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1.  Periodontal Disease Status in Gullah African Americans with Type 2 Diabetes living in South Carolina 
Journal of periodontology  2009;80(7):1062-1068.
African Americans have a disproportionate burden of diabetes. Gullah African Americans are the most genetically homogeneous population of African descent in the US, with an estimated European Caucasian admixture of only 3.5%. This study assessed the previously unknown prevalence of periodontal disease among a sample of Gullah African Americans with diabetes and investigated the association between diabetes control and presence of periodontal disease.
Gullah African Americans with Type 2 diabetes (n=235) were included. Diabetes control was assessed by HbA1C, and divided into three categories: well controlled, <7%; moderately controlled, 7–8.5%; and poorly controlled, >8.5%. Participants were categorized as healthy, having no clinical attachment loss (CAL) or bleeding on probing (BOP); early periodontitis, having CAL ≥1 mm in ≥2 teeth; moderate periodontitis, having 3 sites with CAL ≥4 mm and at least 2 sites with probing depth (PD) ≥3 mm; and severe periodontitis, having CAL ≥6 mm in ≥2 teeth and PD ≥5 mm in ≥1 site. Observed prevalences of periodontitis were compared to rates reported for the NHANES studies.
All subjects had evidence of periodontal disease: 70.6% had moderate periodontitis and 28.5% had severe disease. Diabetes control was not associated with periodontal disease. The periodontal disease proportions were significantly higher than the reported national prevalence of 10.6% among African Americans without diabetes.
Our sample of Gullah African Americans with type 2 diabetes exhibits higher prevalence of periodontal disease than African Americans, both with and without diabetes, described in NHANES III and NHANES 1999–2000.
PMCID: PMC2862011  PMID: 19563285
Type 2 diabetes; Gullah African Americans; Periodontal disease
2.  Systemic Lupus Erythematosus and Vitamin D Deficiency Are Associated with Shorter Telomere Length among African Americans: A Case-Control Study 
PLoS ONE  2013;8(5):e63725.
Systemic lupus erythematosus (SLE) is a chronic systemic autoimmune disease that disproportionately affects African American females. The causes of SLE are unknown but postulated to be a combination of genetic predisposition and environmental triggers. Vitamin D deficiency is one of the possible environmental triggers. In this study we evaluated relationships between vitamin D status, cellular aging (telomere length) and anti-telomere antibodies among African American Gullah women with SLE. The study population included African American female SLE patients and unaffected controls from the Sea Island region of South Carolina. Serum 25-hydroxyvitamin D levels were measured using a nonchromatographic radioimmunoassay. Telomere length was measured in genomic DNA of peripheral blood mononuclear cells (PBMCs) by monochrome multiplex quantitative PCR. Anti-telomere antibody levels were measured by enzyme-linked immunosorbent assay (ELISA). Patients with SLE had significantly shorter telomeres and higher anti-telomere antibody titers compared to age- and gender-matched unaffected controls. There was a positive correlation between anti-telomere antibody levels and disease activity among patients and a significant correlation of shorter telomeres with lower 25-hydroxyvitamin D levels in both patients and controls. In follow-up examination of a subset of the patients, the patients who remained vitamin D deficient tended to have shorter telomeres than those patients whose 25-hydroxyvitamin D levels were repleted. Increasing 25-hydroxyvitamin D levels in African American patients with SLE may be beneficial in maintaining telomere length and preventing cellular aging. Moreover, anti-telomere antibody levels may be a promising biomarker of SLE status and disease activity.
PMCID: PMC3658981  PMID: 23700431
3.  The United States to Africa lupus prevalence gradient revisited 
Lupus  2011;20(10):1095-1103.
Systemic lupus erythematosus (SLE) is a systemic autoimmune disease that has a significantly higher prevalence, morbidity and mortality in African Americans compared with Americans of European descent. The pathogenesis of lupus is unclear but appears to be a result of environmental factors interacting with a genetically susceptible host. Despite the high disease load of SLE in African Americans, there is the perception that lupus is relatively rare in Africa. This prevalence gradient suggests that comparative studies of related cohorts from the two continents may provide insight into the genetic/environmental interactions that result in the development of lupus. To define if a lupus gradient exists, we began a study of autoimmunity prevalence utilizing two unique cohorts. The first is the Gullah population of the Sea Islands of South Carolina, who are unique in their low genetic admixture and their known ancestral heritage. The second is the population of young women served by the West Africa Fistula Foundation in Bo, Sierra Leone. Anthropologic studies indicate a direct ancestral link between the Gullah population and Sierra Leoneans. Since it is impossible to perform an epidemiologic study of lupus in Sierra Leone at this time, we assessed the prevalence of lupus serum autoantibodies, serologic evidence of specific infections and levels of serum 25-OH vitamin D in young women in the two cohorts who have no known relatives with lupus. Our results indicate similar prevalence of serum antinuclear antibodies in the two cohorts, though there was a significantly increased prevalence of antiphospholipid and anti-Sm antibodies in the Sierra Leone cohort. Seropositivity to common viral infections was significantly higher in women from Sierra Leone, while serum 25-OH vitamin D levels were markedly lower in the Gullah population. These data suggest that the prevalence of autoimmunity is similar in the two populations, but that there are significant environmental differences that may impact progression to autoimmune disease. Further studies comparing these two cohorts is likely to provide important insight into the impact of environmental factors on development of lupus.
PMCID: PMC3535487  PMID: 21917913
African American; lupus; prevalence gradient; vitamin D
4.  Intake of Seafood in the US Varies by Age, Income, and Education Level but Not by Race-Ethnicity 
Nutrients  2014;6(12):6060-6075.
Current US federal dietary guidance recommends regular consumption of seafood (fish + shellfish) to promote health; however, little is known about how well Americans meet the guideline, particularly population subgroups that may be at risk for inadequate intake. The purposes of this study were to describe the prevalence of seafood consumption and, among consumers, the amounts of seafood eaten by sex, age group, income and education level, and race-ethnicity. Data from 15,407 adults aged 19+ participating in the 2005–2010 National Health and Nutrition Examination Surveys were analyzed using methods to account for sporadic intake of seafood. Over 80% of Americans reported consuming any seafood over the past 30 days, 74% reported consuming fish, and 54% reported eating shellfish. The percentages varied by socio-demographic group. Younger age and lower income and education levels were associated with lower odds of being a seafood consumer (p < 0.0001). Among those who reported eating seafood, the average amount eaten of any seafood was 158.2 ± 5.6 g/week. Among seafood consumers, women and individuals of lower age and education levels consumed less seafood. Approximately 80%–90% of seafood consumers did not meet seafood recommendations when needs were estimated by energy requirements. A great deal of work remains to move Americans toward seafood consumption at current recommended levels.
PMCID: PMC4277015  PMID: 25533013
seafood intake; fish; shellfish
5.  Role of MYH9 and APOL1 in African and non-African populations with Lupus Nephritis 
Genes and Immunity  2011;13(3):232-238.
Systemic lupus erythematosus (SLE) is a complex autoimmune disease characterized by autoantibody production and organ damage. Lupus nephritis (LN) is one of the most severe manifestations of SLE. Multiple studies reported associations between renal diseases and variants in the non-muscle myosin heavy chain 9 (MYH9) and the neighboring apolipoprotein L 1 (APOL1) genes. We evaluated 167 variants spanning MYH9 for association with LN in a multiethnic sample. The two previously identified risk variants in APOL1 were also tested for association with LN in European-Americans (EAs) (N = 579) and African-Americans (AAs) (N = 407). Multiple peaks of association exceeding a Bonferroni corrected p-value of p < 2.03 × 10−3 were observed between LN and MYH9 in EAs (N=4620), with the most pronounced association at rs2157257 (p = 4.7 × 10−4; odds ratio [OR]=1.205). A modest effect with MYH9 was also detected in Gullah (rs8136069, p = 0.0019, OR = 2.304). No association between LN and MYH9 was found in AAs, Asians, Amerindians or Hispanics. This study provides the first investigation of MYH9 in LN in non-Africans and of APOL1 in LN in any population and presents novel insight into the potential role of MYH9 in LN in EAs.
PMCID: PMC3330160  PMID: 22189356
MYH9; APOL1; lupus nephritis; systemic lupus erythematosus; multiethnic association study
6.  Spatial Environmental Modeling of Autoantibody Outcomes among an African American Population 
In this study of autoimmunity among a population of Gullah African Americans in South Carolina, the links between environmental exposures and autoimmunity (presence of antinuclear antibodies (ANA)) have been assessed. The study population included patients with systemic lupus erythematosus (n = 10), their first degree relatives (n = 61), and unrelated controls (n = 9) where 47.5% (n = 38) were ANA positive. This paper presents the methodology used to model ANA status as a function of individual environmental influences, both self-reported and measured, while controlling for known autoimmunity risk factors. We have examined variable dimension reduction and selection methods in our approach. Following the dimension reduction and selection methods, we fit logistic spatial Bayesian models to explore the relationship between our outcome of interest and environmental exposures adjusting for personal variables. Our analysis also includes a validation “strip” where we have interpolated information from a specific geographic area for a subset of the study population that lives in that vicinity. Our results demonstrate that residential proximity to exposure site is important in this form of analysis. The use of a validation strip network demonstrated that even with small sample numbers some significant exposure-outcome relationships can be detected.
PMCID: PMC3987002  PMID: 24608900
lupus; autoimmunity; African Americans; environmental metals; soil; groundwater; spatial
7.  African-American mitochondrial DNAs often match mtDNAs found in multiple African ethnic groups 
BMC Biology  2006;4:34.
Mitochondrial DNA (mtDNA) haplotypes have become popular tools for tracing maternal ancestry, and several companies offer this service to the general public. Numerous studies have demonstrated that human mtDNA haplotypes can be used with confidence to identify the continent where the haplotype originated. Ideally, mtDNA haplotypes could also be used to identify a particular country or ethnic group from which the maternal ancestor emanated. However, the geographic distribution of mtDNA haplotypes is greatly influenced by the movement of both individuals and population groups. Consequently, common mtDNA haplotypes are shared among multiple ethnic groups. We have studied the distribution of mtDNA haplotypes among West African ethnic groups to determine how often mtDNA haplotypes can be used to reconnect Americans of African descent to a country or ethnic group of a maternal African ancestor. The nucleotide sequence of the mtDNA hypervariable segment I (HVS-I) usually provides sufficient information to assign a particular mtDNA to the proper haplogroup, and it contains most of the variation that is available to distinguish a particular mtDNA haplotype from closely related haplotypes. In this study, samples of general African-American and specific Gullah/Geechee HVS-I haplotypes were compared with two databases of HVS-I haplotypes from sub-Saharan Africa, and the incidence of perfect matches recorded for each sample.
When two independent African-American samples were analyzed, more than half of the sampled HVS-I mtDNA haplotypes exactly matched common haplotypes that were shared among multiple African ethnic groups. Another 40% did not match any sequence in the database, and fewer than 10% were an exact match to a sequence from a single African ethnic group. Differences in the regional distribution of haplotypes were observed in the African database, and the African-American haplotypes were more likely to match haplotypes found in ethnic groups from West or West Central Africa than those found in eastern or southern Africa. Fewer than 14% of the African-American mtDNA sequences matched sequences from only West Africa or only West Central Africa.
Our database of sub-Saharan mtDNA sequences includes the most common haplotypes that are shared among ethnic groups from multiple regions of Africa. These common haplotypes have been found in half of all sub-Saharan Africans. More than 60% of the remaining haplotypes differ from the common haplotypes at a single nucleotide position in the HVS-I region, and they are likely to occur at varying frequencies within sub-Saharan Africa. However, the finding that 40% of the African-American mtDNAs analyzed had no match in the database indicates that only a small fraction of the total number of African haplotypes has been identified. In addition, the finding that fewer than 10% of African-American mtDNAs matched mtDNA sequences from a single African region suggests that few African Americans might be able to trace their mtDNA lineages to a particular region of Africa, and even fewer will be able to trace their mtDNA to a single ethnic group. However, no firm conclusions should be made until a much larger database is available. It is clear, however, that when identical mtDNA haplotypes are shared among many ethnic groups from different parts of Africa, it is impossible to determine which single ethnic group was the source of a particular maternal ancestor based on the mtDNA sequence.
PMCID: PMC1618861  PMID: 17038170
8.  Periodontal disease progression and glycaemic control among Gullah African Americans with type-2 diabetes 
To evaluate associations between glycaemic control and periodontitis progression among Gullah African Americans with type-2 diabetes mellitus (T2DM).
Materials and Methods
From an ongoing clinical trial among T2DM Gullah, we extracted a cohort previously in a cross-sectional study (N 5 88). Time from baseline (previous study) to follow-up (trial enrollment, before treatment interventions) ranged 1.93–4.08 years [mean 5 2.99, standard deviation (SD) = 0.36]. We evaluated tooth site-level periodontitis progression [clinical attachment loss (CAL) worsening of ≥ 2 mm, periodontal probing depth (PPD) increases of ≥ 2 mm and bleeding on probing (BOP) from none to present] by glycaemic control status (well-controlled = HbA1c < 7%, poorly-controlled = HbA1c ≥ 7%) using multivariable generalized estimating equations logistic regression, nesting tooth sites/person.
Poorly-controlled T2DM (68.18%) was more prevalent than well-controlled T2DM (31.82%). Proportions of tooth sites/person with CAL progression between baseline and follow-up ranged 0.00–0.59 (mean = 0.12, SD = 0.12), while PPD and BOP progression ranged 0.00–0.44 (mean = 0.09, SD = 0.11) and 0.00–0.96 (mean = 0.24, SD = 0.18), respectively. Site-level PPD at baseline was a significant effect modifier of associations between poorly-controlled T2DM and site-level CAL and PPD progression [adjusted odds ratios (OR) according to poorly-controlled T2DM among PPD at baseline = 3, 5 and 7 mm, respectively: CAL progression = 1.93, 2.64, and 3.62, PPD progression = 1.98, 2.76, and 3.84; p < 0.05 for all]. Odds of site-level BOP progression were increased (OR = 1.24) for poorly-controlled T2DM, yet the results were not significant (p = 0.32).
These findings from a distinct, homogenous population further support the clinical relevance of identifying patients with poor glycaemic control and periodontitis, particularly among those with disparities for both diseases.
PMCID: PMC2891073  PMID: 20507373
diabetes; glycaemic control; Gullah African Americans; multivariable regression analysis; progression of periodontal disease
9.  Metabolic Syndrome and Periodontitis in Gullah African Americans With Type 2 Diabetes Mellitus 
To assess associations of metabolic syndrome, and its individual components, with extent of severe periodontitis among patients with type 2 diabetes mellitus (T2DM).
Materials and Methods
We performed a secondary data analysis (N=283) using a cross-sectional study population of Gullah African Americans with T2DM. Extent of severe periodontitis was assessed as total diseased tooth-sites/person (evaluated as separate outcomes: 6+mm clinical attachment level [CAL], 5+mm periodontal probing depth [PPD]) using negative binomial regression techniques. Primary independent variables assessed in separate models included metabolic syndrome (yes/no), each metabolic syndrome component (low HDL, hypertension, high triglycerides, large waist circumference) and glycemic control (poor/good).
Multivariable CAL-model results showed a significant association for metabolic syndrome status with extent of severe periodontitis (RR=2.77, p=0.03). The separate multivariable CAL-model including each metabolic syndrome component showed marginally increased rates among those with large waist circumference (RR=2.33, p=0.09) and those with HbA1c ≥ 7% (RR=1.73, p=0.06). Multivariable PPD-models showed marginally increased rates among those with metabolic syndrome (RR=2.18, p=0.06).
Metabolic syndrome is associated with the extent of severe periodontitis in this Gullah population with T2DM.
PMCID: PMC3664194  PMID: 23557538
Metabolic syndrome; diabetes mellitus; obesity; periodontitis; Gullah population
10.  Health insurance status is associated with periodontal disease progression among Gullah African Americans with type-2 diabetes mellitus 
Assess periodontal disease progression among Gullah-African-Americans with Type-2 diabetes-mellitus (T2DM) according to health insurance coverage.
From an ongoing clinical trial among T2DM Gullah, we extracted a cohort that was previously enrolled in a cross-sectional study (N=93). Comparing prior exam to trial initiation, total tooth-sites/person with periodontal-disease-progression-events (evaluated separately: 2+mm of clinical-attachment-loss [CAL], 2+mm increased periodontal-probing-depths [PPD], bleeding-on-probing [BOP] emergence) were evaluated according to health insurance coverage using regression techniques appropriate for data with different counts of potential events per subject (varying tooth-sites available). We used negative-binomial regression techniques to account for overdispersion and fit multivariable models that also included baseline glycemic-control (poor: glycated-hemoglobin ≥7%, well: glycated-hemoglobin <7%), history of established-periodontitis, age, gender, body-mass-index (BMI), annual income, and oral hygiene behaviors. Final models included health insurance status, other significant predictors, and any observed confounders.
Privately-insured were most prevalent (41.94%), followed by uninsured (23.66%), Medicare (19.35%), and Medicaid (15.05%). Those with poor-glycemic-control (65.59%) were more prevalent than well-controlled (34.41%). CAL-events ranged 0–58.8% tooth-sites/person (11.83±12.44%), while PPD-events ranged 0–44.2% (8.66±10.97%) and BOP-events ranged 0–95.8% (23.65±17.21%). Rates of CAL-events were increased among those who were uninsured (RR=1.75, p=0.02), Medicare-insured (RR=1.90, p=0.03), and Medicaid-insured (RR=1.89, p=0.06).
Increased access to healthcare, including dental services, may achieve reduction in chronic periodontal disease progression (as determined by CAL) for this study population. These results are very timely given the March 2010 passing of the U.S. healthcare reform bills.
PMCID: PMC4234040  PMID: 21774138
negative binomial regression; periodontal disease; periodontal disease progression; diabetes; Gullah African Americans; access to healthcare; health insurance; glycemic-control; income
11.  Health of Gullah families in South Carolina with Type 2 diabetes: Diabetes self-management analysis from Project SuGar 
The Diabetes educator  2009;35(1):117-123.
The purpose of this study was to describe diabetes self-management practices and service utilization among Gullah families in South Carolina.
Data were obtained from 1,276 persons with type 2 diabetes through interviews using the Family Health History Questionnaire. This was a primary analysis of a project conducted in conjunction with a parent study (Project SuGar) which focused on the molecular aspects of diabetes. Descriptive statistics were used for data analysis.
Diabetes self-management behaviors were not consistent with recommendations from the American Diabetes Association. Over half (55.6%) reported exercising, but only 27.7% reported self-glucose monitoring. Service utilization was poor, less than half, (41.1%) reported referral to a diabetic class/diet, 32.8% reported making yearly visits to the ophthalmologist; 22.3% reported visiting the dentist, and only 12.8% reported visiting the podiatrist.
Although some self-management behaviors were identified, Gullah family members remain at risk for preventable diabetes complications. Education must reflect behaviors and beliefs valued by Gullah individuals. Culturally appropriate educational programs may increase use of health care services aimed at decreasing preventable complications of type 2diabetes in the Gullah population.
PMCID: PMC2709834  PMID: 19244567
12.  Quality of life in patients with systemic lupus erythematosus (SLE) compared with related controls within a unique African American population 
Lupus  2011;21(5):563-569.
The patient’s perspective of how their health affects their function is health-related quality of life (HRQOL). HRQOL is poorer in patients with systemic lupus erythematosus (SLE). Few HRQOL studies in SLE patients have focused on African Americans despite an increased disease burden compared with Caucasians. The African American Gullah population of South Carolina has a homogeneous genetic and environmental background and a high prevalence of multi-patient families with SLE. Demographics, medical history, and Short-Form 36 (SF-36) were measured within a cohort of Gullah SLE cases and related controls. Compared with related controls (n = 37), cases (n = 89) had a lower Physical Component Summary (PCS, 41.8 vs. 52.3, p < 0.01), but not Mental Component Summary (MCS, 55.0 vs. 56.0, p = 0.70). The difference in PCS was no longer significant upon adjustment for working status, disability, and medical conditions. None of the 11 SLE American College of Rheumatology criteria, disease duration, or Systemic Lupus International Collaborating Clinics Damage Index were associated with either PCS or MCS. Cases and controls had similar MCS scores. We hypothesize that this lack of effect of SLE on MCS may be due to disease-coping mechanisms interplaying with cultural factors unique to the Gullah.
PMCID: PMC3535475  PMID: 22031537
quality of life; SLE; systemic lupus erythematosus
13.  Variable association of reactive intermediate genes with systemic lupus erythematosus (SLE) in populations with different African ancestry 
The Journal of rheumatology  2013;40(6):842-849.
Little is known about the genetic etiology of systemic lupus erythematosus (SLE) in individuals of African ancestry, despite its higher prevalence and greater disease severity. Overproduction of nitric oxide (NO) and reactive oxygen species are implicated in the pathogenesis and severity of SLE, making NO synthases and other reactive intermediate related genes biological candidates for disease susceptibility. This study analyzed variation in reactive intermediate genes for association with SLE in two populations with African ancestry.
A total of 244 SNPs from 53 regions were analyzed in non-Gullah African Americans (AA; 1432 cases and 1687 controls) and the genetically more homogeneous Gullah of the Sea Islands of South Carolina (133 cases and 112 controls) and. Single-marker, haplotype, and two-locus interaction tests were computed for these populations.
The glutathione reductase gene GSR (rs2253409, P=0.0014, OR [95% CI]=1.26 [1.09–1.44]) was the most significant single-SNP association in AA. In the Gullah, the NADH dehydrogenase NDUFS4 (rs381575, P=0.0065, OR [95%CI]=2.10 [1.23–3.59]) and nitric oxide synthase gene NOS1 (rs561712, P=0.0072, OR [95%CI]=0.62 [0.44–0.88]) were most strongly associated with SLE. When both populations were analyzed together, GSR remained the most significant effect (rs2253409, P=0.00072, OR [95%CI]=1.26 [1.10–1.44]). Haplotype and two-locus interaction analyses also uncovered different loci in each population.
These results suggest distinct patterns of association with SLE in African-derived populations; specific loci may be more strongly associated within select population groups.
PMCID: PMC3735344  PMID: 23637325
systemic lupus erythematosus; African Americans; genetic association studies; oxygen compounds; single nucleotide polymorphism
14.  Trans-Ancestral Studies Fine Map the SLE-Susceptibility Locus TNFSF4 
PLoS Genetics  2013;9(7):e1003554.
We previously established an 80 kb haplotype upstream of TNFSF4 as a susceptibility locus in the autoimmune disease SLE. SLE-associated alleles at this locus are associated with inflammatory disorders, including atherosclerosis and ischaemic stroke. In Europeans, the TNFSF4 causal variants have remained elusive due to strong linkage disequilibrium exhibited by alleles spanning the region. Using a trans-ancestral approach to fine-map the locus, utilising 17,900 SLE and control subjects including Amerindian/Hispanics (1348 cases, 717 controls), African-Americans (AA) (1529, 2048) and better powered cohorts of Europeans and East Asians, we find strong association of risk alleles in all ethnicities; the AA association replicates in African-American Gullah (152,122). The best evidence of association comes from two adjacent markers: rs2205960-T (P = 1.71×10−34, OR = 1.43[1.26–1.60]) and rs1234317-T (P = 1.16×10−28, OR = 1.38[1.24–1.54]). Inference of fine-scale recombination rates for all populations tested finds the 80 kb risk and non-risk haplotypes in all except African-Americans. In this population the decay of recombination equates to an 11 kb risk haplotype, anchored in the 5′ region proximal to TNFSF4 and tagged by rs2205960-T after 1000 Genomes phase 1 (v3) imputation. Conditional regression analyses delineate the 5′ risk signal to rs2205960-T and the independent non-risk signal to rs1234314-C. Our case-only and SLE-control cohorts demonstrate robust association of rs2205960-T with autoantibody production. The rs2205960-T is predicted to form part of a decameric motif which binds NF-κBp65 with increased affinity compared to rs2205960-G. ChIP-seq data also indicate NF-κB interaction with the DNA sequence at this position in LCL cells. Our research suggests association of rs2205960-T with SLE across multiple groups and an independent non-risk signal at rs1234314-C. rs2205960-T is associated with autoantibody production and lymphopenia. Our data confirm a global signal at TNFSF4 and a role for the expressed product at multiple stages of lymphocyte dysregulation during SLE pathogenesis. We confirm the validity of trans-ancestral mapping in a complex trait.
Author Summary
Systemic lupus erythematosus (SLE/lupus) is a complex disease in which the body's immune cells cause inflammation in one or more systems to cause the associated morbidity. Hormones, the environment and genes are all causal contributors to SLE and over the past several years the genetic component of SLE has been firmly established. Several genes which are regulators of the immune system are associated with disease risk. We have established one of these, the tumour-necrosis family superfamily member 4 (TNFSF4) gene, as a lupus susceptibility gene in Northern Europeans. A major obstacle in pinpointing the marker(s) at TNFSF4 which best explain the risk of SLE has been the strong correlation (linkage disequilibrium, LD) between adjacent markers across the TNFSF4 region in this population. To address this, we have typed polymorphisms in several populations in addition to the European groups. The mixed ancestry of these populations gives a different LD pattern than that found in Europeans, presenting a method of pinpointing the section of the TNFSF4 region which results in SLE susceptibility. The Non-European populations have allowed identification of a polymorphism likely to regulate expression of TNFSF4 to increase susceptibility to SLE.
PMCID: PMC3715547  PMID: 23874208
15.  Two Independent Functional Risk Haplotypes in TNIP1 are Associated with Systemic Lupus Erythematosus 
Arthritis and rheumatism  2012;64(11):3695-3705.
Systemic lupus erythematosus (SLE) is an autoimmune disease characterized by autoantibody production and altered type I interferon expression. Genetic surveys and genome-wide association studies have identified more than 30 SLE susceptibility genes. One of these genes, TNIP1, encodes the ABIN1 protein. ABIN1 functions in the immune system by restricting the NF-κB signaling. In order to better understand the genetic factors that influence association with SLE in genes that regulate the NF-κB pathway, we analyzed a dense set of genetic markers spanning TNIP1 and TAX1BP1, as well as the TNIP1 homolog, TNIP2, in case-control sets of diverse ethnic origins.
We fine-mapped TNIP1, TNIP2, and TAX1BP1 in a total of 8372 SLE cases and 7492 healthy controls from European-ancestry, African-American, Hispanic, East Asian, and African-American Gullah populations. Levels of TNIP1 mRNA and ABIN1 protein were analyzed using quantitative RT-PCR and Western blotting, respectively, in EBV-transformed human B cell lines.
We found significant associations between genetic variants within TNIP1 and SLE but not in TNIP2 or TAX1BP1. After resequencing and imputation, we identified two independent risk haplotypes within TNIP1 in individuals of European-ancestry that were also present in African-American and Hispanic populations. These risk haplotypes produced lower levels of TNIP1 mRNA and ABIN1 protein suggesting they harbor hypomorphic functional variants that influence susceptibility to SLE by restricting ABIN1 expression.
Our results confirmed the association signals between SLE and TNIP1 variants in multiple populations and provide new insight into the mechanism by which TNIP1 variants may contribute to SLE pathogenesis.
PMCID: PMC3485412  PMID: 22833143
16.  Reinterpreting Ethnic Patterns among White and African American Men Who Inject Heroin: A Social Science of Medicine Approach 
PLoS Medicine  2006;3(10):e452.
Street-based heroin injectors represent an especially vulnerable population group subject to negative health outcomes and social stigma. Effective clinical treatment and public health intervention for this population requires an understanding of their cultural environment and experiences. Social science theory and methods offer tools to understand the reasons for economic and ethnic disparities that cause individual suffering and stress at the institutional level.
Methods and Findings
We used a cross-methodological approach that incorporated quantitative, clinical, and ethnographic data collected by two contemporaneous long-term San Francisco studies, one epidemiological and one ethnographic, to explore the impact of ethnicity on street-based heroin-injecting men 45 years of age or older who were self-identified as either African American or white. We triangulated our ethnographic findings by statistically examining 14 relevant epidemiological variables stratified by median age and ethnicity. We observed significant differences in social practices between self-identified African Americans and whites in our ethnographic social network sample with respect to patterns of (1) drug consumption; (2) income generation; (3) social and institutional relationships; and (4) personal health and hygiene. African Americans and whites tended to experience different structural relationships to their shared condition of addiction and poverty. Specifically, this generation of San Francisco injectors grew up as the children of poor rural to urban immigrants in an era (the late 1960s through 1970s) when industrial jobs disappeared and heroin became fashionable. This was also when violent segregated inner city youth gangs proliferated and the federal government initiated its “War on Drugs.” African Americans had earlier and more negative contact with law enforcement but maintained long-term ties with their extended families. Most of the whites were expelled from their families when they began engaging in drug-related crime. These historical-structural conditions generated distinct presentations of self. Whites styled themselves as outcasts, defeated by addiction. They professed to be injecting heroin to stave off “dopesickness” rather than to seek pleasure. African Americans, in contrast, cast their physical addiction as an oppositional pursuit of autonomy and pleasure. They considered themselves to be professional outlaws and rejected any appearance of abjection. Many, but not all, of these ethnographic findings were corroborated by our epidemiological data, highlighting the variability of behaviors within ethnic categories.
Bringing quantitative and qualitative methodologies and perspectives into a collaborative dialog among cross-disciplinary researchers highlights the fact that clinical practice must go beyond simple racial or cultural categories. A clinical social science approach provides insights into how sociocultural processes are mediated by historically rooted and institutionally enforced power relations. Recognizing the logical underpinnings of ethnically specific behavioral patterns of street-based injectors is the foundation for cultural competence and for successful clinical relationships. It reduces the risk of suboptimal medical care for an exceptionally vulnerable and challenging patient population. Social science approaches can also help explain larger-scale patterns of health disparities; inform new approaches to structural and institutional-level public health initiatives; and enable clinicians to take more leadership in changing public policies that have negative health consequences.
Bourgois and colleagues found that the African American and white men in their study had a different pattern of drug use and risk behaviors, adopted different strategies for survival, and had different personal histories.
Editors' Summary
There are stark differences in the health of different ethnic groups in America. For example, the life expectancy for white men is 75.4 years, but it is only 69.2 years for African-American men. The reasons behind these disparities are unclear, though there are several possible explanations. Perhaps, for example, different ethnic groups are treated differently by health professionals (with some groups receiving poorer quality health care). Or maybe the health disparities are due to differences across ethnic groups in income level (we know that richer people are healthier). These disparities are likely to persist unless we gain a better understanding of how they arise.
Why Was This Study Done?
The researchers wanted to study the health of a very vulnerable community of people: heroin users living on the streets in the San Francisco Bay Area. The health status of this community is extremely poor, and its members are highly stigmatized—including by health professionals themselves. The researchers wanted to know whether African American men and white men who live on the streets have a different pattern of drug use, whether they adopt varying strategies for survival, and whether they have different personal histories. Knowledge of such differences would help the health community to provide more tailored and culturally appropriate interventions. Physicians, nurses, and social workers often treat street-based drug users, especially in emergency rooms and free clinics. These health professionals regularly report that their interactions with street-based drug users are frustrating and confrontational. The researchers hoped that their study would help these professionals to have a better understanding of the cultural backgrounds and motivations of their drug-using patients.
What Did the Researchers Do and Find?
Over the course of six years, the researchers directly observed about 70 men living on the streets who injected heroin as they went about their usual lives (this type of research is called “participant observation”). The researchers specifically looked to see whether there were differences between the white and African American men. All the men gave their consent to be studied in this way and to be photographed. The researchers also studied a database of interviews with almost 7,000 injection drug users conducted over five years, drawing out the data on differences between white and African men. The researchers found that the white men were more likely to supplement their heroin use with inexpensive fortified wine, while African American men were more likely to supplement heroin with crack. Most of the white men were expelled from their families when they began engaging in drug-related crime, and these men tended to consider themselves as destitute outcasts. African American men had earlier and more negative contact with law enforcement but maintained long-term ties with their extended families, and these men tended to consider themselves as professional outlaws. The white men persevered less in attempting to find a vein in which to inject heroin, and so were more likely to inject the drug directly under the skin—this meant that they were more likely to suffer from skin abscesses. The white men generated most of their income from panhandling (begging for money), while the African American men generated most of their income through petty crime and/or through offering services such as washing car windows at gas stations.
What Do These Findings Mean?
Among street-based heroin users, there are important differences between white men and African American men in the type of drugs used, the method of drug use, their social backgrounds, the way in which they identify themselves, and the health risks that they take. By understanding these differences, health professionals should be better placed to provide tailored and appropriate care when these men present to clinics and emergency rooms. As the researchers say, “understanding of different ethnic populations of drug injectors may reduce difficult clinical interactions and resultant physician frustration while improving patient access and adherence to care.” One limitation of this study is that the researchers studied one specific community in one particular area of the US—so we should not assume that their findings would apply to street-based heroin users elsewhere.
Additional Information.
Please access these Web sites via the online version of this summary at
The US Centers for Disease Control (CDC) has a web page on HIV prevention among injection drug users
The World Health Organization has collected documents on reducing the risk of HIV in injection drug users and on harm reduction approaches
The International Harm Reduction Association has information relevant to a global audience on reducing drug-related harm among individuals and communities
US-focused information on harm reduction is available via the websites of the Harm Reduction Coalition and the Chicago Recovery Alliance
Canada-focused information can be found at the Street Works Web site
The Harm Reduction Journal publishes open-access articles
The CDC has a web page on eliminating racial and ethnic health disparities
The Drug Policy Alliance has a web page on drug policy in the United States
PMCID: PMC1621100  PMID: 17076569
17.  The role of the African-American physician in reducing traffic-related injury and death among African Americans: consensus report of the National Medical Association. 
ISSUE: Traffic-related injuries and fatalities disproportionately affect the African American community. These high rates of traffic-related death and injury among African Americans manifest in multiple areas of traffic safety, including: Failure to use seat belts and child restraints. High incidence of alcohol-impaired driving. Failure to follow child passenger and seat belt safety laws and recommendations. High rates of pedestrian accidents, ofen brought on by impairments of drivers and/or pedestrians. Research indicates that national public information campaigns, with general messages only slightly modified for African American audiences, have not been culturally appropriate or effective in changing traffic safety behavior. In addition, traditional distribution mechanisms for these messages have not effectively reached the target population. Evidence suggests that in the African American community, there is a pervasive lack of knowledge of the devastating impact of traffic-related accidents on the overall health status of the community. This lack of information has resulted in a tragic cycle, in which parents fail to model safe operation of motor vehicles, and generation after generation copy this behavior, increasing the community's vulnerability to serious injuries and untimely deaths. This trend toward improper traffic safety habits among African Americans persists despite federal, state and local laws to enforce and promote sound traffic safety practices. OBJECTIVE: To study the existence of disparities in traffic-related injury and death among African Americans and to determine what kinds of traffic safety messages and campaigns will be effective in encouraging African Americans to respond to safety laws in sufficient numbers to reduce the disproportionately high rate of injury and death. Traffic safety issues were examined to effectively recommend policy, address barriers, best practices, and intervention strategies for the National Medical Association, its physician members, their patients, and their communities. CONSENSUS PROCESS: A literature review, driven by research instruments from numerous organizations included reports and materials from the National Highway Traffic Safety Administration (NHTSA), American Academy of Pediatrics, National Committee for Injury Prevention and Control, U.S. Centers for Disease Control and Prevention (CDC), Mothers Against Drunk Driving (MADD), and the National SAFE KIDS Campaign. Both the Meharry Medical College report, Achieving a Credible Health and Safety Approach to Increasing Seat Belt Use Among African-Americans, and the U.S. Department of Transportation's Blue Ribbon Panel to Increase Seat Belt Use Among African Americans: A Report to the Nation, provided substantial background for the panel. More than 60 pieces of traffic safety literature have been examined to date. Based on the literature review, a short list of the most relevant issues affecting African Americans and traffic safety was devised. It includes: The disproportionately high rate of traffic-related injury and death among African Americans. The cost in health, monetary costs and other associated costs of traffic safety accidents and injuries. The number of traffic-related injuries and deaths that could be prevented if more African Americans observed good traffic safety practices. Barriers to practicing good traffic safety habits among African Americans. Failure of laws and public information campaigns to influence improved traffic safety practices among African Americans sufficient to reduce disparities in traffic-related injury and death. In July 2001, NMA convened a consensus panel of experts in St. Thomas, U.S. Virgin Islands, to review a briefing document summarizing the most salient traffic safety issues among African Americans. The panel elaborated on key issues, including existing policy and standards for the use of child restraint devices to secure infants and toddlers, existing data regarding disparities in traffic-related injury and death among African Americans, and the cultural, age and developmental appropriateness of existing safety campaigns. SUMMARY: Public information campaigns have successfully improved traffic safety practices among the general public but in large part have been unsuccessful among minority populations-including African Americans. This may be due to: A failure to use techniques and messages that are culturally sensitive to African Americans. Campaigns that have targeted geographic and social centers where African Americans are not broadly present. Lack of awareness of the disproportionate effect motor vehicle crashes are having on African Americans. Scientifically based, culturally appropriate intervention strategies need to be devised and implemented by African American institutions and organizations to improve traffic safety practices and reduce the high rate of traffic-related injury and deaths among African Americans.
PMCID: PMC2594128  PMID: 11858225
18.  Risks of consumption of contaminated seafood: the Quincy Bay case study. 
A recent EPA-sponsored study of sediment and seafood contamination in Quincy Bay revealed elevated levels of several complex organic pollutants frequently of concern in human health assessments. A seafood consumption risk assessment was conducted using data from samples collected in Quincy Bay in the methodology developed for EPA's Office of Marine and Estuarine Protection for such assessments. Results showed estimated plausible, upperbound excess cancer risks in the 10(-5) to 10(-2) range. These results are comparable to those found in other seafood contamination risk assessments for areas where consumption advisories and fishing restrictions were implemented. Regulatory response included consumption advisories for lobster tomalley (hepatopancreas) and other types of locally caught seafood. Uncertainties inherent in seafood risk assessment in general and for the Quincy Bay case are discussed, along with implications for further action.
PMCID: PMC1519503  PMID: 2050051
19.  Early disease onset is predicted by a higher genetic risk for lupus and is associated with a more severe phenotype in lupus patients 
Annals of the rheumatic diseases  2010;70(1):151-156.
Systemic lupus erythematosus (SLE) is a chronic, multiorgan, autoimmune disease that affects people of all ages and ethnicities.
To explore the relationship between age at disease onset and many of the diverse manifestations of SLE. Additionally, to determine the relationship between age of disease onset and genetic risk in patients with SLE.
The relationship between the age at disease onset and SLE manifestations were explored in a multiracial cohort of 1317 patients. Patients with SLE were genotyped across 19 confirmed genetic susceptibility loci for SLE. Logistic regression was used to determine the relationships between the number of risk alleles present and age of disease onset.
Childhood-onset SLE had higher odds of proteinuria, malar rash, anti-dsDNA antibody, haemolytic anaemia, arthritis and leucopenia (OR=3.03, 2.13, 2.08, 2.50, 1.89, 1.53, respectively; p values <0.0001, 0.0004, 0.0005, 0.0024, 0.0114, 0.045, respectively). In female subjects, the odds of having cellular casts were 2.18 times higher in childhood-onset than in adult-onset SLE (p=0.0027). With age of onset ≥50, the odds of having proteinuria, cellular casts, anti-nRNP antibody, anti-Sm antibody, anti-dsDNA antibody and seizures were reduced. However, late adult-onset patients with SLE have higher odds of developing photosensitivity than early adult-onset patients. Each SLE-susceptibility risk allele carried within the genome of patients with SLE increased the odds of having a childhood-onset disease in a race-specific manner: by an average of 48% in Gullah and 25% in African-Americans, but this was not significant in Hispanic and European-American lupus patients.
The genetic contribution towards predicting early-onset disease in patients with SLE is quantified for the first time. A more severe SLE phenotype is found in patients with early-onset disease in a large multi-racial cohort, independent of gender, race and disease duration.
PMCID: PMC3034281  PMID: 20881011
20.  An evaluation of serum albumin, root caries, and other covariates in Gullah African Americans with type-2 diabetes 
Associations between dental conditions and overall health have been previously reported. Investigators have also shown significant inverse relationships between serum albumin (a general health status marker) and root caries. This relationship was explored among a study population of Gullah African Americans (who have a considerably lower level of non-African genetic admixture when compared to other African American populations) with type-2 diabetes (T2DM) and self-reported history of normal kidney function (N = 280).
Root caries indices were defined as total decayed and/or filled root surfaces. The coronal caries index [total decayed, missing, and/or filled coronal surfaces (DMFS)], level of glycemic control, total number of teeth, and other covariates were also evaluated. Logistic regression models were used to evaluate the associations between these factors and hypoalbuminemia (serum albumin concentrations <4 g/dl).
Serum albumin concentrations ranged 2.4–4.5 g/dl (mean = 3.8, SD = 0.3), with 70.4% exhibiting hypoalbuminemia. Root caries totals ranged 0–38 (mean = 1.3, SD = 4.5) surfaces decayed/filled, while total teeth ranged 1–28 (mean = 19.4, SD = 6.2). DMFS totals ranged 2–116 (mean = 55.2, SD = 28.0). We failed to detect significant associations for root caries; however, the final multivariable logistic regression models showed significant associations between hypoalbuminemia and total teeth [odds ratio (OR) = 0.93, P = 0.01], poor glycemic control (OR = 2.49, P < 0.01), elevated C-reactive protein (OR = 1.57, P < 0.01), glomerular filtration rates ≥60 (OR = 0.31, P = 0.03), and age (OR = 0.97, P = 0.03).
Previously reported inverse relationships between serum albumin and root caries were not evident in our study population. We propose that these null findings are because of the considerably lower level of root caries as well as other differing characteristics (including oral health status, the chronic presence of T2DM, and predominantly younger age) within our study population compared to these previously assessed groups.
PMCID: PMC3071686  PMID: 21070320
diabetes; Gullah African Americans; root caries; serum albumin
21.  Pregnancy outcomes among African–American patients with systemic lupus erythematosus compared with controls 
Lupus science & medicine  2014;1(1):e000020.
In a study of Gullah African–Americans, we compared pregnancy outcomes before and after systemic lupus erythematosus (SLE) diagnosis to controls to test whether there is a predisease state that negatively affects pregnancy outcomes.
Cases and controls reporting at least one pregnancy were included. Controls were all Gullah African-American females. We collected demographic, socioeconomic and pregnancy data. We modelled pregnancy outcome associations with case status using multiple logistic regression to calculate ORs.
After adjustment for age, years of education, medical coverage and pregnancy number, compared with controls, cases were more likely to have any adverse outcome (OR 2.35, 95% CI 1.78 to 3.10), including stillbirth (OR 4.55, 95% CI 1.53 to 13.50), spontaneous abortion (OR 2.05, 95% CI 1.40 to 3.00), preterm birth (OR 2.58, 95% CI 1.58 to 4.20), low birth weight (OR 2.64, 95% CI 1.61 to 4.34) and preeclampsia (OR 1.80, 95% CI 1.08 to 3.01). The odds of adverse pregnancy outcomes all increased after SLE diagnosis compared with before diagnosis, even after adjustment for age, years of education, pregnancy number and medical coverage.
From a large cohort of African–American women, our findings suggest there may be a predisease state that predisposes to adverse pregnancy outcomes.
PMCID: PMC4211631  PMID: 25360323
22.  Pregnancy outcomes among African–American patients with systemic lupus erythematosus compared with controls 
Lupus Science & Medicine  2014;1(1):e000020.
In a study of Gullah African–Americans, we compared pregnancy outcomes before and after systemic lupus erythematosus (SLE) diagnosis to controls to test whether there is a predisease state that negativelyaffects pregnancy outcomes.
Cases and controls reporting at least one pregnancy were included. Controls were all Gullah African-American females. We collected demographic, socioeconomic and pregnancy data. We modelled pregnancy outcome associations with case status using multiple logistic regression to calculate ORs.
After adjustment for age, years of education, medical coverage and pregnancy number, compared with controls, cases were more likely to have any adverse outcome (OR 2.35, 95% CI 1.78 to 3.10), including stillbirth (OR 4.55, 95% CI 1.53 to 13.50), spontaneous abortion (OR 2.05, 95% CI 1.40 to 3.00), preterm birth (OR 2.58, 95% CI 1.58 to 4.20), low birth weight (OR 2.64, 95% CI 1.61 to 4.34) and preeclampsia (OR 1.80, 95% CI 1.08 to 3.01). The odds of adverse pregnancy outcomes all increased after SLE diagnosis compared with before diagnosis, even after adjustment for age, years of education, pregnancy number and medical coverage.
From a large cohort of African–American women, our findings suggest there may be a predisease state that predisposes to adverse pregnancy outcomes.
PMCID: PMC4211631  PMID: 25360323
systemic lupus erythematosus; pregnancy
23.  A Quantitative Synthesis of Mercury in Commercial Seafood and Implications for Exposure in the United States 
Environmental Health Perspectives  2012;120(11):1512-1519.
Background: Mercury (Hg) is a toxic metal that presents public health risks through fish consumption. A major source of uncertainty in evaluating harmful exposure is inadequate knowledge of Hg concentrations in commercially important seafood.
Objectives: We examined patterns, variability, and knowledge gaps of Hg in common commercial seafood items in the United States and compared seafood Hg concentrations from our database to those used for exposure estimates and consumption advice.
Methods: We developed a database of Hg concentrations in fish and shellfish common to the U.S. market by aggregating available data from government monitoring programs and the scientific literature. We calculated a grand mean for individual seafood items, based on reported means from individual studies, weighted by sample size. We also compared database results to those of federal programs and human health criteria [U.S. Food and Drug Administration Hg Monitoring Program (FDA-MP), U.S. Environmental Protection Agency (EPA)].
Results: Mean Hg concentrations for each seafood item were highly variable among studies, spanning 0.3–2.4 orders of magnitude. Farmed fish generally had lower grand mean Hg concentrations than their wild counterparts, with wild seafood having 2- to12-fold higher concentrations, depending on the seafood item. However, farmed fish are relatively understudied, as are specific seafood items and seafood imports from Asia and South America. Finally, we found large discrepancies between mean Hg concentrations estimated from our database and FDA-MP estimates for most seafood items examined.
Conclusions: The high variability in Hg in common seafood items has considerable ramifications for public health and the formulation of consumption guidelines. Exposure and risk analyses derived from smaller data sets do not reflect our collective, available information on seafood Hg concentrations.
PMCID: PMC3556626  PMID: 22732656
aquaculture; consumption advisory; contaminants; fisheries; Seafood Hg Database; seafood safety
24.  Maternal fish and shellfish intake and pregnancy outcomes: A prospective cohort study in Brittany, France 
Environmental Health  2007;6:33.
Recommendations about risks and benefits of seafood intake during pregnancy have been published in the last decade, but the specific health effects of the different categories of seafood remain unknown. Fish and shellfish may differ according to their fatty acid content and their concentration of chemical pollutants and toxins. Not taking these particularities into account may result in underestimating of both the positive and negative effects of seafood on birth outcomes and partly explains inconsistent results on the subject.
In the PELAGIE cohort study, including 2398 pregnant women from Brittany, we fit multiple linear and logistic regression models to examine associations of fish (salt-water fish only) and shellfish intake before pregnancy with length of gestation, birthweight, and risks of preterm births, low birthweight or small-for-gestational-age (SGA) babies.
When fish and shellfish consumptions were considered simultaneously, we observed a decrease in the risk of SGA birth with increasing frequency of fish intake: OR = 0.57 (95%CI: 0.31 to 1.05) for women eating fish twice a week or more compared with those eating it less than once a month. The risk of SGA birth was significantly higher among women eating shellfish twice a week or more than among those eating it less than once a month: OR = 2.14 (95%CI: 1.13 to 4.07). Each additional monthly meal including fish was significantly related to an increase in gestational length of 0.02 week (95%CI: 0.002 to 0.035). No association was observed with birthweight or preterm birth.
These results suggest that different categories of seafood may be differently associated with birth outcomes, fish consumption with increased length of gestation and shellfish consumption with decreased fetal growth.
PMCID: PMC2211746  PMID: 17958907
25.  Trends and correlates in meat consumption patterns in the US adult population 
Public health nutrition  2010;13(9):1333-1345.
Few studies have examined recent shifts in meat consumption (MC), differences among US population groups, and the influence of psychosocial–behavioural factors.
Nationally representative data collected for US adults aged ≥18 years in the 1988–1994 and 1999–2004 National Health and Nutrition Examination Survey (NHANES) and the 1994–1996 Continuing Survey of Food Intakes by Individuals (CSFII) and Diet and Health Knowledge Survey (DHKS) were used.
We found a U-shaped trend in MC, a decrease between 1988–1994 and 1994–1996, and an increase from 1994–1996 to 1999–2004. NHANES 1988–1994 and 1999–2004 indicate that MC did not change significantly, particularly for all meat, red meat, poultry and seafood. Between 1994–1996 and 1999–2004, average MC, including red meat, poultry, seafood and other meat products, increased in men. Women’s total MC decreased, mainly due to decreased red meat and other meat products, except for increased seafood. Noticeable differences existed in the changes across population groups. Black men had the largest increase in consumption of total meat, poultry and seafood; Mexican American men had the smallest increase in poultry, seafood and other meat products. In 1999–2004, ethnic differences in MC became greater in women than among women in 1994–1996. Associations between MC and energy intake changed over time. Perceived benefit of dietary quality and food label use were associated with reduced red MC.
Noticeable differences exist in the shifts in MC across population groups and surveys. MC increased in men but decreased in women in recent years.
PMCID: PMC2916052  PMID: 20188005
Meat consumption; Food intake; Trend; Diet; NHANES; CSFII; United States

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