/mL) 1.068±0.1167 1.0059±0.1471 0.14 0.0624 -0.0256 0.1505
38
Table 4. Peak torque normalized by body mass of the quadriceps and hamstrings in the angular velocities of 60°/s and 180°/s Elderly Pacebo group (t test stopped).
Note - * Statistical significance (p ≤ 0.05). PT = peak torque, Nm = Newton meter; kg = body mass; ISQ = hamstrings,QUA = quadriceps, and ISQ/QUA = hamstrings to quadriceps ratio; Δ = difference between the averages before and after
ElderlyPlacebo Confidenceinterval95%
Before
(n = 10)
Mean ± SD
After
(n = 10)
Mean ± SD
p Δ
LowerLimit UpperLimit
PT/kg IQS 60°/s Nm
60.03±18.56
58.53±16.37
0.61
1.50
-4.91 7.91
PT/kg QUA 60°/s Nm
115.34±29.24
127.87±33.04
0.02
-12.53*
-22.60 -2.45
IQS/QUA 60°/s Nm
51.59±7.74
45.74±8.24
0.001
5.84*
3.09 8.59
PT/kg IQS 180°/s Nm
48.09±8.63
45.03±9.18
0.32
0.06
-3.54 9.66
PT/kg QUA180°/s Nm
79.33±15.55
84.06±18.54
0.15
-4.73
-11.54 2.08
IQS/QUA 180°/s Nm
61.69±11.95
53.51±6.02
0.07
8.18
-1.03 17.39
Zinc (μg/mL) 1.0796±0.0472 0.9593±.0612 0.001 0.1202 0.0692 0.1712
39
Table 5. Difference of averages before and after 90 days (independent t test) of peak torque/body mass of the quadriceps and hamstrings, angular velocities of 60°/s and 180°/s, between Elderly Zinc and ElderlyPlacebogroups
Note - * Statistical significance (p ≤ 0.05). PT = peak torque, Nm = Newton.meter; kg = body mass ; QUA = quadriceps, ISQ = hamstrings, Δ = average difference between
Elderly
Zinc(n=10)
Elderly Placebo
(n=10)
Confidence Interval
Mean ± SD Mean ± SD Δ P Lowest Highest
PT/kg IQS 60°/s Nm 8.29±9.44 -1.50±8.97 9.97* 0.02 1.13 18.44
PT/kgQUA 60°/s Nm 15.95±19.29 11.82±15.65 4.13 0.60 -12.30 20.56
PT/kg IQS 180°/s Nm 8.82±9.45 -3.06±9.15 11.88* 0.01 3.13 20.62
PT/kg QUA 180°/s Nm 7.83±8.03 4.73±9.53 3.10 0.44 -5.18 11.38
40
6 ANEXAÇÃO DO ARTIGO 2 ARTIGO 2
Título: Influence of basal energy expenditure and body composition on bone mineral
density in postmenopausal women
Periódico: International Journal of General Medicine
ISSN: 1178-7074 (Electronic) Qualis: B2 (Medicina II – QUALIS CAPES) Status: Publicado
41 International Journal of General Medicine Dovepress
open access to scientific and medical research
Open Access Full Text Article O r i g i n a l R e s e a r c h
Influence of basal energy expenditure
and body composition on bone mineral density
in postmenopausal women
This article was published in the following Dove Press journal: International Journal of General
Medicine 2 November 2012 Number of times this article has been viewed
Maria Aparecida
Bezerra Quirino1 João Modesto-Filho2
Sancha Helena de
Lima Vale3 Camila Xavier
Alves3 Lúcia Dantas
Leite4 José Brandão-
Neto5 1Department of Physiotherapy, 2Department of Clinical Medicine,
Universidade Federal da Paraíba, João Pessoa, Brazil; 3Postgraduate Health
Science Program, 4Department of
Nutrition, 5Department of Clinical
Medicine, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Background: The aim of this study was to investigate the influence of body mass index,
body weight, lean mass, fat mass, and basal energy expenditure on bone mineral density in
postmenopausal women. Methods: This was a cross-sectional, descriptive study of a sample of 50 women, with mini-
mum time since menopause between 1 and 10 years. Bone mineral density was assessed at
the lumbar spine (L2–L4), femoral neck, Ward’s triangle, and trochanter using dual-energy
X-ray absorptiometry. Body mass index, lean mass, fat mass, and basal energy expenditure
were measured by bioimpedance. Results: The mean age of the women was 51.49 3.86 years and time since menopause was 3.50
2.59 years. Significant negative correlations were found between chronological age and lumbar
spine, femoral neck, Ward’s triangle, and trochanteric bone mineral density. In regard to time
since menopause, we also observed significant negative correlations with bone mineral density at
the lumbar spine and Ward’s triangle. The following significant positive correlations were
recorded: body mass index with bone mineral density at the femoral neck and trochanter; fat mass
with bone mineral density at the femoral neck and trochanter; lean mass with bone mineral density
at the lumbar spine, femoral neck, and trochanter; and basal energy expenditure with bone mineral
density at all sites assessed. On the other hand, the multiple linear regression model showed that:
20.2% of bone mineral density variability at the lumbar spine is related to lean mass and time
since menopause; 22.3% of bone mineral density variability at the femoral neck is related to body
weight and age; 18.9% of bone mineral density variability at Ward’s triangle is related to age and
basal energy expenditure; and 39% of bone mineral density vari-ability at the trochanter is related
to body mass index, age, and menarche. Conclusion: Changes in bone mineral density, specific for each skeletal site, are influenced
by age, time since menopause, body weight, body mass index, lean mass, and basal energy
expen-diture. Lean mass and basal energy expenditure positively influenced bone mineral
density at the lumbar spine and Ward’s triangle, with a predominance of trabecular bone. Keywords: women, menopause, bone mineral density, body composition, energy
expenditure Correspondence: José Brandão-Neto Av Gal Gustavo Cordeiro de Farias, s/n, Natal-RN, CEP 59012-
570, Brazil Tel 55 84 3342 9748 Fax 55 84 3342 9776
Email [email protected]
Introduction Demographic changes predicted for the next 50 years indicate that the number of
elderly people will increase worldwide, together with metabolism-related diseases.1
Among these, osteoporosis in postmenopausal women is recognized as an important
public health problem because it is associated with a high risk of fracture, elevated
morbidity and mortality rates, and incurs high financial and societal costs.2
42 Quirino et al Dovepress
Bone mineral density (BMD) increases during childhood,
adolescence, and early adulthood, until reaching peak bone
mineralization. It is a negative predictor of osteoporosis and
risk of fracture over time, and is influenced by genetic,
mechanical, nutritional, and hormonal factors.3
Peak bone mineralization in the entire skeleton, occurring
on average at 18 years of age, varies little up to the age of 50
years, with a slight and progressive increase in BMD of
around 0.2% per year in cortical bone-rich regions. However,
in areas with a larger amount of trabecular bone, such as the
proximal femur and the inner area of the vertebral body, an
immediate decline is initiated at the age of 18 years, with an
annual loss in BMD of 0.3% (trochanter), 0.4% (femoral
neck), 0.6% (Ward’s triangle), and 0.5% (lumbar spine).4 This
reveals a 50% loss of BMD, mainly in Ward’s triangle. One
study indicates that a 10% increase in peak bone miner-
alization could delay the development of osteoporosis by 13
years, while a 10% increase in time since menopause would
delay it by only 2 years.5
As with BMD, lean mass in the third decade of life varies
little until the fifth decade, showing a sharp decline from the
sixth decade onwards.6 The difference in muscle strength
between young and elderly individuals is less when these
values were adjusted for lean mass and muscle mass.7
Menopause is associated with diminished serum estrogen
levels, which may provoke a decrease in BMD and lean mass,
and a rise in body fat.8 These alterations can affect gait and
balance in the elderly,9 reducing physical activity at work,
home, during leisure time, and in sport. This causes a decline
in total and basal energy expenditure, which is influenced by
age, sex, body composition, and hormonal factors, including
estrogen.10–12
Studies show that body weight has a positive influence on
BMD.13–15
However, this influence is different between
skeletal sites.15
There is no consensus regarding the effect of
body composition on BMD. Some research has shown that fat
mass and lean mass are correlated with lumbar spine and hip
BMD, respectively.15
However, other studies demonstrate
that obesity does not protect against fracture in
postmenopausal women. On the contrary, it is associated with
an increased risk of ankle and femur fractures.16
Lean mass
plays a relevant role in BMD, possibly acting positively on
cortical bone mass.17
Aging is accompanied by a decrease in lean mass and
basal energy expenditure.11
Individuals with low basal energy
expenditure are predisposed to gaining weight at the expense
of a proportional increase in fat mass.10,11
Studies show a
posi-tive association between basal energy expenditure and
BMD in North American women, which is much more
significant than body weight.10,11
In order to understand the impact of body composition on
BMD in the first 10 years after menopause, we studied the
influence of age, time since menopause, body mass index, fat
mass, and basal energy expenditure on lumbar spine, femoral
neck, Ward’s triangle, and trochanteric BMD. Materials and methods Patients and study design This was a cross-sectional, quantitative, descriptive study
performed at the Lauro Wanderley University Hospital
gynecology outpatient clinic of the Universidade Federal da
Paraíba, Brazil. Participants were selected from those
responding to posters put up at the hospital, university cam-
pus, and family health units in nearby neighborhoods. The
sample consisted of 50 women with minimum and maximum
time since postmenopause of one and 10 years, respectively,
and body mass index between 18.5 and 39.9 kg/m2. A stan-
dard deviation of 6 and maximum error of estimation of 20%
were used to calculate sample size, with a 5% significance
level. All the women in the study were of mixed ethnicity.
Exclusion criteria were: use of hormone replacement therapy;
immunosuppressants, glucocorticoids, diuretics, anticon-
vulsants, or calcium supplementation; tobacco or alcoholic
beverages; previous surgery (colostomy and oophorectomy);
and history of disease (neoplasia, diabetes mellitus, liver,
kidney, and thyroid disorders, and rheumatoid arthritis).
All participants gave written informed consent. The
project was approved by the research ethics committee of
Lauro Wanderley University Hospital, Universidade Federal
da Paraíba (protocol number 335/03). After assessment, the
women were referred for specialized clinical follow-up. Instruments and data
collection procedures A form was used to record sociodemographic, clinical, and
anthropometric data. Weight and height were measured while
fasting and after bladder emptying. Subjects were barefoot,
wearing Bermuda shorts and a t-shirt, and standing in the
bipedal position, with their chin parallel to the floor. The
head, buttocks, and heels were aligned with the stadiometer
of a 150 kg anthropometric scale in 100 g increments and a 2
m metal rod in 1 cm increments (Filizola, Personalline E, São
Paulo, Brazil). Body mass index was calculated to obtain
classification of nutritional status as follows: eutrophic at
18.5–24.9 kg/m2; overweight at 25.0–29.9 kg/m
2; and first-
degree obesity at 30–34.9 kg/m2, in accordance with World
43 Dovepress BMD in postmenopausal women Health Organization criteria.18 Next, we determined basal energy
expenditure, fat mass, and lean mass by bioimpedance (RJL
Systems, Quantum II, Clinton Twp, MI). All care was taken to
inform subjects adequately regarding bioimpedance
procedures.12,19 Bone densitometry was conducted using dual energy x-ray
absorptiometry (Lunar DPX-L; Lunar Radiation Corporation,
Madison, WI), in order to measure BMD at L2–L4, femoral
neck, Ward’s triangle, and the trochanter. Results were
calculated by bone area (cm²) and bone mineral content (g), with
BMD expressed in g/cm2. World Health Organization criteria
were used to classify BMD, as normal, osteopenic, or
osteoporotic.20 Statistical analyses Data were analyzed using the Statistical Package for the Social
Sciences (SPSS) version 16.0 (IBM Corporation, Armonk, NY).
To characterize sociodemographic, anthro-pometric,
bioimpedance, and BMD variables, descriptive statistics
procedures such as central tendency (mean) and dispersion
(standard deviation) measures were applied. Pearson’s
correlation coefficient (r) was used to determine the relationship
between independent (time since menopause, age, age of
menarche, body mass, body mass index, basal energy
expenditure, lean mass, and fat mass) and dependent variables
(lumbar spine, femoral neck, Ward’s triangle, and trochanteric
BMD). The Chi-squared test was used to verify the association
between nutritional status (eutrophy, over-weight, obesity) and
diagnostic classification of BMD (nor-mal, osteopenic, and
osteoporotic). Results with P # 0.05 were considered to be
statistically significant. Multiple linear regression was used to
evaluate linear predictor functions.
Results A total of 50 women completed the study, with a mean age of
51.49 3.86 years and mean time since menopause of 3.50
2.59 years. None of the participants were illiterate; 40 were
able to read and write, 44 had secondary school education,
and 16% were educated to university level. Moreover, 62%
had a household income of up to three minimum monthly
wages (US$795), 24% had four to six minimum wages
(US$1060–US$1590) and 14% had seven to ten minimum
wages (US$1860–US$2650). With respect to professional
activity, 64% were economically active, 16% were retired,
and 20% were homemakers.
Descriptive statistics for bioanthropometric results are
shown in Table 1. The results for BMD and its diagnos-tic
classification are shown in Table 2. There was a high
Table 1 Bioanthropometric characteristics Variables Mean SD Minimum–maximum
Age (years) 51.49 3.86 45–58 Menopause (years) 3.5 2.59 1–10 Menarche (years) 13.04 1.67 10–17 Body mass (kg) 63.84 10.5 44–86.7 Height (m) 1.52 0.06 1.43–1.65 BMI (kg/m2) 27.49 4.74 19.3–39.9 Body water (kg) 31.04 3.19 26–39 LM (kg) 41.58 4.9 31–51 FM 21.92 6.78 11–36 BEE (BIA) 1354 102.38 1159–1554 Lumbar spine BMD 1.04 0.18 0.69–1.52 Femoral neck BMD 0.9 0.11 0.68–1.29 Ward’s triangle BMD 0.77 0.17 0.44–1.2 Trochanteric BMD 0.75 0.11 0.58–1.08 Abbreviations: BMI, body mass index; LM, lean mass; FM, fat mass; BEE, basal
energy expenditure; BIA, bioelectrical impedance analysis; BMD, bone mineral
density; SD, standard deviation.
occurrence of osteopenia at all skeletal sites, and 24% and 12%
of osteoporosis at skeletal sites L2–L4 and Ward’s triangle,
respectively.
Figure 1 shows the occurrence of normal BMD, osteope-nia,
and osteoporosis in women with eutrophic nutritional status,
overweight, and obesity. There was a significant asso-ciation
between BMD at all skeletal sites and the differing nutritional
status of the patients.
Table 3 shows the relationship between independent
variables and BMD at all skeletal sites studied. Basal energy
expenditure (bioelectrical impedance analysis) had a positive
correlation with all skeletal sites studied.
Table 4 presents the multiple linear regression model,
demonstrating that 20.2% of BMD variability at the lumbar spine
was related to lean mass and time since menopause, 22.3% of
BMD variability at the femoral neck was related to body weight
and age, 18.9% of BMD variability at Ward’s triangle was
related to age and basal energy expenditure, and 39% of BMD
variability at the trochanter was related to body mass index, age,
and menarche.
Table 2 Bone mineral density (g/cm2) and diagnostic
classification of bone mineral density at four skeletal sites Variables Normal Osteopenia Osteoporosis
N % n % N %
LS 18 36 20 40 12 24 FN 26 52 24 48
WT 20 40 25 50 5 10 T 34 68 16 32 Abbreviations: BMD, bone mineral density; LS, lumbar spine (L2–L4); FN,
femoral neck; WT, Ward’s triangle; T, trochanter.
44
Quirino et al Dovepress
A B
100 100
(%)
Lu
mb
ar 80
( % ) F e m o r a l
80
sp
ine 60
nec
k 60
40 40
BM
D
20
B M D
20
0 0
Eutrophic Overweight Obesity Normal Osteopenia Osteoporosis
Eutrophic Overweight Obesity
Normal Osteopenia
C
Wa
rd’s
tria
ng
le
(%)B
MD
D
100
Tro
ch
an
ter 100
80 80
60 60
40
(%) 40
20
BM
D
20
0 0
Eutrophic Overweight Obesity Eutrophic Overweight Obesity Normal Osteopenia Osteoporosis Normal Osteopenia
Figure 1 Relationship between BMD (normal, osteopenic, and osteoporotic) and nutritional status (eutrophia, overweight, and obesity) in menopausal patients. Notes: Chi-square test (P , 0.05): association between diagnostic classification of BMD and nutritional status of lumbar spine (A) (χ² 9.83; df 4, P , 0.05); in the femoral
neck (B) (χ² 12.77; df 2, P , 0.01); in Ward’s triangle (C) (χ² 12.74; df 4, P , 0.05); and in the trochanter (D) (χ² 9.23; df 2, P , 0.01). Bars are shown as
percentage. Abbreviation: BMD, bone mineral density.
Discussion In the present study, we observed osteopenia at all skeletal sites under study and osteoporosis only at L2–L4 (24%) and
Ward’s triangle (10%). There were significant negative cor-relations between age and BMD at all skeletal sites analyzed.
However, with time since menopause, significant negative
correlations were recorded only for bone mineral density at the lumbar spine and Ward’s triangle. In this respect, Guthrie
et al21
demonstrated that the degree of bone loss at the
lumbar spine and femoral neck was similar, although the rate
of such loss was greater at the lumbar spine in the early Table 3 Correlation coefficients (Pearson) between bioanthro-
pometric variables and bone mineral density Independent Dependent variables
variables
LS FN WT T
Age (years) 0.315* 0.303* 0.311* 0.332*
Menopause (years) 0.338* 0.202 0.304* 0.194
Menarche (years) 0.263 0.256 0.179 0.454**
BW (kg) 0.267 0.368** 0.268 0.454**
BMI (kg/m2) 0.188 0.367** 0.258 0.463**
LM (kg) 0.311* 0.343* 0.257 0.336*
FM (kg) 0.227 0.348* 0.225 0.454**
BEE (BIA) 0.281* 0.355* 0.292* 0.376**
Notes: *Statistical significance (P , 0.05); **statistical significance (P , 0.01).
Abbreviations: BW, body weight; BMI, body mass index; LM, lean mass; FM, fat
mass; BEE, basal energy expenditure; BIA, bioelectrical impedance analysis; BMD,
bone mineral density; LS, lumbar spine (L2–L4); FN, femoral neck; WT, Ward’s
triangle; T, trochanter.
postmenopausal years. This indicates significant BMD loss in the
first 3 years after menopause in areas with a predominance
of trabecular bone. In an attempt to minimize these losses, studies have been
conducted to describe the protective effect of body weight on
BMD in menopausal women.13,14,22
In our study, we observed
significant positive correlations between body weight and BMD
at all skeletal sites studied, except for Ward’s triangle.
Michaelsson et al13
reported that body weight above 70 kg could
be used to exclude women from an osteoporosis pre-vention
program. This was contested by Bedogni et al,22
who
demonstrated that anthropometric measures could not be used to
classify individual bone mineral status, because there was no
evidence that body weight altered bone mineral status.
On the other hand, low body mass index may be asso-ciated
with lower BMD at the femoral neck, with greater risk of
osteoporotic fracture.17 Elevated body mass index could be
associated with ankle and femur fractures in post-menopausal
women.16 Therefore, these studies highlight the controversy
concerning the effect of body weight on maintaining BMD. The
protective effect of elevated weight on BMD in postmenopausal
women is attributed to adipose tissue, which may be an extra-
ovarian source of estrogen,23 and the magnitude of the
mechanical load to strengthen the osteogenic response.24 In a physiological state, mechanical overloads increase
muscle strength during physical activity. This muscle strength
45 Dovepress BMD in postmenopausal women
Table 4 Multiple linear regression model and predictive equations
Dependent R R2 Adjusted SE of Predictive equations* variables R2 estimate
LS 0.449 0.202 0.168 0.160 BMD 0.678 0.022 (age) 0.011 (LM) FN 0.473 0.223 0.190 0.109 BMD 1.096 0.004 (BW) 0.009 (TSM) WT 0.434 0.189 0.154 0.155 BMD 0.801 0.014 (age) 0.001 (BEE) T 0.624 0.390 0.350 0.094 BMD 1.152 0.009 (BMI) 0.008 (age) 0.018 (menarche) Note: *All statistical variables were significant (P , 0.05). Abbreviations: LS, lumbar spine; FN, femoral neck; WT, Ward’s triangle; TSM, time since menopause; T, trochanter; LM, lean mass; BW, body we ight; BEE, basal energy
expenditure; BMD, bone mineral density; BMI, body mass index; SE, standard error. acts on specific bone levers and modifies bone metabolism
to the point of stress.25
Thus, bone responds immediately
to the mechanical loads it bears,26
involving both cellular
and tissue reactions.27
During disuse, the metabolic
activity of bone tissue is suppressed. It is normalized by
brief expo-sure to very low mechanical stimuli,26
responding better to dynamic than static loads.28
In relation to body mass index and fat mass, the present
study revealed significant positive correlations (Table 3) only
with BMD at the femoral neck and trochanter. When these
variables were fit to the multiple linear regression model, a 0.9%
reduction in femoral neck BMD was observed for each year of
life and a 0.4% increase for each kg of body weight gain. For
trochanteric BMD, a 0.9% increase was associated with higher
body mass index. This indicated that excess weight, represented
by body fat, reinforces the biomechani-cal theory,24–28
given that
we found strong correlations with BMD in weightbearing areas
such as the femoral neck and trochanter. With respect to the
theory about an extraovarian source of estrogen, attributed to
adipose tissue,23
we question whether it could prevent bone loss
in these women, given that no significant positive correlations
were observed between fat mass and BMD at the lumbar spine or
Ward’s triangle (Table 3). These areas exhibit the greatest bone
density loss in the first years of menopause.21
One study showed
that fat mass was inversely correlated with bone mass,
suggesting that fat mass in itself does not have a protective effect
on bone mass.24
However, lean mass shows significant positive
correlations not only with BMD at the femoral neck and
trochanter, but also at the lumbar spine (L2–L4, Table 3). The
multiple linear regression model demonstrated a 2.2% reduction
in BMD at the lumbar spine for time since meno-pause and a
1.1% increase of that BMD for each kg of lean body mass (Table
4). This means that lean mass is represented primarily by the
large muscles, which transmit greater and more frequent
mechanical loads to the skeleton.24,29
Thus, lean mass and psoas
muscle volume at L3 were associated with low loss of BMD at
the lumbar spine, indicating the importance of applying
muscle strength at the site where BMD is maintained.30 In the
long run, the effect of strong dorsal extensor muscles reduced the
incidence of vertebral fracture in women with estrogen
deficiency.31 There is evi-dence that skeletal muscle is also an
extraovarian source of estrogen, and the capacity to synthesize
this hormone likely depends on the proportion of lean mass.32 Age is accompanied by an increase in fat mass, and a
decrease in BMD, lean mass, and basal energy expen-
diture,6,10,11,19
which may lead to disturbances in gait and
balance, and increased risk of falling.9,16
These factors may
generate insecurity, contribute to a sedentary lifestyle and
potentially induce changes in body composition to less lean mass
and more fat mass, culminating in sarcopenia.8,9
In post-
menopausal women from the fifth decade onwards, the drop in
estrogen levels has an important role in decreasing muscle mass.8
It was also demonstrated that basal energy expenditure falls with
menopause and is related to the decline in lumbar spine.19
In our
study, we observed a reduction of 1.4% in Ward’s triangle BMD
for each year of life and an increase of 0.1% in that BMD for
every calorie of basal energy expendi-ture (Table 4). Therefore,
in this area of predominance of tra-becular bone, the basal
energy expenditure improved BMD. This result corroborates the
study conducted by Choi and Pai,19
demonstrating that BMD is
more strongly correlated with basal energy expenditure than are
lumbar spine, fat mass, and body mass index. Additionally, basal
energy expenditure was the best covariable of bone mineral
content and BMD in a cohort of African-American women,11
displaying a strong correlation with hip and whole body BMD
when compared with other anthropometric measures.10
Furthermore, the present study also shows a significant
association between nutritional status and BMD. Overweight
women exhibited twice as much osteoporosis at the lumbar spine
and Ward’s triangle compared with eutrophic women, while the
femoral neck showed a 23.2% increase in osteopenia, indicating
that being overweight did not increase BMD (Figure 1). A
number of studies have demonstrated that obesity does not
protect
46 Quirino et al Dovepress
menopausal women against osteoporosis, and as such, is a risk
factor for fracture.16 One study reported that visceral adi-posity
and low-density lipoprotein were inversely associated with BMD
and that high-density lipoprotein was positively associated with
BMD.33 Finally, the present study, using the multiple linear
regression model, demonstrated BMD variability at the lumbar
spine related to lean mass and time since menopause, BMD
variability at the femoral neck related to body weight and age,
BMD variability at Ward’s triangle related to age and basal
energy expenditure, and BMD variability at the trochanter
related to body mass index, age, and menarche. Thus, a change
in lifestyle, and consequent increase in lean mass, along with a
rise in basal energy expenditure, could improve metabolic
disorders related to aging, obesity, and diabetes mellitus, thereby
minimizing BMD loss.
Conclusion In conclusion, we observed the occurrence of osteopenia at all
skeletal sites under study and osteoporosis only at L2–L4 and
Ward’s triangle. These areas are associated with lean mass and
basal energy expenditure, and could prevent osteoporosis. Given
that our study sample was not probabilistic, other studies with a
more representative population are needed.
Acknowledgment This study was supported by the National Council for Scien-
tific and Technological Development (472832/2011-5). Disclosure The authors report no conflicts of interest directly relevant
to the content or publication of this article.
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population ageing. Nature. 2008;451(7179):716–719. 2. Marks R. Hip fracture epidemiological trends, outcomes, and risk
factors, 1970–2009. Int J Gen Med. 2010;8(3):1–17. 3. Ackerman KE, Misra M. Bone health and the female athlete triad in
adolescent athletes. Phys Sportsmed. 2011;39(1):131–141. 4. Matkovic V, Jelic T, Wardlaw GM, et al. Timing of peak bone mass
in Caucasian females and its implication for the prevention of
osteoporosis. Inference from a cross-sectional model. J Clin Invest.
1994;93(2):799–808. 5. Hernandez CJ, Beaupre GS, Carter DR. A theoretical analysis of the
relative influences of peak BMD, age-related bone loss and
menopause on the development of osteoporosis. Osteoporos Int.
2003;14(10): 843–847.
6. Cheng Q, Zhu YX, Zhang MX, Li LH, Du PY, Zhu MH. Age and sex
effects on the association between body composition and bone
mineral density in healthy Chinese men and women. Menopause.
2012;19(4):448–455.
7. Frontera WR, Hughes VA, Lutz KJ, Evans WJ. A cross-sectional
study of muscle strength and mass in 45- to 78-yr-old men and
women. J Appl Physiol. 1991;71(2):644–650. 8. Messier V, Rabasa-Lhoret R, Barbat-Artigas S, Elisha B, Karelis
AD, Aubertin-Leheudre M. Menopause and sarcopenia: a potential
role for sex hormones. Maturitas. 2011;68(4):331–336. 9. Waters DL, Hale L, Grant AM, Herbison P, Goulding A. Osteoporosis
and gait and balance disturbances in older sarcopenic obese New
Zealanders. Osteoporos Int. 2010;21(2):351–357. 10. Afghani A, Barrett-Connor E. Resting energy expenditure: a stronger
marker than body weight for bone mineral density in white women
but not men? The Rancho Bernardo study. Clin J Sport Med. 2009;
19(1):39–45. 11. Afghani A, Barrett-Connor E, Wooten WJ. Resting energy
expenditure: a better marker than BMI for BMD in African-
American women. Med Sci Sports Exerc. 2005;37(7):1203–1210. 12. de Oliveira FCE, de Mello Cruz A, Oliveira CG, et al. Energy
expenditure of healthy Brazilian adults: a comparison of methods.
Nutr Hosp. 2008;23(6):554–561. Spanish. 13. Michaelsson K, Bergström R, Mallmin H, Holmberg L, Wolk A,
Ljunghall S. Screening for osteopenia and osteoporosis: selection by
body composition. Osteoporos Int. 1996;6(2):120–126. 14. Morin S, Tsang JF, Leslie WD. Weight and body mass index predict
bone mineral density and fractures in women aged 40 to 59 years.
Osteoporos Int. 2009;20(3):363–370. 15. Sheng Z, Xu K, Ou Y, et al. Relationship of body composition with
prevalence of osteoporosis in central south Chinese postmenopausal
women. Clin Endocrinol (Oxf). 2011;74(3):319–324. 16. Compston JE, Watts NB, Chapurlat R, et al. Obesity is not protective
against fracture in postmenopausal women: GLOW. Am J Med.
2011; 124(11):1043–1050. 17. Genaro PS, Pereira GAP, Pinheiro MM, Szejnfeld VL, Martini LA.
Influence of body composition on bone mass in postmenopausal
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Biol. 1999;26:561–568. 23. Suzuki N, Yano T, Nakazawa N, Yoshikawa H, Taketani Y. A
possible role of estrone produced in adipose tissues in modulating
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Relationship of obesity with osteoporosis. J Clin Endocrinol Metab.
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by disuse, is normalized by brief exposure to extremely low-magnitude
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Influence of muscle forces on femoral strain distribution. J
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30. Reeve J, Walton J, Russell L, et al. Determinants of the first decade
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1999;92(5): 261–273. 31. Sinaki M, Itoi E, Wahner H, et al. Stronger back muscles reduce the
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32. Larionov A, Vasyliev D, Mason J, Howie AF, Berstein LM, Miller
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International Journal of General Medicine Dovepress
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49
7 COMENTÁRIOS, CRÍTICAS E CONCLUSÕES
A experiência adquirida nesses anos dedicados ao presente estudo, mostrou
que o aprendizado ocorre de forma diversificada. Estudar o fenômeno do
envelhecimento humano relacionado com a dinâmica muscular revelou um enorme
potencial de investigação científica para a fisioterapia em um contexto interdisciplinar,
como foi referido na introdução.
O músculo é muito mais do que apenas um aparato mecânico. Ele é também
reconhecido como um órgão endócrino capaz de produzir e liberar citocinas (myokines)
em resposta à contração muscular(29). Essa descoberta proporciona uma mudança de
paradigma e revela novos horizontes científicos, tecnológicos e acadêmicos. A
caracterização dos efeitos biológicos de peptídeos (conhecidos e desconhecidos),
secretados durante a contração muscular, será objeto de investigação nesses próximos
anos(30).
Ficamos diante de grandes paradoxos: ações simples e sem custo para toda
pessoa capaz de contrair voluntariamente os músculos e tão negligenciada por muitos.
A contração muscular, que afeta o metabolismo de nutrientes, como a excreção de
zinco na restrição de atividade motora(22) depende de aspectos motivacionais e de
capacidade de fazer escolhas. Essas ações podem ser empreendidas no âmbito da
Atenção Básica de Saúde, com custo operacional muito baixo para prevenir o avanço
da osteoporose e do diabetes. Ao mesmo tempo, são publicadas novas patentes
biotecnológicas com base na identificação de novas miocinas e seus receptores,
podendo servir como alvos farmacológicos para o tratamento de doenças musculares,
de distúrbios metabólicos e de outras doenças associadas com o desuso muscular(31).
O projeto de pesquisa encaminhado para o processo seletivo do doutorado teve
o seguinte título: Correlação entre índice de recrutamento das unidades motoras e a
densidade mineral óssea em homens e mulheres sedentários de meia idade. Esse
projeto, que já estava em andamento, teve de ser abandonado por ter desabado
durante um final de semana, parte do teto do Laboratório e ter danificado a estrutura
elétrica e o equipamento, muito sensível, o que poderia comprometer a validade interna
da pesquisa.
50
Entretanto, nossa primeira publicação foi fruto de parte dos dados parciais desse
projeto e não só evidenciou significativas correlações positivas da massa magra com a
densidade mineral óssea (DMO) no colo do fêmur e trocânter, mas também com a
coluna lombar (L2-L4). O modelo de regressão linear múltipla mostrou que a redução
de 2,2% na DMO da coluna lombar, relacionada ao tempo da menopausa, pode ter
aumentado 1,1% por cada kg de massa magra, e na DMO do triângulo de Ward,
redução de 1,4%, relacionada com a idade, podendo ter um aumento de 0,1% para
cada caloria de gasto energético basal(8).
Motivada por esses achados e com a aquisição do Dinamômetro Isocinético,
“padrão ouro” para avaliação de desempenho muscular, pelo PPGCSA e Departamento
de Fisioterapia da UFRN, encaminhamos o projeto “Influência do zinco na performance
muscular em jovens e idosas” ao Comitê de Ética em Pesquisa do Centro de Ciências
da Saúde nº. 0193/09 (ANEXO). Posteriormente, concorremos ao Edital FAPERN
011/2009 – PPSUS III – Pesquisa para o SUS: Gestão Compartilhada em Saúde. O foi
aprovado e teve seus resultados apresentados no II CONGRESSO FAPERN DE
CIÊNCIA, TECNOLOGIA E INOVAÇÃO DO RIO GRANDE DO NORTE, em outubro de
2012.
Resultaram também em duas publicações uma em 2010(32,33) e outra em 2012(34)
projetos a que estou vinculada na UFPB e que também enfocam aspectos relacionados
com a motricidade humana.
Como base nos resultados desses estudos, temos elementos importantes para
programar ações de saúde que visem a recuperar a força, a resistência e o equilíbrio
muscular em idosas e prevenir a osteoporose(35) e, deste modo, poder contribuir para a
finalidade primordial da Política Nacional de Saúde da Pessoa Idosa (Portaria nº 2.528
de 19 de outubro de 2006). A referida portaria visa “recuperar, manter e promover a
autonomia e a independência dos indivíduos idosos”(28). O mais importante é que essa
ação seja fruto da avaliação prévia dessa comunidade, com os resultados voltados
para ela, e não apenas mero material de discurso acadêmico. Isso é possível, pois
essas unidades de saúde da família fazem parte das áreas de campo de estágio da
UFPB.
51
É importante salientar que foi uma tarefa árdua selecionar uma amostra de
mulheres com o perfil das mulheres do nosso estudo no âmbito das unidades de saúde
da família. Essas unidades de saúde, embora estivessem inseridas em um raio de
continuidade de aproximadamente dois quilômetros, tinham peculiaridades marcantes
entre si. Em uma delas, onde o perfil socioeconômico revelou escores mais baixos,
nenhuma mulher com idade entre os 60 e os 80 anos atendeu aos critérios de inclusão
no estudo. Revelaram adoecimento precoce em relação às mulheres da mesma idade
das mulheres das outras unidades de saúde do estudo.
Também nos chamou a atenção o fato de os escores de atividade física das
mulheres jovens terem sido menores (Tabela 1 do artigo 1) que os escores das idosas.
Isso nos coloca em situação de alerta sobre essas jovens, pois assumem um estilo de
vida sedentário e com escolhas de alimentos que eram mais práticos em detrimento do
aspecto nutricional. Essas jovens são potenciais- alvo de cuidados preventivos para o
envelhecimento sadio futuro.
Agora será mais fácil estimular a prática de um estilo de vida mais sadio para a
população deste estudo, porquanto elas foram os atores principais e vivenciaram,
durante a pesquisa, mudanças em suas sensações e em suas ações.
Essas ações também podem ser incentivadas na Atenção Básica de Saúde, em
todos os municípios do Brasil, uma vez que é uma ação efetiva e de baixo custo.
52
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55
ANEXO A
56
APÊNDICE A
UNIVERSIDADE FEDERAL DA PARAIBA CENTRO DE CIENCIAS DA SAÚDE
DEPARTAMENTO DE FISIOTERAPIA
TTEERRMMOO DDEE CCOONNSSEENNTTIIMMEENNTTOO LLIIVVRREE EE EESSCCLLAARREECCIIDDOO
Título do Projeto
Influencia do zinco na performance muscular em jovens e idosos
Profa. Maria Aparecida Bezerra Quirino (Fisioterapeuta/UFPB, Doutoranda/PPGSA/UFRN) Prof. Dr. José Brandão Neto (Médico-Endocrinologista/UFRN-Orientador).
O propósito desta pesquisa é de estudar as relações entre performance muscular
(torque isocinético, potência e fadiga) do músculo quadríceps e dos ísquios tibiais em
mulheres idosas e mulheres jovens e correlacioná-las com o nível de atividade física e
a nutrição de zinco.
Neste estudo a Sra. (Srta) irá responder a um formulário de perfil social, demográfico e
de saúde, um questionário sobre o desempenho de atividade física habitual e avaliação
nutricional. Fará exames laboratoriais, com coleta de sangue e urina. Também será
avaliada sua capacidade de força muscular, flexibilidade e fadiga. Estes dois últimos
exames serão realizados na UFRN na Cidade de Natal –RN, e haverá, portanto, um
deslocamento de automóvel particular com duração da viagem de aproximadamente 4
horas (ida e vinda), guiado por motorista particular e profissional. Os resultados dos
testes serão entregues e explicados para a compreensão do seu estado de saúde.
Faremos um acompanhamento do tratamento com suplementação de zinco em doses
fisiológica (25 mg Zn++ na forma de ZnSO4.7H2O) durante um período de três meses e
repetiremos todas as avaliações iniciais. Como se trata de um estudo duplo cego nem
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a pesquisadora nem o voluntário saberão qual é o seu grupo, se o placebo ou
experimental.
Não encontramos na literatura relatos de riscos conhecidos com a administração oral
de 25 mg do elemento zinco. Nos outros procedimentos de avaliação, todos os
cuidados com a biossegurança serão respeitados.
Os resultados desta pesquisa poderão ser publicados para informação e benefício de
todos os profissionais envolvidos diretamente com a área da saúde, embora sua
identidade permaneça anônima. Seu nome não será publicado ou usado sem seu
consentimento. Sua recusa não vai, de maneira alguma, envolver penalidade ou perda
de benefícios. Sua participação é estritamente voluntária e a Sra. (Sta.) pode retirar-se
desta pesquisa a qualquer hora.
Se em qualquer momento sentir que houve infração de seus direitos, deve contatar o
Comitê de Ética em Pesquisa do Centro de Ciências da Saúde da UFPB para
respostas sobre qualquer questão da pesquisa e de seus direitos, ou a Professora
Maria Aparecida Bezerra Quirino, pelo telefone: (83) 3216-7183. End.: Departamento
de Fisioterapia/ Centro de Ciências da Saúde /UFPB – Campus I.
Diante do exposto, eu admito que revisei totalmente o conteúdo deste termo de
consentimento, estando participando deste estudo de livre e espontânea vontade.
Desta forma, aceito participar do estudo fazendo parte de qualquer um dos grupos.
________________________________________ ____________
Assinatura do voluntário, Número da identidade
________________________________________
Testemunha
Impressão digital do participante
_________________________________________________________ Pesquisadora Profa. Maria Aparecida Bezerra Quirino (Assinatura) Data: ___/___/___
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