Letters We compared salt and sodium consumption in China in 2000 with 2009-2012.

RESEARCH LETTER

Salt and Sodium Intake in China Noncommunicable diseases are increasing globally, with major soc ioeconomic implic ations. 1 The World Health Organization 2 proposed 9 noncommunicable disease– related targets, including 30% reduction in salt/sodium intake to reduce risk of hypertension. In China, hypertension prevalence is rising3 and salt intake is high (12 g/person/d).4 However, this estimate derives from 2002, and China’s dietary habits are changing.

Method | The National Centre for Food Safety Risk Assessment Ethics Committee approved China’s total diet studies. All participating householders provided oral consent. Total diet studies include weighed food intake and laboratory analysis of prepared foods representing dietary intake, using a standardized design.5 They are designed to assess food consumed and its biochemical content, accounting for losses during processing, preparation, and storage. By 2011,

Table. Weighed Daily Salt Intake and Laboratory-Analyzed Sodium Intake of a Standard Person in 12 Provinces of China in 2000 and 2009-2011 and in 8 Additional Provinces in 2009-2012 Weighed Salt Intake, g

Analyzed Sodium Intake, g

Year

Year

2000

2009-2011

Change, %

2000

2009-2011

Proportion of Chinese Population, % Change, %

2000a

2010a 6.6

12 Provincesb Heilongjiang

10.1

7.6

−24.8

5.3

4.9

−7.6

6.7

Liaoning

10.6

11.7

10.4

5.2

5.0

−4.6

7.4

7.5

Hebei

11.3

11.3

0.0

7.4

6.0

−18.2

11.7

12.4

Shaanxi

17.9

11.7

−34.6

9.0

6.5

−28.0

6.4

6.4

Henan

13.5

12

−11.1

6.3

7.1

12.0

16.7

16.2

Ningxia

10

7

−30.0

4.4

3.8

−12.8

1.0

1.1

Shanghai

10.3

6.7

−35.0

4.9

4.7

−3.9

2.9

4.0

Fujian

10.5

6.8

−35.2

6.2

6.9

11.4

6.0

6.4

Jiangxi

11.5

6.3

−45.2

5.1

3.7

−26.7

7.3

7.7

Hubei

15.2

8.9

−41.4

8.2

5.9

−28.7

10.5

9.9

Sichuan

10.1

5.6

−44.6

6.4

3.4

−47.0

15.1

13.9

7.6

9.8

28.9

61.0

8.4

7.9

Guangxi Unweighted, mean (SD)

11.6 (2.8)c

Population-weighted intake, mean

11.8

4.5

7.2

8.8 (2.4)c

−24.1

6.1 (1.5)

5.4 (1.4)

−11.5

9.2

−22.2

6.4

5.6

−12.3

8 Additional Provincesa

2009-2012

2009-2012

Beijing

11.7

7.5

Jilin

10.2

4.5

6.4

Qinghai

9.4

5.8

13.1

Inner Mongolia

8.7

4.7

5.7

Jiangsu

9.8

5.1

18.2

Zhejiang

8

5.7

12.6

Hunan

9.2

6.7

15.2

Guangdong

7.4

3.4

24.2

Unweighted intake, mean (SD)

9.3 (1.3)

5.4 (1.3)

Population-weighted intake, mean

8.9

5.2

Unweighted intake, mean (SD)

9.0 (2.0)

5.4 (1.3)

Population-weighted intake, mean

9.1

4.5

All 20 Provinces (2009-2012)

a

Census year.

b

The sample size in each province was 90 households, averaging 3.5 persons in 2000 and 3.4 persons in 2009-2012.

5.4 c

Yields a calculated sodium intake of 4.6 g/d in 2000, and 3.5 g/d in 2009-2011, based on the molecular mass of salt (58.4 g/mol) and atomic weight of sodium (23 g/mol).

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Letters

30 countries, including 5 in Europe, had conducted total diet studies.5 Total diet studies were undertaken in 2000 and 20092011 in 12 of China’s 31 mainland provinces. These provinces were selected to represent its geographic regions and dietary habits, and housed approximately 50% of its population. Eight additional provinces housing 29% of the population were studied in 2009-2012, expanding geographic coverage; only China’s far west region was not studied. In each province’s total diet study, 1 urban district and 2 rural counties were randomly selected from lists of nonpoor districts and counties, representing typical dietary intake. Within each district or county, 2 communities or townships, then 5 neighborhoods or villages, and then 30 households were randomly selected. Study personnel recorded all residents’ dietary intake by recording food consumption and weighing ingredients, including salt, during 3 consecutive daily visits. No households refused to participate. Using local ingredients, matching foods were prepared and analyzed at China’s national reference laboratory. Using the age, weight, sex, and occupation of those surveyed, the daily salt and sodium consumption of a standard person (man, aged 18–45 years, weighing 63 kg, and engaging in light activity) was calculated for each province, to represent a value around which the sampled householders’ salt/sodium consumption varies. Meals consumed outside the home were excluded from the calculation. Salt consumption, based on household measurements, and laboratory-analyzed sodium in prepared food samples were analyzed. We compared salt and sodium intake in the 12 provinces surveyed twice using a 2-sided t test (P < .05 for significance) in SPSS Statistics (IBM), version 13. To derive national estimates, we calculated population-weighted intakes. To verify previous research on dietary salt intake in China, we also compared calculated sodium intake, based on salt consumption, with laboratory-analyzed sodium intake. Results | In 2000, 1080 households participated (n = 3725; mean age, 34.7 years [SD, 19.6]; 49% men); from 2009 through 2012, 1800 households participated (n = 6072; mean age, 42 years [SD, 20.1]; 47% men). Five percent of data was missing. Among 20 provinces surveyed from 2009 through 2012, the population-weighted, mean weighed salt intake of a standard person was 9.1 g per day and laboratory-analyzed sodium intake was 5.4 g per day (Table). Among 12 provinces surveyed twice, salt intake decreased 22.2% between 2000 (11.8 g/d) and 2009-2011 (9.2 g/d) (t = 2.53, P = .03). However, the 12.3% decrease in sodium intake (from 6.4 g/d in 2000 to 5.6 g/d in 2009-2011) was nonsignificant (t = 1.21, P = .25). Weighed salt consumption yielded a calculated sodium intake (4.6 g/d in 2000 vs 3.5 g/d in 2009-2011) much less than laboratory-analyzed sodium intake (see Table footnote). Discussion | All provinces exceeded the recommended daily maximum intake of salt (5 g/d) and sodium (2 g/d). Although salt added during food preparation has decreased over time, total sodium intake has not (noting the large increase in Guangxi). 704

These findings update studies using different methodologies in the 1990s6 and 20024 and confirm that simply weighing dietary salt intake underestimates sodium consumption in China.6 Limitations of the total diet studies include the small samples, but China’s ethnic and socioeconomic homogeneity suggests mostly uniform dietary habits within provinces. For the same reason, clustering and studying different households in 2000 and 2009-2011 should not have affected the findings. Inclusion of meals consumed outside the home was impracticable; they may be more highly seasoned. Poor communities were excluded, but their number is small. China’s diet is changing and refrigeration is replacing salt for food preservation. High sodium intake persists due to addition of salt and other seasonings during food preparation, and increasing consumption of processed food. Further efforts are needed to limit salt/sodium intake, and regular monitoring is needed to assess progress.2 David B. Hipgrave, MBBS, PhD, FRACP Suying Chang, MSc, PhD Xiaowei Li, PhD Yongning Wu, PhD Author Affiliations: UNICEF Headquarters, New York, New York (Hipgrave); UNICEF, Beijing, China (Chang); Key Laboratory for Food Safety Risk Assessment, China National Centre for Food Safety Risk Assessment, Beijing, China (Li, Wu). Corresponding Author: Yongning Wu, PhD, Key Laboratory for Food Safety Risk Assessment, China National Centre for Food Safety Risk Assessment, Bldg 2, No. 37 Guangqu Rd, Chaoyang District, Beijing, 100022, China ([email protected]). Author Contributions: Drs Wu and Hipgrave had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Hipgrave, Chang, Li, Wu. Acquisition, analysis, or interpretation of data: Hipgrave, Chang, Li, Wu. Drafting of the manuscript: Hipgrave, Li. Critical revision of the manuscript for important intellectual content: Hipgrave, Chang, Li, Wu. Statistical analysis: Hipgrave, Chang, Li. Obtained funding: Wu. Administrative, technical, or material support: Hipgrave, Chang, Li, Wu. Study supervision: Wu. Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported. Funding/Support: This work was supported by the National Natural Science Foundation of China (grant 21537001; 2007 and 2009 surveys), the National Basic Research Program of China (973 Program 2012CB720804; 2009 survey), the China Ministry of Health (grant 200902009; 2009 survey), and UNICEF (2009 survey). The authors were entirely funded by their institutions. Role of the Funder/Sponsor: UNICEF played a role in the design and conduct of the study, collection, management, analysis and interpretation of the data, preparation, review and approval of the manuscript, and the decision to submit the manuscript for publication. 1. Lozano R, Naghavi M, Foreman K, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380(9859): 2095-2128. 2. World Health Organization. Global Action Plan for the Prevention and Control of Noncommunicable Diseases 2013-2020. Geneva, Switzerland: WHO; 2013.

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3. Liang Y, Liu R, Du S, Qiu C. Trends in incidence of hypertension in Chinese adults, 1991-2009: the China Health and Nutrition Survey. Int J Cardiol. 2014;175 (1):96-101. 4. Zhai F, Yang X. Report of National Nutrition and Health Survey of China Residents in 2002: Part 2: Diet and Nutrition Intake. Beijing, China: People's Health Press; 2006. 5. World Health Organization, Food and Agriculture Organization of the United Nations, European Food Safety Authority. Towards a harmonised total diet study approach: a guidance document. http://www.who.int/foodsafety /publications/tds_guidance/en/. Accessed January, 12, 2016. 6. Anderson CA, Appel LJ, Okuda N, et al. Dietary sources of sodium in China, Japan, the United Kingdom, and the United States, women and men aged 40 to 59 years: the INTERMAP study. J Am Diet Assoc. 2010;110(5):736-745.

Corresponding Author: Dianna J. Magliano, PhD, Baker IDI Heart and Diabetes Institute, 99 Commercial Rd, Melbourne, Victoria, Australia 3004 ([email protected]). Conflict of Interest Disclosures: The authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported. 1. Menke A, Casagrande S, Geiss L, Cowie CC. Prevalence of and trends in diabetes among adults in the United States, 1988-2012. JAMA. 2015;314(10): 1021-1029. 2. Xu Y, Wang L, He J, et al; 2010 China Noncommunicable Disease Surveillance Group. Prevalence and control of diabetes in Chinese adults. JAMA. 2013;310 (9):948-959. 3. Engelgau MM, Thompson TJ, Herman WH, et al. Comparison of fasting and 2-hour glucose and HbA1c levels for diagnosing diabetes: diagnostic criteria and performance revisited. Diabetes Care. 1997;20(5):785-791.

COMMENT & RESPONSE

US Trends for Diabetes Prevalence Among Adults To the Editor Dr Menke and colleagues1 provided a comprehensive study of diabetes prevalence and trends in the United States from 1988 to 2012. The prevalence of diabetes was high at 14.3%. In particular, the highest prevalence rates (>20%) were seen among participants who were non-Hispanic black, nonHispanic Asian, and Hispanic. These data could be a cause for great concern. However, this study defined undiagnosed diabetes by any of 3 glycemic markers (ie, hemoglobin A1C, fasting plasma glucose [FPG], and 2-hour plasma glucose [2-hour PG] from the oral glucose tolerance test). The authors suggested that this allows for full accounting of diabetes. This is 1 of at least 2 studies2 reporting diabetes prevalence in this way in recent years. Each of the 3 measures of glycemia identifies separate but overlapping groups of individuals with diabetes.3 When diabetes is so defined, diabetes prevalence will be higher. Most previous studies have used only 1 or 2 measures of glycemia. We argue that there is little evidence supporting the value of using all 3 measures. Combining FPG and 2-hour PG to define diabetes is logical because they represent different pathophysiological processes of diabetes with respect to the relative contributions of insulin secretory defects and hepatic and peripheral insulin resistance. However, there is limited understanding of how hemoglobin A1C contributes independently to the estimate of diabetes prevalence. Furthermore, given the modest repeatability of the FPG and 2-hour PG tests on different days,4 which results in a significant proportion of those identified as having diabetes on 1 day as not having diabetes on a subsequent day, the estimated prevalence of diabetes using these glycemic markers alone will already be somewhat inflated. Hemoglobin A1C is a more practical test to use to define diabetes, but a more expensive means of assessing prevalence. Diabetes prevalence should not be estimated using any of the 3 tests until there is improved understanding of how the approach relates to more traditional and better understood methods. Dianna J. Magliano, PhD Paul Zimmet, PhD, FRACP Jonathan Shaw, FRACP

Author Affiliations: Baker IDI Heart and Diabetes Institute, Melbourne, Australia.

4. Mooy JM, Grootenhuis PA, de Vries H, et al. Intra-individual variation of glucose, specific insulin and proinsulin concentrations measured by two oral glucose tolerance tests in a general Caucasian population: the Hoorn Study. Diabetologia. 1996;39(3):298-305.

In Reply Dr Magliano and colleagues raise concern regarding our use of all 3 glycemic markers (hemoglobin A1c, FPG, and 2-hour PG) in defining undiagnosed diabetes, and of the lack of repeat testing in the National Health and Nutrition Examination Survey (NHANES). We agree that FPG and 2-hour PG may represent complementary pathophysiological processes of diabetes and using both may be logical when defining diabetes. However, hemoglobin A1c is a valid diagnostic marker that is commonly used in clinical practice and has less day-to-day variability than the other markers.1 All 3 markers are associated with diabetes complications.2 Based on this evidence, the American Diabetes Association (ADA) revised its diagnostic criteria in 2010 recommending the addition of hemoglobin A1c as a diagnostic test for diabetes,2 and the World Health Organization (WHO) made a similar revision to its diagnostic criteria in 2011.3 Magliano and colleagues state that few previous studies used all 3 measures, but this is expected because the ADA and WHO guidelines were only recently revised and prior studies would not be expected to have used hemoglobin A1c when defining diabetes. We agree that a diagnosis based on the 3 markers may not be perfectly aligned because individuals may be positive for some but not all markers; thus, using all 3 markers will result in a higher prevalence rate than using any 1 or 2 markers. However, the ADA does not state a preference for any specific marker because any 1 marker is sufficient to diagnose diabetes regardless of the results of the other 2 markers. In addition, Magliano and colleagues state there is limited understanding of how adding hemoglobin A1c contributes independently to diabetes prevalence. A previous 20052006 NHANES study found that 5.1% of the US population had either FPG or 2-hour PG above the diabetes cut point, whereas an additional 0.3% had hemoglobin A1c above the diabetes cut point. This suggests that the addition of hemoglobin A1c has a relatively small effect on estimates of undiagnosed diabetes.4 The marker that increased prevalence the most was 2-hour PG;

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